Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 18, 2026.

Wounding in the plant tissue: the defense of a dangerous passage

Daniel V. Savatin, Giovanna Gramegna, Vanessa Modesti and 1 more

Frontiers in Plant Science · 2014 · Review

doi:10.3389/fpls.2014.00470

Abstract

Plants are continuously exposed to agents such as herbivores and environmental mechanical stresses that cause wounding and open the way to the invasion by microbial pathogens. Wounding provides nutrients to pathogens and facilitates their entry into the tissue and subsequent infection. Plants have evolved constitutive and induced defense mechanisms to properly respond to wounding and prevent infection. The constitutive defenses are represented by physical barriers, i.e., the presence of cuticle or lignin, or by metabolites that act as toxins or deterrents for herbivores. Plants are also able to sense the injured tissue as an altered self and induce responses similar to those activated by pathogen infection. Endogenous molecules released from wounded tissue may act as Damage-Associated Molecular Patterns (DAMPs) that activate the plant innate immunity. Wound-induced responses are both rapid, such as the oxidative burst and the expression of defense-related genes, and late, such as the callose deposition, the accumulation of proteinase inhibitors and of hydrolytic enzymes (i.e., chitinases and gluganases). Typical examples of DAMPs involved in the response to wounding are the peptide systemin, and the oligogalacturonides, which are oligosaccharides released from the pectic component of the cell wall. Responses to wounding take place both at the site of damage (local response) and systemically (systemic response) and are mediated by hormones such as jasmonic acid, ethylene, salicylic acid, and abscisic acid.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 18, 2026. Paragraph numbers are ours, so an answer can point at one.

INTRODUCTION

The sessile condition exposes plants to any possible environmental stress. Injury, one of the most frequent stress conditions that plants must face, may cause both loss of nutrients and entry of microbes. Therefore, plants have evolved sophisticated mechanisms to promptly respond to wounding, rapidly heal the tissue and prevent microbe infections. Unlike animals, plants do not have mobile cells specialized for defense, but each plant cell has the capability to activate protective mechanisms upon injury sensing. The capacity of cells to activate defense responses upon “danger” sensing and recognition of non-self microbe-associated molecular patterns (MAMPs) and/or endogenous damage-associated molecular patterns (DAMPs) is characteristic of the plant innate immunity. Defense responses activated by wounding are similar and overlapping with those activated by MAMPs and DAMPs, indicating that both injury and pathogens are limited by plants in a similar manner. Most of our knowledge on wounding derives from studies in which plants are mechanically damaged. Mechanical injury activates defenses that are similar to those induced by herbivores and insects, although the damage caused by herbivores has peculiar characteristics and mechanical wounding is necessary but not sufficient to trigger the full response activated by insects. Differences between mechanical wounding and attacks by herbivores and insects will be discussed in other reviews of this issue.

Plants contrast wounding with both constitutive structures, such as epicuticular films and crystals of wax, and secretory conduits for latices or resins, that restrict the access of opportunistic microorganisms to the tissue, as well as wound-induced responses that, unlike the constitutive defenses, are energetically costly and thereby regulated and triggered only when required. The primary events of the response to wounding occur at the injured site (local response) while the undamaged tissues respond later (systemic response), upon perception of mobile signals that communicate the existence of a critical condition. Extracellular signals such as cell wall-derived oligogalacturonides (OGs) and peptides, like systemin, have been characterized as typical signals of wounding. Genes involved in biosynthesis of jasmonic acid (JA) and ethylene (ET) as well as genes for general stress responses (oxidative stress, dehydration stress, heat-shock proteins, etc.) are rapidly induced. Later, events of protein turnover and transport processes involving aquaporins, lipid transfer proteins, ABC transporters, sugar, and peptide transporters occur. Finally, the modulation of primary metabolism (carbohydrate and lipid metabolism, nitrogen assimilation) and the expression of genes involved in the biosynthesis of secondary metabolites with repellent or anti-digestive activity [i.e., glucosinolates, cyanogenic glucosides, alkaloids, phenolics, and proteinase inhibitors (PI)] may occur. Transcriptional profiling analyses performed on 8.200 Arabidopsis genes revealed that approximately 8% of these genes are differential expressed after wounding and about 20% of the wounding-regulated genes encode proteins involved in signal transduction, such as members in the AP2, WRKY, and MYB families. A large fraction of the wound-responsive genes are also responsive to pathogens, suggesting that signaling pathways activated by these stimuli are shared (see below). This clearly indicates that an important reprograming of gene expression occurs in plants to defend the damaged tissue, which represents an easy passage for pathogen invasion. Receptors and signal transduction elements usually involved in pathogen response as well as several putative disease resistance genes (R genes) are up-regulated by wounding. This review is focused on what is currently known about the putative signals that are released upon wounding, on the mechanism of their perception and transduction and on plant defense responses activated upon injury sensing.

SENSING THE WOUNDING THROUGH THE CELL WALL INTEGRITY

The cuticle, composed of cutin and cuticular waxes, covers the outermost epidermal cell wall in the aerial portions of plants. The integrity of cuticle and cell wall (CWI) is affected by wounding and may be sensed by the plant cells. Studies on Arabidopsis plants expressing cutinase and on mutants impaired in cuticle biosynthesis have indicated that a more permeable cuticle allows the passage of diffusates with growth-inhibiting activity against phytopathogenic fungi. A breach in the cuticle caused by wounding also favors the diffusion of elicitors that, therefore, have an easier access to the cell surface, while an intact cuticle may prevent their passage from the surface. An early recognition of elicitors may lead to a prompt and efficient activation of the immune responses.

The cell wall is a dynamic structure that play a critical role in growth and development as well as in preventing wounding and pathogen attack. The perception of an altered CWI is a key event during wounding. Subtle modifications caused by physical perturbations such as light touch, soft mechanical stress, wind or contact with insects may be sensed at the level of the plasma membrane through stretch-activated mechano-sensitive channels that increase the intracellular Ca2+ concentration and trigger further signal transduction events. Expression of the Arabidopsis calcium channels MATING INDUCED DEATH 1 (MID1)-COMPLEMENTING ACTIVITY 1 (MCA1) and MCA2 in yeast complements the lethal effect of loss-of-function mutations in the MID1 and MID2 genes encoding stretch-activated calcium channels and promote calcium influx upon mechanical stimulation. Putative cation channels belonging to the GLUTAMATE RECEPTOR-LIKE (GLR) family, which mediate calcium influxes in response to MAMPs, are also required for the expression of several JA-inducible genes upon wounding in Arabidopsis.

Several Arabidopsis receptor like kinases (RLKs), among which those belonging to the Catharanthus roseus receptor-like kinase 1 family that includes THESEUS 1 (THE1), HERCULES 1, and FERONIA, have been proposed as possible sensors of CWI. Loss of THE1 function attenuates the growth defects and ectopic lignification phenotype caused by a mutation in the CELLULOSE SYNTHASE 6. Moreover, THE1 is involved in the accumulation of reactive oxygen species (ROS) and lignin deposition induced by isoxaben, an inhibitor of cellulose synthesis. This evidence clearly shows that defects in the cell wall caused by a disturbance of cellulose biosynthesis are sensed through THE1.

The monitoring of the status of pectin contributes to the sensing of CWI alterations. Plants carrying mutations that significantly alter pectin integrity, such as quasimodo 2 or tumorous shoot development 2, exhibit constitutive induction of defense responses. However, minor modifications in the methylation status, which occur in transgenic plants overexpressing the inhibitors of pectin methylesterases or in KO mutants of PECTIN METHYLESTERASE 3, do not influence the expression of defense genes. Possible indicator of an altered pectin integrity is the presence of OGs, a well-known class of DAMPs that, similarly to MAMPs, act as danger signals for the activation of the immune responses. OGs are released from the plant cell walls upon partial degradation of homogalacturonan, the main component of pectin, by wound-induced hydrolytic enzymes or, during infections, by microbial hydrolytic enzymes. The size of OGs is critical for their elicitor activity, being OGs with a degree of polymerization (DP) between 10 and 15 most active while shorter oligomers are inactive. OGs induce in several plant species a wide range of defense responses, including production of ROS, nitric oxide, phytoalexins, glucanase, chitinase, and callose. In tomato, OGs, probably generated by the action of a wound-inducible plant-derived polygalacturonase (PG; ), induce the accumulation of PI. OGs may act only locally, because their oligoanionic nature confers them a limited mobility in the tissues. In Arabidopsis, both wounding and OG treatment induce a strong local resistance against the necrotrophic fungus Botrytis cinerea that is independent of salicylic acid (SA)- and JA-mediated signaling. OGs also antagonize auxin responses, but the auxin-OG antagonism is uncoupled from their activity as defense elicitors. Indeed, the Arabidopsis mitogen-activated protein (MAP) kinase kinase kinases ANPs have been identified as elements in the OG-mediated induction of defenses, but do not play a major role in the inhibition of the auxin-induced gene expression.

OG sensing in Arabidopsis may involve wall-associated kinases (WAKs;; ). WAKs are RLKs consisting of an extracellular domain, containing epidermal growth factor repeats, a transmembrane domain and a cytoplasmic Ser/Thr kinase domain. The extracellular domain of WAK1 and WAK2 also contains an N-terminal portion that binds pectin in vitro. OGs with a DP > 9 bind reversibly WAK1 and the binding increases when OGs are present as dimers in a calcium-mediated “egg box” conformation. Five WAK genes are clustered on chromosome 1 and additional 21 WAK-like genes (WAKL) are present in Arabidopsis. WAK1, WAK2, WAKL5, and WAKL7 are induced by wounding. In rice, OsWAK1 is also induced by mechanical wounding as well as by SA and methyl-JA (MeJA) but not by abscisic acid (ABA; ). A role of WAK2 in the wound response was suggested by the analysis of gene expression in plants overexpressing WAK2 fused to a TAP epitope.

A lectin receptor kinase-I.9 (DORN1), which plays a role in the perception of extracellular ATP, is also involved in the wound responses. Indeed, ectopic expression of DORN1 enhances expression of genes co-regulated by wounding and ATP. A maize wound-induced gene encoding a leucine-rich RLK (WPK1) is involved in JA- and phytochrome-mediated signaling. In tobacco, a leucine-rich repeat RLK (WRK) is involved in the JA-dependent wound signaling and acts upstream of the SA- and wound-induced protein kinases SIPK and WIPK, respectively. WRK expression increases 15 min after wounding. WRK orthologs are present in dicots (Arabidopsis and tomato) but not in monocots (rice and wheat; ).

WOUND-ASSOCIATED DAMPs

Peptides that function as DAMPs have been isolated in wounded tissues. Systemin, a 18-aminoacid peptide, was identified in tomato after wounding or insect attack as a cleavage product released into the apoplast from prosystemin, i.e., a larger cytoplasmic precursor protein that accumulates in the cytosol of phloem parenchyma cells. Sensing of systemin activates the biosynthesis of JA, which, in turn, activates defenses responses in neighboring cells. The systemin receptor was identified as the tomato homolog of the brassinosteroid receptor BRI1, SR160, but more recent findings argued against this evidence. Hydroxyproline-rich systemins (HypSys) that trigger plant immunity during herbivore or pathogen attack have been identified in Solanaceae and in sweet potato. HypSys peptides, as systemin, are processed from precursor proteins which are induced by wounding.

A peptide, Pep1, was identified in Arabidopsis for its capability of inducing alkalinization in suspension-cultured cells. Pep1 is a 23-amino acid peptide released from the C-terminus of a 92 amino acid precursor protein, PROPEP1, which is induced by wounding, MeJA and ET. PROPEP1 belongs to a gene family of eight members. The family members PROPEP2 and PROPEP3, and, to a lesser extent, PROPEP1 are strongly induced by microbial pathogens such as B. cinerea, Phytophthora infestans, and Pseudomonas syringae as well as by various MAMPs and DAMPs elicitors, including NPP1, HrpZ, flg22, and OGs. PROPEPs are localized in the cytosol and the tonoplast and may function in the amplification/modulation of elicitor-triggered responses rather than being signals responsible for the initiation of the defense responses. Homologues of AtPeps have been identified in maize. ZmPep1 regulates disease responses whereas ZmPep3 triggers the biosynthesis of JA and ET and induces the production of anti-herbivore volatiles. AtPeps are perceived by two RLKs (PEPR1 and PEPR2), which share structural and functional similarity to the MAMP receptors FLS2 and EFR. PEPR1 and PEPR2 are induced by wounding and MeJA but not by SA and 1-aminocyclopropane-1-carboxylic acid (ACC) synthase. They are also differentially induced by DAMPs (AtPeps and OGs) and MAMP (flg22 and elf18;,;; ).

Cutin monomers, that are formed as a breakdown of the cuticle, have been proposed as signal molecules for the induction of disease resistance in cereals, i.e., barley and rice. Fungal pathogens such as Erysiphe graminis and Magnaporthe grisea are able to produce and secrete cutinases that facilitate the formation of cutin monomers in the infection site. Pretreated barley leaves with cutin monomers display acquired protection against E. graminis and evidences that free cutin monomers can be recognized by plant cells as endogenous stress-related signals were obtained in cultured potato cells.

SIGNAL TRANSDUCTION UPON WOUNDING

Many events triggered by wounding have been uncovered and are discussed here.

ELECTRIC SIGNALS

The involvement of electrical signals in the local and systemic alert in plants was postulated in 1992, when it was found that mechanical wounding in tomato cotyledons causes the transmission of a potential action to the first unwounded leaf concomitantly with the induction of PI proteins at the site of injury. More recently, it has been shown that mechanical wounding at the tips of Arabidopsis leaves generates, within a few seconds, wound-activated surface potential (WASP) changes that are consequent to a plasma membrane depolarization. The WASP signal first moves from tips toward the center of the rosette leaves and then to a restricted and selected number of distal leaves. For example, wounding at the tip of leaf no. 8 causes WASP changes of the same amplitude and duration in leaves no. 5, 11, 13, and 16 but not in other leaves. Both JA and JA-responsive gene expression increases with a total of 313 genes up-regulated both locally and systemically. GLR proteins, putative cation channels, are required for WASP propagation leading to defense gene expression. Similar WASP effects on JA levels and defense gene expression have been reported in tomato plants upon wounding. Electric signals that propagate over distances of 100 cm from the wounded site are generated in avocado trees.

ION FLUXES

One of the earliest responses (0.5–2 min) activated by the elicitors of plant defenses is the membrane depolarization following the influx of H+ and Ca2+ and a concomitant efflux of K+ and nitrate across the membrane. Injury-induced ion fluxes occur in both dicots such as Vicia faba and monocots such as Hordeum vulgare. Calcium spikes are critical for downstream signaling, since the physiological concentration of cytosolic calcium very rapidly increases after “danger” sensing. In plants, as in animals, calcium is a well-known second messenger. Plants discriminate among the various stimuli by generating “calcium signatures” that are characteristic in terms of sub-cellular localization, amplitude, duration and frequency. Intracellular peaks of calcium are detected in both epidermis and vascular cells proximal to the injury within 6 s. Signatures are decoded by three major types of sensor proteins: calmodulins (CAMs) and CAM-like proteins, calcineurin B-like proteins (CBL) and calcium-dependent protein kinases (CDPKs), a class of calcium sensors bearing both protein kinase and CAM-like domains in a single polypeptide. Different studies highlight the role of calcium sensors in plant immunity. For example, the Arabidopsis CAM binding protein (CBP) 60 g contributes to flg22-induced accumulation of SA and is involved in resistance against P. syringae; the rice CBL-interacting protein kinases (CIPKs) 14 and 15 are involved in various MAMP-induced immune responses; the potato and tobacco CDPKs participate in the activation of the oxidative burst. In Arabidopsis, CALCIUM-DEPENDENT PROTEIN KINASE 3 (CPK3) and CPK13 are required for defense gene induction upon feeding by the generalist herbivore Spodoptera littoralis. CPK3 is also activated by flg22 in Arabidopsis protoplasts suggesting that it is involved in MAMP signaling as well. In tomato, LeCDPK2 contributes to wound-triggered ET production by phosphorylating and activating the ET biosynthesis enzyme ACC SYNTHASE 2. In Nicotiana attenuata, CDPK4 and CDPK5 are negative regulators of JA synthesis; plants with silenced expression of these two CDPKs are more resistant to larvae of Manduca sexta and exhibit enhanced responses to mechanical wounding. MeJA, touching and mechanical wounding enhance a calcium-activated CDPK activity that induces systemic wound responses also in maize.

REACTIVE OXYGEN SPECIES

The production of ROS is a highly conserved process among aerobic organisms and is involved in defense and development processes of plants. ROS are emerging as signal molecules in plant immunity activation in response to both pathogens and wounding. In tomato, hydrogen peroxide is detected within 1 h after wounding and increases at 4–6 h both locally and in the upper unwounded leaves. OGs generated by a plant PG probably act as mediators of this process. A tomato mutant unable to properly respond to wounding neither induce PG nor generates hydrogen peroxide and is more susceptible to larvae of Manduca sexta. Given its toxicity, hydrogen peroxide must be tightly regulated to work as a signal molecule, and this is achieved through a complex mechanism involving calcium, protein phosphorylation, and production of ROS-scavenging enzymes that determine its steady-state levels in the cell. Wound-induced apoplastic hydrogen peroxide is produced by transmembrane NADPH oxidases (RBOHs) and by peroxidases, which also have a role in detoxification of other ROS. The C-terminal region of plant RBOHs contains cytosolic FAD- and NADPH-binding domains and six conserved transmembrane domains while the cytosolic N-terminal region contains two EF-hand motifs which bind calcium. Indeed, the wound-induced oxidative burst is dependent on calcium spikes and occurs also in the absence of the stimulus through artificially increasing the calcium levels in the cells. On the other hand, wound-related production of hydrogen peroxide is abolished by pretreatments with the calcium channel blocker verapamil or calcium chelators EGTA and oxalate. A calcium-dependent protein kinase CPK5 phosphorylates RBOHD and, probably, represents the link between calcium accumulation and ROS production. CPK5 phosphorylates in vitro and in vivo the N-terminal serine residues S39, S148, S163, and S347 of AtRBOHD while, in a contradicting report, ROS production triggered by pathogen infection is reduced in cpk1 cpk2 double mutant plants. RBOHD forms complexes with EFR and FLS2 as well as with the plasma membrane-associated kinase BOTRYTIS-INDUCED KINASE 1 (BIK1), which is also required for the protection conferred by wounding against pathogens. BIK1 directly interacts with and phosphorylates different residues of RBOHD in response to elicitors. In addition, RBOHF activity is regulated both through direct binding of Ca2+ to EF-hands and through calcium-dependent phosphorylation by CBL1/9-CIPK26 complexes.

MITOGEN-ACTIVATED PROTEIN KINASES (MAPKs)

Mitogen-activated protein kinase cascades amplify several abiotic and biotic stimuli leading to appropriate physiological responses. They consist of a core module of three kinases that perform sequential phosphorylation reactions: a MAP kinase kinase kinase (MAP3K) activates a MAP kinase kinase (MAP2K), which activates a MAPK. Involvement of MAPKs in wounding has been widely described in various plant species. In Arabidopsis, wounding activates MEKK1, MPK3, MPK19 and, consequently, MEKK1 phosphorylates MKK1. Wounding also activates MPK4 and MPK6 and plants overexpressing the PP2C-type phosphatase AP2C1, which dephosphorylates and inactivates MPK4 and MPK6, do not respond to wounding. On the contrary, ap2c1 mutants display enhanced responses to wounding and are more resistant to phytophagous mites (Tetranychus urticae; ). On the other hand, MPK8, which is activated through direct binding of CAMs in a Ca2+-dependent manner and through a MKK3-mediated phosphorylation, negatively regulate the expression of RBOHD and ROS homeostasis triggered by wounding. In tobacco, the SA-induced protein kinase kinase SIPKK and MPK4, which are orthologs of Arabidopsis MKK1/MKK2 and MPK4, respectively, are required for wound-induced expression of JA-responsive genes, being MPK4 activated by SIPKK. Moreover, WIPK and SIPK, which are orthologs of the Arabidopsis MPK3 and MPK6, respectively, are also involved in wounding signaling.

HORMONES

Wounding induces de novo synthesis of JA, ABA, and ET, which are known to activate a network of interconnected pathways that coordinate host defense responses. JA accumulates in wounded plants and activates expression of various defense genes such as those encoding PI, thionin, and enzymes involved in secondary metabolism. Jasmonates, including the active form jasmonoyl-isoleucine (JA-Ile), derive from plastidial fatty acids through at least 10 intermediates and the involvement of three cellular compartments. In Arabidopsis, wounding at leaf no. 8 promptly (90 s) induces an increase of JA amount in leaf no. 13, which shares a connected vasculature with leaf no. 8. Plant 13-lipoxygenases (13-LOXs) catalyze the first event in JA synthesis, i.e., the dioxygenation of fatty acids. In Arabidopsis, LOX2 is required for the JA synthesis proximal to the wound while LOX6 is required for JA and JA-Ile accumulation in the wounded as well as in the distal unwounded leaves. The conversion of JA to JA-Ile takes 50 s in the wounded leaf and about 100 s in the distal connected leaf no. 13. JA and JA-Ile accumulation in response to wounding have been demonstrated to be dependent on WASPs (see above, ). Another important step in JA synthesis is the accumulation of the JA precursor 12-oxo-phytodienoic acid (OPDA) catalyzed by allene oxidase (AOS), which is induced by tissue injury. In potato, two putative AOS genes, StAOS1 and StAOS2, are differentially induced upon wounding and are required for OPDA and JA accumulation both in wounded and in unchallenged tissues. A possible link between JA signaling and CWI alterations is suggested by the analysis of the Arabidopsis cev1 and cob mutants, which have defects in cellulose synthesis and deposition and produce higher amount of JAs. On the other hand, plants with a reduced expression of StAOS1 and StAOS2, and, consequently, a lower amount of OPDA, display reduced PME activity, increased methyl esterification level of pectins and an increased susceptibility to an hypovirulent strain of Dickeya dadantii. In tomato, JA is preferentially generated in vascular bundles and accumulates in the midrib of leaves. AOS and lipoxygenases are located in the companion-cell–sieve-element complex of the vascular bundle. Since systemin accumulates in phloem parenchyma cells and activates the octadecanoid pathway for JA biosynthesis, it may be hypothesized that perception of systemin on the surface of companion cells initiates the synthesis of JA that is rapidly transported along the phloem.

Abscisic acid is a stress hormone that mediates plant responses to drought and salinity as well as the expression of wound-induced PROTEINASE INHIBITOR II (PIN2) gene in tomato and potato. Moreover, ABA positively regulates programmed death in Arabidopsis leaf cells surrounding the wounding site to confine injury and/or pathogen infections. Spreading of programmed cell death from wounded sites is repressed by the transcription factor MYB108 or BOTRYTIS SENSITIVE1 (BOS1; ), and plants lacking this element exhibit mis-regulated cell death after wounding.

Ethylene production upon wounding has been documented. Among the early wound-induced genes there are several ACC synthase genes and many of ET response transcription factors, i.e., EREBPs. In tomato, ET and wound signaling, mediated by systemin and JA, have been reported to independently act on resistance against B. cinerea. ET and JA, besides mediating inducible defenses in response to wounding, have been also proposed to function in the trade-off between growth and defense and the associated changes in resource allocations.

LATE RESPONSES

Early intra- and inter-cellular events activated around the wounded site are required for late responses such as deposition of callose, suberin, lignin, and synthesis of various phenolics that may function both as a physical barrier and as antimicrobial substances. An Arabidopsis callose synthase, PMR4, is required for wound-induced callose formation. Callose is a (1→3)-β-D-glucan synthetized in all types of plant tissues in response to wounding. Its accumulation is dependent on the oxidative burst and occurs at the level of the cell wall either at wounded penetration sites or during attempted infections of fungi. Callose may also prevent the spread of viruses through plasmodesmata. Activity of both copper amine oxidases (CuAO) and flavin-containing amine oxidases (PAO), hydrogen peroxide-producing enzymes responsible for the oxidative de-amination of polyamines, appears to be important in wound healing in tobacco plants. CuAO mediates also the enhanced accumulation of cell wall phenolics, observed on wound surface in tobacco plants over-expressing a fungal endopolygalacturonase, which show constitutively activated defenses. This observation suggests an important role of polyamine catabolism-derived hydrogen peroxide in the response activated by a compromised pectin integrity. Reconstruction of damaged tissues often takes place upon wounding and involves vascular and/or other cells that may divide and differentiate to reunite the existing tissues. Moreover, active biosynthesis and accumulation of pectic substances has been described in the cell wall of the reunion region in the cortex in cucumber and tomato hypocotyls. The transcription factors RAP2.6L and ANAC071 are induced by ET and JA, differentially expressed around the injury site and are essential for tissue reunion of Arabidopsis wounded flowering stems.

CONCLUSION

Pathogens often utilize wounded tissues for their entry into the plant. Wounding is rapidly perceived through an efficient surveillance mechanism of tissue integrity followed by cell-to-cell communication and long-distance signaling. Every cell is able to rapidly produce and propagate different alert messages, such as WASPs and ROS waves (Figure 1), which rapidly prime the rest of the plant to set up defenses against the potential danger. Propagation occurs over long distances, between different parts of the same plant and even between different individuals through volatile molecules production. In the recent years several elements involved in sensing and signaling of wounding have been identified showing that the defense-related responses activated by wounding are comparable and almost overlapping with those activated after elicitor sensing. Thus, injury triggers a similar level of alert as a pathogen does, indicating that a breach in the physical barriers of the plant needs to be efficiently defended.

AUTHOR CONTRIBUTIONS

Daniel V. Savatin and Giovanna Gramegna contributed equally to the manuscript. Daniel V. Savatin, Giovanna Gramegna, and Vanessa Modesti wrote the initial draft of the manuscript. Daniel V. Savatin designed and drew (Figure 1). All authors discussed the content of 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 179

  1. 1.

    Akira S. Uematsu S. Takeuchi O. (2006 ). Pathogen recognition and innate immunity. Cell 124 783–801

    Not in our library10.1016/j.cell.2006.02.015

  2. 2.

    Andreou A. Feussner I. (2009 ). Lipoxygenases – structure and reaction mechanism. Phytochemistry 70 1504–1510

    Not in our library10.1016/j.phytochem.2009.05.008

  3. 3.

    Arimura G. Kost C. Boland W. (2005 ). Herbivore-induced, indirect plant defenses. Biochim. Biophys. Acta 1734 91–111

    Not in our library10.1016/j.bbalip.2005.03.001

  4. 4.

    Asahina M. Azuma K. Pitaksaringkarn W. Yamazaki T. Mitsuda N. Ohme-Takagi M. (2011 ). Spatially selective hormonal control of RAP2.6L and ANAC071 transcription factors involved in tissue reunion in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108 16128–16132

    Not in our library10.1073/pnas.1110443108

  5. 5.

    Asahina M. Iwai H. Kikuchi A. Yamaguchi S. Kamiya Y. Kamada H. (2002 ). Gibberellin produced in the cotyledon is required for cell division during tissue reunion in the cortex of cut cucumber and tomato hypocotyls. Plant Physiol. 129 201–210

    Not in our library10.1104/pp.010886

  6. 6.

    Bartels S. Lori M. Mbengue M. van Verk M. Klauser D. Hander T. (2013 ). The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J. Exp. Bot. 64 5309–5321

    Not in our library10.1093/jxb/ert330

  7. 7.

    Baydoun E. A. H. Fry S. C. (1985 ). The immobility of pectic substances in injured tomato leaves and its bearing on the identity of the wound hormone. Planta 165 269–276

    Not in our library10.1007/bf00395050

  8. 8.

    Bellincampi D. Cardarelli M. Zaghi D. Serino G. Salvi G. Gatz C. (1996 ). Oligogalacturonides prevent rhizogenesis in rol B transformed tobacco explants by inhibiting auxin-induced expression of the rol B gene. Plant Cell 8 477–487

    Not in our library10.1105/tpc.8.3.477

  9. 9.
    Plant cell wall dynamics and wall-related susceptibility in plant–pathogen interactions · 2014
    No notice
  10. 10.

    Bellincampi D. Dipierro N. Salvi G. Cervone F. De Lorenzo G. (2000 ). Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol. 122 1379–1385

    Not in our library10.1104/pp.122.4.1379

  11. 11.

    Beneloujaephajri E. Costa A. L’Haridon F. Metraux J. P. Binda M. (2013 ). Production of reactive oxygen species and wound-induced resistance in Arabidopsis thaliana against Botrytis cinerea are preceded and depend on a burst of calcium. BMC Plant Biol. 13:160

    Not in our library10.1186/1471-2229-13-160

  12. 12.

    Benikhlef L. L’Haridon F. Abou-Mansour E. Serrano M. Binda M. Costa A. (2013 ). Perception of soft mechanical stress in Arabidopsis leaves activates disease resistance. BMC Plant Biol. 13:133

    Not in our library10.1186/1471-2229-13-133

  13. 13.

    Benitez-Alfonso Y. Jackson D. Maule A. (2011 ). Redox regulation of intercellular transport. Protoplasma 248 131–140

    Not in our library10.1007/s00709-010-0243-4

  14. 14.

    Bergey D. R. Howe G. A. Ryan C. A. (1996 ). Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc. Natl. Acad. Sci. U.S.A. 93 12053–12058

    Not in our library10.1073/pnas.93.22.12053

  15. 15.
    A wound- and systemin-inducible polygalacturonase in tomato leaves · 1999
    Not checked
  16. 16.

    Bessire M. Chassot C. Jacquat A. C. Humphry M. Borel S. Petetot J. M. (2007 ). A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 26 2158–2168

    Not in our library10.1038/sj.emboj.7601658

  17. 17.

    Bhattacharya R. Koramutla M. K. Negi M. Pearce G. Ryan C. A. (2013 ). Hydroxyproline-rich glycopeptide signals in potato elicit signaling associated with defense against insects and pathogens. Plant Sci. 207 88–97

    Not in our library10.1016/j.plantsci.2013.03.002

  18. 18.

    Boller T. Felix G. (2009 ). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60 379–406

    Not in our library10.1146/annurev.arplant.57.032905.105346

  19. 19.

    Bonaventure G. Baldwin I. T. (2010 ). Transduction of wound and herbivory signals in plastids. Commun. Integr. Biol. 3 313–317

    Not in our library10.4161/cib.3.4.11834

  20. 20.

    Bostock R. M. Stermer B. A. (1989 ). Perspectives on wound healing in resistance to pathogens. Annu. Rev. Phytopathol. 27 343–371

    Not in our library10.1146/annurev.py.27.090189.002015

  21. 21.

    Boudsocq M. Willmann M. R. McCormack M. Lee H. Shan L. He P. (2010 ). Differential innate immune signaling via Ca2+ sensor protein kinases. Nature 464 418–422

    Not in our library10.1038/nature08794

  22. 22.

    Bouquin T. Lasserre E. Pradier J. Pech J. C. Balague C. (1997 ). Wound and ethylene induction of the ACC oxidase melon gene CM-ACO1 occurs via two direct and independent transduction pathways. Plant Mol. Biol. 35 1029–1035

    Not in our library10.1023/a:1005902226054

  23. 23.

    Branca C. De Lorenzo G. Cervone F. (1988 ). Competitive inhibition of the auxin-induced elongation by α-D-oligogalacturonides in pea stem segments. Physiol. Plant. 72 499–504

    Not in our library10.1111/j.1399-3054.1988.tb09157.x

  24. 24.

    Browse J. (2009 ). The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry 70 1539–1546

    Not in our library10.1016/j.phytochem.2009.08.004

  25. 25.

    Brutus A. Sicilia F. Macone A. Cervone F. De Lorenzo G. (2010 ). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. U.S.A. 107 9452–9457

    Not in our library10.1073/pnas.1000675107

  26. 26.

    Cabrera J. C. Boland A. Messiaen J. Cambier P. Van Cutsem P. (2008 ). Egg box conformation of oligogalacturonides: the time-dependent stabilization of the elicitor-active conformation increases its biological activity. Glycobiology 18 473–482

    Not in our library10.1093/glycob/cwn027

  27. 27.

    Chassot C. Nawrath C. Metraux J. P. (2007 ). Cuticular defects lead to full immunity to a major plant pathogen. Plant J. 49 972–980

    Not in our library10.1111/j.1365-313x.2006.03017.x

  28. 28.

    Chauvin A. Caldelari D. Wolfender J. L. Farmer E. E. (2013 ). Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol. 197 566–575

    Not in our library10.1111/nph.12029

  29. 29.

    Chen X. Y. Kim J. Y. (2009 ). Callose synthesis in higher plants. Plant Signal. Behav. 4 489–492

    Not in our library10.4161/psb.4.6.8359

  30. 30.

    Chen Y. C. Siems W. F. Pearce G. Ryan C. A. (2008 ). Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J. Biol. Chem. 283 11469–11476

    Not in our library10.1074/jbc.m709002200

  31. 31.

    Cheong Y. H. Chang H. S. Gupta R. Wang X. Zhu T. Luan S. (2002 ). Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129 661–677

    Not in our library10.1104/pp.002857

  32. 32.

    Choi J. Tanaka K. Cao Y. R. Qi Y. Qiu J. Liang Y. (2014 ). Identification of a plant receptor for extracellular ATP. Science 343 290–294

    Not in our library10.1126/science.343.6168.290

  33. 33.

    Cona A. Tisi A. Ghuge S. A. Franchi S. De Lorenzo G. Angelini R. (2014 ). Wound healing response and xylem differentiation in tobacco plants over-expressing a fungal endopolygalacturonase is mediated by copper amine oxidase activity. Plant Physiol. Biochem. 82 54–65

    Not in our library10.1016/j.plaphy.2014.05.004

  34. 34.

    Craigon D. J. James N. Okyere J. Higgins J. Jotham J. May S. (2004 ). NASCArrays: a repository for microarray data generated by NASC’s transcriptomics service. Nucleic Acids Res. 32 D575–D577

    Not in our library10.1093/nar/gkh133

  35. 35.

    Creelman R. A. Mullet J. E. (1997 ). Biosynthesis and action of jasmonates in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48 355–381

    Not in our library10.1146/annurev.arplant.48.1.355

  36. 36.

    Cui F. Brosche M. Sipari N. Tang S. Overmyer K. (2013 ). Regulation of ABA dependent wound induced spreading cell death by MYB108. New Phytol. 200 634–640

    Not in our library10.1111/nph.12456

  37. 37.

    Daudi A. Cheng Z. Y. O’Brien J. A. Mammarella N. Khan S. Ausubel F. M. (2012 ). The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24 275–287

    Not in our library10.1105/tpc.111.093039

  38. 38.

    De Lorenzo G. Brutus A. Savatin D. V. Sicilia F. Cervone F. (2011 ). Engineering plant resistance by constructing chimeric receptors that recognize damage-associated molecular patterns (DAMPs). FEBS Lett. 585 1521–1528

    Not in our library10.1016/j.febslet.2011.04.043

  39. 39.

    Decreux A. Messiaen J. (2005 ). Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol. 46 268–278

    Not in our library10.1093/pcp/pci026

  40. 40.

    Delessert C. Wilson I. W. Van Der S. D. Dennis E. S. Dolferus R. (2004 ). Spatial and temporal analysis of the local response to wounding in Arabidopsis leaves. Plant Mol. Biol. 55 165–181

    Not in our library10.1007/s11103-004-0112-7

  41. 41.

    Dengler N. Kang J. (2001 ). Vascular patterning and leaf shape. Curr. Opin. Plant Biol. 4 50–56

    Not in our library10.1016/s1369-5266(00)00135-7

  42. 42.

    Denness L. McKenna J. F. Segonzac C. Wormit A. Madhou P. Bennett M. (2011 ). Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol. 156 1364–1374

    Not in our library10.1104/pp.111.175737

  43. 43.

    Denoux C. Galletti R. Mammarella N. Gopalan S. Werck D. De Lorenzo G. (2008 ). Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1 423–445

    Not in our library10.1093/mp/ssn019

  44. 44.

    Diaz J. ten Have A. van Kan J. A. (2002 ). The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol. 129 1341–1351

    Not in our library10.1104/pp.001453

  45. 45.

    Drerup M. M. Schlucking K. Hashimoto K. Manishankar P. Steinhorst L. Kuchitsu K. (2013 ). The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol. Plant 6 559–569

    Not in our library10.1093/mp/sst009

  46. 46.

    Dubiella U. Seybold H. Durian G. Komander E. Lassig R. Witte C. P. (2013 ). Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc. Natl. Acad. Sci. U.S.A. 110 8744–8749

    Not in our library10.1073/pnas.1221294110

  47. 47.

    Ellis C. Karafyllidis I. Wasternack C. Turner J. G. (2002 ). The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14 1557–1566

    Not in our library10.1105/tpc.002022

  48. 48.

    Farmer E. E. Ryan C. A. (1992 ). Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4 129–134

    Not in our library10.1105/tpc.4.2.129

  49. 49.

    Ferrari S. Galletti R. Denoux C. De Lorenzo G. Ausubel F. M. Dewdney J. (2007 ). Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol. 144 367–379

    Not in our library10.1104/pp.107.095596

  50. 50.

    Ferrari S. Galletti R. Pontiggia D. Manfredini C. Lionetti V. Bellincampi D. (2008 ). Transgenic expression of a fungal endo-polygalacturonase increases plant resistance to pathogens and reduces auxin sensitivity. Plant Physiol. 146 669–681

    Not in our library10.1104/pp.107.109686

  51. 51.
    Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development · 2013
    No notice
  52. 52.

    Finkelstein R. (2013 ). Abscisic acid synthesis and response. Arabidopsis Book 11:e0166

    Not in our library10.1199/tab.0166

  53. 53.

    Fonseca S. Chico J. M. Solano R. (2009 ). The jasmonate pathway: the ligand, the receptor and the core signalling module. Curr. Opin. Plant Biol. 12 539–547

    Not in our library10.1016/j.pbi.2009.07.013

  54. 54.

    Galletti R. Denoux C. Gambetta S. Dewdney J. Ausubel F. M. De Lorenzo G. (2008 ). The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol. 148 1695–1706

    Not in our library10.1104/pp.108.127845

  55. 55.
    Bifurcation of Arabidopsis NLR Immune Signaling via Ca2+-Dependent Protein Kinases · 2013
    No notice
  56. 56.

    Glauser G. Dubugnon L. Mousavi S. A. Rudaz S. Wolfender J. L. Farmer E. E. (2009 ). Velocity estimates for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol. Chem. 284 34506–34513

    Not in our library10.1074/jbc.m109.061432

  57. 57.

    Gomi K. Ogawa D. Katou S. Kamada H. Nakajima N. Saji H. (2005 ). A mitogen-activated protein kinase NtMPK4 activated by SIPKK is required for jasmonic acid signaling and involved in ozone tolerance via stomatal movement in tobacco. Plant Cell Physiol. 46 1902–1914

    Not in our library10.1093/pcp/pci211

  58. 58.

    Guo H. Q. Li L. Ye H. X. Yu X. F. Algreen A. Yin Y. H. (2009 ). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 106 7648–7653

    Not in our library10.1073/pnas.0812346106

  59. 59.

    Hadiarto T. Nanmori T. Matsuoka D. Iwasaki T. Sato K. Fukami Y. (2006 ). Activation of Arabidopsis MAPK kinase kinase (AtMEKK1) and induction of AtMEKK1-AtMEK1 pathway by wounding. Planta 223 708–713

    Not in our library10.1007/s00425-005-0126-7

  60. 60.

    Harper J. F. Harmon A. (2005 ). Plants, symbiosis and parasites: A calcium signalling connection. Nat. Rev. Mol. Cell Biol. 6 555–566

    Not in our library10.1038/nrm1679

  61. 61.

    Haswell E. S. Peyronnet R. Barbier-Brygoo H. Meyerowitz E. M. Frachisse J. M. (2008 ). Two MscS homologs provide mechanosensitive channel activities in the Arabidopsis root. Curr. Biol. 18 730–734

    Not in our library10.1016/j.cub.2008.04.039

  62. 62.

    Hause B. Hause G. Kutter C. Miersch O. Wasternack C. (2003 ). Enzymes of jasmonate biosynthesis occur in tomato sieve elements. Plant Cell Physiol. 44 643–648

    Not in our library10.1093/pcp/pcg072

  63. 63.

    He G. Z. Tarui Y. Iino M. (2005 ). A novel receptor kinase involved in jasmonate-mediated wound and phytochrome signaling in maize coleoptiles. Plant Cell Physiol. 46 870–883

    Not in our library10.1093/pcp/pci092

  64. 64.

    Heiling S. Schuman M. C. Schoettner M. Mukerjee P. Berger B. Schneider B. (2010 ). Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. Plant Cell 22 273–292

    Not in our library10.1105/tpc.109.071449

  65. 65.

    Hematy K. Sado P. E. Van Tuinen A. Rochange S. Desnos T. Balzergue S. (2007 ). A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17 922–931

    Not in our library10.1016/j.cub.2007.05.018

  66. 66.

    Herde O. Atzorn R. Fisahn J. Wasternack C. Willmitzer L. Peña-Cortés H. (1996 ). Localized wounding by heat initiates the accumulation of proteinase inhibitor II in abscisic acid-deficient plants by triggering jasmonic acid biosynthesis. Plant Physiol. 112 853–860

    Not in our library10.1104/pp.112.2.853

  67. 67.

    Hind S. R. Malinowski R. Yalamanchili R. Stratmann J. W. (2010 ). Tissue-type specific systemin perception and the elusive systemin receptor. Plant Signal. Behav. 5 42–44

    Not in our library10.4161/psb.5.1.10119

  68. 68.

    Huffaker A. Dafoe N. J. Schmelz E. A. (2011 ). ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol. 155 1325–1338

    Not in our library10.1104/pp.110.166710

  69. 69.

    Huffaker A. Pearce G. Ryan C. A. (2006 ). An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. U.S.A. 103 10098–10103

    Not in our library10.1073/pnas.0603727103

  70. 70.

    Huffaker A. Pearce G. Veyrat N. Erb M. Turlings T. C. J. Sartor R. (2013 ). Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc. Natl. Acad. Sci. U.S.A. 110 5707–5712

    Not in our library10.1073/pnas.1214668110

  71. 71.

    Ichimura K. Mizoguchi T. Yoshida R. Yuasa T. Shinozaki K. (2000 ). Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 24 655–665

    Not in our library10.1046/j.1365-313x.2000.00913.x

  72. 72.

    Ito N. Takabatake R. Seo S. Hiraga S. Mitsuhara I. Ohashi Y. (2002 ). Induced expression of a temperature-sensitive leucine-rich repeat receptor-like protein kinase gene by hypersensitive cell death and wounding in tobacco plant carrying the N resistance gene. Plant Cell Physiol. 43 266–274

    Not in our library10.1093/pcp/pcf031

  73. 73.

    Jacinto T. McGurl B. Franceschi V. Delano-Freier J. Ryan C. A. (1997 ). Tomato prosystemin promoter confers wound-inducible, vascular bundle-specific expression of the β-glucuronidase gene in transgenic tomato plants. Planta 203 406–412

    Not in our library10.1007/s004250050207

  74. 74.

    Jacobs A. K. Lipka V. Burton R. A. Panstruga R. Strizhov N. Schulze-Lefert P. (2003 ). An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15 2503–2513

    Not in our library10.1105/tpc.016097

  75. 75.

    Kadota Y. Sklenar J. Derbyshire P. Stransfeld L. Asai S. Ntoukakis V. (2014 ). Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54 43–55

    Not in our library10.1016/j.molcel.2014.02.021

  76. 76.

    Kamiyoshihara Y. Iwata M. Fukaya T. Tatsuki M. Mori H. (2010 ). Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation. Plant J. 64 140–150

    Not in our library10.1111/j.1365-313x.2010.04316.x

  77. 77.

    Kanchiswamy C. N. Takahashi H. Quadro S. Maffei M. E. Bossi S. Bertea C. (2010 ). Regulation of Arabidopsis defense responses against Spodoptera littoralis by CPK-mediated calcium signaling. BMC Plant Biol. 10:97

    Not in our library10.1186/1471-2229-10-97

  78. 78.

    Kanzaki M. Nagasawa M. Kojima I. Sato C. Naruse K. Sokabe M. (1999 ). Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285 882–886

    Not in our library10.1126/science.285.5429.882

  79. 79.

    Ketela T. Green R. Bussey H. (1999 ). Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J. Bacteriol. 181 3330–3340

    Not in our library10.1128/jb.181.11.3330-3340.1999

  80. 80.

    Kimura S. Kaya H. Kawarazaki T. Hiraoka G. Senzaki E. Michikawa M. (2012 ). Protein phosphorylation is a prerequisite for the Ca2+-dependent activation of Arabidopsis NADPH oxidases and may function as a trigger for the positive feedback regulation of Ca2+ and reactive oxygen species. Biochim. Biophys. Acta 1823 398–405

    Not in our library10.1016/j.bbamcr.2011.09.011

  81. 81.

    Ko J. H. Kim J. H. Jayanty S. S. Howe G. A. Han K. H. (2006 ). Loss of function of COBRA, a determinant of oriented cell expansion, invokes cellular defense responses in Arabidopsis thaliana. J. Exp. Bot. 57 2923–2936

    Not in our library10.1093/jxb/erl052

  82. 82.

    Kobayashi M. Ohura I. Kawakita K. Yokota N. Fujiwara M. Shimamoto K. (2007 ). Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19 1065–1080

    Not in our library10.1105/tpc.106.048884

  83. 83.

    Kobayashi M. Yoshioka M. Asai S. Nomura H. Kuchimura K. Mori H. (2012 ). StCDPK5 confers resistance to late blight pathogen but increases susceptibility to early blight pathogen in potato via reactive oxygen species burst. New Phytol. 196 223–237

    Not in our library10.1111/j.1469-8137.2012.04226.x

  84. 84.

    Kohorn B. D. Johansen S. Shishido A. Todorova T. Martinez R. Defeo E. (2009 ). Pectin activation of MAP kinase and gene expression is WAK2 dependent. Plant J. 60 974–982

    Not in our library10.1111/j.1365-313x.2009.04016.x

  85. 85.
    The Cell Wall Associated Kinases, WAKs, As Pectin Receptors · 2012
    Not checked
  86. 86.

    Kohorn B. D. Kohorn S. L. Todorova T. Baptiste G. Stansky K. McCullough M. (2012 ). A dominant allele of Arabidopsis pectin-binding wall-associated kinase induces a stress response suppressed by MPK6 but not MPK3 mutations. Mol. Plant 5 841–851

    Not in our library10.1093/mp/ssr096

  87. 87.

    Komarova T. V. Sheshukova E. V. Dorokhov Y. L. (2014 ). Cell wall methanol as a signal in plant immunity. Front. Plant Sci. 5:101

    Not in our library10.3389/fpls.2014.00101

  88. 88.

    Krautz R. Arefin B. Theopold U. (2014 ). Damage signals in the insect immune response. Front. Plant Sci. 5:342

    Not in our library10.3389/fpls.2014.00342

  89. 89.

    Krol E. Mentzel T. Chinchilla D. Boller T. Felix G. Kemmerling B. (2010 ). Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 285 13471–13479

    Not in our library10.1074/jbc.m109.097394

  90. 90.

    Krupkova E. Immerzeel P. Pauly M. Schmulling T. (2007 ). The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J. 50 735–750

    Not in our library10.1111/j.1365-313x.2007.03123.x

  91. 91.

    Kudla J. Batistic O. Hashimoto K. (2010 ). Calcium signals: the lead currency of plant information processing. Plant Cell 22 541–563

    Not in our library10.1105/tpc.109.072686

  92. 92.

    Kurusu T. Hamada J. Nokajima H. Kitagawa Y. Kiyoduka M. Takahashi A. (2010 ). Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol. 153 678–692

    Not in our library10.1104/pp.109.151852

  93. 93.

    Kwaaitaal M. Huisman R. Maintz J. Reinstadler A. Panstruga R. (2011 ). Ionotropic glutamate receptor (iGluR)-like channels mediate MAMP-induced calcium influx in Arabidopsis thaliana. Biochem. J. 440 355–365

    Not in our library10.1042/bj20111112

  94. 94.
    A Permeable Cuticle Is Associated with the Release of Reactive Oxygen Species and Induction of Innate Immunity · 2011
    No notice
  95. 95.

    Laluk K. Luo H. L. Chai M. F. Dhawan R. Lai Z. B. Mengiste T. (2011 ). Biochemical and genetic requirements for function of the immune response regulator BOTRYTIS-INDUCED KINASE1 in plant growth, ethylene signaling, and PAMP-triggered immunity in Arabidopsis. Plant Cell 23 2831–2849

    Not in our library10.1105/tpc.111.087122

  96. 96.

    Lecourieux D. Ranjeva R. Pugin A. (2006 ). Calcium in plant defense-signaling pathways. New Phytol. 171 249–269

    Not in our library10.1111/j.1469-8137.2006.01777.x

  97. 97.

    Leon J. Rojo E. Sanchez-Serrano J. J. (2001 ). Wound signaling in plants. J. Exp. Bot. 52 1–9

    Not in our library10.1093/jexbot/52.354.1

  98. 98.

    Li H. Zhou S. Y. Zhao W. S. Su S. C. Peng Y. L. (2008 ). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol. Biol. 69 337–346

    Not in our library10.1007/s11103-008-9430-5

  99. 99.

    Lionetti V. Cervone F. Bellincampi D. (2012 ). Methyl esterification of pectin plays a role during plant-pathogen interactions and affects plant resistance to diseases. J. Plant Physiol. 169 1623–1630

    Not in our library10.1016/j.jplph.2012.05.006

  100. 100.

    Lionetti V. Francocci F. Ferrari S. Volpi C. Bellincampi D. Galletti R. (2010 ). Engineering the cell wall by reducing de-methyl-esterified homogalacturonan improves saccharification of plant tissues for bioconversion. Proc. Natl. Acad. Sci. U.S.A. 107 616–621

    Not in our library10.1073/pnas.0907549107

  101. 101.

    Lionetti V. Raiola A. Camardella L. Giovane A. Obel N. Pauly M. (2007 ). Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by botrytis cinerea. Plant Physiol. 143 1871–1880

    Not in our library10.1104/pp.106.090803

  102. 102.

    Liu J. H. Lee-Tamon S. H. Reid D. M. (1997 ). Differential and wound-inducible expression of 1-aminocylopropane-1-carboxylate oxidase genes in sunflower seedlings. Plant Mol. Biol. 34 923–933

    Not in our library10.1023/a:1005801420172

  103. 103.

    Luan S. (2009 ). The CBL-CIPK network in plant calcium signaling. Trends Plant Sci. 14 37–42

    Not in our library10.1016/j.tplants.2008.10.005

  104. 104.

    Luan S. Kudla J. Rodriguez-Concepcion M. Yalovsky S. Gruissem W. (2002 ). Calmodulins and calcineurin B-like proteins: calcium sensors for specific signal response coupling in plants. Plant Cell 14 S389–S400

    Not in our library10.1105/tpc.001115

  105. 105.

    Ludwig A. A. Saitoh H. Felix G. Freymark G. Miersch O. Wasternack C. (2005 ). Ethylene-mediated cross-talk between calcium-dependent protein kinase and MAPK signaling controls stress responses in plants. Proc. Natl. Acad. Sci. U.S.A. 102 10736–10741

    Not in our library10.1073/pnas.0502954102

  106. 106.

    Maffei M. E. Mithofer A. Boland W. (2007 ). Before gene expression: early events in plant-insect interaction. Trends Plant Sci. 12 310–316

    Not in our library10.1016/j.tplants.2007.06.001

  107. 107.

    Mengiste T. Chen X. Salmeron J. Dietrich R. (2003 ). The BOTRYTIS SUSCEPTIBLE1 gene encodes an R2R3MYB transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell 15 2551–2565

    Not in our library10.1105/tpc.014167

  108. 108.

    Minibayeva F. Beckett R. P. Kranner I. (2014 ). Roles of apoplastic peroxidases in plant response to wounding. Phytochemistry [Epub ahead of print]

    Not in our library10.1016/j.phytochem.2014.06.008

  109. 109.

    Mithofer A. Ebel J. Felle H. H. (2005 ). Cation fluxes cause plasma membrane depolarization involved in beta-glucan elicitor-signaling in soybean roots. Mol. Plant Microbe Interact. 18 983–990

    Not in our library10.1094/mpmi-18-0983

  110. 110.

    Mittler R. Vanderauwera S. Suzuki N. Miller G. Tognetti V. B. Vandepoele K. (2011 ). ROS signaling: the new wave? Trends Plant Sci. 16 300–309

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

  111. 111.

    Monshausen G. B. Bibikova T. N. Messerli M. A. Shi C. Gilroy S. (2007 ). Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl. Acad. Sci. U.S.A. 104 20996–21001

    Not in our library10.1073/pnas.0708586104

  112. 112.

    Mouille G. Ralet M. C. Cavelier C. Eland C. Effroy D. Hematy K. (2007 ). Homogalacturonan synthesis in Arabidopsis thaliana requires a Golgi-localized protein with a putative methyltransferase domain. Plant J. 50 605–614

    Not in our library10.1111/j.1365-313x.2007.03086.x

  113. 113.

    Mousavi S. A. R. Chauvin A. Pascaud F. Kellenberger S. Farmer E. E. (2013 ). GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500 422–426

    Not in our library10.1038/nature12478

  114. 114.

    Nakagami H. Pitzschke A. Hirt H. (2005 ). Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci. 10 339–346

    Not in our library10.1016/j.tplants.2005.05.009

  115. 115.

    Nakagawa Y. Katagiri T. Shinozaki K. Qi Z. Tatsumi H. Furuichi T. (2007 ). Arabidopsis plasma membrane protein crucial for Ca2+ influx and touch sensing in roots. Proc. Natl. Acad. Sci. U.S.A. 104 3639–3644

    Not in our library10.1073/pnas.0607703104

  116. 116.

    Narvaez-Vasquez J. Pearce G. Ryan C. A. (2005 ). The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc. Natl. Acad. Sci. U.S.A. 102 12974–12977

    Not in our library10.1073/pnas.0505248102

  117. 117.

    Narvaez-Vasquez J. Ryan C. A. (2004 ). The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 218 360–369

    Not in our library10.1007/s00425-003-1115-3

  118. 118.

    Nawrath C. (2006 ). Unraveling the complex network of cuticular structure and function. Curr. Opin. Plant Biol. 9 281–287

    Not in our library10.1016/j.pbi.2006.03.001

  119. 119.

    Nemoto K. Seto T. Takahashi H. Nozawa A. Seki M. Shinozaki K. (2011 ). Autophosphorylation profiling of Arabidopsis protein kinases using the cell-free system. Phytochemistry 72 1136–1144

    Not in our library10.1016/j.phytochem.2011.02.029

  120. 120.

    Nuhse T. S. (2012 ). Cell wall integrity signaling and innate immunity in plants. Front. Plant Sci. 3:280

    Not in our library10.3389/fpls.2012.00280

  121. 121.

    Nurnberger T. Brunner F. Kemmerling B. Piater L. (2004 ). Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198 249–266

    Not in our library10.1111/j.0105-2896.2004.0119.x

  122. 122.

    O’Brien J. A. Daudi A. Butt V. S. Bolwell G. P. (2012 ). Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236 765–779

    Not in our library10.1007/s00425-012-1696-9

  123. 123.

    O’Donnell P. J. Calvert C. Atzorn R. Wasternack C. Leyser H. M. O. Bowles D. J. (1996 ). Ethylene as a signal mediating the wound response of tomato plants. Science 274 1914–1917

    Not in our library10.1126/science.274.5294.1914

  124. 124.

    Oda T. Hashimoto H. Kuwabara N. Akashi S. Hayashi K. Kojima C. (2010 ). Structure of the N-terminal regulatory domain of a plant NADPH oxidase and its functional implications. J. Biol. Chem. 285 1435–1445

    Not in our library10.1074/jbc.m109.058909

  125. 125.

    Onkokesung N. Baldwin I. T. Galis I. (2010 ). The role of jasmonic acid and ethylene crosstalk in direct defense of Nicotiana attenuata plants against chewing herbivores. Plant Signal. Behav. 5 1305–1307

    Not in our library10.4161/psb.5.10.13124

  126. 126.

    Orozco-Cardenas M. McGurl B. Ryan C. A. (1993 ). Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc. Natl. Acad. Sci. U.S.A. 90 8273–8276

    Not in our library10.1073/pnas.90.17.8273

  127. 127.

    Orozco-Cardenas M. Ryan C. A. (1999 ). Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. U.S.A. 96 6553–6655

    Not in our library10.1073/pnas.96.11.6553

  128. 128.

    Oyarce P. Gurovich L. (2011 ). Evidence for the transmission of information through electric potentials in injured avocado trees. J. Plant Physiol. 168 103–108

    Not in our library10.1016/j.jplph.2010.06.003

  129. 129.

    Pearce G. Bhattacharya R. Chen Y. C. Barona G. Yamaguchi Y. Ryan C. A. (2009 ). Isolation and characterization of hydroxyproline-rich glycopeptide signals in black nightshade leaves. Plant Physiol. 150 1422–1433

    Not in our library10.1104/pp.109.138669

  130. 130.

    Pearce G. Moura D. S. Stratmann J. Ryan C. A. (2001 ). Production of multiple plant hormones from a single polyprotein precursor. Nature 411 817–820

    Not in our library10.1038/35081107

  131. 131.

    Pearce G. Ryan C. A. (2003 ). Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J. Biol. Chem. 278 30044–30050

    Not in our library10.1074/jbc.m304159200

  132. 132.

    Pearce G. Siems W. F. Bhattacharya R. Chen Y. C. Ryan C. A. (2007 ). Three hydroxyproline-rich glycopeptides derived from a single petunia polyprotein precursor activate defensin I, a pathogen defense response gene. J. Biol. Chem. 282 17777–17784

    Not in our library10.1074/jbc.m701543200

  133. 133.

    Peña-Cortés H. Fisahn J. Willmitzer L. (1995 ). Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. Proc. Natl. Acad. Sci. U.S.A. 92 4106–4113

    Not in our library10.1073/pnas.92.10.4106

  134. 134.

    Proels R. K. Oberhollenzer K. Pathuri I. P. Hensel G. Kumlehn J. Huckelhoven R. (2010 ). RBOHF2 of barley is required for normal development of penetration resistance to the parasitic fungus Blumeria graminis f. sp. hordei. Mol. Plant Microbe Interact. 23 1143–1150

    Not in our library10.1094/mpmi-23-9-1143

  135. 135.

    Raiola A. Lionetti V. Elmaghraby I. Immerzeel P. Mellerowicz E. J. Salvi G. (2011 ). Pectin methylesterase is induced in Arabidopsis upon infection and is necessary for a successful colonization by necrotrophic pathogens. Mol. Plant Microbe Interact. 24 432–440

    Not in our library10.1094/mpmi-07-10-0157

  136. 136.

    Rasul S. Dubreuil-Maurizi C. Lamotte O. Koen E. Poinssot B. Alcaraz G. (2012 ). Nitric oxide production mediates oligogalacturonide-triggered immunity and resistance to Botrytis cinerea in Arabidopsis thaliana. Plant Cell Environ. 35 1483–1499

    Not in our library10.1111/j.1365-3040.2012.02505.x

  137. 137.

    Reddy A. S. Ali G. S. Celesnik H. Day I. S. (2011 ). Coping with stresses: roles of calcium- and calcium/calmodulin-regulated gene expression. Plant Cell 23 2010–2032

    Not in our library10.1105/tpc.111.084988

  138. 138.

    Rehrig E. M. Appel H. Jones A. D. Schultz C. J. (2014 ). Roles for jasmonate- and ethylene-induced transcription factors in the ability of Arabidopsis to respond differentially to damage caused by two insect herbivores. Front. Plant Sci. 5:407

    Not in our library10.3389/fpls.2014.00407

  139. 139.

    Reymond P. Weber H. Damond M. Farmer E. E. (2000 ). Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12 707–720

    Not in our library10.1105/tpc.12.5.707

  140. 140.

    Riederer M. Schreiber L. (2001 ). Protecting against water loss: analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52 2023–2032

    Not in our library10.1093/jexbot/52.363.2023

  141. 141.

    Roberts K. (1992 ). Potential awareness of plants. Nature 360 14–15

    Not in our library10.1038/360014a0

  142. 142.

    Rodriguez M. C. Petersen M. Mundy J. (2010 ). Mitogen-activated protein kinase signaling in plants. Annu. Rev. Plant Biol. 61 621–649

    Not in our library10.1146/annurev-arplant-042809-112252

  143. 143.

    Ryan C. A. Jagendorf A. (1995 ). Self defense by plants. Proc. Natl. Acad. Sci. U.S.A. 92:4075

    Not in our library10.1073/pnas.92.10.4075

  144. 144.

    Sanders D. Pelloux J. Brownlee C. Harper J. F. (2002 ). Calcium at the crossroads of signaling. Plant Cell 14 S401–S417

    Not in our library10.1105/tpc.002899

  145. 145.

    Savatin D. V. Ferrari S. Sicilia F. De Lorenzo G. (2011 ). Oligogalacturonide-auxin antagonism does not require posttranscriptional gene silencing or stabilization of auxin response repressors in Arabidopsis. Plant Physiol. 157 1163–1174

    Not in our library10.1104/pp.111.184663

  146. 146.

    Savatin D. V. Gigli B. N. Marti L. Fabbri C. Cervone F. De Lorenzo G. (2014 ). The Arabidopsis NPK1-related protein kinases ANPs are required for elicitor-induced oxidative burst and immunity. Plant Physiol. 165 1188–1202

    Not in our library10.1104/pp.114.236901

  147. 147.

    Schaller A. Stintzi A. (2009 ). Enzymes in jasmonate biosynthesis – structure, function, regulation. Phytochemistry 70 1532–1538

    Not in our library10.1016/j.phytochem.2009.07.032

  148. 148.

    Scheer J. M. Ryan C. A. (1999 ). A 160-kD systemin receptor on the surface of Lycopersicon peruvianum suspension-cultured cells. Plant Cell 11 1525–1535

    Not in our library10.1105/tpc.11.8.1525

  149. 149.

    Schilmiller A. L. Howe G. A. (2005 ). Systemic signaling in the wound response. Curr. Opin. Plant Biol. 8 369–377

    Not in our library10.1016/j.pbi.2005.05.008

  150. 150.

    Schweighofer A. Kazanaviciute V. Scheikl E. Teige M. Doczi R. Hirt H. (2007 ). The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis. Plant Cell 19 2213–2224

    Not in our library10.1105/tpc.106.049585

  151. 151.

    Schweizer P. Felix G. Buchala A. Müller C. Métraux J. P. (1996a ). Perception of free cutin monomers by plant cells. Plant J. 10 331–341

    Not in our library10.1046/j.1365-313x.1996.10020331.x

  152. 152.

    Schweizer P. Jeanguenat A. Whitacre D. Metraux J. P. Mosinge E. (1996b ). Induction of resistance in barley against Erysiphe graminis f.sp. hordei by free cutin monomers. Physiol. Mol. Plant Pathol. 49 103–120

    Not in our library10.1006/pmpp.1996.0043

  153. 153.

    Schweizer P. Jeanguenat A. Mosinger E. Metraux J. P. (1994 ). Plant protection by free cutin monomers in two cereal pathosystems. Adv. Mol. Gen. Plant Microbe Interact. 21 371–374

    Not in our library10.1007/978-94-011-0177-6_55

  154. 154.

    Seo S. Katou S. Seto H. Gomi K. Ohashi Y. (2007 ). The mitogen-activated protein kinases WIPK and SIPK regulate the levels of jasmonic and salicylic acids in wounded tobacco plants. Plant J. 49 899–909

    Not in our library10.1111/j.1365-313x.2006.03003.x

  155. 155.

    Seo S. Okamoto N. Seto H. Ishizuka K. Sano H. Ohashi Y. (1995 ). Tobacco MAP kinase: a possible mediator in wound signal transduction pathways. Science 270 1988–1992

    Not in our library10.1126/science.270.5244.1988

  156. 156.

    Sieber P. Schorderet M. Ryser U. Buchala A. Kolattukudy P. Metraux J. P. (2000 ). Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12 721–737

    Not in our library10.1105/tpc.12.5.721

  157. 157.

    Staswick P. E. Tiryaki I. (2004 ). The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16 2117–2127

    Not in our library10.1105/tpc.104.023549

  158. 158.

    Stenzel I. Hause B. Maucher H. Pitzschke A. Miersch O. Ziegler J. (2003 ). Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato – amplification in wound signalling. Plant J. 33 577–589

    Not in our library10.1046/j.1365-313x.2003.01647.x

  159. 159.

    Suzuki N. Mittler R. (2012 ). Reactive oxygen species-dependent wound responses in animals and plants. Free Radic. Biol. Med. 53 2269–2276

    Not in our library10.1016/j.freeradbiomed.2012.10.538

  160. 160.

    Szczegielniak J. Borkiewicz L. Szurmak B. Lewandowska-Gnatowska E. Statkiewicz M. Klimecka M. (2012 ). Maize calcium-dependent protein kinase (ZmCPK11): local and systemic response to wounding, regulation by touch and components of jasmonate signaling. Physiol. Plant. 146 1–14

    Not in our library10.1111/j.1399-3054.2012.01587.x

  161. 161.

    Takabatake R. Seo S. Ito N. Gotoh Y. Mitsuhara I. Ohashi Y. (2006 ). Involvement of wound-induced receptor-like protein kinase in wound signal transduction in tobacco plants. Plant J. 47 249–257

    Not in our library10.1111/j.1365-313x.2006.02781.x

  162. 162.

    Takeda S. Gapper C. Kaya H. Bell E. Kuchitsu K. Dolan L. (2008 ). Local positive feedback regulation determines cell shape in root hair cells. Science 319 1241–1244

    Not in our library10.1126/science.1152505

  163. 163.

    Taurino M. Abelenda J. A. Rio-Alvarez I. Navarro C. Vicedo B. Farmaki T. (2014 ). Jasmonate-dependent modifications of the pectin matrix during potato development function as a defense mechanism targeted by Dickeya dadantii virulence factors. Plant J. 77 418–429

    Not in our library10.1111/tpj.12393

  164. 164.

    Tisi A. Angelini R. Cona A. (2008 ). Wound healing in plants: cooperation of copper amine oxidase and flavin-containing polyamine oxidase. Plant Signal. Behav. 3 204–206

    Not in our library10.4161/psb.3.3.5372

  165. 165.

    Toufighi K. Brady S. M. Austin R. Ly E. Provart N. J. (2005 ). The Botany array resource: e-northerns, expression angling, and promoter analyses. Plant J. 43 153–163

    Not in our library10.1111/j.1365-313x.2005.02437.x

  166. 166.

    Verica J. A. Chae L. Tong H. Y. Ingmire P. He Z. H. (2003 ). Tissue-specific and developmentally regulated expression of a cluster of tandemly arrayed cell wall-associated kinase-like kinase genes in Arabidopsis. Plant Physiol. 133 1732–1746

    Not in our library10.1104/pp.103.028530

  167. 167.

    Wagner T. A. Kohorn B. D. (2001 ). Wall-Associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell 13 303–318

    Not in our library10.1105/tpc.13.2.303

  168. 168.
    Arabidopsis CaM Binding Protein CBP60g Contributes to MAMP-Induced SA Accumulation and Is Involved in Disease Resistance against Pseudomonas syringae · 2009
    No notice
  169. 169.

    Wildon D. C. Thain J. F. Minchin P. E. H. Gubb I. R. Reilly A. J. Skipper Y. D. (1992 ). Electrical signaling and systemic proteinase inhibitor induction in the wounded plant. Nature 360 62–65

    Not in our library10.1038/360062a0

  170. 170.

    Wolf S. Hematy K. Hofte H. (2012 ). Growth control and cell wall signaling in plants. Annu. Rev. Plant Biol. 63 381–407

    Not in our library10.1146/annurev-arplant-042811-105449

  171. 171.

    Yamaguchi Y. Huffaker A. Bryan A. C. Tax F. E. Ryan C. A. (2010 ). PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22 508–522

    Not in our library10.1105/tpc.109.068874

  172. 172.

    Yamaguchi Y. Pearce G. Ryan C. A. (2006 ). The cell surface leucine-rich repeat receptor for AtPEP1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc. Natl. Acad. Sci. U.S.A. 103 10104–10109

    Not in our library10.1073/pnas.0603729103

  173. 173.

    Yamanaka T. Nakagawa Y. Mori K. Nakano M. Imamura T. Kataoka H. (2010 ). MCA1 and MCA2 that mediate Ca2+ uptake have distinct and overlapping roles in Arabidopsis. Plant Physiol. 152 1284–1296

    Not in our library10.1104/pp.109.147371

  174. 174.

    Yang D. H. Hettenhausen C. Baldwin I. T. Wu J. (2012 ). Silencing Nicotiana attenuata calcium-dependent protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic acid accumulations. Plant Physiol. 159 1591–1607

    Not in our library10.1104/pp.112.199018

  175. 175.

    Zhang S. Q. Klessig D. F. (1998a ). The tobacco wounding-activated mitogen-activated protein kinase is encoded by SIPK. Proc. Natl. Acad. Sci. U.S.A. 95 7225–7230

    Not in our library10.1073/pnas.95.12.7225

  176. 176.

    Zhang S. Q. Klessig D. F. (1998b ). Resistance gene N-mediated de novo synthesis and activation of a tobacco mitogen-activated protein kinase by tobacco mosaic virus infection. Proc. Natl. Acad. Sci. U.S.A. 95 7433–7438

    Not in our library10.1073/pnas.95.13.7433

  177. 177.

    Zimmermann M. R. Maischak H. Mithofer A. Boland W. Felle H. H. (2009 ). System potentials, a novel electrical long-distance apoplastic signal in plants, induced by wounding. Plant Physiol. 149 1593–1600

    Not in our library10.1104/pp.108.133884

  178. 178.

    Zipfel C. Kunze G. Chinchilla D. Caniard A. Jones J. D. G. Boller T. (2006 ). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125 749–760

    Not in our library10.1016/j.cell.2006.03.037

  179. 179.

    Zipfel C. Robatzek S. Navarro L. Oakeley E. J. Jones J. D. Felix G. (2004 ). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428 764–767

    Not in our library10.1038/nature02485

Cited by papers we hold 5

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.