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Evolution and functional diversification of R2R3-MYB transcription factors in plants

Yun Wu, Jing Wen, Yiping Xia and 2 more

Horticulture Research · 2022 · CC BY

Abstract

R2R3-MYB genes (R2R3-MYBs) form one of the largest transcription factor gene families in the plant kingdom, with substantial structural and functional diversity. However, the evolutionary processes leading to this amazing functional diversity have not yet been clearly established. Recently developed genomic and classical molecular technologies have provided detailed insights into the evolutionary relationships and functions of plant R2R3-MYBs. Here, we review recent genome-level and functional analyses of plant R2R3-MYBs, with an emphasis on their evolution and functional diversification. In land plants, this gene family underwent a large expansion by whole genome duplications and small-scale duplications. Along with this population explosion, a series of functionally conserved or lineage-specific subfamilies/groups arose with roles in three major plant-specific biological processes: development and cell differentiation, specialized metabolism, and biotic and abiotic stresses. The rapid expansion and functional diversification of plant R2R3-MYBs are highly consistent with the increasing complexity of angiosperms. In particular, recently derived R2R3-MYBs with three highly homologous intron patterns (a, b, and c) are disproportionately related to specialized metabolism and have become the predominant subfamilies in land plant genomes. The evolution of plant R2R3-MYBs is an active area of research, and further studies are expected to improve our understanding of the evolution and functional diversification of this gene family.

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From PubMed Central, U.S. National Library of Medicine, as current on Oct 23, 2026. Paragraph numbers are ours, so an answer can point at one.

Introduction

1The V-myb avian myeloblastosis viral oncogene homolog (MYB) genes encode a group of pan-eukaryotic transcription factors (TFs) characterized by a highly conserved N-terminal DNA-binding domain repeat (R) plus a variable C-terminal regulatory region. MYB genes constitute the second largest TF superfamily in flowering plants, accounting for ~13% of the 1500 TFs in the model plant Arabidopsis thaliana. Conversely, only a few MYB genes are present in unikonts; for example, only three have been reported in the Homo sapiens genome, the human c-MYB proto-oncogene product (c-MYB) and two related vertebrate MYB factors. Each MYB repeat contains approximately 50 amino acid residues forming three α-helices and special DNA motifs, including MYB binding site I (MBSI), MBSII, or MBSIIG, with some exceptions. According to sequence similarity, MYB domain repeats are classified as R1, R2, or R3 type. Typically, plant MYB superfamily members include 1–4 imperfect MYB repeat(s) and are therefore subdivided into four families: 1R-MYB (consisting of one or two separated repeats), 2R-MYB (R2R3-MYB, consisting of two adjacent repeats), 3R-MYB (consisting of three adjacent repeats), and 4R-MYB (consisting of four adjacent repeats). The R2R3-MYB family has expanded substantially in the plant lineage and is the predominant family.

2Since the first plant R2R3-MYB gene, COLORED1 (C1), was identified in Zea mays and was demonstrated to be essential for anthocyanin biosynthesis in aleurone tissues, a tremendous number of R2R3-MYB genes (R2R3-MYBs) have been identified. In the past decade, based on substantial genome sequence data, the whole R2R3-MYB gene family has been comprehensively identified in numerous plant genomes (Supplemental Table 1), with counts ranging from dozens to hundreds, e.g. 126 genes in A. thaliana, 192 in Populus, 244 in soybean, and 406 in Gossypium hirsutum. A comparative phylogenetic analysis of R2R3-MYBs revealed considerable diversification and conservation of this gene family in plants. Concomitantly, the functions and characteristics of R2R3-MYB proteins have been studied extensively (Supplemental Table 2), including their roles in various plant-specific processes, such as responses to ambient stimuli, specialized metabolism, development, and cell differentiation. Given their important roles in plants, the separate biological processes regulated by R2R3-MYBs have recently been reviewed in detail elsewhere.

3A number of studies have shown that this gene family underwent a large expansion with functional diversification in land plants. This may have contributed to the origin and diversity of this kind of plant, as it conferred on them the ability to adapt from aquatic to terrestrial environments during evolution. To capture the most significant developments in this area, this review focuses on (a) the identification and classification of the R2R3-MYB gene family in plants, (b) the characterization of conserved and diverse functions in different species and biological processes, and (c) the use of comparative genomics to clarify the expansion and functional diversification of the R2R3-MYB family. Finally, we discuss new research directions to improve our understanding of R2R3-MYB evolution and functions.

Identification and classification of R2R3-MYBs

4Since its initial identification in 1982, the R2R3-MYB family has been an important area of research. In the past 20 years, an increasing number of sequenced plant genomes have enabled integrative genome-wide overviews of this gene family in the plant kingdom. To date, the R2R3-MYB gene family has been evaluated in about 74 plant species, ranging from aquatic plants (such as Mesostigma viride) to angiosperms (e.g. A. thaliana, Z. mays, Populus trichocarpa, Gossypium spp., and Solanum tuberosum) (Fig. 1 and Supplemental Table 1), and a pipeline for the automatic identification of MYBs has been created in order to make genome- or transcriptome-wide investigations more consistent. These studies have revealed that R2R3-MYBs are widely distributed in the plant kingdom, with a sharp increase in number from aquatic to angiosperm plants, forming one of the largest and most diverse TF gene families (ranging from one to hundreds of members) in land plants, especially angiosperms (Fig. 1).

5The R2R3-MYB gene family clearly underwent functional diversification to form different subfamilies/groups during evolution. Accordingly, there are many classification schemes for plant R2R3-MYBs, and the differences primarily reflect the existence of lineage- or species-specific “orphan” genes, differences in sampling coverage, and phylogenetic analysis methods. On the whole, three landmark classification systems have been developed and improved. First, the canonical classification and nomenclature of this gene family were initially established in A. thaliana and included 25 groups based on the MYB domain and the amino acid motifs in the C-terminal regions. Thereafter, many studies have applied this system with varying degrees of modification. Notably, in A. thaliana, around 30 of the 126 (~23.81%) R2R3-MYBs were not assigned to any subfamily/subgroup in this classification owing to the lack of different representative species and the limited gene number (generally only one per species), resulting in scattered studies with relatively small sample sizes. Second, we performed a systematic comparative analysis of 50 major eukaryotic lineages with a total of 1548 R2R3-MYBs. As expected, we not only confirmed the 25 well-defined subfamilies of the R2R3-MYB gene family in A. thaliana but also defined many new species- or lineage-specific subfamilies in major eukaryotic lineages that had previously been neglected. Ultimately, we classified the gene family into as many as 73 subfamilies supported by highly conserved gene structures and motif compositions. The validity of this classification was further supported by our recent study of Brassicaceae. In addition, a more systematic classification with a high resolution based on 87 species and 4312 sequences has recently been released, covering the major lineages of Archaeplastida. In that study, ten clades were designated as land plant R2R3-MYB subfamilies by applying a progressive phylogenetic analysis strategy aimed at eliminating the imbalance in resolution and species sampling. We speculated that there may be more subfamilies specific to individual species or lineages, as there are still many “orphan” genes in the phylogenetic analyses. Third, the genome sequences for Marchantia polymorpha and M. viride have enabled the development of a macroscopic classification regime, resulting in three clades of R2R3-MYBs that correspond to their biological functions. Each clade is correlated with different functions associated with essential developmental processes, from the basic life cycle to specialized metabolism and organismal complexity, corresponding to a very recent classification in 2020. In that study, genes encoding R2R3-MYBs from Rhodophytes, Glaucophytes, Chromista, Chlorophytes, Charophytes, and Embryophytes were divided into three major clades (I, II, and III) (named subgroups in the original paper). Subgroup I is the most ancient group and includes members from all plant lineages, whereas subgroup III has become predominant in land plants. The former two classification schemes share overlaps and are based on domain conservation, whereas this final classification system provides a macroscopic perspective based on broad evolutionary patterns.

6Notably, a uniform nomenclature within the classification of this gene family in plants is still lacking. Currently, there is almost no dispute at the family (R2R3-MYB) and superfamily (MYB) levels, except for a few studies that refer to R2R3-MYBs as a subfamily or subgroup. However, the nomenclature after R2R3-MYB is inconsistent, e.g. ~7% of studies refer to groups, ~31% refer to subfamilies, and ~54% refer to subgroups, with clade or cluster used occasionally. Subfamilies and subgroups are the most common subsequent appellations after family. Given that subfamily is used after the family level in many other TF gene families, e.g. basic helix–loop–helix proteins (bHLHs), MADS-Box, and GRAS, we propose an improved nomenclature system from superfamily (MYB) and family (R2R3-MYB) to subfamily. “Subgroup” used by Chang and colleagues should be revised to evolutionary clade/group. To avoid confusion, in the following sections, we uniformly refer to the lower classifications within the gene family as subfamilies (abbreviated as S1, S2, etc.).

Structural conservation of R2R3-MYBs

7The R2R3-MYB protein consists of two major functional parts: a DNA-binding domain (MYB domain) located at the N terminus and a regulatory region (non-MYB region) located at the C terminus. The MYB domain is a signature, highly conserved feature in the gene family, whereas the non-MYB regions have diverged among plant species (Fig. 2a). In addition, the intron patterns in the MYB domains of the R2R3-MYBs are highly conserved within each subfamily across land plants. In most cases, the MYB domain has one or two conserved intron insertion sites, with rare intron-less and multi-intron genes. Although the number of intron patterns differs slightly among taxonomic groups, there is clearly high structural conservation of MYB domains across land plants. In our previous study, we identified 12 highly conserved intron patterns across the plant kingdom that may have arisen early in the transition from aquatic to terrestrial plants based on conserved intron numbers, insertion positions, and intron phases (Supplemental Fig. 1). The majority (~70%) of the tested R2R3-MYBs share three types (patterns a, b, and c) of the 12 intron patterns (patterns a to l), suggesting biased expansion during evolution. A recent study has shown that some charophyte R2R3-MYBs exhibit intron–exon structures identical to those of their corresponding land homologs in the same subfamily, whereas others show clear differences, indicating a difference among ancestral genes.

8R2R3-MYB proteins can act as transcriptional activators as well as repressors. Most are activators that bind to cis-elements in gene promoters to recruit transcriptional machinery and stimulate gene expression. For instance, many R2R3-MYBs have a bHLH-interacting motif “(D/E)Lx2(R/K)x3Lx6Lx3R” in the R3 MYB domain (Fig. 2a), enabling physical interactions with the bHLH protein to form the MYB-bHLH-WDR (MBW) transcriptional complex. Notably, although the conservation of the non-MYB region is much lower than that of the MYB domain, the C-terminal regions of closely related members within each subfamily or close subfamilies in an evolutionary clade generally share short conserved protein motifs (some called short linear motifs, SLiMs), such as EAR (ethylene-responsive element binding, “pdLNL(D/E)L” or “DLNxxP” in S4), “(R/K)PRPRx(F/L)” in S6, SID (sensitive to ABA and Drought 2 protein interact motif), and TLLLFR (Fig. 2a), indicating their common origin, functional similarities, and structural conservation. Recently, Millard et al. reported that the interactions between MYB TFs from S12 and bHLH were mediated by one of the conserved motifs ([L/F]LN[K/R]VA) located in the center of the non-MYB region. Two novel SLiMs with roles in protein–protein interaction were uncovered by Rodrigues et al. in the disordered C-terminal region. For more detailed information, see the recent reviews by LaFountain and Yuan and Chen et al.. MYB activators and repressors often operate in a hierarchy. Furthermore, many subfamily- and/or branch-specific motifs have been detected within R2R3-MYBs. For instance, based on a large number of species, up to 102 highly conserved motifs have been identified in non-MYB regions. Interestingly, non-MYB regions across the entire A. thaliana R2R3-MYB gene family contain extensive intrinsically disordered regions (IDRs) with special post-translational modification sites, binding sites for physical interactions, and activation domains. These features may explain the substantial functional diversity and the structure–function relationships in plant R2R3-MYBs. However, owing to the high divergence in non-MYB regions, a systematic analysis of motif(s) and/or IDRs covering broad and representative plant lineages is still lacking. Moreover, further experimental evidence is needed, including for IDRs.

Functional conservation and diversification of R2R3-MYBs in land plants

9The biological functions of R2R3-MYBs have been verified in an increasing number of non-model crops with high economic value, especially in the last decade. More than 500 R2R3-MYBs have been functionally characterized in around 130 plant species (Fig. 2b and Supplemental Table 2), and their roles in many biological processes have been reported. Notably, research progress related to R2R3-MYB gene function is based mainly on studies of the model plant A. thaliana; approximately 80% of its 126 R2R3-MYBs have been experimentally characterized (Fig. 2c). Overall, the functions of R2R3-MYBs can be classified into three major processes: development and cell differentiation, specialized metabolism (especially the phenylpropanoid biosynthesis pathway), and stress responses (biotic and abiotic stresses).

R2R3-MYBs are required for developmental and cell differentiation processes

10Plant R2R3-MYBs are involved in the regulation of many important aspects of plant growth and development (Supplemental Table 2), e.g. trichome initiation and branching, cuticle development, and regulation of different organs, including the flower, seed, shoot, and root. In general, genes from the S9 (e.g. AtMYB16), S15 (e.g. AtMYB66), S18 (e.g. AtMYB33), S25 (e.g. AtMYB64), and S27 (e.g. AtMYB91) subfamilies are exclusively associated with the above-mentioned biological functions (Supplemental Table 2). For instance, genes in S9 are involved in cuticle formation and trichome branching in A. thaliana (AtMYB16 and AtMYB106) and M. polymorpha (MpSBG9), conical epidermal cell outgrowth in Antirrhinum majus (AmMYBML1), photosynthesis and growth in Betula platyphylla (BpMYB106), and fiber development in cotton (GhMML3). The genes in S18 mainly regulate the development of flower organs such as stamens (AtMYB33, AtMYB65, and BcMF28) and anthers (OsGAMYB), as well as pollen tube–synergid interactions (AtMYB97, AtMYB101, and AtMYB120). Interestingly, the above processes are usually mediated by hormones and/or hormone signaling, e.g. JA and GA. R2R3-MYBs (e.g. members of S25) are also involved in plant reproductive growth (Supplemental Table 2). More recently, MpFGMYB, a member of S25, was identified as a critical factor in sexual dimorphism determination in M. polymorpha, and similar results regarding spore and sexual organ development were obtained in Selaginella moellendorffii (SmGAMB) and Physcomitrella patens (PpGAMYB1 and PpGAMYB2). Members of S27 contribute to the regulation of vegetative organ formation, including leaf patterning and development (NbPHAN and PHANTASTICA), stomatal cell differentiation and formation, and axillary meristem formation (ZmRS2 and SlPHAN) (Supplemental Table 2). S14 also functions in meristem initiation as well as root formation (CRY1) (Supplemental Table 2). A good example in this subfamily is the MpGCAM1 gene, which precisely controls gemma cup formation in liverworts. Another example of genes that regulate cell growth during gametophytic development are MpPp1 and MpPp2 in P. patens. Furthermore, some subfamilies have species-specific functions. For instance, AtMYB21, AtMYB24, and AtMYB57 in S19 have key roles in stamen development. However, their homologs in almost all other species studied, including Freesia hybrids, Gentian tutea, Ficus carica, Malus domestica, and Petunia hybrida, regulate specialized metabolism (Supplemental Table 2). Further research should focus on S16, S24, S28, S31, S33, S36, and S37, for which experimental data are rather limited (Supplemental Table 2).

11In summary, R2R3-MYBs are a class of important TFs necessary for the basic life cycle of plants. Therefore, there is a need for more extensive field studies of R2R3-MYBs in the future to determine their functions in basic developmental processes.

R2R3-MYBs respond to various environmental stresses

12Over the past few decades, R2R3-MYBs have emerged as key regulators of responses to diverse abiotic stresses, such as drought, temperature, salinity, and phosphate starvation (Supplemental Table 2); see previous reviews. Representative subfamilies are S1, S2, S11, S17, S20, S22, and S38. In A. thaliana, members of S1 (AtMYB30, AtMYB60, and AtMYB96) are involved in drought, heat, salt, and excess-light stresses; members of S2 (AtMYB13, AtMYB14, and AtMYB15) act as positive regulators of drought, wounding, and freezing tolerance; AtMYB41 and AtMYB74 in S11 are involved in osmotic and/or salt stress; members of S20 (AtMYB2, AtMYB62, and AtMYB108) are responsive to a wide range of environmental stresses; similar roles have been observed for S22 members (AtMYB44, AtMYB73, and AtMYB77). AtMYB48 in S38 is involved in potassium stress possibly via alternative splicing, which modulates DNA-binding motifs. Some genes from S3, S4, S8, and S23 also show stress-induced functionality in A. thaliana. In addition to the R2R3-MYBs in A. thaliana, around 70 genes identified in 26 species have also been found to participate in distinct abiotic stresses (Supplemental Table 2). As in A. thaliana, such proteins are abundant in S2, S11, S20, and S22. However, distinct differences have been noted. Some groups have been confirmed only in A. thaliana (e.g. AtMYB1 from S23a and AtMYB72 from S3) or only in non-model species, such as S44, S4, S17, S28, S43, S7, S39, and S79. Taken together, these results suggest that R2R3-MYBs control responses to multiple abiotic stresses and act as major regulators. However, more research is needed to improve our understanding of the functional divergence and conservation of this gene family in plants. This understanding could provide a theoretical basis for the development of strategies to resolve the adverse effects of abiotic stresses, which are exacerbated by climate change.

13Many R2R3-MYBs contribute to the biotic stress response, and at least 13 R2R3-MYBs have been reported to date (Supplemental Table 2). Interestingly, eight of these genes belong to S2. OsMYB30 directly upregulates OsPAL6 and OsPAL8 to enhance resistance to the brown planthopper in rice. The overexpression of CmMYB15 in chrysanthemum confers resistance to aphids by regulating lignin biosynthesis. GmMYB29A2 regulates soybean resistance to Phytophthora sojae. SlHM1 and SlMYB52 alter trichome density to confer spider mite tolerance in tomato via auxin signaling. VdMYB1 in Vitis davidii and TaRIM1 in wheat regulate pathogen defense. Other examples include AtMYB30 (S1), AtMYB96 (S1), AtMYB102 (S11), and AtMYB72 (S3) in A. thaliana and OsJAmyb (S39) in Oryza sativa.

14In summary, R2R3-MYBs could improve plant responses to multiple abiotic and biotic stresses in agriculture and could be targets of advanced technologies, such as CRISPR technology, to improve crop resistance to environmental stimuli in order to maintain the food supply.

Key roles of R2R3-MYBs in metabolite biosynthesis

15The principal roles of plant R2R3-MYBs (~70%) reported to date are in the regulation of plant specialized metabolism, including the benzenoid, phenylpropanoid, terpenoid, and glucosinolate (GSL) pathways (Supplemental Table 2). Nearly half of the functionally characterized A. thaliana R2R3-MYBs are related to core and specialized metabolism reactions (Fig. 3 and Supplemental Table 2). Notably, the majority of these R2R3-MYBs are involved as activators or repressors in the transcriptional regulation of the phenylpropanoid biosynthesis pathway, which gives rise to a class of phenylpropanoid-derived compounds such as flavonoids (proanthocyanidins, anthocyanins, flavones, flavonols, isoflavonoids, and phlobaphenes), lignins, and other general phenylpropanoids (Fig. 3a).

16Flavonoids are a vast group of plant specialized metabolites with a common diphenylpropane (C6-C3-C6) backbone that have important functions as pigments and/or light protectants. Typical subfamilies in the R2R3-MYB gene family that are involved in the regulation of flavonoid biosynthesis are S6, S5, S4, S7, S44, and S79 (Supplemental Table 2). In addition to their roles in A. thaliana, there is substantial emerging evidence for the roles of R2R3-MYBs in the transcriptional regulation of flavonoid metabolism in various plants, including important food crops (41), horticultural crops (fruits, 77; ornamentals, 61; vegetables, 37), economically valuable woody crops (27), and edible and medicinal plants (30). With respect to edible crops, including fruits and vegetables, research has mainly focused on substances such as anthocyanins and flavonols that determine their quality and nutritional properties. However, flower colors are key traits for flower crops. Potato StMYB44 has recently been identified as a repressor of anthocyanin biosynthesis in tuber flesh under high temperatures, and whole-genome resequencing-based QTL-seq indicated that AhTc1 controls the purple testa color in peanut. In addition, the overexpression of MdMYB24L resulted in higher anthocyanin contents in transgenic ‘Orin’ apple calli. Similar studies have examined R2R3-MYBs in other fruit trees, including PaMYB10 in apricot, AcMYB123 in kiwifruit, LcMYB5 in litchi, and FcMYB123 in fig. In M. polymorpha, MpMYB14 and MpMYB02 regulate anthocyanin accumulation. Moreover, different types of flavonoid regulation are broadly observed. For instance, regulatory roles have been reported for PhMYB15 and PpMYBF1 in flavonol biosynthesis in peach fruit, FhMYB21L2 in flavonol biosynthesis in Freesia, CsPH4 in proanthocyanidin biosynthesis in citrus, SlMYB72 in carotenoid biosynthesis in tomato, CaMYB108 in capsaicinoid biosynthesis in pepper, AgMYB1 in apigenin biosynthesis in celery, HaMYB111 in floral ultraviolet patterning in sunflower, and SmMYB2 in phenolic acid biosynthesis in Salvia miltiorrhiza. Apart from model flowers such as Petunia and Antirrhinum, a number of flowering bulbs have also been studied recently, including Freesia, Cattleya, and Narcissus.

17Lignin is another major end-product of the phenylpropanoid pathway and a key component of secondary cell walls (SCWs) in wood; it is polymerized from phenylpropanoid-derived monolignols. The role of R2R3-MYBs in the lignin biosynthesis pathway is a major focus of research. As wood is widely used for pulp, papermaking, and biofuels and wood quality is largely determined by lignin synthesis, most studies of the regulatory effects of R2R3-MYBs on lignin synthesis are based on woody plants. For example, the overexpression of PtoMYB055 upregulates the expression of lignin biosynthetic genes in transgenic poplar, resulting in an increase in the thickness of the SCW. By contrast, PtMYB189 acts as a repressor to regulate SCW biosynthesis in poplar. Likewise, the positive or negative regulation of the SCW by R2R3-MYBs has also been reported in Z. mays, G. hirsutum, O. sativa, Pyrus × bretschneideri, and Eriobotrya japonica; however, additional studies are still needed.

18In addition to phenylpropanoid metabolism, which has been investigated extensively in plants, other representative specialized metabolic compounds have been studied, such as those produced by the GSL and terpenoid pathways (Fig. 3b–c). GSLs have well-established anticarcinogenic and antioxidative effects in humans. Interestingly, consistent with the distribution of GSLs, members of S12 are widely distributed in species from the family Brassicaceae and are predominantly related to GSL biosynthesis in this family (Supplemental Table 2). It has been reported that indolic GSL synthesis is regulated mainly by AtMYB34, AtMYB51, and AtMYB122, whereas aliphatic GSL synthesis is regulated by AtMYB28, AtMYB29, and AtMYB76. For example, silencing BjMYB28 homologs reduces the seed GSL content in Brassica juncea, BoMYB29 increases the methylsulphinyl GSL content in Brassica oleracea var. acephala, and BnMYB28.1 was identified by a QTL analysis using near-isogenic lines. These studies provide good examples of the adaptive evolution of the R2R3-MYB gene family in land plants, especially in angiosperm diversification. Some plants can produce and emit fragrant molecules such as benzenoids and terpenoids, especially in flowers, and these processes are strictly regulated at the transcriptional level by R2R3-MYBs. For instance, two R2R3-MYBs, FhMYB21L1 and FhMYB21L2, are expressed synchronously with FhTPS1 and can activate its expression to affect monoterpene synthase synthesis when overexpressed. In addition, BpMYB21 and BpMYB61 in B. platyphylla are involved in triterpenoid synthesis. R2R3-MYBs regulate terpenoid compounds in several medicinal plants, including S. miltiorrhiza, Panax ginseng, and Mentha spicata.

19The research summarized above clearly demonstrates that plant R2R3-MYBs, which are related to plant specialized metabolism, are mainly involved in the phenylpropanoid biosynthesis pathway, and each subfamily member has key roles in distinct processes, such as proanthocyanidin or lignin biosynthesis. Accordingly, this gene family has probably contributed to functional evolution in land plants.

The origin and expansion of R2R3-MYBs in land plants are associated with functionality

20Gene duplication is a prominent event in plant genome evolution and contributes to the establishment of multi-gene families. Genes can be duplicated by various mechanisms, such as whole genome duplication (WGD), chromosomal segmental duplication, tandem duplication, and retrotransposition. Based on systematic analyses of many land plants, we previously found that WGD/polyploidy events and small-scale duplications (e.g. segmental duplications) accounted for the large expansion of the R2R3-MYB gene family. Similar results have been obtained in studies of broad plant lineages. It is well known that WGD events are a driving force in angiosperm diversification. The tremendous expansion of R2R3-MYBs in land plants is consistent with WGD in angiosperms, indicating an important role for the expansion of R2R3-MYBs in the increased complexity of angiosperms. Small-scale duplications (e.g. tandem/segmental duplications) have also contributed to the rapid expansion and large size of this gene family in land plants, as well as the evolution of novel gene functions.

21R2R3-MYBs underwent a rapid expansion over the course of plant evolution (i.e. from algae to land plants), resulting in a gradual increase in number together with an increase in organismal complexity. Accordingly, the number of genes in this family in land plants is large, showing a huge expansion after the divergence of angiosperms from other vascular plants. For example, only eight R2R3-MYBs were detected in the single-celled chlorophyte Chlamydomonas reinhardtii, whereas up to 429 R2R3-MYBs were observed in the allotetraploid Brassica napus (Fig. 1). Based on an analyses of 50 eukaryotes, the R2R3-MYB gene family was classified into 73 subfamilies, most of which were newly defined (S26–S73), with the exception of the first 25 subfamilies from Arabidopsis. Based on the distribution of subfamily members across the 27 plant genomes investigated in the study, it was speculated that a few subfamilies (S18, S21, S22, S26, and S27) were established soon after the origin of land plants and may be the ancestors of land plant R2R3-MYBs, whereas the major subfamilies formed a monophyletic clade in land plants. In summary, plant R2R3-MYBs experienced three major expansion events: one early in the origin of land plants from Chlorophyta, one after the divergence of spermatophytes from vascular plants, and one in the common ancestor of angiosperms before the divergence of monocots and eudicots, forming the majority of R2R3-MYB subfamilies. Notably, members of this gene family exhibit an uneven phylogenetic distribution; the expansion was significantly biased toward subfamilies with three highly homologous intron patterns (a, b, and c) during evolution, resulting in an enormous expansion in the number of R2R3-MYBs in the plant lineage (Fig. 4a and Supplemental Fig. 1). For instance, in the 12 land plants investigated in our previous study, 2R-MYBs with patterns a–c generally accounted for ~66–81% of this gene family in 10 angiosperms, including Z. mays (66%), Arabidopsis (73%), and Vitis vinifera (81%). A similar situation (73%) was found in B. napus. By contrast, the corresponding percentages were 59% in P. patens and 20% in S. moellendorffii (Fig. 4a). Accordingly, up to 43 subfamilies have intron pattern a, and 12 and 19 subfamilies have intron patterns a and b, respectively, and have generally been integrated into the subfamilies with pattern a (Fig. 4b and Supplemental Fig. 2). Novel subfamilies have commonly been derived from these three categories. By contrast, the numbers of genes with the last nine intron patterns (d–l) are relatively conserved in land plants (Fig. 4a). Relatively few genes have the last nine intron patterns (d–l), which generally account for less than 30% of this gene family in most angiosperms. With the exception of patterns d and j, which are shared by 7 and 2 subfamilies, respectively, each of the last 7 patterns are shared by only one subfamily (e.g. pattern e in S21 and pattern f in S19) (Fig. 4b and Supplemental Fig. 2). Thus, the number of genes with patterns d–l is relatively conserved in land plants.

22As discussed above, plant R2R3-MYBs are crucial for the regulation of many plant-specific processes related to metabolism (22 subfamilies), development (16 subfamilies), and biotic and abiotic stress processes (14 subfamilies) (Fig. 4b and Supplemental Fig. 2). Notably, the expansion of this gene family is closely accompanied by increases in the functional diversity of R2R3-MYBs in the plant kingdom. Interestingly, older subfamilies are generally involved in development and/or stress-related processes, whereas the majority of new/derived subfamilies in angiosperms are related to metabolism (Fig. 4b and Supplemental Fig. 2), suggesting a bias in functional diversification toward specialized metabolism. In particular, the evolution of R2R3-MYBs in plants is related to specific expansions giving rise to species- or lineage-specific subfamilies. For example, 5 of 43 B. napus subfamilies are Brassicaceae specific. Several of the 43 pineapple subfamilies, such as C2, C8, and C22, are likely to be species or lineage specific. Similarly, three dicot-specific and six grass-specific subfamilies have been observed based on a comparative genomic analysis of R2R3-MYBs in Arabidopsis, poplar, rice, maize, and switchgrass. Although the functions of most species- or lineage-specific subfamilies are unknown, the distributions suggest that they have lineage-specific functions. For instance, members of the Brassicaceae-specific S12 subfamily (e.g. AtMYB28/HAG1, AtMYB29/HAG3, AtMYB34, AtMYB51/HIG1, AtMYB76/HAG2, and AtMYB122 in A. thaliana) are regulators of Brassicaceae-specific GSL biosynthesis (Supplemental Table 2 and Supplemental Fig. 2). Three expanded subfamilies in Eucalyptus grandis, including a significantly higher number in woody perennial species (E. grandis, V. vinifera, and P. trichocarpa), and five subfamilies preferentially found in woody plants are potentially involved in cambium-derived woody growth. Several sugar beet MYBs with an atypical amino acid composition in the R3 domain are species-specific regulators of the betalain red pigment pathway. Together, these results indicate an obvious expansion and functional trend toward specialized metabolism in this gene family during angiosperm evolution.

Concluding remarks and prospects

23R2R3-MYBs are ubiquitous in eukaryotes and are not plant specific, but the numbers of this type of MYB gene are generally higher in plants (especially in angiosperms) than in other eukaryotes, and they constitute one of the largest TF gene families in plant genomes. As the number of sequenced plant genomes has increased, the plant R2R3-MYB gene family has been systematically identified and analyzed in about 74 species at a genome-wide level (Fig. 1). These data have substantially improved our understanding of R2R3-MYB distribution, origin, classification, expansion, and evolutionary mechanisms in plants.

24As sessile organisms, plants have had to adapt to constantly changing environments during evolution. Through time, plants have differentiated into highly complex organisms and have developed a large number of specialized metabolites with beneficial functions for survival and adaptation. R2R3-MYBs have undergone rapid expansion during plant evolution via WGD and small-scale duplications. These drastic expansion/duplication events have played a key role in generating diversity, producing many conserved subfamilies and also lineage-specific subfamilies with specific biological functions (e.g. S12 in GSL biosynthesis), especially those related to specialized metabolism. About 70% of functionally characterized R2R3-MYBs and most subfamilies are related to specialized metabolic processes focused on phenylpropanoid-derived secondary metabolites (Fig. 4b and Supplemental Table 2). The rapid expansion and diversification of R2R3-MYBs have been ongoing processes throughout the evolution of angiosperms. It is not surprising that this large gene family has contributed to the evolution of physiological or developmental processes that are specific to plants. The expansion of R2R3-MYBs in land plants may underpin the emergence of tremendous plant diversity, providing new functional characteristics related to protection against stress and changing environmental conditions. Thus, uncovering the genomic and molecular basis of the origin and evolution of such functional characteristics is a major research goal.

25Owing to the availability of resources for gene functional analyses (e.g. genomic data, genetic populations, and experimental tools), a large proportion of the Arabidopsis R2R3-MYB gene family has been functionally characterized (about 100 of 126 genes). However, our current knowledge of the functions of plant R2R3-MYBs is based mainly on the model plant Arabidopsis, whereas studies of non-traditional models (such as crops) are in an early stage. More information about the functions of R2R3-MYBs in a broader array of plant taxa will undoubtedly improve our understanding of the mechanisms underlying their evolution and functional diversification. Newly developed genomic technologies (e.g. third-generation long-read sequencing technology) combined with traditional and novel molecular technologies (e.g. genome editing tools) offer excellent opportunities for further improving our understanding of the functions and functional diversification of R2R3-MYBs.

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88.
Perez-Rodriguez M, Jaffe FW, Butelli E et al. 2005 development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development. 2005;132:359–70.
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89.
A R2R3-MYB transcription factor BpMYB106 of birch (Betula platyphylla) confers increased photosynthesis and growth rate through up-regulating photosynthetic gene expression · 2016
Not checked
90.
Wu H, Tian Y, Wan Q et al. Genetics and evolution of MIXTA genes regulating cotton lint fiber development. New Phytol. 2018;217:883–95.
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91.
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92.
Shen X, Hu Z, Xiang X et al. Overexpression of a stamen-specific R2R3-MYB gene BcMF28 causes aberrant stamen development in transgenic Arabidopsis. Biochem Biophys Res Commun. 2019;518:726–31.
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93.
Aya K, Ueguchi-Tanaka M, Kondo M et al. Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell. 2009;21:1453–72.
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94.
MYB97, MYB101 and MYB120 Function as Male Factors That Control Pollen Tube-Synergid Interaction in Arabidopsis thaliana Fertilization · 2013
No notice
95.
Rabiger DS, Drews GN. MYB64 and MYB119 are required for cellularization and differentiation during female gametogenesis in Arabidopsis thaliana. PLoS Genet. 2013;9:e1003783.
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96.
Hisanaga T, Okahashi K, Yamaoka S et al. A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort. EMBO J. 2019;38:e100240.
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97.
Aya K, Hiwatashi Y, Kojima M et al. The gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution. Nat Commun. 2011;2:544.
Not in our library10.1038/ncomms1552
98.
Huang C, Hu G, Li F et al. NbPHAN, a MYB transcriptional factor, regulates leaf development and affects drought tolerance in Nicotiana benthamiana. Physiol Plant. 2013;149:297–309.
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99.
Ge L, Chen R. PHANTASTICA regulates leaf polarity and petiole identity in Medicago truncatula. Plant Signal Behav. 2014;9:e28121–1.
Not in our library10.4161/psb.28121
100.
Tsiantis M, Schneeberger R, Golz JF et al. The maize rough sheath2 gene and leaf development programs in monocot and dicot plants. Science. 1999;284:154–6.
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101.
Morimoto R, Nishioka E, Murai K et al. Functional conservation of wheat orthologs of maize rough sheath1 and rough sheath2 genes. Plant Mol Biol. 2009;69:273–85.
Not in our library10.1007/s11103-008-9422-5
102.
Zoulias N, Koenig D, Hamidi A et al. A role for PHANTASTICA in medio-lateral regulation of adaxial domain development in tomato and tobacco leaves. Ann Bot. 2012;109:407–18.
Not in our library10.1093/aob/mcr295
103.
Hong SH, Kim HJ, Ryu JS et al. CRY1 inhibits COP1-mediated degradation of BIT1, a MYB transcription factor, to activate blue light-dependent gene expression in Arabidopsis. Plant J. 2008;55:361–71.
Not in our library10.1111/j.1365-313x.2008.03508.x
104.
Fernández-Marcos M, Desvoyes B, Manzano C et al. Control of Arabidopsis lateral root primordium boundaries by MYB36. New Phytol. 2017;213:105–12.
Not in our library10.1111/nph.14304
105.
Yasui Y, Tsukamoto S, Sugaya T et al. GEMMA CUP-ASSOCIATED MYB1, an ortholog of axillary meristem regulators, is essential in vegetative reproduction in Marchantia polymorpha. Curr Biol. 2019;29:3987–3995.e5.
Not in our library10.1016/j.cub.2019.10.004
106.
Leech MJ, Kammerer W, Cove DJ et al. Expression of myb-related genes in the moss. Plant J. 1993;3:51–61.
Not in our library10.1046/j.1365-313x.1993.t01-3-00999.x
107.
Mandaokar A, Thines B, Shin B et al. Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J. 2006;46:984–1008.
Not in our library10.1111/j.1365-313x.2006.02756.x
108.
Gibberellin Acts through Jasmonate to Control the Expression of MYB21, MYB24, and MYB57 to Promote Stamen Filament Growth in Arabidopsis · 2009
No notice
109.
Shan X, Li Y, Yang S et al. The spatio-temporal biosynthesis of floral flavonols is controlled by differential phylogenetic MYB regulators in Freesia hybrida. New Phytol. 2020;228:1864–79.
Not in our library10.1111/nph.16818
110.
Yang Z, Li Y, Gao F et al. MYB21 interacts with MYC2 to control the expression of terpene synthase genes in flowers of Freesia hybrida and Arabidopsis thaliana. J Exp Bot. 2020;71:4140–58.
Not in our library10.1093/jxb/eraa184
111.
Nakatsuka T, Haruta KS, Abe Y et al. Identification and characterization of R2R3-MYB and bHLH transcription factors regulating anthocyanin biosynthesis in gentian flowers. Plant Cell Physiol. 2008;49:1818–29.
Not in our library10.1093/pcp/pcn163
112.
Li J, An Y, Wang L. Transcriptomic analysis of Ficus carica peels with a focus on the key genes for anthocyanin biosynthesis. Int J Mol Sci. 2020;21:1245.
Not in our library10.3390/ijms21041245
113.
Wang Y, Liu W, Jiang H et al. The R2R3-MYB transcription factor MdMYB24-like is involved in methyl jasmonate-induced anthocyanin biosynthesis in apple. Plant Physiol Biochem. 2019;139:273–82.
Not in our library10.1016/j.plaphy.2019.03.031
114.
Spitzer-Rimon B, Marhevka E, Barkai O et al. EOBII, a gene encoding a flower-specific regulator of phenylpropanoid volatiles' biosynthesis in petunia. Plant Cell. 2010;22:1961–76.
Not in our library10.1105/tpc.109.067280
115.
Yang SW, Jang IC, Henriques R et al. FAR-RED ELONGATED HYPOCOTYL1 and FHY1-LIKE associate with the Arabidopsis transcription factors LAF1 and HFR1 to transmit phytochrome a signals for inhibition of HYPOCOTYL elongation. Plant Cell. 2009;21:1341–59.
Not in our library10.1105/tpc.109.067215
116.
Gibbs DJ, Vob U, Harding SA et al. AtMYB93 is a novel negative regulator of lateral root development in Arabidopsis. New Phytol. 2014;203:1194–207.
Not in our library10.1111/nph.12879
117.
Transcriptional regulation of MdPIN3 and MdPIN10 by MdFLP during apple self-rooted stock adventitious root gravitropism · 2019
Not checked
118.
Yuan Y, Xu X, Luo Y et al. R2R3 MYB-dependent auxin signalling regulates trichome formation, and increased trichome density confers spider mite tolerance on tomato. Plant Biotechnol J. 2021;19:138–52.
Not in our library10.1111/pbi.13448
119.
Zhu J, Chen H, Li H et al. Defective in tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 2008;55:266–77.
Not in our library10.1111/j.1365-313x.2008.03500.x
120.
Zhang Y, Cao G, Qu LJ et al. Characterization of Arabidopsis MYB transcription factor gene AtMYB17 and its possible regulation by LEAFY and AGL15. J Genet Genomics. 2009;36:99–107.
Not in our library10.1016/s1673-8527(08)60096-x
121.
Liang G, He H, Li Y et al. MYB82 functions in regulation of trichome development in Arabidopsis. J Exp Bot. 2014;65:3215–23.
Not in our library10.1093/jxb/eru179
122.
Zhang Y, Zhu H, Shao C et al. PaMYB82 from Platanus acerifolia regulates trichome development in transgenic Arabidopsis. Plant Sci. 2019;287:110177.
Not in our library10.1016/j.plantsci.2019.110177
123.
Yang A, Dai X, Zhang WH. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot. 2012;63:2541–56.
Not in our library10.1093/jxb/err431
124.
Zhao Y, Cheng X, Liu X et al. The wheat MYB transcription factor TaMYB(31) is involved in drought stress responses in Arabidopsis. Front Plant Sci. 2018;9:1426–6.
Not in our library10.3389/fpls.2018.01426
125.
Agarwal P, Mitra M, Banerjee S et al. MYB4 transcription factor, a member of R2R3-subfamily of MYB domain protein, regulates cadmium tolerance via enhanced protection against oxidative damage and increases expression of PCS1 and MT1C in Arabidopsis. Plant Sci. 2020;297:110501.
Not in our library10.1016/j.plantsci.2020.110501
126.
Fichman Y, Zandalinas SI, Sengupta S et al. MYB30 orchestrates systemic reactive oxygen signaling and plant acclimation. Plant Physiol. 2020;184:666.
Not in our library10.1104/pp.20.00859
127.
Yao L, Yang B, Xian B et al. The R2R3-MYB transcription factor BnaMYB111L from rapeseed modulates reactive oxygen species accumulation and hypersensitive-like cell death. Physiologie Végétale. 2020;147:280–8.
Not in our library10.1016/j.plaphy.2019.12.027
128.
Li C, Ng CKY, Fan LM. MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot. 2015;114:80–91.
Not in our library
129.
Regulating the Regulators: The Control of Transcription Factors in Plant Defense Signaling · 2018
No notice
130.
Cominelli E, Galbiati M, Vavassuer A et al. A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol. 2005;15:1196–200.
Not in our library10.1016/j.cub.2005.05.048
131.
Seo PJ, Xiang F, Qiao M et al. The MYB96 transcription factor mediates abscisic acid signaling during drought stress response in Arabidopsis. Plant Physiol. 2009;151:275–89.
Not in our library10.1104/pp.109.144220
132.
Seo PJ, Lee SB, Chung M et al. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell. 2011;23:1138–52.
Not in our library10.1105/tpc.111.083485
133.
Marino D, Froidure S, Canonne J et al. Arabidopsis ubiquitin ligase MIEL1 mediates degradation of the transcription factor MYB30 weakening plant defence. Nat Commun. 2013;4:1476.
Not in our library10.1038/ncomms2479
134.
Rusconi F, Simeoni F, Francia P et al. The Arabidopsis thaliana MYB60 promoter provides a tool for the spatio-temporal control of gene expression in stomatal guard cells. J Exp Bot. 2013;64:3361–71.
Not in our library10.1093/jxb/ert180
135.
Lee HG, Seo PJ. The MYB96–HHP module integrates cold and abscisic acid signaling to activate the CBF–COR pathway in Arabidopsis. Plant J. 2015;82:962–77.
Not in our library10.1111/tpj.12866
136.
Liao C, Zheng Y, Guo Y. MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN-mediated cytosolic calcium signaling in Arabidopsis. New Phytol. 2017;216:163–77.
Not in our library10.1111/nph.14679
137.
Yan J, Yu L, He L et al. Comparative transcriptome analysis of celery leaf blades identified an R2R3-MYB transcription factor that regulates apigenin metabolism. J Agric Food Chem. 2019;67:5265–77.
Not in our library10.1021/acs.jafc.9b01052
138.
Kirik V, Kölle K, Miséra S et al. Two novel MYB homologues with changed expression in late embryogenesis-defective Arabidopsis mutants. Plant Mol Biol. 1998;37:819–27.
Not in our library10.1023/a:1006011002499
139.
Ding Z, Li S, An X et al. Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics. 2009;36:17–29.
Not in our library10.1016/s1673-8527(09)60003-5
140.
Chen Y, Chen Z, Kang J et al. AtMYB14 regulates cold tolerance in Arabidopsis. Plant Mol. Biol. Report. 2013;31:87–97.
Not in our library10.1007/s11105-012-0481-z
141.
Chezem WR, Memon A, Li FS et al. SG2-type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. Plant Cell. 2017;29:1907–26.
Not in our library10.1105/tpc.16.00954
142.
Hoang MHT, Nguyen XC, Lee K et al. Phosphorylation by AtMPK6 is required for the biological function of AtMYB41 in Arabidopsis. Biochem Biophys Res Commun. 2012;422:181–6.
Not in our library10.1016/j.bbrc.2012.04.137
143.
Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis · 2015
No notice
144.
Devaiah BN, Madhuvanthi R, Karthikeyan AS et al. Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Mol Plant. 2009;2:43–58.
Not in our library10.1093/mp/ssn081
145.
Baek D, Kim MC, Chun HJ et al. Regulation of miR399f transcription by AtMYB2 affects phosphate starvation responses in Arabidopsis. Plant Physiol. 2013;161:362–73.
Not in our library10.1104/pp.112.205922
146.
Chou ML, Liao WY, Wei WC et al. The direct involvement of dark-induced Tic55 protein in chlorophyll catabolism and its indirect role in the MYB108-NAC signaling pathway during leaf senescence in Arabidopsis thaliana. Int J Mol Sci. 2018;19:1854.
Not in our library10.3390/ijms19071854
147.
Zhao Y, Xing L, Wang X et al. The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Sci Signal. 2014;7:ra53.
Not in our library10.1126/scisignal.2005051
148.
Nguyen NH, Cheong JJ. The AtMYB44 promoter is accessible to signals that induce different chromatin modifications for gene transcription. Plant Physiol Biochem. 2018;130:14–9.
Not in our library10.1016/j.plaphy.2018.06.030
149.
Nishida S, Kakei Y, Shimada Y et al. Genome-wide analysis of specific alterations in transcript structure and accumulation caused by nutrient deficiencies in Arabidopsis thaliana. Plant J. 2017;91:741–53.
Not in our library10.1111/tpj.13606
150.
MYB10 and MYB72 Are Required for Growth under Iron-Limiting Conditions · 2013
No notice
151.
Cui MH, Shin-Yoo K, Hyoung S et al. An Arabidopsis R2R3-MYB transcription factor, AtMYB20, negatively regulates type 2C serine/threonine protein phosphatases to enhance salt tolerance. FEBS Lett. 2013;587:1773–8.
Not in our library10.1016/j.febslet.2013.04.028
152.
Wang T, Tohge T, Ivakov A et al. Salt-related MYB1 coordinates abscisic acid biosynthesis and signaling during salt stress in Arabidopsis. Plant Physiol. 2015;169:1027–41.
Not in our library10.1104/pp.15.00962
153.
Agarwal M, Hao Y, Kapoor A et al. A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem. 2006;281:37636–45.
Not in our library10.1074/jbc.m605895200
154.
He Y, Li W, Lv J et al. Ectopic expression of a wheat MYB transcription factor gene, TaMYB73, improves salinity stress tolerance in Arabidopsis thaliana. J Exp Bot. 2012;63:1511–22.
Not in our library10.1093/jxb/err389
155.
NtMYB4 and NtCHS1 Are Critical Factors in the Regulation of Flavonoid Biosynthesis and Are Involved in Salinity Responsiveness · 2019
Not checked
156.
Liao W, Yang Y, Li Y et al. Genome-wide identification of cassava R2R3 MYB family genes related to abscission zone separation after environmental-stress-induced abscission. Sci Rep. 2016;6:32006–6.
Not in our library10.1038/srep32006
157.
Fang Q, Jiang T, Xu L et al. A salt-stress-regulator from the poplar R2R3 MYB family integrates the regulation of lateral root emergence and ABA signaling to mediate salt stress tolerance in Arabidopsis. Plant Physiol Biochem. 2017;114:100–10.
Not in our library10.1016/j.plaphy.2017.02.018
158.
Zhang X, Chen L, Shi Q et al. SIMYB102, an R2R3-type MYB gene, confers salt tolerance in transgenic tomato. Plant Sci. 2020;291:110356.
Not in our library10.1016/j.plantsci.2019.110356
159.
Zhang Z, Liu X, Wang X et al. An R2R3 MYB transcription factor in wheat, TaPIMP1, mediates host resistance to Bipolaris sorokiniana and drought stresses through regulation of defense- and stress-related genes. New Phytol. 2012;196:1155–70.
Not in our library10.1111/j.1469-8137.2012.04353.x
160.
Zhang Z, Hu X, Zhang Y et al. Opposing control by transcription factors MYB61 and MYB3 increases freezing tolerance by relieving C-repeat binding factor suppression. Plant Physiol. 2016;172:1306–23.
Not in our library10.1104/pp.16.00051
161.
Zhang S, Zhao Q, Zeng D et al. RhMYB108, an R2R3-MYB transcription factor, is involved in ethylene- and JA-induced petal senescence in rose plants. Hortic Res. 2019;6:131.
Not in our library10.1038/s41438-019-0221-8
162.
Shukla PS, Agarwal P, Gupta K et al. Molecular characterization of an MYB transcription factor from a succulent halophyte involved in stress tolerance. Aob Plants. 2015;7:plv054.
Not in our library10.1093/aobpla/plv054
163.
Gao F, Zhao HX, Yao HP et al. Identification, isolation and expression analysis of eight stress-related R2R3-MYB genes in tartary buckwheat (Fagopyrum tataricum). Plant Cell Rep. 2016;35:1385–96.
Not in our library10.1007/s00299-016-1971-5
164.
Hu DG, Li YY, Zhang QY et al. The R2R3-MYB transcription factor MdMYB73 is involved in malate accumulation and vacuolar acidification in apple. Plant J. 2017;91:443–54.
Not in our library10.1111/tpj.13579
165.
Zhao Y, Yang Z, Ding Y et al. Over-expression of an R2R3 MYB gene, GhMYB73, increases tolerance to salt stress in transgenic Arabidopsis. Plant Sci. 2019;286:28–36.
Not in our library10.1016/j.plantsci.2019.05.021
166.
Lee TG, Jang CS, Kim JY et al. A MYB transcription factor (TaMyb1) from wheat roots is expressed during hypoxia: roles in response to the oxygen concentration in root environment and abiotic stresses. Physiol Plant. 2007;129:375–85.
Not in our library
167.
Garg B, Lata C, Prasad M. A study of the role of gene TaMYB2 and an associated SNP in dehydration tolerance in common wheat. Mol Biol Rep. 2012;39:10865–71.
Not in our library10.1007/s11033-012-1983-3
168.
Genome Wide Analysis of the Apple MYB Transcription Factor Family Allows the Identification of MdoMYB121 Gene Confering Abiotic Stress Tolerance in Plants · 2013
No notice
169.
Wang RK, Cao ZH, Hao YJ. Overexpression of a R2R3 MYB gene MdSIMYB1 increases tolerance to multiple stresses in transgenic tobacco and apples. Physiol Plant. 2014;150:76–87.
Not in our library10.1111/ppl.12069
170.
Zhang L, Liu G, Zhao G et al. Characterization of a wheat R2R3-MYB transcription factor gene, TaMYB19, involved in enhanced abiotic stresses in Arabidopsis. Plant Cell Physiol. 2014;55:1802–12.
Not in our library10.1093/pcp/pcu109
171.
Dong W, Song Y, Zhao Z et al. The Medicago truncatula R2R3-MYB transcription factor gene MtMYBS1 enhances salinity tolerance when constitutively expressed in Arabidopsis thaliana. Biochem Biophys Res Commun. 2017;490:225–30.
Not in our library10.1016/j.bbrc.2017.06.025
172.
Wei H, Zhao H, Su T et al. Chicory R2R3-MYB transcription factors CiMYB5 and CiMYB3 regulate fructan 1-exohydrolase expression in response to abiotic stress and hormonal cues. J Exp Bot. 2017;68:4323–38.
Not in our library10.1093/jxb/erx210
173.
Geng D, Chen P, Shen X et al. MdMYB88 and MdMYB124 enhance drought tolerance by modulating root vessels and cell walls in apple. Plant Physiol. 2018;178:1296–309.
Not in our library10.1104/pp.18.00502
174.
He Y, Yang X, Xu C et al. Overexpression of a novel transcriptional repressor GmMYB3a negatively regulates salt-alkali tolerance and stress-related genes in soybean. Biochem Biophys Res Commun. 2018;498:586–91.
Not in our library10.1016/j.bbrc.2018.03.026
175.
Xie Y, Chen P, Yan Y et al. An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytol. 2018;218:201–18.
Not in our library10.1111/nph.14952
176.
Meng C, Sui N. Overexpression of maize MYB-IF35 increases chilling tolerance in Arabidopsis. Physiologie Végétale. 2019;135:167–73.
Not in our library10.1016/j.plaphy.2018.11.038
177.
Xing C, Liu Y, Zhao L et al. A novel MYB transcription factor regulates ascorbic acid synthesis and affects cold tolerance. Plant Cell Environ. 2019;42:832–45.
Not in our library10.1111/pce.13387
178.
He Y, Dong Y, Yang X et al. Functional activation of a novel R2R3-MYB protein gene, GmMYB68, confers salt-alkali resistance in soybean (Glycine max L.). Genome. 2020b;63:13–26.
Not in our library10.1139/gen-2018-0132
179.
An C, Sheng L, Du X et al. Overexpression of CmMYB15 provides chrysanthemum resistance to aphids by regulating the biosynthesis of lignin. Hortic Res. 2019;6:84.
Not in our library10.1038/s41438-019-0166-y
180.
Jahan MA, Harris B, Lowery M et al. Glyceollin transcription factor GmMYB29A2 regulates soybean resistance to Phytophthora sojae. Plant Physiol. 2020;183:530–46.
Not in our library10.1104/pp.19.01293
181.
Yu Y, Guo D, Li G et al. The grapevine R2R3-type MYB transcription factor VdMYB1 positively regulates defense responses by activating the stilbene synthase gene 2 (VdSTS2). BMC Plant Biol. 2019;19:478.
Not in our library10.1186/s12870-019-1993-6
182.
Shan T, Rong W, Xu H et al. The wheat R2R3-MYB transcription factor TaRIM1 participates in resistance response against the pathogen Rhizoctonia cerealis infection through regulating defense genes. Sci Rep. 2016;6:28777.
Not in our library10.1038/srep28777
183.
Raffaele S, Vailleau F, Leger A et al. A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008;20:752–67.
Not in our library10.1105/tpc.107.054858
184.
Seo PJ, Park CM. MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol. 2010;186:471–83.
Not in our library10.1111/j.1469-8137.2010.03183.x
185.
Zhu L, Guo J, Ma Z et al. Arabidopsis transcription factor MYB102 increases plant susceptibility to aphids by substantial activation of ethylene biosynthesis. Biomol Ther. 2018;8:39.
Not in our library10.3390/biom8020039
186.
Segarra G, Van der Ent S, Trillas I et al. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol. 2009;11:90–6.
Not in our library10.1111/j.1438-8677.2008.00162.x
187.
Stringlis IA, Yu K, Fuessner K et al. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci U S A. 2018;115:E5213–22.
Not in our library10.1073/pnas.1722335115
188.
Lee MW, Qi M, Yang Y. A novel jasmonic acid-inducible rice MYB gene associates with fungal infection and host cell death. Mol Plant-Microbe Interact. 2001;14:527–35.
Not in our library10.1094/mpmi.2001.14.4.527
189.
Deng Y, Lu S. Biosynthesis and regulation of phenylpropanoids in plants. Front Plant Sci. 2017;36:257–90.
Not in our library
190.
Dong NQ, Lin HX. Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol. 2021;63:180–209.
Not in our library10.1111/jipb.13054
191.
Mitreiter S, Gigolashvili T. Regulation of glucosinolate biosynthesis. J Exp Bot. 2021;72:70–91.
Not in our library10.1093/jxb/eraa479
192.
Liu Y, Wang KL, Espley RV et al. StMYB44 negatively regulates anthocyanin biosynthesis at high temperatures in tuber flesh of potato. J Exp Bot. 2019;70:3809–24.
Not in our library10.1093/jxb/erz194
193.
Zhao Y, Ma J, Li M et al. Whole-genome resequencing-based QTL-seq identified AhTc1 gene encoding a R2R3-MYB transcription factor controlling peanut purple testa colour. Plant Biotechnol J. 2020;18:96–105.
Not in our library10.1111/pbi.13175
194.
Xi W, Feng J, Liu Y et al. The R2R3-MYB transcription factor PaMYB10 is involved in anthocyanin biosynthesis in apricots and determines red blushed skin. BMC Plant Biol. 2019;19.
Not in our library10.1186/s12870-019-1898-4
195.
Lai B, Du LN, Hu B et al. Characterization of a novel litchi R2R3-MYB transcription factor that involves in anthocyanin biosynthesis and tissue acidification. BMC Plant Biol. 2019;19:62.
Not in our library10.1186/s12870-019-1658-5
196.
Kubo H, Nozawa S, Hiwatashi T et al. Biosynthesis of riccionidins and marchantins is regulated by R2R3-MYB transcription factors in Marchantia polymorpha. J Plant Res. 2018;131:849–64.
Not in our library10.1007/s10265-018-1044-7
197.
Cao Y, Xie L, Ma Y et al. PpMYB15 and PpMYBF1 transcription factors are involved in regulating flavonol biosynthesis in peach fruit. J Agric Food Chem. 2019;67:644–52.
Not in our library10.1021/acs.jafc.8b04810
198.
Zhang Y, Ye J, Liu C et al. Citrus PH4-Noemi regulatory complex is involved in proanthocyanidin biosynthesis via a positive feedback loop. J Exp Bot. 2020;71:1306–21.
Not in our library10.1093/jxb/erz506
199.
Wu M, Xu X, Hu X et al. SlMYB72 regulates the metabolism of chlorophylls, carotenoids, and flavonoids in tomato fruit. Plant Physiol. 2020;183:854–68.
Not in our library10.1104/pp.20.00156
200.
Sun B, Zhu Z, Chen C et al. Jasmonate-inducible R2R3-MYB transcription factor regulates capsaicinoid biosynthesis and stamen development in capsicum. J Agric Food Chem. 2019;67:10891–903.
Not in our library10.1021/acs.jafc.9b04978
201.
Todesco M, Bercovich N, Kim A et al. Genetic basis and dual adaptive role of floral pigmentation in sunflowers. Elife. 2022;11:e72072.
Not in our library10.7554/elife.72072
202.
Deng C, Wang Y, Huang F et al. SmMYB2 promotes salvianolic acid biosynthesis in the medicinal herb Salvia miltiorrhiza. J Integr Plant Biol. 2020;62:1688–702.
Not in our library10.1111/jipb.12943
203.
Li Y, Shan X, Zhou L et al. The R2R3-MYB factor FhMYB5 from Freesia hybrida contributes to the regulation of anthocyanin and proanthocyanidin in biosynthesis. Front Plant Sci. 2019;9:1935.
Not in our library10.3389/fpls.2018.01935
204.
Li Y, Shan X, Tong L et al. The conserved and particular roles of R2R3-MYB regulator FhPAP1 from Freesia hybrida in flower anthocyanin biosynthesis. Plant Cell Physiol. 2020;61:1365–80.
Not in our library10.1093/pcp/pcaa065
205.
Li BJ, Zheng BQ, Wang JY et al. New insight into the molecular mechanism of colour differentiation among floral segments in orchids. Commun Biol. 2020;3:89.
Not in our library10.1038/s42003-020-0821-8
206.
Anwar M, Yu W, Yao H et al. NtMYB3, an R2R3-MYB from narcissus, regulates flavonoid biosynthesis. Int J Mol Sci. 2019;20:5456.
Not in our library10.3390/ijms20215456
207.
Zhao Q, Dixon RA. Transcriptional networks for lignin biosynthesis: more complex than we thought?Trends Plant Sci. 2011;16:227–33.
Not in our library10.1016/j.tplants.2010.12.005
208.
Sun Y, Ren S, Ye S et al. Identification and functional characterization of PtoMYB055 involved in the regulation of the lignin biosynthesis pathway in Populus tomentosa. Int J Mol Sci. 2020;21:4857.
Not in our library10.3390/ijms21144857
209.
Jiao B, Zhao X, Lu W et al. The R2R3 MYB transcription factor MYB189 negatively regulates secondary cell wall biosynthesis in Populus. Tree Physiol. 2019;39:1187–200.
Not in our library10.1093/treephys/tpz040
210.
Fornalé S, Sonbol FM, Maes T et al. Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors. Plant Mol Biol. 2006;62:809–23.
Not in our library10.1007/s11103-006-9058-2
211.
Huang J, Guo Y, Sun Q et al. Genome-wide identification of R2R3-MYB transcription factors regulating secondary cell wall thickening in cotton fiber development. Plant Cell Physiol. 2019;60:687–701.
Not in our library10.1093/pcp/pcy238
212.
Ye Y, Liu B, Zhao M et al. CEF1/OsMYB103L is involved in GA-mediated regulation of secondary wall biosynthesis in rice. Plant Mol Biol. 2015;89:385–401.
Not in our library10.1007/s11103-015-0376-0
213.
Xue C, Yao JL, Xue YS et al. PbrMYB169 positively regulates lignification of stone cells in pear fruit. J Exp Bot. 2019;70:1801–14.
Not in our library10.1093/jxb/erz039
214.
Zhang J, Ge H, Zhang C et al. EjODO1, a MYB transcription factor, regulating lignin biosynthesis in developing loquat (Eriobotrya japonica) fruit. Front Plant Sci. 2016a;7:1360–0.
Not in our library10.3389/fpls.2016.01360
215.
Seo MS, Kim JS. Understanding of MYB transcription factors involved in glucosinolate biosynthesis in Brassicaceae. Molecules. 2017;22:1549.
Not in our library10.3390/molecules22091549
216.
Augustine R, Mukhopadhyay A, Bisht NC. Targeted silencing of BjMYB28 transcription factor gene directs development of low glucosinolate lines in oilseed Brassica juncea. Plant Biotechnol J. 2013;11:855–66.
Not in our library10.1111/pbi.12078
217.
Araki R, Hasumi A, Sasaki K et al. Novel bioresources for studies of Brassica oleracea: identification of a kale MYB transcription factor responsible for glucosinolate production. Plant Biotechnol J. 2013;11:1017–27.
Not in our library10.1111/pbi.12095
218.
Liu Y, Zhou X, Yan M et al. Fine mapping and candidate gene analysis of a seed glucosinolate content QTL, qGSL-C2, in rapeseed (Brassica napus L.). Theor Appl Genet. 2020;133:479–90.
Not in our library10.1007/s00122-019-03479-x
219.
Yin J, Sun L, Li Y et al. Functional identification of BpMYB21 and BpMYB61 transcription factors responding to MeJA and SA in birch triterpenoid synthesis. BMC Plant Biol. 2020;20:374–4.
Not in our library10.1186/s12870-020-02521-1
220.
Hao X, Pu Z, Cao G et al. Tanshinone and salvianolic acid biosynthesis are regulated by SmMYB98 in Salvia miltiorrhiza hairy roots. J Adv Res. 2020;23:1–12.
Not in our library10.1016/j.jare.2020.01.012
221.
Liu L, Yang D, Xing B et al. SmMYB98b positive regulation to tanshinones in Salvia miltiorrhiza Bunge hairy roots. Plant Cell Tissue Organ Cult. 2020;140:459–67.
Not in our library
222.
Liu T, Luo T, Guo X et al. PgMYB2, a MeJA-responsive transcription factor, positively regulates the dammarenediol synthase gene expression in Panax Ginseng. Int J Mol Sci. 2019;20:2219.
Not in our library10.3390/ijms20092219
223.
Reddy VA, Wang Q, Dhar N et al. Spearmint R2R3−MYB transcription factor MsMYB negatively regulates monoterpene production and suppresses the expression of geranyl diphosphate synthase large subunit (MsGPPS. LSU). Plant Biotechnol J. 2017;15:1105–19.
Not in our library10.1111/pbi.12701
224.
Soler M, Corocha V, Cassan-Wang H et al. The Eucalyptus grandis R2R3-MYB transcription factor family: evidence for woody growth-related evolution and function. New Phytol. 2015;206:1364–77.
Not in our library10.1111/nph.13039
225.
Li X, Xue C, Li J et al. Genome-wide identification, evolution and functional divergence of MYB transcription factors in Chinese white pear (Pyrus bretschneideri). Plant Cell Physiol. 2016;57:824–47.
Not in our library10.1093/pcp/pcw029
226.
Zhao K, Bartley LE. Comparative genomic analysis of the R2R3 MYB secondary cell wall regulators of Arabidopsis, poplar, rice, maize, and switchgrass. BMC Plant Biol. 2014;14:135.
Not in our library10.1186/1471-2229-14-135
227.
Stracke R, Holtgrawe D, Schneider J et al. Genome-wide identification and characterisation of R2R3-MYB genes in sugar beet (Beta vulgaris). BMC Plant Biol. 2014;14:17.
Not in our library10.1186/s12870-014-0249-8
228.
Hatlestad GJ, Akhavan NA, Sunnadeniya RM et al. The beet Y locus encodes an anthocyanin MYB-like protein that activates the betalain red pigment pathway. Nat Genet. 2015;47:92.
Not in our library10.1038/ng.3163

Cited by papers we hold 1

The Transcription Factor MYB37 Positively Regulates Photosynthetic Inhibition and Oxidative Damage in Arabidopsis Leaves Under Salt Stress · 2022
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