Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 22, 2026.

Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny

Polavarapu B. Kavi Kishor

Frontiers in Plant Science · 2015 · Review

doi:10.3389/fpls.2015.00544

Abstract

Proline is a proteogenic amino acid and accumulates both under stress and non-stress conditions as a beneficial solute in plants. Recent discoveries point out that proline plays an important role in plant growth and differentiation across life cycle. It is a key determinant of many cell wall proteins that plays important roles in plant development. The role of extensins, arabinogalactan proteins and hydroxyproline- and proline-rich proteins as important components of cell wall proteins that play pivotal roles in cell wall signal transduction cascades, plant development and stress tolerance is discussed in this review. Molecular insights are also provided here into the plausible roles of proline transporters modulating key events in plant development. In addition, the roles of proline during seed developmental transitions including storage protein synthesis are discussed.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 22, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

Glutamate is an important amino acid and acts as a precursor for the biosynthesis of γ-aminobutyric acid, arginine, glutamine, and proline in plants as well as in other eukaryotes. Proline can be distinguished among all other amino acids due to its unique structure with its α-amino group as a secondary amine and possesses distinctive cyclic structure which causes exceptional conformational rigidity to the protein structure. It has also specific chemical properties like zwitterionic nature, neutral pH, high compatibility with cell milieu and extreme solubility as 14 kgs of it can be dissolved in 1 kg of water. Though evidence has been presented for the synthesis of proline from glutamate and ornithine in higher plants, the role of ornithine as proline precursor is doubtful as pointed out by. The pathway for proline biosynthesis in higher plants differs from that of bacteria. The genes that encode the enzymes involved in proline biosynthesis like pyrroline-5-carboxylate synthetase (P5CS), pyrroline-5-carboxylate reductase (P5CR), and ornithine-δ-aminotransferase (OAT) and proline catabolism such as proline dehydrogenase (PDH) and pyrroline-5-carboxylate dehydrogenase (P5CDH) have been identified and isolated. P5CS1 was first cloned from Vigna aconitifolia by complementation technique, and found to be a novel bifunctional enzyme (with activities of both γ-glutamy kinase and glutamic γ-semialdehyde dehydrogenase) that catalyzes glutamate to pyrroline-5 carboxylate, an intermediate in proline biosynthesis. This is a rate limiting step in proline biosynthesis. P5CS is encoded by two differentially regulated genes (P5CS1 and P5CS2) and P5CS2 was first cloned from Arabidopsis thaliana. While P5CS1 is abundantly expressed in most plant parts but not in dividing cells, P5CS2 is highly expressed at the transcriptional level in dividing cells. Besides acting as a proteogenic amino acid, it accumulates in large quantities and plays a role during abiotic stress tolerance in plants. Thus, it is known that proline participates in the biosynthesis of primary metabolism, but also has special functions to carry as a metabolite during growth and development. Proline not only accumulates during abiotic stress, but also in different tissues of plants under non-stress conditions too. The role of proline as osmoprotectant in stress tolerance has been extensively reviewed. Though many amino acids constitute a major source of the components used for cellular growth and differentiation in higher plants, proline is distinct from others. The emerging roles of proline in plant growth and development from the perspective of proline homeostasis in mediating growth and development has been reviewed. Over and above, proline is an important source of cell wall matrix. As a component of cell wall proteins, it plays pivotal role in plant development but understanding of its diverse functions appears to be enigmatic. Cell walls contain hydroxyproline-rich O-glycoproteins (HRGPs) as complex macromolecules with varying structures and functions and encompass a broad category of extracellular proteins. HRGPs contain variations of Pro-Pro repeats and are lightly glycosylated. Their classification is based on proline residue-containing proteins. It is a superfamily that is classified into extensins (EXTs) that are moderately glycosylated, arabinogalactan-proteins (AGPs) that are hyperglycosylated and Hyp/Pro-rich proteins (H/PRPs) that may not be glycosylated at all, or either weakly- or highly glycosylated. HRGPs undergo post-translational modifications like conversion of proline to hydroxyproline (Hyp) by a membrane-bound prolyl 4-hydroxylases (P4Hs) or glycosylation of HRGPs by glycosyltransferases. This sub-family is characterized by O-Hyp linked arabinosides and arabinogalactan polysaccharides which define the molecular surface. Arabinosylation and arabinogalactosylation would depend upon contiguous Hyp and clustered non-contiguous Hyp. What directs the Hyp glycosylation is a code based on peptide sequence. While Ser-Hyp4 motifs of EXTs are preferred sites for the addition of arabinoside, Ser-Hyp and Ala-Hyp repeats of the AGPs are the usual sites of arabinogalactan heteropolysaccharide addition. Studies carried out by many suggest that species variation and tissue specific Hyp glycosylation occurs. HRGPs appear to be not solubilized in cell walls as a response to the stress. They are expressed during wounding and pathogen attack in some tissues and implicated in different stages of plant growth and development, nodule formation, fertilization, cytokinesis, apoptosis, senescence, and cell wall lignification. Different roles of proline in plant ontogeny and during key transitions are summarized in Table 1. In the present endeavor, we aim at reviewing the progress of multidimensional functions of proline in plant ontogeny which is contributing to cell wall modifications and also during key transitional events especially reproductive development. In addition, the implications of proline during seed development and seed storage metabolism has been highlighted.

Significance of Proline in Developing Seeds and in Protein Synthesis

It is known that proline plays a vital role in regulating general protein synthesis in plants. Seed mutants with opaque phenotypes have been discovered in maize. These mutants have been found to be associated with zein (a prolamin protein in seeds) synthesis. The auxotrophic recessive opaque mutant in maize, named as Proline responding1 (pro1), displays not only collapsed starchy endosperm morphology but also seedling lethality. Later, it was found out that mutants can be restored as normal phenotypes with the supply of exogenous proline and they have predicted that these mutants might have a defect in the biosynthesis of proline. Recently, reported positional cloning and functional characterization of proline responding1 gene (pro1). The conclusion of that maize Pro1 encodes a P5CS2 is based on the phylogenetic tree built on the P5CS full-length protein sequences taken from the genomes of A. thaliana, rice and maize. It has been found that this protein is localized in cytoplasm and expressed in roots, stems, silk, tassels, and kernels in these mutants and external feeding of proline rescued the viability of pro1 seedlings. They also unraveled the mechanism related to this mutation. In these pro1 mutants, lack of proline results in enhanced accumulation of uncharged tRNAproAGG. But, such an accumulation leads to a sequence of consequences, first the phosphorylation of eukaryotic initiation factor 2α (elF2α) in the mutant pro1 and subsequently a reduction in general protein synthesis. Thus, in pro1 mutants, lack of proline affects protein accumulation. Interestingly, further revealed that proline deficiency also leads to downregulation of cyclin genes at the transcriptional level and thus the cell cycle in the pro1 mutants is significantly affected. RT-PCR analysis revealed that CDC6 and MCM7 genes encoding proteins involved in the formation of prereplicative complex are downregulated in pro1 mutants, but external supply of proline induces the expression of A, B, and D cyclins, H2, H3, and H4 histones and DNA replication related genes in pro1 mutants. These studies point out that lack of proline affects cyclin genes at the transcriptional level and ultimately protein accumulation in seeds.

Proline Accumulation and Root Biomass

Though proline is produced at low levels in all tissues in unstressed conditions, it is actively transported to the roots under stress conditions. Further, it is compartimentalized into the mitochondria where it is degraded back to glutamate releasing energy in the form of FADH2 and NAD(P)H by two different enzymes. At low water potentials, maize primary roots have been shown to accumulate proline. Maintenance of root elongation at low water potential depends on enhanced ABA content. When endogenous ABA levels were decreased either by using fluridone or vp5 mutant, proline concentrations also decreased in the root elongation zone. But, proline concentrations in fluridone treated roots were restored back by the addition of 7 μM ABA. These experiments demonstrate that increased ABA is necessary for the deposition of proline in maize primary root growth zone. also demonstrated that proline levels are high toward the root apex (120 m.mol growing at a water potential of -1.6 mpa), where elongation rates of roots are maintained under a range of water deficit conditions. They suggested that proline deposition in the growing root zone is important for osmotic adjustment. But, how proline deposition plays a role in the maintenance of root elongation at low water potentials is not clearly known. found out that proline synthesis in maize root tips from [3H]glutamate and [14C]ornithine did not increase significantly at low water potential and accounted for only a small fraction of the proline deposition. Proline is also not catabolized and utilized in the root tips under low water potential. But, increased uptake was noticed suggesting increased transport of it. Removal of endosperm from the germinated seedlings decreased the proline accumulation in root tips at low water potentials in maize. They conclude that endosperm is the source of proline accumulation in the root tips of intact seedlings constituting 10% of the free amino acids released from endosperm. Labeling experiments also revealed that proline is transported from the scutellum to other parts of the seedlings and peaked in the root tips. Though the biosynthetic capacity of roots to produce proline is low, proline accumulation perhaps is regulated by the rates of its transport and utilization. A unique salt-inducible proline transporter was isolated from barley (Hordeum vulgare) and found to express strongly in root cap cells under salt stress. Hence, it may play a role in the root tip region when plants are exposed to salt stress. analyzed the spatial distribution of transcript changes in the maize primary root elongation zone at low water potential. They concluded that different signaling and metabolic response mechanisms (wall loosening proteins in region I, and for elements of ABA and ethylene signaling) are involved in the response to water stress in different regions of the maize primary root elongation zone. Further, overexpression of Vigna P5CS in tobacco and Sorghum bicolor resulted in better root biomass under salt stress conditions. Proline accumulation by overexpression of P5CSF129A, a mutated version of Vigna P5CS in transgenic chickpea also resulted in root elongation and higher root biomass both under salt and drought stress conditions. It appears therefore, proline may play a direct or indirect role in enhancing root biomass in transgenics under stress conditions perhaps by supplying necessary energy [FADH2 and NAD(P)H] and nitrogen.

Several studies related to seed germination have suggested that oxidative pentose phosphate pathway (OPPP) is important in triggering seed germination. Since this pathway generates NADPH, the energy may be utilized for anabolic reactions during seed germination. also suggested a link between proline and OPPP. But, the molecular events leading to upregulation of OPPP and its precise role in triggering seed germination is not known completely. have analyzed the dehydrogenase enzymes involved in OPPP during Arabidopsis seed germination and found activation of this pathway along with fourfold increase in proline content before the emergence of the radicle. When AtP5CS1 gene was inserted in an antisense orientation into Arabidopsis, delayed emergence of radicle was noticed. Proline synthesis might replenish the NADP+ pool and therefore activate OPPP. This indicates a functional link between elevated proline biosynthesis and enhanced OPPP activity and coupling of both the pathways may be important in stimulating germination.

Effects of Proline Accumulation in Reproductive Tissues under Non-Stressed Conditions

Under normal physiological (non-stressed) conditions, plants accumulate large amounts of proline during the transition to flower initiation, a common phenomenon but often an overlooked fact. Similarly, proline content in tomato flowers was 60 times higher than any other vegetative tissue and >70% of total free amino acids was noticed in pollen grains. A wide range of plants like mature fruits of citrus, pollen grains of petunia and tomato, ovules of broad bean, inflorescences and siliques of Brassica napus also contain very high levels of proline. Accumulation of proline is due to upregulation of proline biosynthetic pathway gene P5CS, downregulation of ProDH and activation of a proline transporter T (ProT) in flowers. Proline accumulation predominantly in reproductive tissues suggests that it may be associated with their development. It is also transported to reproductive organs as has been pointed out by and. These findings suggest that proline may play a role during flower initiation and its subsequent development.

Overexpression of P5CS in tobacco resulted in higher accumulation of proline, and enhanced flowering with more number of flowers per plant and coflorescence (cluster of flowers) formation under stress conditions. Over expression of P5CS1 and over-accumulation of proline lead to early flowering and bolting promotion during the early stages of plant development in Arabidopsis. But, during the later stages, downregulation occurred probably because of gene silencing, leading to low proline and bushy appearance of the plants. On the contrary, antisense expression of P5CS1 inhibited bolting in Arabidopsis. The p5cs1 loss-of-function mutants exhibit delay in flowering implying that P5CS1 plays an important role in flowering time. They also noticed that down-regulation of P5CS1 caused reduction in proline content, impaired flowering, and stunted growth. made a detailed analysis of the proline biosynthetic pathway enzymes to dissect out their roles during vegetative and reproductive development of Arabidopsis. In their conditions, they found alteration in flowering time in p5cs1 mutants, but significant flowering delay in p5cs2 mutants. It is hypothesized that the flowering delay of the 35S-P5CS1 plants as reported by could be accounted for by the homology-based co-silencing of P5CS2 triggered by the expression of P5CS1. found that AtP5CS2 is a target of CONSTANS (CO), a transcriptional activator associated with flowering time. Besides, rolD oncogene from Agrobacterium rhizogenes is known to encode a functional ornithine cyclodeaminase enzyme in bacteria which ultimately converts ornithine to proline. The main trait induced by overexpression of rolD gene in tobacco is precocity in flower setting and a strong enhancement of the flowering potential in tobacco and tomato. These experiments thus point out that proline plays a vital role during flower transition, bolting, and in changing the architecture of inflorescence (coflorescence formation). However, we are not sure about the molecular events leading exactly how proline influences flowering time and changes the inflorescence architecture in higher plants when produced in optimum concentrations.

Proline Contribution to Plant Cell Wall Architecture in Root Development and Reproductive Organs

It is a fact that proline and Hyp are the major amino acid constituents of hydrolysates of cell wall proteins. As pointed out by, morphogenesis takes place in plants because of differential growth of organs at the cell wall. Therefore, studies on cell walls are vital though they are highly intricate and complex. Cell wall matrix encoding proteins are enriched with proline residues which are integrated in the form of HRGPs classified into three categories: (i) moderately glycosylated EXTs; (ii) hyperglycosylated arabinogalactanproteins (AGPs); and (iii) Hyp/proline (Pro)-Rich proteins (H/PRPs).

Role of Extensins in Cell Wall Modification During Root and Pollen Development

The extracellular matrices of plants and animals contain structural glycoproteins which are important scaffolding components. Some of these glycoproteins like collagens in animals and HRGPs of plants share functions like enhancing tensile strength and contributing tissue integrity. In all the three subgroups, proline, and Hyp residues are abundant and play an important role in cell wall development. EXTs are self-assembling amphiphiles. They are modular in nature and contain Hyp and are usually characterized by pentameric Ser-Hyp peptide repeats. EXTs exhibit 35–65% glycosylation on Ser-(Hyp)n ≥ 2 motifs and the side chains contain oligosaccharides of arabinose and galactose. The genome of A. thaliana encodes 63 putative EXTs with high amino acid sequence similarity between them. Out of the 63 members, some are classical, while others are EXT-like chimeras and hybrid EXTs. It is not clear whether they have redundant or specific functions to carry in different cell types of various plant tissues. EXTs exhibit repetitive nature of their sequences with many post-transcriptional modifications in plant genomes like signal peptide processing in the ER, hydroxylation of proline to Hyp residues by P4H, O-glycosylation on Hyp and Ser residues with chains of up to four linear Ara residues on each Hyp by arabinosyltransferases, and cross-linking of glycosylated EXTs at the tyrosine residues in the cell wall forming intra- and inter- EXT linkages. This helps EXTs to form a three-dimensional structure of protein and to interact with pectins in the cell walls. The coordination of EXTs with other components and their functions during cell wall architecture and plant development are not completely known. This is mostly because of their modular nature, existence in large numbers, hydroxylation by different P4Hs, complex structure, and redundant expression of these proteins in the same plant tissues (Genevestigator database, http://www.genevestigator.com). EXTs can also interact with pectins and serve as templates for cell wall deposition. Recently, found an ARABINOXYLAN PECTIN ARABINOGALACTAN PROTEIN1 (APAP1) in A. thaliana which consists of pectin and arabinoxylan that are covalently linked to an AGP. They suggested a role for APAP1 proteoglycan in plant cell wall architecture and function. However, the exact coordinated control of EXTs and pectin interaction during cell wall formation is unclear.

Several groups have used root hair as a model to study the functions of EXTs. Mutants lacking the synthesis of wall polymer in the root hair are impaired in growth. Since posttranslational modifications of HRGPs are carried out by (P4Hs), this defines the subsequent O-glycosylation sites in EXTs (mostly arabinosylated) and polarized growth in root hairs. O-glycans enhance the HRGP solubility and resistance to proteolytic degradation. proved that O-glycosylation on EXTs is essential for cell-wall assembly and root hair elongation. Root hairs develop by tip growth akin to pollen tubes, axons, and fungal hyphae. recently carried out genetic analysis related to the regulation of P4H. They proved that P4H5 and P4H2 and P4H13 are pivotal for root hair tip growth. The impact of deficient proline hydroxylation on the cell wall architecture has also been shown by them. Their results demonstrate that peptidyl-proline hydroxylation on EXTs is required for cell wall assembly and therefore root hair elongation in Arabidopsis. The above works point out that changes in the O-glycosylation status impact the functions of EXTs during cell wall assembly, cell shape, and expansion. Genes that encode P4Hs are also linked to hypoxia, and P4H proteins are regarded as oxygen sensors under hypoxic stress. found out that P4H genes are subjected to alternative splicing in roots of maize seedlings under waterlogging conditions. The diverse transcripts generated due to alternative splicing are expressed at different levels clearly indicate that ZmP4H genes are under specific control by post-transcriptional regulation under waterlogging stress in maize. identified that cell wall Hyp-rich glycoprotein ROOT-SHOOT-HYPOCOTYL-DEFECTIVE (RSH) is necessary for normal embryo development in Arabidopsis. further found out the role of HRGPs during somatic embryogenesis of Musa sp. Their results suggest that HRGPs play a vital role in regeneration and germination of embryos during early plant development via somatic embryogenesis (Table 1). Proper localization and appropriate quantities of HRGPs seem to be critical for the formation and regeneration of somatic embryos. But, the exact mechanism by which HRGPs trigger somatic embryogenesis in callus or suspension cultures is not known. Thus, the functions proline-rich and Hyp-rich glycoproteins appear to be complex, but clearly associated with developmental regulation in different plant systems. Using protein blots and immunohistochemistry, EXTs have been found to be abundantly expressed in vivo for pollen tubes and transmitting tissues. When inhibitors of HRGP were used, decreased pollen tube growth and stylar length were recorded. It appears that HRGPs especially EXTs play a critical role in the pollen tube and style cell growth. demonstrated that EXTs are involved in pollen recognition and fertilization. These evidences along with the works of,,, and infer that cross-linked EXTs play pivotal roles during cell expansion and growth of pollen tube.

Arabinogalactan Protein Involvement in Vegetative and Reproductive Growth

Arabinogalactan proteins are Hyp-rich extracellular proteins with a high proportion of sugars (up to 90%). Among them, arabinose and galactose are predominant residues, but minor sugars like rhamnose, fucose, glucuronic, acid, and xylose are common. AGPs are characterized by extensive glycosylation with arabinose, galactose or both and analogous to animal proteoglycans. AGPs possess repetitive Alanine (Ala) or Serine (Ser) motifs that interact with Hyp molecules. They are chemically stable, and resistant to proteolytic enzymes in their native state due to the presence of carbohydrates. AGPs contain glycosylphosphatidylinositols (GPIs) which tethers them to the plasma membranes in plants. The biosynthesis, structure, expressions, and functions of AGPs have been well studied and reviewed. pointed out that carbohydrate groups (D-galactose and L-arabinose) are mostly linked by O-glycosylation to the hydroxyl group of Ser and Hyp of the AGP backbone. However, diversity exists in the degree and pattern of O-glycosylation depending on the type and length of glycan chains attached to the proteins. Many studies suggest that AGPs play important roles in vegetative and reproductive growth. AGPs were observed throughout the plant kingdom, in leaves, stems, roots, floral parts, and seeds. They were found in plasma membranes, cell walls, intracellular multivesicular bodies, and also as secretions to intercellular spaces.

Some AGPs are also implicated with redundant architectural functions of cell walls. Several lines of evidence indicate that AGPs are associated with growth and differentiation in lower as well as in higher plants. For example, when inhibitors of AGP biosynthesis were used, the growth of leaf primordia was suppressed in a liverwort. Yariv reagent inhibited cell division in cell suspension cultures and roots in carrot and Arabidopsis, respectively,. This indicated that AGPs are involved in cellular growth and development. While certain AGPs promote somatic embryogenesis in Daucus carota,, and Picea abies, others inhibit it as noticed by in carrot.

AGPs were noticed in xylem, stylar transmitting tissues and cell suspension cultures. In targeting certain AGPs to the specific cell surface locations, the role of certain sequence determinants in the carbohydrate or protein need to be determined. Their multi-location (organs, tissues, and cell-types) occurrence indicates specific functions of AGPs in different tissues like flowers and other cell types. Many AGPs possess a C-terminal Ole e 1 domain (pollen allergens, named after a secreted protein isolated from Olea europeae pollen; ). Developmental and tissue specific expressions were noticed for several AGPs in different plants, consistent with the assumption that they play a role in plant development. Altered expression of AGP in pea plants has changed the sexual development as shown by. Some AGPs like stylar transmitting tissue-specific PRPs (TTS proteins) play vital roles in reproductive growth and development like pollen-pistil interactions. When the gene knockdown experiments were carried out, TTS proteins have been found important for pollen–pistil interactions. This may be possible for TTS proteins which act as cell surface adhesives. AGPs are also implicated in cellular signaling events. They are the important components in plant exudates and gums, as shown in the case of gum arabic extracted from Acacia senegal and used as an additive in the food industry. Type II arabinogalactans have also been found to stimulate animal immune systems and thus may be useful in medicine as well. Further, chimeric proteins containing AGP domains may interact with polysaccharides. In this connection, the experiments of have proved that CELLULOSE SYNTHASE5 (CESA5) and the SALT-OVERLY SENSITIVE5 (SOS5), a Fasciclin-AGP are required for mucilage adherence in seeds of A. thaliana. They conclude that SOS5 mediates adherence through pectin. AGPs are involved in cell–cell/intercellular communications involved in tracheary element differentiation and thus AGPs are found to be associated with the differentiation of xylem and programmed cell death. Thus, AGPs perform several functions in different aspects of plant growth and development, though the underlying molecular mechanisms are not clearly known.

Pursuit of Hyp/Pro-Rich Proteins (H/PRPs) in Plant Development

Hyp/Pro-rich proteins belong to the HRGP superfamily like that of EXTs and AGPs. Based on repetitive motifs and domain organization, PRP proteins are classified into three subtypes; (a) repetitive PRPs, (b) non-repetitive PRPs, and (c) multi-domain hybrid PRPs. Proline residues in PRPs are hydroxylated and form Hyps which are then glycosylated as mentioned earlier. But, O-glycosylation of H/PRPs and their interactions with polysaccharides is not completely known. Twelve H/PRP proteins have been identified so far in Arabidopsis thaliana, carrot, cotton, tobacco, common bean, capsicum, and petunia., and pointed out that H/PRPs may be cross-linked in cell walls, but evidence is lacking for such an assumption.

Pro-rich proteins are involved in cell elongation, abscission and senescence. As shown in Table 1, HRGPs are essential for the structure and function of cell wall as well as plasma membrane-cytoskeleton continuum. It is highly interesting to note that the PRP genes show developmental stage-, organ-, tissue-, and even cell-specific expressions., ) reported the characterization of three developmentally regulated proline-rich cell wall protein genes from Glycine max. Marked differences were observed in the pattern of expression of PRPs in different organs like hypocotyls, roots, stems, immature embryos, immature seed coats and developing seeds and in cells that are undergoing lignifications. characterized and expressed four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins. Their studies support a model for the involvement of PRPs in specifying cell-type specific wall structures, and provide the basis for a genetic approach to dissect the function of PRPs during growth and development. While S. bicolor PRP1 (SbPRP1) mRNA is abundant in elongating regions of hypocotyl epidermal cells, SbPRP2 mRNA is more expressed in phloem cells. Further, it has been found that SbPRP3 mRNA is localized in the endodermoid layer of cells in the hypocotyl elongating region. demonstrated that expression of AtPRP3, a proline-rich structural cell wall protein is regulated by cell-type-specific developmental pathways involved in root hair (single cells that develop by tip growth and are specialized in absorption of nutrients) formation. They noticed enhanced expression of AtPRP3/β-glucuronidase (GUS) in roots of transgenic seedlings treated with 1-aminocyclopropane-1-carboxylic acid (ACC) or α-naphthaleneacetic acid, two compounds known to promote root hair formation. The results indicate that AtPRP3 is regulated by developmental pathways involved in root hair formation. Overexpression of GhPRP5 in A. thaliana resulted in smaller cell size, but knock-down of GhPRP5 expression by RNA interference in cotton increased the fiber length. Their data suggest that this protein participates in modulating fiber development of cotton.

Involvement of PRPs as Signaling Proteins in Reproductive Tissues

Pro-rich proteins perform a whole spectrum of functions like providing structural integrity to mediate cell–cell integrations and communications. They are also involved and play a vital role in wall assembly and remodeling during cell growth and development. characterized several profilin isoforms from maize pollen and showed that their function depends on interaction with proline-rich motifs. They found out that profilin isoforms expressed in a single cell can have different effects on actin in living cells and the poly-L-proline binding function of profilin may have important consequences for the regulation of actin cytoskeletal dynamics. Two stylar transmitting tissue specific PRPs (TTS-1 and TTS-2) have also been reported in tobacco. TTS-1 and TTS-2 mRNAs have been induced in floral buds, during the later stages of flower development especially when style elongation is rapid and are active at anthesis. The occurrence of PRPs in transmitting tissues has been predicted to play a vital role in maintaining the structural integrity of the style. Transgenic Arabidopsis overexpressing Atext1 displayed altered inflorescence and affected stem thickening and height. However, the functions of all PRPs are not completely known during different developmental stages, thus leaving a gap in our understanding of PRPs.

Role of PRPs in Cell Wall Modification under Stress

Genes that encode PRPs and the localization of these proteins in plant cell walls have been studied. During growth, differentiation and also during different environmental stress conditions, cells may expand up to 200 times their original length. Water stress could result in alterations in cell volume and shape, as well need to deal with loss of turgor. Therefore, cell walls must possess tensile strength to withstand the turgor pressures. This involves very large chemical and biochemical modifications of cell wall constituents including cell wall proteins representing 1 to 2% of the genome in plants such as Arabidopsis. Cell wall protein transcripts are also affected under salt, drought, and temperature stress conditions. PRPs are insolubilized in the cell walls with the involvement of H2O2-mediated oxidative cross linking and it precedes the expression of transcription-dependent defences. Though cell wall bound PRPs may play a role in the structural integrity of plant cells, participate in defence related activities, and plant cell surface interactions as pointed out by,, interestingly, the mRNA levels of PRPs increase in response to water scarcity in higher plants.

characterized two proline-rich glycoproteins of 33 and 36 kDa (p33 and p36) which are found in the cell wall soluble fraction of common bean (Phaseolus vulgaris). They observed the highest accumulation of these proteins in growing regions, predominantly in phloem tissues in response to drought indicating that cell wall modifications are induced in actively growing cells of common bean. reported a flower specific PRP from rice (OsPRP3) that is expressed during the late stages of flower development. While AtPRP3 is associated with root hair formation, overexpression of Oryza sativa PRP3 (OsPRP3) showed an increase in cold tolerance compared to the wild-type plants. They showed that this OsPRP3 enhances cell wall integrity in the cold tolerant plants. Knockout mutants displayed defects in floral organogenesis suggesting a role for PRPs in reproductive tissues. reported ABA-induced expression of a family of four genes, REPETETIVE PROLINE-RICH PROTEIN (RePRP) in rice. These genes encode proline-rich glycoproteins with highly repetitive PX1PX2 motifs, RePRP1, and RePRP2. Their work also revealed that ABA treatment increases RePRP expression and that these proteins are localized to the plasma membrane. It has been found that knockdown of the expression of RePRP1 and RePRP2 decreases the sensitivity of roots to ABA. Thus, these experiments reveal that RePRP proteins play an essential role in ABA/stress regulation of root growth and development. It has also been noticed that rice RePRPs interact with arabinogalactan polysaccharide in a dosage-dependent manner. recently identified a PRP called SICKLE (SIC) in Arabidopsis. This protein is critical for not only development in Arabidopsis but also in imparting abiotic stress tolerance. The loss-of-function sic-1 mutants displayed reduction in plant height, delay in flowering, and abnormal inflorescence phyllotaxy. These mutants accumulated reduced levels of a subset of miRNAs and transacting siRNAs but enhanced levels of primary miRNAs than the controls. The sic-1 mutant plants are also sensitive to cold and salt stresses. Therefore, it appears that SIC is a PRP associated with the biogenesis of some miRNAs and degradation of some spliced introns and is vital for plant development.

Hybrid Proline-Rich Proteins (HyPRPs) are Crucial Players in Cell Elongation

Out of the three subclasses of PRPs, one of them contains several copies of POVEKPOVXK motif, while the other two subclasses show a hybrid structure and are called hybrid proline-rich proteins (HyPRPs). Plant HyPRPs represent putative cell wall proteins consisting of a repetitive proline-rich N-terminal domains and a conserved C-terminal domain. They are unique to seed plants and analysis of the families from different plant species suggests rapid diversification of their sequences and expression patterns. Their functions are not clearly known, but their occurrence indicates that they may be involved in basic cellular processes. To understand the functions of HyPRPs, modulated the expression of three HyPRP genes in tobacco and potato. Transgenic plants displayed cell elongation, and enhanced size of calli. HyPRPs contain two regions, and one of them is rich in proline and the other in cystein residues. Further, it has been shown that the third sub-class, namely NHyPRPs displays high percentage of proline residues organized in repetitive sequence motifs in C-terminus region. Thus, it appears that HyPRPs are important players in plant cell elongation, though the molecular mechanism is not yet elucidated.

Proline-Rich Extensin-Like Receptor Kinases (PERKs)

A family of receptor kinase-like proteins has been discovered that are involved in cell wall signaling. In A. thaliana, 11 members of the PERK family have been discovered which share some features of EXTs. Altered expression of PERK receptor kinases resulted in changes of plant growth and floral organ formation. In a novel work, it has been elucidated by that the gene PERK4 (coding for a protein kinase located in the plasma membrane) is required for the ABA-dependent influx of Ca2+ and normal ABA sensitivity in seeds and roots of A thaliana. Their experiments suggest that PERK4 is associated in ABA perception and also might interact with wall polymers. Thus, PRPs are implicated in cell wall signal transduction cascades. Further work is necessary since it is not yet clear about how many PERK proteins are associated with this process and also their additional roles if any during growth and stress tolerance.

Proline Deficiency Affects the Biosynthesis of Cell Wall Matrix Proteins

The experiments conducted by demonstrated initially in tobacco that HRGPs are critical for cell morphology and osmotic stability. Strong evidence has come later from who created Arabidopsis plants with antisense P5CS. Interestingly, the transgenics displayed morphological defects in leaves and elongation of inflorescences. Further, they observed that protein biosynthesis was normal in proline deficient plants, but structural proteins localized in the cell walls were strikingly altered indicating a direct evidence for a key role of proline in cell walls. Specifically, proline and Hyp contents were reduced in the cell wall preparations of Arabidopsis transgenic leaves. They pointed out that PRPs and HRGPs are responsible for morphological abnormalities observed in the leaves of antisense Arabidopsis plants since these proteins provide mechanical support for cells under stressed conditions. Such a role in cell morphology and the mechanical support for the PRPs and HRGPs also has been demonstrated by and. Thus, proline-related growth abnormalities are correlated well with the effects of proline on plant cell wall development. found out that proline deficiency causes downregulation of cyclin genes and affects general protein synthesis. However, they did not find out its effect on the cell wall proteins. It would be interesting to find out if there would be any changes that take place in H/PRPs associated with cell wall development. Several overexpressions and knockout mutations of plants containing PRPs and HRGPs are needed to demonstrate the exact role(s) of these proteins during cell wall synthesis and growth.

Proline Transporters Play an Important Role in Plant Development Including Xylogenesis

Proline transporters have been isolated from several species and three from Arabidopsis (AtProTs) so far. Transcript levels of Arabidopsis ProT2, mangrove ProT homologues, barley HvProT as well as proline levels are elevated under salt stress. Like in bacteria, proline transporters also act as glycinebetaine transporters in plants but with different affinities. Further, they also transport other compatible solutes like γ-aminobutyric acid (GABA) in plants. Though intracellular localization, substrate selectivity, and affinity of the three AtProTs are similar, they exhibited differential expression patterns in various plant organs indicating differential transport of these molecules. By fusing transporter genes with GUS, they demonstrated that AtProT1, AtProT2, and AtProT3 are localized in lignified tissues like phloem of all organs, epidermis, and cortex of roots and in epidermis of leaves respectively,. ProT1 isolated from tomato has shown to be expressed specifically in pollen grains. Further, clearly showed a relation between uneven distribution of proline in the lower epidermis and rest of the leaf with the expression levels of AtProT3. In spite of the fact, that single, double, and triple knockout mutants of the AtProT1, AtProT2, and AtProT3 genes responsible for proline transport in plants have been isolated and characterized, these mutants did not reveal any differences when compared to wild type plants. This underlays the complex situation and therefore needs further elucidation. The functions of these transporters might be highly redundant and possibly complemented by other transporters, since transporters mediating proline uptake across the plasma membrane have also been noticed in the amino acid transporter (ATF) or amino acid/auxin permease (AAAP) and in the amino acid-polyamine-choline (APC) families. Along with glutamate, amino acid permease (AAP) family mediates proton coupled uptake of neutral amino acids such as proline. isolated AAP11 from Populus trichocarpa and overexpressed it in poplar and yeast. PtAAP11 was highly expressed in differentiating xylem cells in different organs. Further, functional characterization revealed that it is a high affinity amino ATF, more particularly for proline. Therefore, the authors suggested that PtAAP11 may play an important role in xylogenesis by providing proline which is required for xylem cell wall proteins in poplar. Lysine-histidine transporter (LHT) family transports neutral and acidic amino acids including proline. Contrary to the AAP and LHT families, ProTs transport proline and other compatible solutes like GABA but not other proteogenic amino acids. The fact that both low and high affinity-proline transporters exist in plants implicate that they play a role in general transfer of nitrogen and also proline for its specific functions in different cells and tissues. Selective transport of proline by ProTs and also their expression analysis during drought/salt stresses or in pollen grains suggests that they play a vital role in proline homeostasis both under stress and non-stress conditions. The list of proline/betaine transporters and transport mutants known from different plants is shown in Table 2. In summary, proline transporters (AAPs) play an important role in plant development by providing proline as a source of nitrogen and energy which is required for lignifications, xylem differentiation and cell wall modification during plant development (as a component of plant cell wall proteins). But the exact mechanisms how proline can mediate these functions are not known.

Mutations in p5cs2 and p5cr Cause Embryo Lethality and Affect Seed Development

The amount of free proline and its metabolism modulates transition to flowering, pollen, and embryo development. Several studies found that immature/mature seeds of Vicia faba and Arabidopsis accumulate proline before ripening. In support of it, concomitant expression of genes encoding enzymes of proline metabolism was observed in seeds. It was noticed that P5CS2 is expressed mostly in actively dividing meristematic cells, developing tissues, callus, and cell suspension cultures. p5cs2 mutations cause embryo abortion during late stages of seed development though both P5CS mRNAs are detectable throughout embryonic development under warmer climate. Their experiments indicated exogenous proline can rescue p5cs2 mutants by ex vivo cultivation of developing seeds, but the mutant plants undergo aberrant development and become sterile. It has also been reported that homozygous p5cs2 mutant plants died before the onset of flowering. Therefore, specific role of P5CS2 in reproductive development could not be analyzed. When Arabidopsis plants were simultaneously silenced or co-suppressed with P5CS1 and P5CS2 genes, they resulted in retarded growth, delayed flowering and reduced apical dominance. The above results indicate that Arabidopsis P5CS1 is insufficient for compensation of developmental defects caused by knockout of P5CS2. Expression of P5CS2-GFP was observed in leaf primordia, where the levels of P5CS1-GFP levels are very low. P5CS2-GFP also displayed cell-type specific subcellular localization pattern compared to P5CS1-GFP in root tips, leaves, flower organs, and embryonic cells. Taken together, the data demonstrate that these two genes have non-redundant functions in plants. In A. thaliana, did not observe developmental defects in single mutants devoid of P5CS1 gene. p5cs1/p5cs2 double mutants displayed pollen sterility, while egg cells are fertile. Thus, these results emphasize the role(s) of P5CS in pollen fertility. p5cs2 T-DNA insertion lines have been described as embryo lethal or conditionally embryo lethal. It has been found that P5CS2 is not essential for sexual reproduction. They obtained homozygous p5cs2 mutants that are viable and could produce fertile seeds by in vitro culture of immature mutant seeds on MS medium supplemented with 60 mM sucrose and 2 mM proline. This allowed generating homozygous plants that are phenotypically normal, but showed reduced growth compared to the wild type plants. Under short day and low-light conditions, these plants produced viable seeds. pointed out that embryo lethality in heterozygous atp5cs2 plants might be due to premature desiccation of homozygous embryos that develop more slowly than heterozygous embryos. In a contrast to p5cs1/p5cs2 double mutants, normal pollen fertility was observed in the absence of a functional P5CR gene indicating that P5CR is not needed for pollen fertility. These results implicate that P5CS1/P5CS2 genes are crucial for pollen fertility, but not P5CR. It has been found that p5cr mutations cause embryonic lethality, however. Disruption of P5CR gene using T-DNA insertions resulted in embryo defective mutation emb2722 in Arabidopsis. They reported arrest of the embryo development after the second division of the embryo proper in p5cr mutants. All attempts to rescue putative homozygous p5cr mutant embryos in vitro by proline feeding failed. Their efforts to promote embryo development of homozygous seeds in siliques of heterozygous parents in situ by feeding the proline exogenously or induction of internal proline accumulation through salt stress were not fruitful. Thus, activities of both P5CS and P5CR enzymes have been found essential for sexual reproduction in plants.

Conclusion

Proline not only participates in protein synthesis, but regulates several important functions like osmotic adjustment and protection of proteins during stress conditions. Its multifarious functions are always enigmatic in plants. However, it is increasingly becoming evident that proline modulates a wide-array of functions like regulation of cyclin genes at the transcriptional level, cell wall elongation and modifications, xylogenesis, stem elongation, root, and shoot growth, inflorescence architecture, embryo formation/seed development, and seed germination during the life cycle of a plant. Deficiency in proline biosynthesis leads to abnormal plants and cell wall defects, thus implicating its role in structural proteins. But, clear evidence is lacking for attributing several specific functions to this amino acid. We do not know yet how the genes like P5CS1, P5CS2, P5CR, OAT, PDH, and P5CDH interact with other genes and we still do not have an interactome map of the network of genes. Unless such maps are available along with their experimental validation, we cannot pinpoint the exact metabolic functions of proline other than its role in primary metabolism in protein biosynthesis.

Author Contributions

All the authors of the manuscript meet the essential criteria of the publication. All authors have read and approved the manuscript.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References 221

  1. 1.

    Alm J. Ohnmeiss T. E. Lanza J. Vriesenga L. (1990 ). Preference of cabbage white butterflies and honey bees for nectar that contains amino acids. Oecologia 84 53–57.

    Not in our library10.1007/bf00665594

  2. 2.

    Armengaud P. Thiery L. Buhot N. March G. Savoure A. (2004 ). Transcriptional regulation of proline biosynthesis in Medicago truncatula reveals developmental and environmental specific features. Physiol. Plant. 120 442–450.

    Not in our library10.1111/j.0031-9317.2004.00251.x

  3. 3.

    Bai L. Zhang G. Zhou Y. Zhang Z. Wang W. Du Y. (2009 ). Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca signaling, is required for abscisic acid responses in Arabidopsis thaliana. Plant J. 60 314–327.

    Not in our library10.1111/j.1365-313x.2009.03956.x

  4. 4.

    Basile D. V. Basile M. R. (1993 ). The role and control of the place-dependent suppression of cell division in plant morphogenesis and phylogeny. Mem. Torrey Botanical. Club 25 63–68.

    Not in our library

  5. 5.

    Battaglia M. Solorzano R. M. Hernandez M. Ortiz S. C. Gomez B. G. Marquez J. (2007 ). Proline-rich cell wall proteins accumulate in growing regions and phloem tissue in response to water deficit in common bean seedlings. Planta 225 1121–1133.

    Not in our library10.1007/s00425-006-0423-9

  6. 6.

    Bernhardt C. Tierney M. L. (2000 ). Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiol. 122 705–714.

    Not in our library10.1104/pp.122.3.705

  7. 7.

    Besse I. Buchanan B. B. (1997 ). Thioredoxin-linked plant and animal processes: the new generation. Bot. Bull. Acad. Sin. 38 1–11.

    Not in our library10.1046/j.1469-8137.1997.00784.x

  8. 8.

    Bettini P. Michelotti S. Bindi D. Giannini R. Capuana M. Buiatti M. (2003 ). Pleiotropic effect of the insertion of the Agrobacterium rhizogenes rolD gene in tomato (Lycopersicon esculentum Mill). Theore. Appl. Genet. 107 831–836.

    Not in our library10.1007/s00122-003-1322-0

  9. 9.

    Bo Z. Xiao-Ping Z. Zhang-Cheng Z. (2000 ). Studies on pollen free proline content and seed yield of Gordonia acuminata in different communities. Acta Phytoecol. Sin. 24 617–620.

    Not in our library

  10. 10.

    Bosch M. Sommer-Knudsen J. Derksen J. Mariani C. (2001 ). Class III pistil-specific extensin-like proteins from tobacco have characteristics of arabinogalactan proteins. Am. Soc. Plant Phys. 125 2180–2188.

    Not in our library10.1104/pp.125.4.2180

  11. 11.

    Botha F. C. Potgieter G. P. Botha A. M. (1992 ). Respiratory metabolism and gene expression during seed germination. Plant Growth Regul. 11 211–224.

    Not in our library10.1007/bf00024560

  12. 12.

    Bradley D. J. Kjellbom P. Lamb C. J. (1992 ). Elicitor-induced and wound induced oxidative cross-linking of a proline rich plant cell wall protein: a novel, rapid defense response. Cell 70 21–30.

    Not in our library10.1016/0092-8674(92)90530-p

  13. 13.

    Buttery R. G. Ling L. C. Juliano B. O. (1982 ). 2-Acetyl-1-pyrroline: an important aroma component of cooked rice. Chem. Industry (London) 12 958–959.

    Not in our library

  14. 14.

    Cannon M. C. Terneus K. Hall Q. Tan L. Wang Y. Wegenhart B. L. (2008 ). Self-assembly of the plant cell wall requires an extensin scaffold. Proc. Natl. Acad. Sci. U.S.A. 105 2226–2231.

    Not in our library10.1073/pnas.0711980105

  15. 15.

    Carter C. Shafir S. Yehonatan L. Palmer R. G. Thornburg R. (2006 ). A novel role for proline in plant floral nectars. Naturwissenschaften 93 72–79.

    Not in our library10.1007/s00114-005-0062-1

  16. 16.

    Cassab G. I. (1998 ). Plant cell wall proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 281–309.

    Not in our library10.1146/annurev.arplant.49.1.281

  17. 17.

    Cassab G. I. Varner J. E. (1988 ). Cell wall proteins. Ann. Rev. Plant Physiol. Plant Mol. Biol. 39 321–353.

    Not in our library10.1146/annurev.pp.39.060188.001541

  18. 18.

    Castonguay Y. Laberge S. Nadeau P. Vezina L. P. (1994 ). A cold induced gene from Medicago sativa encodes a bimodular protein similar to developmentally regulated protein. Plant Mol. Biol. 24 799–804.

    Not in our library10.1007/bf00029861

  19. 19.

    Chen C. G. Pu Z. Y. Moritz R. L. Simpson R. J. Bacic A. Clarke A. E. (1994 ). Molecular cloning of a gene encoding an arabinogalactan-protein from pear (Pyrus communis) cell suspension culture. Proc. Natl. Acad. Sci. U.S.A. 91 10305–10309.

    Not in our library10.1073/pnas.91.22.10305

  20. 20.

    Chen L. Bush D. R. (1997 ). LHT1, a lysine- and histidinespecific amino acid transporter in Arabidopsis. Plant Physiol. 115 1127–1134.

    Not in our library10.1104/pp.115.3.1127

  21. 21.

    Chen S. Yang Y. Shi W. Ji Q. He F. Zhang Z. (2008 ). Badh2, encoding betaine aldehyde aldehyde dehydrogenase, inhibits the biosynthesis of 2-acetyl-1-pyrroline, a major component in rice fragrance. Plant Cell 20 1850–1861.

    Not in our library10.1105/tpc.108.058917

  22. 22.

    Cheung A. Y. May B. Kawata E. E. Gu Q. Wu H.-M. (1993 ). Characterization of cDNAs for stylar transmitting tissue-specific proline-rich proteins in tobacco. Plant J. 3 151–160.

    Not in our library10.1046/j.1365-313x.1993.t01-7-00999.x

  23. 23.

    Chiang H. H. Dandekar A. M. (1995 ). Regulation of proline accumulation in Arabidopsis thaliana (L.) Heynh during development and in response to desiccation. Plant Cell Environ. 18 1280–1290.

    Not in our library10.1111/j.1365-3040.1995.tb00187.x

  24. 24.

    Clarke A. Gleeson P. Harrison S. Knox R. B. (1979 ). Pollen-stigma interactions: identification and characterization of surface components with recognition potential (cell surface receptors/plant glycoproteins/adhesion/concanavalin A/tridacnin). Proc. Natl. Acad. Sci. U.S.A. 76 3358–3362.

    Not in our library10.1073/pnas.76.7.3358

  25. 25.

    Clements R. L. Leland H. V. (1962 ). An ion-exchange study of the free amino acids in the juices of six varieties of citrus. J. Food Sci. 27 20–25.

    Not in our library10.1111/j.1365-2621.1962.tb00051.x

  26. 26.

    Coleman C. E. Lopes M. A. Gillikin J. W. Boston R. S. Larkins B. A. (1995 ). A defective signal peptide in the maize high lysine mutant floury 2. Proc. Natl. Acad. Sci. U.S.A. 92 6828–6831.

    Not in our library10.1073/pnas.92.15.6828

  27. 27.

    Colmenero-Flores J. M. Campos F. Garciarrubio A. Covarrubias A. A. (1997 ). Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit: identification of a novel late embryogenesis abundant-like protein. Plant Mol. Biol. 35 393–405.

    Not in our library10.1023/a:1005802505731

  28. 28.

    Cooper J. B. Heuser J. E. Varner J. E. (1994 ). 3,4-dehydroproline inhibits cell wall assembly and cell division in tobacco protoplasts. Plant Physiol. 104 747–752.

    Not in our library10.1104/pp.104.2.747

  29. 29.

    Couturier J. Fay E. D. Fitz M. Wipf D. Blaudez D. Chalot M. (2010 ). PtAAP11, a high affinity amino acid transporter specifically expressed in differentiating xylem cells of poplar. J. Exp. Bot. 61 1671–1682.

    Not in our library10.1093/jxb/erq036

  30. 30.

    Covarrubias A. A. Ayala J. W. Reyes J. L. Hernandez M. Garciarrubio A. (1995 ). Cell-wall proteins induced by water deficit in bean (Phaseolus vulgaris L.) seedlings. Plant Physiol. 107 1119–1128.

    Not in our library10.1104/pp.107.4.1119

  31. 31.

    Creelman R. A. Mullet J. E. (1991 ). Water deficit modulates gene expression in growing zones of soybean seedlings. Analysis of differentially expressed cDNAs, a new β-tubulin gene, and expression of genes encoding cell wall proteins. Plant Mol. Biol. 17 591–608.

    Not in our library10.1007/bf00037046

  32. 32.

    Delauney A. J. Hu C. A. A. Kishor P. B. K. Verma D. P. S. (1993 ). Cloning of ornithine δ-aminotransferase cDNA from Vigna aconitifolia by trans-complementation in Escherichia coli and regulation of proline biosynthesis. J. Biol. Chem. 268 18673–18678.

    Not in our library

  33. 33.

    Delauney A. J. Verma D. P. S. (1990 ). A soybean Δ1-pyrroline-5-carboxylate reductase gene was isolated by functional complementation in Escherichia coli and is found to be osmoregulated. Mol. Gen. Genet. 221 299–305.

    Not in our library10.1007/bf00259392

  34. 34.

    Delauney A. J. Verma D. P. S. (1993 ). Proline biosynthesis and osmoregulation in plants. Plant J. 4 215–223.

    Not in our library10.1046/j.1365-313x.1993.04020215.x

  35. 35.

    Deuschle K. Funck D. Forlani G. Stransky H. Biehl A. Leister D. (2004 ). The role of Δ1-pyrroline-5-carboxylate dehydrogenase in proline degradation. Plant Cell 16 3413–3425.

    Not in our library10.1105/tpc.104.023622

  36. 36.

    Deuschle K. Funck D. Hellman H. Daschner K. Binder S. Frommer W. B. (2001 ). A nuclear gene encoding mitochondrial Δ1-pyrroline-5-carboxylate dehydrrogenase and its potential role in protection from proline toxicity. Plant J. 27 345–356.

    Not in our library10.1046/j.1365-313x.2001.01101.x

  37. 37.

    Deutch C. E. Winicov I. (1995 ). Post-transcriptional regulation of a salt-inducible alfalfa gene encoding a putative chimeric proline-rich cell wall protein. Plant Mol. Biol. 27 411–418.

    Not in our library10.1007/bf00020194

  38. 38.

    Dick-Perez M. Zhang Y. Hayes J. Salazar A. Zabotina O. A. Hong M. (2011 ). Structure and interactions of plant cell-wall polysaccharides by two and three-dimensional magic-angle-spinning solid-state NMR. Biochemistry 50 989–1000.

    Not in our library10.1021/bi101795q

  39. 39.

    Diet A. Link B. Seifert G. J. Schellenberg B. Wagner U. Pauly M. (2006 ). The Arabidopsis root hair cell wall formation mutant lrx1 is suppressed by mutations in the RHM1 gene encoding a UDP-L-rhamnose synthase. Plant Cell 18 1630–1641.

    Not in our library10.1105/tpc.105.038653

  40. 40.

    Ding L. Zhu J.-K. (1997 ). A role for arabinogalactan-proteins in root epidermal cell expansion. Planta 203 289–294.

    Not in our library10.1007/s004250050194

  41. 41.

    Doblin M. S. Pettolino F. Bacic A. (2010 ). Plant cell walls: the skeleton of the plant world. Funct. Plant Biol. 37 357–381.

    Not in our library10.1071/fp09279

  42. 42.

    Dvorakova L. Cvrckova F. Fischer L. (2007 ). Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genomics 8:412

    Not in our library10.1186/1471-2164-8-412

  43. 43.

    Dvorakova L. Srba M. Opatrny Z. Fischer L. (2012 ). Hybrid proline-rich proteins: novel players in plant cell elongation? Ann. Bot. 109 453–462.

    Not in our library10.1093/aob/mcr278

  44. 44.

    Egertsdotter U. von Arnold S. (1995 ). Importance of arabinogalactan proteins for the development of somatic embryos of Norway spruce (Picea abies). Physiol. Plant. 93 334–345.

    Not in our library10.1111/j.1399-3054.1995.tb02237.x

  45. 45.

    Ellis M. Egelund J. Schultz C. J. Bacic A. (2010 ). Arabinogalactanproteins: key regulators at the cell surface? Plant Physiol. 153 403–419.

    Not in our library10.1104/pp.110.156000

  46. 46.

    Fincher G. B. Stone B. A. Clarke A. E. (1983 ). Arabinogalactan-proteins: structure, biosynthesis, and function. Ann. Rev. Plant Physiol. 34 47–70.

    Not in our library10.1146/annurev.pp.34.060183.000403

  47. 47.

    Fischer W. N. Andre B. Rentsch D. Krolkiewicz S. Tegedar M. Breitkreuz K. (1998 ). Amino acid transport in plants. Trends Plant Sci. 3 188–195.

    Not in our library10.1016/s1360-1385(98)01231-x

  48. 48.

    Fischer W. N. Kwart M. Hummel S. Frommer W. B. (1995 ). Substrate specificity and expression profile of amino acid transporters (AAPs) in Arabidopsis. J. Biol. Chem. 270 16315–16320.

    Not in our library10.1074/jbc.270.27.16315

  49. 49.

    Flasinski S. Rogozinska J. (1985 ). Effect of water deficit on proline accumulation, protein and chlorophyll content during flowering and seed formation in winter rape (Brassica napus L. var. oleifera). Acta Agrobot. 38 11–21.

    Not in our library

  50. 50.

    Foster J. Lee Y. H. Tegeder M. (2008 ). Distinct expression of members of the LHT amino acid transporter family in flowers indicates specific roles in plant reproduction. Sexual Plant Rep. 21 143–152.

    Not in our library10.1007/s00497-008-0074-z

  51. 51.

    Fowler T. J. Bernhardt C. Tierney M. L. (1999 ). Characterization and expression of four proline-rich cell wall protein genes in arabidopsis encoding two distinct subsets of multiple domain proteins. Plant Physiol. 121 1081–1091.

    Not in our library10.1104/pp.121.4.1081

  52. 52.

    Frommer W. B. Hummel S. Riesmeier J. W. (1993 ). Expression cloning in yeast of a cDNA encoding a broad specificity amino acid permease from Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 90 5944–5948.

    Not in our library10.1073/pnas.90.13.5944

  53. 53.

    Frommer W. B. Hummel S. Unseld M. Ninnemann O. (1995 ). Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 92 12036–12040.

    Not in our library10.1073/pnas.92.26.12036

  54. 54.

    Frueauf J. B. Dolata M. Leykam J. F. Lloyd E. Gonzales M. Vandenbosch K. (2000 ). Peptides isolated from cell walls of Medicago truncatula nodules and uninfected root. Phytochem. 55 429–438.

    Not in our library10.1016/s0031-9422(00)00336-8

  55. 55.

    Fujita T. Maggio A. Garcia-Rios M. Bressan R. A. Csonka L. N. (1998 ). Comparative analysis of the regulation of expression and structures of two evolutionarily divergent genes for Δ1-pyrroline-5-carboxylate synthetase. Plant Physiol. 118 661–674.

    Not in our library10.1104/pp.118.2.661

  56. 56.

    Fujiwara T. Mitsuya S. Miyake H. Hattori T. Takabe T. (2010 ). Characterization of novel glycinebetaine/proline transporter gene expressed in the mestome sheath and lateral root cap cells in barley. Planta 232 133–143.

    Not in our library10.1007/s00425-010-1155-4

  57. 57.

    Funck D. Eckard S. Muller G. (2010 ). Non-redundant functions of two proline dehydrogenase isoforms in Arabidopsis. BMC Plant Biol. 10:70

    Not in our library10.1186/1471-2229-10-70

  58. 58.
    Ornithine-δ-aminotransferase is essential for Arginine Catabolism but not for Proline Biosynthesis · 2008
    No notice
  59. 59.

    Funck D. Winter G. Baumgarten L. Forlani G. (2012 ). Requirement of proline synthesis during Arabidopsis reproductive development. BMC Plant Biol. 12:191

    Not in our library10.1186/1471-2229-12-191

  60. 60.

    Gao M. Showalter A. M. (2000 ). Immunolocalization of LeAGP-1, a modular arabinogalactan-protein, reveals its developmentally regulated expression in tomato. Planta 210 865–874.

    Not in our library10.1007/s004250050691

  61. 61.

    Gavazzi G. Nava-Racchi M. Tonelli C. (1975 ). A mutation causing proline requirement in Zea mays. Theor. Appl. Genet. 46 339–345.

    Not in our library10.1007/bf00281675

  62. 62.

    Ghanti K. K. S. Sujata K. G. Kumar B. M. V. Karba N. N. Reddy K. J. Rao M. S. (2011 ). Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biol. Plant. 55 634–640.

    Not in our library10.1007/s10535-011-0161-0

  63. 63.

    Gibbon B. C. Zonia L. E. Kovar D. R. Hussey P. J. Staiger C. J. (1998 ). Pollen profiling function depends on interaction with proline-rich motifs. Plant Cell 10 981–993.

    Not in our library10.1105/tpc.10.6.981

  64. 64.

    Gothandam K. M. Nalini E. Karthikeyan S. Shin J. S. (2010 ). OsPRP3, a flower specific proline-rich protein of rice, determines extracellular matrix structure of floral organs and its overexpression confers cold-tolerance. Plant Mol. Biol. 72 125–135.

    Not in our library10.1007/s11103-009-9557-z

  65. 65.

    Grallath S. Weimar T. Meyer A. Gumy C. Suter-Grotemeyer M. Neuhaus J. (2005 ). The AtProT family. Compatible solute transporters with similar substrate specificity but differential expression patterns. Plant Physiol. 137 117–126.

    Not in our library10.1104/pp.104.055079

  66. 66.

    Griffiths J. S. Tsai A. Y. Xue H. Voiniciuc C. Šola K. Seifert G. J. (2014 ). SALT-OVERLY SENSITIVE5 mediates Arabidopsis seed coat mucilage adherence and organization through pectins. Plant Physiol. 165 991–1004.

    Not in our library10.1104/pp.114.239400

  67. 67.

    Haffani Y. Z. Silva-Gagliardi N. F. Sewter S. K. Grace Aldea M. Zhao Z. Nakhamchik A. (2006 ). Altered expression of PERK receptor kinases in Arabidopsis leads to changes in growth and floral organ formation. Plant Signal. Behav. 1 251–260.

    Not in our library10.4161/psb.1.5.3324

  68. 68.

    Hall Q. Cannon M. (2002 ). The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell 14 1161–1172.

    Not in our library10.1105/tpc.010477

  69. 69.

    Hancock C. N. Kent L. McClure B. A. (2005 ). The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J. 43 716–723.

    Not in our library10.1111/j.1365-313x.2005.02490.x

  70. 70.

    Hare P. D. Cress W. (1997 ). Metabolic implications of stress induced proline accumulation in plants. Plant Growth Reg. 21 79–102.

    Not in our library10.1023/a:1005703923347

  71. 71.

    Hare P. D. Cress W. A. Van Staden J. (1999 ). Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J. Exp. Bot. 50 413–434.

    Not in our library10.1093/jxb/50.333.413

  72. 72.

    Hare P. D. Cress W. A. Van Staden J. (2003 ). A regulatory role for proline metabolism in stimulating Arabidopsis thaliana seed germination. Plant Growth Reg. 39 41–50.

    Not in our library10.1023/a:1021835902351

  73. 73.

    Hayashi F. Ichino T. Osanai M. Wada K. (2000 ). Oscillation and regulation of proline content by P5CS and ProDH gene expressions in the light/dark cycles in Arabidopsis thaliana. Plant Cell Physiol. 41 1096–1101.

    Not in our library10.1093/pcp/pcd036

  74. 74.

    Held M. A. Tan L. Kamyab A. Hare M. Shpak E. Kieliszewksi M. J. (2004 ). Di-isodityrosine is the intermolecular cross-link of isodityrosine-rich extensin analogs cross-linked in vitro. J. Biol. Chem. 279 55474–55482.

    Not in our library10.1074/jbc.m408396200

  75. 75.

    Henrissat B. Coutinho P. M. Davies G. J. (2001 ). A census of carbohydrate-active enzymes in the genome of Arabidopsis thaliana. Plant Mol. Biol. 47 55–72.

    Not in our library10.1023/a:1010667012056

  76. 76.

    Hibino T. Meng Y. L. Kawamitsu Y. Uehara N. Matsuda N. Tanaka Y. (2001 ). Molecular cloning and functional characterization of two kinds of betaine-aldehyde dehydrogenase in betaine-accumulating mangrove Avicennia marina (Forsk.) Vierh. Plant Mol. Biol. 45 353–363.

    Not in our library10.1023/a:1006497113323

  77. 77.

    Hijazi M. Roujol D. Nguyen-Kim H. Del Rocio Cisneros Castillo L. Saland E. Jamet E. (2014 ). Arabinogalactan protein 31 (AGP31), a putative network-forming protein in Arabidopsis thaliana cell walls? Ann. Bot. 114 1087–1097.

    Not in our library10.1093/aob/mcu038

  78. 78.

    Hirner B. Fischer W. N. Rentsch D. Kwart M. Fommer W. B. (1998 ). Developmental control of H+/amino acid permease gene expression during seed development of Arabidopsis. Plant J. 14 535–544.

    Not in our library10.1046/j.1365-313x.1998.00151.x

  79. 79.

    Holding D. R. Meeley R. B. Hazebroek J. Selinger D. Gruis F. Jung R. (2010 ). Identification and characterization of the maize arogenate dehydrogenase gene family. J. Exp. Bot. 61 3663–3673.

    Not in our library10.1093/jxb/erq179

  80. 80.

    Hong J. C. Nagao R. T. Key J. L. (1987 ). Characterization and sequence analysis of a developmentally regulated putative cell wall protein gene isolated from soybean. J. Biol. Chem. 262 8367–8376.

    Not in our library

  81. 81.

    Hong J. C. Nagao R. T. Key J. L. (1989 ). Developmentally regulated expression of soybean proline-rich cell wall protein genes. Plant Cell 1 937–943.

    Not in our library10.1105/tpc.1.9.937

  82. 82.

    Hong J. C. Nagao R. T. Key J. L. (1990 ). Characterization of a proline-rich cell wall protein gene family of soybean. A comparative analysis. J. Biol. Chem. 265 2470–2475.

    Not in our library

  83. 83.

    Hu C. A. A. Delauney A. J. Verma D. P. S. (1992 ). A bifunctional enzyme (Δ1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc. Natl. Acad. Sci. U.S.A. 89 9354–9358.

    Not in our library10.1073/pnas.89.19.9354

  84. 84.

    Hur J. Jung K. H. Lee C. H. An G. (2004 ). Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Sci. 167 417–426.

    Not in our library10.1016/j.plantsci.2004.04.009

  85. 85.

    Igarashi Y. Yoshiba Y. Takeshita T. Nomura S. Otomo J. Yamaguchi-Shinozaki K. (2000 ). Molecular cloning and characterization of a cDNA encoding proline transporter in rice. Plant Cell Physiol. 41 750–756.

    Not in our library10.1093/pcp/41.6.750

  86. 86.

    Ito M. Kodama H. Komamine A. Watanabe A. (1998 ). Expression of extensin genes is dependent on the stage of the cell cycle and cell proliferation in suspension-cultured Catharanthus roseus cells. Plant Mol. Biol. 36 343–351.

    Not in our library10.1023/a:1005913818129

  87. 87.

    Jackson P. A. Galinha C. I. Pereira C. S. Fortunato A. Soares N. C. Amancio S. B. (2001 ). Rapid deposition of extensin during the elicitation of grapevine callus cultures is specifically catalyzed by a 40-kilodalton peroxidase. Plant Physiol. 127 1065–1076.

    Not in our library10.1104/pp.010192

  88. 88.

    Jose-Estanyol M. Puigdomenech P. (2000 ). Plant cell wall glycoproteins and their genes. Plant Physiol. Biochem. 38 97–108.

    Not in our library10.1016/s0981-9428(00)00165-0

  89. 89.

    Jose-Estanyol M. Ruiz-Avila L. Puigdomenench P. (1992 ). A maize embryo-specific gene encodes a proline-rich and hydrophobic protein. Plant Cell 4 413–423.

    Not in our library10.1105/tpc.4.4.413

  90. 90.

    Kaplan D. R. Hagemann W. (1991 ). The relationship of cell and organism in vascular plants. Bioscience 41 693–703.

    Not in our library10.2307/1311764

  91. 91.

    Kieliszewski M. J. Lamport D. T. A. (1994 ). Extensin: repetitive motifs, functional sites, post-translation codes and phylogeny. Plant J. 5 157–172.

    Not in our library10.1046/j.1365-313x.1994.05020157.x

  92. 92.

    Kieliszewski M. J. Leykam J. F. Lamport D. T. (1989 ). Trypsin cleaves lysylproline in a hydroxyproline-rich glycoprotein from Zea mays. Pept. Res. 2 246–248.

    Not in our library

  93. 93.

    Kieliszewski M. J. Shpak E. (2001 ). Synthetic genes for the elucidation of glycosylation codes for arabinogalactan-proteins and other hydroxyproline-rich glycoproteins. Cell Mol. Life Sci. 58 1386–1398.

    Not in our library10.1007/pl00000783

  94. 94.

    Kim C. S. Gibbon B. C. Gillikin J. W. Larkins B. A. Boston R. S. Jung R. (2006 ). The maize mucronate mutation is a deletion in the 16-kDa gamma-zein gene that induces the unfolded protein response. Plant J. 48 440–451.

    Not in our library10.1111/j.1365-313x.2006.02884.x

  95. 95.

    Kishor P. B. K. Hong Z. Miao G. H. Hu C. A. A. Verma D. P. S. (1995 ). Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiol. 108 1387–1394.

    Not in our library10.1104/pp.108.4.1387

  96. 96.

    Kishor P. B. K. Sangam S. Amrutha R. N. Laxmi P. S. Naidu K. R. Rao K. R. S. S. (2005 ). Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: Its implications in plant growth and abiotic stress tolerance. Curr. Sci. 88 424–438.

    Not in our library

  97. 97.

    Kishor P. B. K. Sreenivasulu N. (2014 ). Is proline accumulation per se correlated with stress tolerance or is proline homoeostasis a more critical issue? Plant Cell Environ. 37 300–311.

    Not in our library10.1111/pce.12157

  98. 98.

    Kiyosue T. Yoshiba Y. Yamaguchi-Shinozaki K. Shinozaki K. (1996 ). A nuclear gene encoding mitochondrial proline dehydogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. Plant Cell 8 1323–1335.

    Not in our library10.1105/tpc.8.8.1323

  99. 99.

    Knoch E. Dilokpimol A. Geshi N. (2014 ). Arabinogalactan proteins: focus on carbohydrate active enzymes. Front. Plant Sci. 5:198

    Not in our library10.3389/fpls.2014.00198

  100. 100.

    Kreuger M. van Holst G. (1993 ). Arabinogalactan proteins are essential in somatic embryogenesis of Daucus carota L. Planta 189 243–248.

    Not in our library10.1007/bf00195083

  101. 101.

    Kwart M. Hirner B. Hummel S. Frommer W. B. (1993 ). Differential expression of two related amino-acid transporters with differing substrate specificity in Arabidopsis thaliana. Plant J. 4 993–1002.

    Not in our library10.1046/j.1365-313x.1993.04060993.x

  102. 102.

    Lamport D. T. A. (1967 ). Hydroxyproline-O-glycosidic linkage of the plant cell wall glycoprotein extensin. Nature 216 1322–1324.

    Not in our library10.1038/2161322a0

  103. 103.

    Lamport D. T. A. (1977 ). “Structure, biosynthesis and signifi cance of cell wall glycoproteins,” in Recent Advances in Phytochemistry, 11th Edn, eds Loewus F. A. Runeckles V. C. (New York: Plenum Press), 79–115.

    Not in our library

  104. 104.

    Lamport D. T. A. Kieliszewski M. J. Chen Y. Cannon M. C. (2011 ). Role of the extensin superfamily in primary cell wall architecture. Plant Physiol. 156 11–19.

    Not in our library10.1104/pp.110.169011

  105. 105.

    Lamport D. T. A. Kieliszewski M. J. Showalter A. M. (2006 ). Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol. 169 479–492.

    Not in our library10.1111/j.1469-8137.2005.01591.x

  106. 106.

    Lamport D. T. A. Várnai P. (2013 ). Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol. 197 58–64.

    Not in our library10.1111/nph.12005

  107. 107.

    Lee J. A. Pallas D. C. (2007 ). Leucine carboxyl methyltransferase-1 is necessary for normal progression through mitosis in mammalian cells. J. Biol. Chem. 282 30974–30984.

    Not in our library10.1074/jbc.m704861200

  108. 108.

    Lee Y. H. Tegeder M. (2004 ). Selective expression of a novel high-affinity transport system for acidic and neutral amino acids in the tapetum cells of Arabidopsis flowers. Plant J. 40 60–74.

    Not in our library10.1111/j.1365-313x.2004.02186.x

  109. 109.

    Lehmann S. Funck D. Szabados L. Rentsch D. (2010 ). Proline metabolism and transport in plant development. Amino Acids 39 949–962.

    Not in our library10.1007/s00726-010-0525-3

  110. 110.

    Lehmann S. Gumy C. Blatter E. Boeffel S. Fricke W. Rentsch D. (2011 ). In planta function of compatible solute transporters of the AtProT family. J. Exp. Bot. 62 787–796.

    Not in our library10.1093/jxb/erq320

  111. 111.

    LeRudulier D. Strom A. R. Dandekar A. M. Smith L. T. Valentaine R. C. (1984 ). Molecular biology of osmoregulation. Science 224 1064–1068.

    Not in our library10.1126/science.224.4653.1064

  112. 112.

    Lord E. M. Sanders L. C. (1992 ). Roles for the extracellular matrix in plant development and pollination: a special case of cell movement in plants. Dev. Biol. 153 16–28.

    Not in our library10.1016/0012-1606(92)90088-x

  113. 113.

    Ma Y. Nelson O. E. (1975 ). Amino acid composition and storage proteins in two new high-lysine mutants of maize. Cereal Chem. 52 412–419.

    Not in our library

  114. 114.

    MacArthur M. W. Thornton J. M. (1991 ). Influence of proline residues on protein conformation. J. Mol. Biol. 218 397–412.

    Not in our library10.1016/0022-2836(91)90721-h

  115. 115.

    Mattioli R. Costantino P. Trovato M. (2009a ). Proline accumulation in plants-Not only stress. Plant Sig. Behav. 4 1016–1018.

    Not in our library10.4161/psb.4.11.9797

  116. 116.

    Mattioli R. Falascb G. Sabatini S. Altamura M. M. Costantino P. Trovato M. (2009b ). The proline biosynthetic genes P5CS1 and P5CS2 play overlapping roles in Arabidopsis flower transition but not in embryo development. Physiol. Plant. 137 72–85.

    Not in our library10.1111/j.1399-3054.2009.01261.x

  117. 117.

    Mattioli R. Marchese D. D’Angeli S. Altamura M. M. Costantino P. Trovato M. (2008 ). Modulation of intracellular proline levels affects flowering time and inflorescence architecture in Arabidopsis. Plant Mol. Biol. 66 277–288.

    Not in our library10.1007/s11103-007-9269-1

  118. 118.

    Mauro M. L Trovato M. De Paolis A. Gallelli A. Costantino P. Altamura M. M. (1996 ). The plant oncogene rolD stimulates flowering in transgenic tobacco plants. Dev. Biol. 180 693–700.

    Not in our library10.1006/dbio.1996.0338

  119. 119.

    Mayer U. Jurgens G. (2004 ). Cytokinesis: lines of division taking shape. Curr. Opin. Plant Biol. 7 599–604.

    Not in our library10.1016/j.pbi.2004.07.008

  120. 120.

    McCann M. C. Bush M. Milioni D. Sado P. Stacey N. J. Catchpole G. (2001 ). Approaches to understanding the functional architecture of the plant cell wall. Phytochemistry 57 811–821.

    Not in our library10.1016/s0031-9422(01)00144-3

  121. 121.

    Meinke D. Muralla R. Sweeney C. Dickerman A. (2008 ). Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci. 13 483–491.

    Not in our library10.1016/j.tplants.2008.06.003

  122. 122.

    Menke U. Renault N. Mueller-Roeber B. (2000 ). StGCPRP, a potato gene strongly expressed in stomatal guard cells, defines a novel type of repetitive proline-rich proteins. Plant Physiol. 122 677–686.

    Not in our library10.1104/pp.122.3.677

  123. 123.

    Merkouropoulos G. Shirsat A. H. (2003 ). The unusual Arabidopsis extensin gene Atext1 is expressed throughout plant development and is induced by a variety of biotic and abiotic stresses. Planta 217 356–366.

    Not in our library10.1007/s00425-003-1002-y

  124. 124.

    Motose H. Sugiyama M. Fukuda H. (2001 ). An arabinogalactan protein(s) is a key component of a fraction that mediates local intercellular communication involved in tracheary element differentiation of Zinnia mesophyll cells. Plant Cell Physiol. 42 129–137.

    Not in our library10.1093/pcp/pce014

  125. 125.

    Munoz F. J. Dopico B. Labrador E. (1998 ). A cDNA encoding a proline-rich protein from Cicer arietinum. Changes in expression during development and abiotic stress. Physiol. Plant. 102 582–590.

    Not in our library10.1034/j.1399-3054.1998.1020413.x

  126. 126.

    Nanjo T. Kobayashi M. Yoshiba Y. Sanada Y. Wada K. Tsukaya H. (1999 ). Biological functions of proline in morphogenesis and osmotolerance revealed in antisense transgenic Arabidopsis thaliana. Plant J. 18 185–193.

    Not in our library10.1046/j.1365-313x.1999.00438.x

  127. 127.

    Nguema-Ona E. Vicré-Gibouin M. Cannesan M. A. Driouich A. (2013 ). Arabinogalactan proteins in root-microbe interactions. Trends Plant Sci. 18 440–449.

    Not in our library10.1016/j.tplants.2013.03.006

  128. 128.

    Nothnagel E. A. (1997 ). Proteoglycans and related components in plant cells. Inter. Rev. Cytol. 174 195–291.

    Not in our library10.1016/s0074-7696(08)62118-x

  129. 129.

    Nunez A. Fishman M. L. Fortis L. L. Cooke P. H. Hotchkiss A. T. J. (2009 ). Identification of extensin protein associated with sugar beet pectin. J. Agric. Food Chem. 57 10951–10958.

    Not in our library10.1021/jf902162t

  130. 130.

    Ober E. S. Sharp R. E. (1994 ). Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. (I Requirement for increased levels of abscisic acid). Plant Physiol. 105 981–987.

    Not in our library10.1104/pp.105.3.981

  131. 131.

    Ogawa-Ohnishi M. Matsushita W. Matsubayashi Y. (2013 ). Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat. Chem. Biol. 9 726–730.

    Not in our library10.1038/nchembio.1351

  132. 132.

    Okumoto S. Koch W. Tegeder M. Fischer W. N. Biehl A. Leister D. (2004 ). Root phloem-specific expression of the plasma membrane amino acid proton co-transporter AAP3. J. Exp. Bot. 55 2155–2168.

    Not in our library10.1093/jxb/erh233

  133. 133.

    Okumoto S. Schmidt R. Tegeder M. Fischer W. N. Rentsch D. Frommer W. B. (2002 ). High affinity amino acid transporters specifically expressed in xylem parenchyma and developing seeds of Arabidopsis. J. Biol. Chem. 277 45338–45346.

    Not in our library10.1074/jbc.m207730200

  134. 134.

    Park S. Szumlanski A. L. Gu F. Guo F. Nielsen E. (2011 ). A role for CSLD3 during cell-wall synthesis in apical plasma membranes of tip-growing root-hair cells. Nat. Cell Biol. 13 973–980.

    Not in our library10.1038/ncb2294

  135. 135.

    Pennell R. I. Janniche L. Kjellbom P. Scofield G. N. Peart J. M. Roberts K. (1991 ). Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 3 1317–1326.

    Not in our library10.1105/tpc.3.12.1317

  136. 136.

    Pennell R. I. Roberts K. (1990 ). Sexual development in the pea is presaged by altered expression of arabinogalactan protein. Nature 344 547–549.

    Not in our library10.1038/344547a0

  137. 137.

    Pope D. G. (1977 ). Relationships between hydroxyproline-containing proteins secreted into the cell wall and medium by suspension- cultured Acer pseudoplatanus cells. Plant Physiol. 59 894–900.

    Not in our library10.1104/pp.59.5.894

  138. 138.

    Price N. J. Pinheiro C. Soares C. M. Ashford D. A. Ricardo C. P. Jackson P. A. (2003 ). A biochemical and molecular characterization of LEP1, an extensin peroxidase from lupin. J. Biol. Chem. 278 41389–41399.

    Not in our library10.1074/jbc.m304519200

  139. 139.

    Racchi M. L. Gavazzi G. Monti D. Manitto P. (1978 ). An analysis of the nutritional requirements of thepromutants in Zea mays. Plant Sci. Lett. 13 357–364.

    Not in our library10.1016/0304-4211(78)90213-4

  140. 140.

    Raymond M. J. Smirnoff N. (2002 ). Proline metabolism and transport in maize seedlings at low water potential. Ann. Bot. 89 813–823.

    Not in our library10.1093/aob/mcf082

  141. 141.

    Reddy P. S. Jogeswar G. Rasineni G. K. Maheswari M. Reddy A. R. Varshney R. K. (2015 ). Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol. Biochem. 94 104–113.

    Not in our library10.1016/j.plaphy.2015.05.014

  142. 142.

    Rentsch D. Hirner B. Schmelzer E. Frommer W. B. (1996 ). Salt-stress induced proline transporters and salt-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. Plant Cell 8 1437–1446.

    Not in our library10.1105/tpc.8.8.1437

  143. 143.

    Rentsch D. Schmidt S. Tegeder M. (2007 ). Transporters for uptake and allocation of organic nitrogen compounds in plants. FEBS Lett. 581 2281–2289.

    Not in our library10.1016/j.febslet.2007.04.013

  144. 144.

    Rhee S. Y. Osborne E. Poindexter P. D. Somerville C. R. (2003 ). Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol. 133 1170–1180.

    Not in our library10.1104/pp.103.028266

  145. 145.

    Rhodes D. Handa S. Bressan R. A. (1986 ). Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol. 82 890–903.

    Not in our library10.1104/pp.82.4.890

  146. 146.

    Ringli C. (2010 ). The hydroxyproline-rich glycoprotein domain of the Arabidopsis LRX1 requires Tyr for function but not for insolubilization in the cell wall. Plant J. 63 662–669.

    Not in our library10.1111/j.1365-313x.2010.04270.x

  147. 147.

    Roberts K. (1989 ). The plant extracellular matrix. Cur. Opin. Cell Biol. 1 1020–1027.

    Not in our library10.1016/0955-0674(89)90074-4

  148. 148.

    Roberts K. Shirsat A. H. (2006 ). Increased extension levels in Arabidopsis affect inflorescence stem thickening and height. J. Exp. Bot. 57 537–545.

    Not in our library10.1093/jxb/erj036

  149. 149.

    Romanczyk L. J. Jr. McClelland C. A. Post L. S. Aitken W. M. (1995 ). Formation of 2-acetyl-1-pyrroline by several Bacillus cereus strains isolated from cocoa fermentation boxes. J. Agric. Food Chem. 43 469–475.

    Not in our library10.1021/jf00050a040

  150. 150.

    Samach A. Onouchi H. Gold S. E. Ditta G. S. Schwarz-Sommer Z. Yanofsky M. F. (2000 ). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288 1613–1616.

    Not in our library10.1126/science.288.5471.1613

  151. 151.

    Sauer N. Tanner W. (1985 ). Selection and characterization of Chlorella mutants deficient in amino acid transport. Plant Physiol. 79 760–764.

    Not in our library10.1104/pp.79.3.760

  152. 152.

    Savoure A. Jaoua S. Hua X. Ardiles W. Montagu M. V. Verbruggen N. (1995 ). Isolation, characterization, and chromosomal location of a gene encoding the Δ1-pyrroline-5-carboxylate synthetase in Arabidopsis thaliana. FEBS Lett. 372 13–19.

    Not in our library10.1016/0014-5793(95)00935-3

  153. 153.

    Schindler T. Bergfeld R. Schopfer P. (1995 ). Arabinogalactan proteins in maize coleoptiles: developmental relationship to cell death during xylem differentiation but not to extension growth. Plant J. 5 157–172.

    Not in our library10.1046/j.1365-313x.1995.07010025.x

  154. 154.

    Schmidt R. J. Burr F. A. Burr B. (1987 ). Transposon tagging and molecular analysis of the maize regulatory locus opaque-2. Science 238 960–963.

    Not in our library10.1126/science.2823388

  155. 155.

    Schmidt R. Stransky H. Koch W. (2007 ). The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226 805–813.

    Not in our library10.1007/s00425-007-0527-x

  156. 156.

    Schultz C. J. Ferguson K. L. Lahnstein J. Bacic A. (2004 ). Post-translational modifications of arabinogalactan-peptides of Arabidopsis thaliana: endoplasmic reticulum and glycosylphosphatidylinositol-anchor signal cleavage sites and hydroxylation of proline. J. Biol. Chem. 279 45503–45511.

    Not in our library10.1074/jbc.m407594200

  157. 157.

    Schultz C. Gilson P. Oxley D. Youl J. Bacic A. (1998 ). GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci. 3 426–431.

    Not in our library10.1016/s1360-1385(98)01328-4

  158. 158.

    Schwacke R. Grallath S. Breitkreuz K. E. Stransky H. Frommer W. B. Rentsch D. (1999 ). LeProT1, a transporter for proline, glycine betaine and γ-aminobutyric acid in tomato pollen. Plant Cell 11 377–391.

    Not in our library10.1105/tpc.11.3.377

  159. 159.

    Serpe M. D. Nothnagel E. A. (1999 ). Arabinogalactan-proteins in the multiple domains of the plant cell surface. Adv. Bot. Res. 30 207–289.

    Not in our library10.1016/s0065-2296(08)60229-3

  160. 160.

    Sharma S. Shinde S. Verslues P. E. (2013 ). Functional characterization of an ornithine cyclodeaminase-like protein of Arabidopsis thaliana. BMC Plant Biol. 13:182

    Not in our library10.1186/1471-2229-13-182

  161. 161.

    Sharma S. Verslues P. E. (2010 ). Mechanisms independent of abscisic acid (ABA) or proline feedback have a predominant role in transcriptional regulation of proline metabolism during low water potential and stress recovery. Plant Cell Environ. 33 1838–1851.

    Not in our library10.1111/j.1365-3040.2010.02188.x

  162. 162.

    Shen Y. G. Zhang W. K. Yan D. Q. Du B. X. Zhang J. S. Chen S. Y. (2002 ). Overexpression of proline transporter gene isolated from halophyte confers salt tolerance in Arabidopsis. Acta Bot. Sin. 44 956–962.

    Not in our library

  163. 163.

    Shetty K. (2004 ). Role of proline-linked pentose phosphate pathway in biosynthesis of plant phenolics for functional food and environmental applications: a review. Process Biochem. 39 789–803.

    Not in our library10.1016/s0032-9592(03)00088-8

  164. 164.

    Shirsat A. H. Wieczorek D. Kozbial P. (1996 ). A gene for Brassica napus extensin is differentially expressed on wounding. Plant Mol. Biol. 30 1291–1300.

    Not in our library10.1007/bf00019559

  165. 165.

    Showalter A. M. (1993 ). Structure and function of plant cell wall proteins. Plant Cell 5 9–23.

    Not in our library10.1105/tpc.5.1.9

  166. 166.

    Showalter A. M. (2001 ). Arabinogalactan-proteins: structure, expression, and function. Cell. Mol. Life Sci. 58 1399–1417.

    Not in our library10.1007/pl00000784

  167. 167.

    Showalter A. M. Keppler B. Lichtenberg J. Gu D. Welch L. R. (2010 ). A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol. 153 485–513.

    Not in our library10.1104/pp.110.156554

  168. 168.

    Showalter A. M. Varner J. E. (1989 ). “Plant hydroxyproline-rich glycoproteins,” in The Biochemistry of Plants, ed. Abraham M. (New York: Academic Press), 485–520.

    Not in our library

  169. 169.

    Shpak E. Barbar E. Leykam J. F. Kieliszewski M. J. (2001 ). Contiguous hydroxyproline residues direct hydroxyproline arabinosylation in Nicotiana tabacum. J. Biol. Chem. 276 11272–11278.

    Not in our library10.1074/jbc.m011323200

  170. 170.

    Somerville C. Bauer S. Brininstool G. Facette M. Hamann T. Milne J. (2004 ). Toward a systems approach to understanding plant cell walls. Science 306 2206–2211.

    Not in our library10.1126/science.1102765

  171. 171.

    Spoljarevic M. Agic D. Lisjak M. Gumze A. Wilson I. D. Hancock J. T. (2011 ). The relationship of proline content and metabolism on the productivity of maize plants. Plant Sign. Behav. 6 251–257.

    Not in our library10.4161/psb.6.2.14336

  172. 172.
    Spatial distribution of transcript changes in the maize primary root elongation zone at low water potential · 2008
    Not checked
  173. 173.

    Stines A. P. Grubb J. Gockowiak H. Henschke P. A. Hoj P. B. van Heeswijck R. (2000 ). Proline and arginine accumulation in developing berries of Vitis vinifera L. in Australian vineyards: Influence of vine cultivar, berry maturity and tissue type. Aust. J. Grape Wine Res. 6 150–158.

    Not in our library10.1111/j.1755-0238.2000.tb00174.x

  174. 174.

    Strizhov N. Abraham E. Okresz L. Blickling S. Zilberstein A. Schell J. (1997 ). Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. Plant J. 12 557–569.

    Not in our library10.1111/j.0960-7412.1997.00557.x

  175. 175.

    Szabados L. Savoure A. (2010 ). Proline: a multifunctional amino acid. Trends Plant Sci. 15 89–97.

    Not in our library10.1016/j.tplants.2009.11.009

  176. 176.

    Szekely G. Abraham E. Cseplo A. Rigo G. Zsigmond L. Csiszar J. (2008 ). Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J. 53 11–28.

    Not in our library10.1111/j.1365-313x.2007.03318.x

  177. 177.

    Tan L. Eberhard S. Pattathil S. Warder C. Glushka J. Yuan C. (2013 ). An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell 25 270–287.

    Not in our library10.1105/tpc.112.107334

  178. 178.

    Tan L. Showalter A. M. Egelund J. Hernandez-Sanchez A. Doblin M. S. Bacic A. (2012 ). Arabinogalactan-proteins and the research challenges for these enigmatic plant cell surface proteoglycans. Front. Plant Sci. 3:140

    Not in our library10.3389/fpls.2012.00140

  179. 179.

    Tegeder M. Ward J. M. (2012 ). Molecular evolution of plant AAP and LHT amino acid transporters. Front Plant Sci. 3:21

    Not in our library10.3389/fpls.2012.00021

  180. 180.

    Thornburg R. W. (2007 ). “Molecular biology of the Nicotiana floral nectar,” in Nectaries and Nectar, eds Nicolson S. W. Nepi M. Pacini E. (Heidelberg: Springer-Verlag), 265–287.

    Not in our library

  181. 181.

    Toka I. Planchais S. Cabassa C. Justin A. M. De Vos D. Richard L. (2010 ). Mutations in the hyperosmotic stress-responsive mitochondrial BASIC AMINOACID CARRIER2 enhance proline accumulation in Arabidopsis. Plant Physiol. 152 1851–1862.

    Not in our library10.1104/pp.109.152371

  182. 182.

    Tonelli C. Gavazzi G. Manzocchi L. Di Fonzo N. Soave C. (1986 ). Opaque 6 allelic to pro1 mutant. Maize Newslett. 60 100.

    Not in our library

  183. 183.

    Tonelli C. Racchi M. L. Viani I. Gavazzi G. (1984 ). In vitro development of proline requiring mutant maize kernels. Atti. Assoc. Genet. Italy 30:231.

    Not in our library

  184. 184.

    Toonen M. A. J. Schmidt E. D. L. Van Kammen A. De Vries S. C. (1997 ). Promotive and inhibitory effects of diverse arabinogalactan proteins on Daucus carota L. somatic embryogenesis. Planta 203 188–195.

    Not in our library10.1007/s004250050181

  185. 185.

    Trovato M. Maras B. Linhares F. Costantino P. (2001 ). The plant oncogenic rolD encodes a functional ornithine cyclodeaminase. Proc. Nat. Acad. Sci. U.S.A. 98 13449–13453.

    Not in our library10.1073/pnas.231320398

  186. 186.

    Tseng I. C. Hong C. Y. Yu S. M. Ho T. H. (2013 ). Abscisic acid- and stress-induced highly proline-rich glycoproteins regulate root growth in rice. Plant Physiol. 163 118–134.

    Not in our library10.1104/pp.113.217547

  187. 187.

    Ueda A. Shi W. Sanmiya K. Shono M. Takabe T. (2001 ). Functional analysis of salt-inducible proline transporter of barley roots. Plant Cell Physiol. 42 1282–1289.

    Not in our library10.1093/pcp/pce166

  188. 188.

    Ueda A. Shi W. Shimada T. Miyake H. Takabe T. (2008 ). Altered expression of barley proline transporter causes different growth responses in Arabidopsis. Planta 227 277–286.

    Not in our library10.1007/s00425-007-0615-y

  189. 189.

    Varner J. E. Lin L. S. (1989 ). Plant cell wall architecture. Cell 56 231–239.

    Not in our library10.1016/0092-8674(89)90896-9

  190. 190.

    Velasquez S. M. Ricardi M. M. Dorosz J. G. Fernandez P. V. Nadra A. D. Pol-Fachin L. (2011 ). O-glycosylated cell wall proteins are essential in root hair growth. Science 332 1401–1403.

    Not in our library10.1126/science.1206657

  191. 191.

    Velasquez S. M. Ricardi M. M. Poulsen C. P. Oikawa A. Dilokpimol A. Halim A. (2015 ). Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. Mol. Plant 8 734–746.

    Not in our library10.1016/j.molp.2014.11.017

  192. 192.

    Velasquez S. M. Salgado Salter J. Petersen B. L. Estevez J. M. (2012 ). Recent advances on the post-translational modifications of EXTs and their roles in plant cell walls. Front. Plant Sci. 3:93

    Not in our library10.3389/fpls.2012.00093

  193. 193.

    Venekamp J. H. Koot J. T. M. (1984 ). The distribution of free amino acids, especially of proline, in the organs of field bean plants. Vicia faba L., during development in the field. J. Plant Physiol. 116 343–349.

    Not in our library10.1016/s0176-1617(84)80113-3

  194. 194.

    Verbruggen N. Hermans C. (2008 ). Proline accumulation in plants: a review. Amino Acids 35 753–759.

    Not in our library10.1007/s00726-008-0061-6

  195. 195.

    Verbruggen N. Villarroel R. Van Montagu M. (1993 ). Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis. Plant Physiol. 103 771–781.

    Not in our library10.1104/pp.103.3.771

  196. 196.

    Verslues P. E. Sharp R. E. (1999 ). Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone. Plant Physiol. 119 1349–1360.

    Not in our library10.1104/pp.119.4.1349

  197. 197.

    Vignols F. Jose-Estanyol M. Caparros-Ruiz D. Rigau J. Puigdomenech P. (1999 ). Involvement of a maize proline-rich protein in secondary cell wall formation as deduced from its specific mRNA localization. Plant Mol. Biol. 39 945–952.

    Not in our library10.1023/a:1006129703262

  198. 198.

    Villalba M. Batanero E. Monsalve R. I. Gonzalez M. A. Lahoz C. Rodriguez R. (1994 ). Cloning and expression of Ole e I, the major allergen from olive tree pollen. Polymorphism analysis and tissue specificity. J. Biol. Chem. 269 15217–15222.

    Not in our library

  199. 199.

    Voetberg G. S. Sharp R. E. (1991 ). Growth of maize primary root at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiol. 96 1125–1130.

    Not in our library10.1104/pp.96.4.1125

  200. 200.

    Waditee R. Hibino T. Tanaka Y. Nakamura T. Incharoensakdi A. Hayakawa S. (2002 ). Functional characterization of betaine/proline transporters in betaine-accumulating mangrove. J. Biol. Chem. 277 18378–18382.

    Not in our library10.1074/jbc.m112012200

  201. 201.

    Wakabayashi K. Hoson T. Kamisaka S. (1997 ). Changes in amounts and molecular mass distribution of cell-wall polysaccharides of wheat (Triticum aestivum L.) coleoptiles under water stress. J. Plant Physiol. 151 33–40.

    Not in our library10.1016/s0176-1617(97)80033-8

  202. 202.

    Wang G. Sun X. Wang G. Wang F. Gao Q. Sun X. (2011 ). Opaque7 encodes an acyl-activating enzyme-like protein that affects storage protein synthesis in maize endosperm. Genetics 189 1281–1295.

    Not in our library10.1534/genetics.111.133967

  203. 203.

    Wang G. Zhang J. Wang G. Fan X. Sun X. Qin H. (2014 ). Proline responding1 plays a critical role in regulating general protein synthesis and the cell cycle in maize. Plant Cell 26 2582–2600.

    Not in our library10.1105/tpc.114.125559

  204. 204.

    Wang Z. Y. He J. X. (2004 ). Brassinosteroid signal transduction - choices of signals and receptors. Trends Plant Sci. 9 91–96.

    Not in our library10.1016/j.tplants.2003.12.009

  205. 205.

    Willats W. G. T. Knox J. P. (1996 ). A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. Plant J. 9 919–925.

    Not in our library10.1046/j.1365-313x.1996.9060919.x

  206. 206.

    Wu H. de Graaf B. Mariani C. Cheung A. Y. (2001 ). Hydroxyproline-rich glycoproteins in plant reproductive tissues: structure, functions and regulation. Cell. Mol. Life Sci. 58 1418–1429.

    Not in our library10.1007/pl00000785

  207. 207.

    Wu H-M. Wong E. Ogdahl J. Cheung A. Y. (2000 ). A pollen tube growth-promoting arabinogalactan protein from Nicotiana alata is similar to the tobacco TTS protein. Plant J. 22 165–176.

    Not in our library10.1046/j.1365-313x.2000.00731.x

  208. 208.

    Wyatt R. E. Nagao R. T. Key J. L. (1992 ). Patterns of soybean proline-rich protein gene expression. Plant Cell. 4 99–110.

    Not in our library10.1105/tpc.4.1.99

  209. 209.

    Xu C. Takc T. Burbach C. Menzel D. Samaj J. (2011 ). Developmental localization and the role of hydroxyproline rich glycoproteins during somatic embryogenesis of banana (Musa spp. AAA). BMC Plant Biol. 11:38

    Not in our library10.1186/1471-2229-11-38

  210. 210.

    Xu W. L. Zhang D. J. Wu Y. F. Qin L. X. Huang G. Q. Li J. (2013 ). Cotton PRP5 gene encoding a proline-rich protein is involved in fiber development. Plant Mol. Biol. 82 353–365.

    Not in our library10.1007/s11103-013-0066-8

  211. 211.

    Xue X. Liu A. Hua X. (2009 ). Proline accumulation and transcriptional regulation of proline biosynthesis and degradation in Brassica napus. BMB Rep. 42 28–34.

    Not in our library10.5483/bmbrep.2009.42.1.028

  212. 212.

    Yamada H. Kiyohara H. (1999 ). “Complement-activating polysaccharides from medicinal herbs,” in Immunomodulatory Agents from Plants, ed. Wagner H. (Reinach: Birkhäuser Basel), 161–202.

    Not in our library10.1007/978-3-0348-8763-2_7

  213. 213.

    Yamada N. Promden W. Yamane K. Tamagake H. Hibino T. Tanaka Y. (2009 ). Preferential accumulation of betaine uncoupled to choline monooxygenase in young leaves of sugar beet-importance of long-distance translocation of betaine under normal and salt stressed conditions. J. Plant Physiol. 166 2058–2070.

    Not in our library10.1016/j.jplph.2011.03.007

  214. 214.

    Yamada N. Sakakibara S. Tsutsumi K. Waditee R. Tanaka Y. Takabe T. (2011 ). Expression and substrate specificity of betaine/proline transporters suggest a novel choline transport mechanism in sugar beet. J. Plant Physiol. 168 1609–1616.

    Not in our library10.1016/j.jplph.2011.03.007

  215. 215.

    Ye Z. H. Song Y. R. Marcus A. Varner J. E. (1991 ). Comparative localization of three classes of cell wall proteins. Plant J. 1 175–183.

    Not in our library10.1111/j.1365-313x.1991.00175.x

  216. 216.

    Ye Z. H. Varner J. E. (1991 ). Tissue-specific expression of cell wall proteins in developing soybean tissues. Plant Cell 3 23–37.

    Not in our library10.1105/tpc.3.1.23

  217. 217.

    Zhan X. Wang B. Li H. Liu R. Kalia R. K. Zhu J. K. (2012 ). Arabidopsis proline-rich protein important for development and abiotic stress tolerance is involved in microRNA biogenesis. Proc. Nat. Acad. Sci. U.S.A. 109 18198–18203.

    Not in our library10.1073/pnas.1216199109

  218. 218.

    Zhang H. Q. Croes A. Linskens H. (1982 ). Protein synthesis in germinating pollen of Petunia: role of proline. Planta 154 199–203.

    Not in our library10.1007/bf00387864

  219. 219.

    Zhang X. Ma H. Qi H. Zhao J. (2014 ). Roles of hydroxyproline-rich glycoproteins in the pollen tube and style cell growth of tobacco (Nicotiana tabacum L.). J. Plant Physiol. 171 1036–1045.

    Not in our library10.1016/j.jplph.2014.02.010

  220. 220.

    Zhao Z. D. Tan L. Showalter A. M. Lamport D. T. A. Kieliszewski M. J. (2002 ). Tomato LeAGP-1 arabinogalactan-protein purified from transgenic tobacco corroborates the Hyp contiguity hypothesis. Plant J. 31 431–444.

    Not in our library10.1046/j.1365-313x.2002.01365.x

  221. 221.

    Zou X. Jiang Y. Zheng Y. Zhang M. Zhang Z. (2011 ). Prolyl 4-hydroxylase genes are subjected to alternative splicing in roots of maize seedlings under waterlogging. Ann. Bot. 108 132–1335.

    Not in our library10.1093/aob/mcr223

Cited by papers we hold 4

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.