Q&A: How does peptide signaling direct plant development?
© Breiden and Simon. 2016
Published: 8 July 2016
A significant part of the communication between plant cells is mediated by signaling peptides and their corresponding plasma membrane-localized receptor-like kinases. This communication mechanism serves as a key regulatory unit for coordination of plant growth and development. In the past years more peptide–receptor signaling pathways have been shown to regulate developmental processes, such as shoot and root meristem maintenance, seed formation, and floral abscission. More detailed understanding of the processes behind this regulation might also be helpful to increase the yield of crop plants.
How were plant peptides discovered?
Growth and development of multicellular organisms is coordinated via cell-to-cell interactions. Different hormones, including small secreted polypeptides, maintain this communication in plants, fulfilling a vast variety of functions in plant growth, development, and stress responses. Their involvement in developmental processes by acting as a key component in cell-to-cell communication will be the focus of this Q&A.
The first described plant signaling peptide was tomato systemin (TomSys), which was discovered in the 1970s by Clarence E. Ryan . Wounded tomato leaves, when added in water to young tomato plants, induced the production of proteinase inhibitors I and II, and this led to the identification of an 18 amino acid signaling peptide termed TomSys. TomSys is involved in the production of jasmonic acid, which is the main wound response signal, initiating, for example, intracellular signaling cascades via mitogen activated protein kinases (MAPKs) [2, 3].
What signaling peptides are now known?
Approximately 13 plant peptide families have been identified so far, including CLE (CLAVATA3/EMBRYO-SURROUNDING REGION, CLV3/ESR) and IDA (INFLORESCENCE DEFICIENT IN ABSCISSION), with more than 1000 genes encoding putative small signaling molecules . They can be grouped into two classes, the small post-translationally modified peptides and the cysteine-rich polypeptides . Small post-translationally modified peptides are usually composed of 5 to 20 amino acids. Cysteine-rich polypeptides have a length of approximately 50 amino acids and are synthesized as precursor proteins . Peptide families that belong to the small post-translationally modified peptides are, for example, the CLE, IDA, and RGF (ROOT GROWTH FACTOR) peptides [7–10]. RALF (RAPID ALKALINIZATION FACTOR) and PDF (PLANT DEFENSIN) peptides are examples of cysteine-rich polypeptides [11, 12].
How are plant peptides processed and post-translationally modified?
For example, members of the CLE peptide family are translated as a prepropeptide with a length of approximately 100 amino acids and are further processed to a 12–14 amino acid peptide [16–18]. The prepropeptides share an N-terminal signal sequence to direct them into the secretory pathway and the conserved CLE motif close to their C-terminus [19–21]. Processing is achieved by serine proteases, most likely members of the subtilisin family that cleave off the N-terminal part of the proprotein at a conserved arginine in the CLE motif. The C-terminal part is then removed by a carboxypeptidase [22, 23]. CLE propeptides are further post-translationally modified by hydroxylation and glycosylation. These modifications are mediated by enzymes during their secretion and enhance the receptor binding activity of the mature CLE peptides .
Cysteine-rich peptides usually have an N-terminal signal sequence to direct them into the secretory pathway. Only some of them are further proteolytically processed, such as STOMAGEN, the EPF peptides, and RALF. However, correct folding and establishment of disulfide bridges is required for their function. RALF was first identified in tobacco and RALF23 was shown to be processed by a subtilisin protease [25, 26]. STOMAGEN and the related EPF-like peptides are involved in epidermal patterning and stomatal development and are also processed from larger precursors .
Small post-translationally modified peptides carry tyrosine sulfations, proline hydroxylations, or arabinosylations . Some of these modifications change the peptide conformation—for example, the hydroxylation of a proline side chain induces a kink into the peptide that could enhance its affinity for the receptor . The peptides might also be protected from proteolysis by masking the recognition sequences of proteases in their sequence .
Tyrosine sulfation is mediated by the tyrosylprotein sulfotransferase (TPST). TPST catalyzes the transfer reaction of sulfate from 3’-phosphoadenosine 5’-phosphosulfate (PAPS) to a tyrosine side chain . Three peptide classes with tyrosine sulfation are known: PSKs (phytosulfokines), PSY1, and RGFs (root meristem growth factors) [9, 32, 33].
Proline hydroxylation is mediated by prolyl-4-hydroxylase (P4H), which is a membrane protein that localizes to the Golgi and endoplasmic reticulum network . Hydroxyproline (Hyp) residues are present in several small post-translationally modified peptides like CLV3, CLE2, and TDIF (tracheary elements differentiation inhibitory factor) [18, 35].
In several small secreted peptides Hyp residues are further linked to an O-linked-I-arabinose chain. Examples of arabinosylated peptides are CLV3 and CLE2 .
How are plant peptides perceived by the cells?
Signaling peptides are perceived via plasma membrane-localized receptor-like kinases (RLKs) . The largest subfamily of RLKs, leucine-rich repeat RLKs (LRR-RLK), consist of more than 200 members in Arabidopsis . LRR-RLKs carry an extracellular LRR domain, a transmembrane domain, and an intracellular kinase domain, which is activated upon peptide binding to the LRR domain . The activated kinase domain can induce several different pathways leading to cell growth, proliferation, differentiation, or a defense response.
Five different crystal structures of peptides (PSK, IDA, FLG22, PEP1, TDIF) bound to their receptors (PSKR, HAE, FLS2, PEPR1, PXY, BAK1, SERK1) have been resolved [29, 38–41]. All show the binding of the peptide to inner surfaces of the LRR domains. In all structures the peptides share a similar orientation, with their C-termini pointing towards the C-termini of their respective receptors. The C-termini of FLG22 and PEP1 receptors mediate receptor interactions. Since their binding mechanism is quite similar, this might also be true for the TDIF receptor, PXY .
So what do plant peptides do?
Are there any well-studied examples of plant peptides
Yes—for example, several peptide-triggered pathways regulate the maintenance of long-lasting populations of stem cells in meristems, which is a prerequisite for continuous plant development. The feedback loop controlling shoot apical meristem size is a well-studied example of the role of signaling peptides in development. This feedback loop comprises the signaling peptide CLV3, the LRR-RLK CLV1, a receptor heteromer consisting of the RLP CLV2 and the pseudokinase CRN (CORYNE), and the RLK RPK2 (RECEPTOR-LIKE PROTEIN KINASE 2)/TOAD2 (TOADSTOOL 2) [10, 47–50]. Binding of CLV3 to the receptors negatively regulates the expression of WUS (WUSCHEL), which encodes a homeodomain transcription factor. WUS is expressed in the organizing center and promotes stem cell identity of cells at the apex of the shoot meristem . WUS thereby positively regulates the expression of stem cell-expressed CLV3 and thus establishes a negative feedback loop that maintains a relatively stable number of stem cells [51, 52].
The closely related peptide CLE40 controls stem cells in the root meristem . In the distal root meristem, CLE40 acts through the RLK ARABIDOPSIS CRINKLY4 (ACR4), which is structurally unrelated to LRR-RLKs, and also the LRR-RLK CLV1 to promote cell differentiation . In the proximal meristem, CLE40 signaling requires the LRR-RLP CLV2 in a complex with CRN to inhibit or delay cell differentiation. In both parts of the root meristem, CLE40 signaling controls the expression of several phytohormone biosynthetic genes and of stem cell-specific transcription factors .
Another example of well-characterized peptide signaling pathways is the IDA peptide-triggered pathway. IDA regulates the separation of cells by inducing degradation of the cell wall during floral organ abscission . The predicted IDA family peptides share a conserved 12 amino acid PIP motif close to their C-termini. The mature IDA peptide consists only of this 12 amino acid motif, contains hydroxyprolinated residues, and shows high activity in a bioassay based on measuring the release of reactive oxygen species . In the abscission zone, IDA interacts with the RLKs HAESA (HAE) and HAESA-LIKE2 (HSL2) . These receptors form complexes with SERKs and trigger the sequential activation of a MAP kinase cascade consisting of MKK4, MKK5, MPK3, and MPK6 , and the release of reactive oxygen species via RESPIRATORY BURST OXIDASE HOMOLOGS (RBOH) activity [55, 58, 59]. IDA signaling leads to the suppression of the transcription factor KNAT1 (KNOTTED-LIKE FROM ARABIDOPSIS THALIANA1), which restricts the related TFs KNAT2 and KNAT6 and thereby controls the expression of genes involved in cell separation .
How were the peptide-signaling pathways that control plant development analyzed?
Many of them were first observed by knock-out mutant phenotypes. Later, related family members were often studied by overexpression analysis. Bioinformatic analysis of plant genomes allowed for prediction and identification of further families. Today, it is estimated that around 1800 peptides are encoded by the Arabidopsis genome. Since signaling peptides might be able to travel long distances within the plant and interact with multiple receptors, the identification of the corresponding receptor is not always easy. In 2014 Tabata et al.  published a novel approach to identify peptide–receptor complexes. They generated an expression library of Arabidopsis LRR-RLKs by overexpressing the proteins in tobacco BY-2 cells. Using photoaffinity-labeled peptides, they could identify new receptors that interact with the peptide. This presented technique is promising for identification of so far unknown receptors for several signaling peptides.
What about pathogen perception?
Some signaling peptides are involved in pathogen perception. One of the best studied pathogen response pathways is the LRR-RLK FLAGELLIN SENSING2 (FLS2)-mediated pathway in the innate immune response. FLS2 plays a critical role in sensing pathogens by binding to bacterial flagellin . Upon flagellin binding, FLS2 interacts with the LRR-RLK BAK1, which leads to intracellular calcium signaling and activation of downstream responses [66, 67]. The receptor-like cytoplasmatic kinase (RLCK) BRI1-ASSOCIATED KINASE1/SOMATIC EMBRYO RECEPTOR KINASE3 (BIK1) interacts with FLS2 and BAK1 and is phosphorylated by BAK1 upon flagellin binding. BIK1 then dissociates from the complex and participates in downstream phosphorylation signaling cascades . BIK1 directly phosphorylates the NADPH oxidase RbohD, which leads to a Ca2+ influx-dependent oxidative burst by the production of reactive oxygen species (ROS) . Other immediate downstream components of this signaling pathway are, for example, the Ca2+ influx channels ACA8 and ACA10 (AUTOINHIBITED Ca2+ ATPase) that interact with FLS2 after flg22 binding and aggregate in lipid rafts . The activation of MAPKs upon flagellin binding to FLS2 is not dependent on BIK1; hence, FLS2 activation leads to the activation of separable downstream pathways including Ca2+ transients . An overview of LRR-RLK FLS2 signaling pathway is represented in Fig. 3.
Besides developmental processes, CLE peptides are also involved in nematode attacks. Nematodes secrete various CLE-like effector proteins, which are injected into the host plant during the parasitic cycle. For example, a CLE-like gene was identified in Heterodera glycines, a soybean cyst nematode, which is thought to be an effector gene required for pathogenicity . Several nematode CLEs can mimic endogenous Arabidopsis CLEs and act as ligands for Arabidopsis receptors, thereby ensuring successful infection by the nematode and development of the syncytium, a multinucleate cell formed by fusion of several plant cells, on which it feeds .
Is there crosstalk between plant peptide signaling pathways?
There is potential for crosstalk because highly similar CLE genes are clustered (CLE4/5/6/7) and some of them even encode peptides with the same amino acid sequence. Due to this probably very recent gene duplication, they might still act redundantly . Indeed, addition of various CLE peptides often leads to similar phenotypes, indicating redundancy but also possible crosstalk between signaling pathways. For example, CLE42 and CLE41/CLE44 inhibit tracheary element differentiation but do not inhibit root growth . In contrast, overexpression of many other CLE genes suppresses root growth.
There is also the potential for crosstalk at the receptor level: CLV3 signaling leads to the repression of not only WUS but also the BARELY ANY MERISTEM (BAM) gene, which encodes a CLV1-related RLK. In clv1 mutant backgrounds, BAM1 is upregulated and can perceive the CLV3 ligand. The normal ligand for BAM1 has not yet been identified but is likely also a CLE peptide. Nimchuk et al.  suggested that BAM expression in the shoot apical meristem could contribute to the robustness of the CLV network against perturbations.
A much-discussed publication in 2011 reported that CLV3 can trigger the innate immune response via binding to the FLS2 receptor , suggesting crosstalk between developmental and pathogen response pathways. The authors indicated that such a mechanism may prime cells at their point of origin, the stem cell zone, for future encounters with pathogenic bacteria. However, the CLE40 peptide, which is closely related to CLV3, could not initiate any response mediated by FLS2. Sengonzac et al.  then meticulously tested the effect of CLV3 on FLS2 in Arabidopsis mesophyll protoplasts and seedlings but could not detect any immune response, leading them and others to the conclusion that FLS2 is not able to perceive CLV3 as a signal.
…and how is specificity of plant peptide signaling generated?
Specific functions and interactions of signaling peptides are generated by their regional expression pattern in the plant and their distinct binding properties to their corresponding receptors. Furthermore, the localized expression of the receptors and availability for only some signaling peptides restrict their signaling activity.
How far do peptides travel in the plant?
Long-distance signaling has been shown for several signaling peptides in plants. In legumes, homologues of CLV3 travel from the root to the shoot to regulate nodule number . The energy-consuming formation of nodules has to be strictly regulated. The shoot receives a signal from the root, which is generated upon root nodulation. In Lotus japanicus, HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1), a CLV1 like receptor kinase, is required in the shoot and binds the CLE-root signal 2 peptide (RS2), which is generated in the root [77, 78]. CLE-RS2 was shown to be transported via the xylem, but the mechanism for how the peptide is loaded into the xylem remains unclear . Transport of CLE2, 3, 4, and 7 via the apoplast is required for expansion of the root system in nitrogen-poor environments .
Are plant peptides relevant for future agriculture?
Analyzing the effect of peptides on plant development can be beneficial for future agriculture. Identification of novel signaling peptides that influence meristem size may help finding mutants which lead to an increased yield. The search for mutant plants that are carrying mutations in the genes for the signaling peptides or their corresponding receptors can be improved by ongoing research in this area. Mutations in the maize orthologue of CLV1 thick tassel dwarf1 (td1) are known to affect female and male inflorescence ear, which ultimately gives rise to seeds . The female inflorescence shows more kernels and the male an increased spikelet density. The maize LRR-RLP FASCIATED EAR3 (FEA3) functions in stem cell control and is repressed by WUS. Je et al.  proposed a feedback model where a CLE peptide signal moves from the organ primordia to the shoot apical meristem and is then perceived by FEA3 to regulate meristem size. Additionally, they could also show that weak alleles of fea3 lead to a significant increase in yield in field experiments.
Overall, we have gained information on only a tiny number of peptide-triggered signaling pathways in plants; many hundreds still await analysis, and these peptides may provide us with very precise tools to modify plant architecture and development for crop improvement.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Ryan CA. Assay and biochemical properties of the proteinase inhibitor-inducing factor, a wound hormone. Plant Physiol. 1974;54(3):328–32.View ArticlePubMedPubMed CentralGoogle Scholar
- Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW. Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol. 2003;132(4):1728–38.View ArticlePubMedPubMed CentralGoogle Scholar
- Lee GI, Howe GA. The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J. 2003;33(3):567–76.View ArticlePubMedGoogle Scholar
- Lease KA, Walker JC. The Arabidopsis Unannotated Secreted Peptide Database, a resource for plant peptidomics. Plant Physiol. 2006;142(3):831–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Grienenberger E, Fletcher JC. Polypeptide signaling molecules in plant development. Curr Opin Plant Biol. 2015;23:8–14.View ArticlePubMedGoogle Scholar
- Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue BPA. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell. 2015;27(8):2095–118.View ArticlePubMedPubMed CentralGoogle Scholar
- Clark SE, Running MP, Meyerowitz EM. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development. 1995;121:2057–67.Google Scholar
- Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, et al. Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell. 2003;15(10):2296–307.View ArticlePubMedPubMed CentralGoogle Scholar
- Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science. 2010;329(5995):1065–7.View ArticlePubMedGoogle Scholar
- Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science. 1999;283(5409):1911–4.View ArticlePubMedGoogle Scholar
- Pearce G, Moura DS, Stratmann J, Ryan Jr CA. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci U S A. 2001;98(22):12843–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Terras FR, Eggermont K, Kovaleva V, Raikhel NV, Osborn RW, Kester A, et al. Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell. 1995;7(5):573–88.View ArticlePubMedPubMed CentralGoogle Scholar
- Farrokhi N, Whitelegge JP, Brusslan JA. Plant peptides and peptidomics. Plant Biotechnol J. 2008;6(2):105–34.View ArticlePubMedGoogle Scholar
- Marmiroli N, Maestri E. Plant peptides in defense and signaling. Peptides. 2014;56:30–44.View ArticlePubMedGoogle Scholar
- Krause C, Richter S, Knöll C, Jürgens G. Plant secretome—from cellular process to biological activity. Biochim Biophys Acta. 2013;1834(11):2429–41.View ArticlePubMedGoogle Scholar
- Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu CM. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell. 2005;17(9):2542–53.View ArticlePubMedPubMed CentralGoogle Scholar
- Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science. 2006;313(5788):845–8.View ArticlePubMedGoogle Scholar
- Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol. 2009;5(8):578–80.View ArticlePubMedGoogle Scholar
- Jun JH, Fiume E, Fletcher JC. The CLE family of plant polypeptide signaling molecules. Cell Mol Life Sci. 2008;65(5):743–55.View ArticlePubMedGoogle Scholar
- Wang G, Fiers M. CLE peptide signaling during plant development. Protoplasma. 2010;240(1–4):33–43.View ArticlePubMedGoogle Scholar
- Betsuyaku S, Sawa S, Yamada M. The function of the CLE peptides in plant development and plant-microbe interactions. Arabidopsis Book. 2011;9:e0149.View ArticlePubMedPubMed CentralGoogle Scholar
- Djordjevic MA, Oakes M, Wong CE, Singh M, Bhalla P, Kusumawati L, Imin N. Border sequences of Medicago truncatula CLE36 are specifically cleaved by endoproteases common to the extracellular fluids of Medicago and soybean. J Exp Bot. 2011;62(13):4649–59.View ArticlePubMedPubMed CentralGoogle Scholar
- Ni J, Guo Y, Jin H, Hartsell J, Clark SE. Characterization of a CLE processing activity. Plant Mol Biol. 2011;75(1–2):67–75.View ArticlePubMedGoogle Scholar
- Matsubayashi Y. Small post-translationally modified peptide signals in arabidopsis. Arabidopsis Book. 2011;9:e0150.View ArticlePubMedPubMed CentralGoogle Scholar
- Pearce G, Moura DS, Stratmann J, Ryan CA. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci U S A. 2001;98(22):12843–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Srivastava R, Liu J-X, Guo H, Yin Y, Howell SH. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J. 2009;59(6):930–9.View ArticlePubMedGoogle Scholar
- Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I. Stomagen positively regulates stomatal density in Arabidopsis. Nature. 2010;463(7278):241–4.View ArticlePubMedGoogle Scholar
- Walsh CT, Garneau-Tsodikova S, Gatto GJ. Protein posttranslational modifications: the chemistry of proteome diversifications. Angew Chem Int Ed. 2005;44(45):7342–72.View ArticleGoogle Scholar
- Zhang H, Lin X, Han Z, Qu L-J, Chai J. Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs. Cell Res. 2016;26(5):543–55.View ArticlePubMedPubMed CentralGoogle Scholar
- Seitz O. Glycopeptide synthesis and the effects of glycosylation on protein structure and activity. ChemBioChem. 2000;1(4):214–46.View ArticlePubMedGoogle Scholar
- Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y. Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci U S A. 2009;106(35):15067–72.View ArticlePubMedPubMed CentralGoogle Scholar
- Matsubayashi Y, Sakagami Y. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci U S A. 1996;93(15):7623–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci U S A. 2007;104(46):18333–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Myllyharju J. Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol. 2003;22(1):15–24.View ArticlePubMedGoogle Scholar
- Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science. 2006;313(5788):842–5.View ArticlePubMedGoogle Scholar
- Shiu SH, Bleecker AB. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A. 2001;98(19):10763–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Torii KU. Leucine-rich repeat receptor kinases in plants: structure, function, and signal transduction pathways. Int Rev Cytol. 2004;234:1–46.View ArticlePubMedGoogle Scholar
- Sun Y, Li L, Macho AP, Han Z, Hu Z, Zipfel C, Zhou JM, Chai J. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science. 2013;342(6158):624–8.View ArticlePubMedGoogle Scholar
- Tang J, Han Z, Sun Y, Zhang H, Gong X, Chai J. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Res. 2015;25(1):110–20.View ArticlePubMedGoogle Scholar
- Wang J, Li H, Han Z, Zhang H, Wang T, Lin G, et al. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature. 2015;525(7568):265–8.View ArticlePubMedGoogle Scholar
- Santiago J, Brandt B, Wildhagen M, Hohmann U, Hothorn LA, Butenko MA, Hothorn M. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife. 2016;5:e15075.View ArticlePubMedPubMed CentralGoogle Scholar
- Stahl Y, Wink RH, Ingram GC, Simon R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol. 2009;19(11):909–14.View ArticlePubMedGoogle Scholar
- Albert M. Peptides as triggers of plant defence. J Exp Bot. 2013;64(17):5269–79.View ArticlePubMedGoogle Scholar
- Czyzewicz N, Yue K, Beeckman T, Smet ID. Message in a bottle: small signalling peptide outputs during growth and development. J Exp Bot. 2013;64(17):5281–96.View ArticlePubMedGoogle Scholar
- Matsubayashi Y. Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol. 2014;65(1):385–413.View ArticlePubMedGoogle Scholar
- Sauter M. Phytosulfokine peptide signalling. J Exp Bot. 2015;66(17):5161–9.View ArticlePubMedGoogle Scholar
- Clark SE, Williams RW, Meyerowitz EM. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell. 1997;89(4):575–85.View ArticlePubMedGoogle Scholar
- Muller R, Bleckmann A, Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell. 2008;20(4):934–46.View ArticlePubMedPubMed CentralGoogle Scholar
- Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development. 2010;137(22):3911–20.View ArticlePubMedGoogle Scholar
- Jeong S, Trotochaud AE, Clark SE. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell. 1999;11(10):1925–34.View ArticlePubMedPubMed CentralGoogle Scholar
- Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science. 2000;289(5479):617–9.View ArticlePubMedGoogle Scholar
- Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell. 2000;100(6):635–44.View ArticlePubMedGoogle Scholar
- Hobe M, Müller R, Grünewald M, Brand U, Simon R. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol. 2003;213(8):371–81.View ArticlePubMedGoogle Scholar
- Pallakies H, Simon R. The CLE40 and CRN/CLV2 signaling pathways antagonistically control root meristem growth in Arabidopsis. Mol Plant. 2014;7(11):1619–36.View ArticlePubMedGoogle Scholar
- Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H, Aalen RB, Felix G. Tools and strategies to match peptide-ligand receptor pairs. Plant Cell. 2014;26(5):1838–47.View ArticlePubMedPubMed CentralGoogle Scholar
- Stenvik G-E, Tandstad NM, Guo Y, Shi C-L, Kristiansen W, Holmgren A, et al. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell. 2008;20(7):1805–17.View ArticlePubMedPubMed CentralGoogle Scholar
- Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC. Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2008;105(40):15629–34.View ArticlePubMedPubMed CentralGoogle Scholar
- Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, et al. Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell. 2007;19(3):1065–80.View ArticlePubMedPubMed CentralGoogle Scholar
- Meng X, Zhou J, Tang J, Li B, de Oliveira Marcos VV, Chai J, et al. Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep. 2016;14(6):1330–8.View ArticlePubMedPubMed CentralGoogle Scholar
- Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, Proveniers M, et al. Arabidopsis class I KNOTTED-like homeobox proteins act downstream in the IDA-HAE/HSL2 floral abscission signaling pathway. Plant Cell. 2011;23(7):2553–67.View ArticlePubMedPubMed CentralGoogle Scholar
- Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T. Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science. 2012;338(6110):1093–7.View ArticlePubMedGoogle Scholar
- Costa LM, Marshall E, Tesfaye M, Silverstein KA, Mori M, Umetsu Y, et al. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science. 2014;344(6180):168–72.View ArticlePubMedGoogle Scholar
- Fiume E, Fletcher JC. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell. 2012;24(3):1000–12.View ArticlePubMedPubMed CentralGoogle Scholar
- Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science. 2014;346(6207):343–6.View ArticlePubMedGoogle Scholar
- Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature. 2004;428(6984):764–7.View ArticlePubMedGoogle Scholar
- Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JDG, et al. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature. 2007;448(7152):497–500.View ArticlePubMedGoogle Scholar
- Boller T, Felix G. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol. 2009;60:379–406.View ArticlePubMedGoogle Scholar
- Macho Alberto P, Zipfel C. Plant PRRs and the activation of innate immune signaling. Mol Cell. 2014;54(2):263–72.View ArticlePubMedGoogle Scholar
- Li L, Li M, Yu L, Zhou Z, Liang X, Liu Z, et al. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe. 2014;15(3):329–38.View ArticlePubMedGoogle Scholar
- Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, Shimosato-Asano H, et al. PAMP (Pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem. 2010;285(50):39140–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S, Ntoukakis V, et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell. 2014;54(1):43–55.View ArticlePubMedGoogle Scholar
- Wang X, Allen R, Ding X, Goellner M, Maier T, de Boer JM, et al. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant-Microbe Interactions. 2001;14(4):536–44.View ArticleGoogle Scholar
- Replogle A, Wang J, Bleckmann A, Hussey RS, Baum TJ, Sawa S, et al. Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE. Plant J. 2011;65(3):430–40.View ArticlePubMedGoogle Scholar
- Nimchuk ZL, Zhou Y, Tarr PT, Peterson BA, Meyerowitz EM. Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases. Development. 2015;142(6):1043–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Lee H, Chah O-K, Sheen J. Stem-cell-triggered immunity through CLV3p-FLS2 signalling. Nature. 2011;473(7347):376–9.View ArticlePubMedPubMed CentralGoogle Scholar
- Segonzac C, Nimchuk ZL, Beck M, Tarr PT, Robatzek S, Meyerowitz EM, Zipfel C. The shoot apical meristem regulatory peptide CLV3 does not activate innate immunity. Plant Cell. 2012;24(8):3186–92.View ArticlePubMedPubMed CentralGoogle Scholar
- Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, Kawaguchi M. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 2009;50(1):67–77.View ArticlePubMedGoogle Scholar
- Okamoto S, Kawaguchi M. Shoot HAR1 mediates nitrate inhibition of nodulation in Lotus japonicus. Plant Signaling Behav. 2015;10(5):e1000138.View ArticleGoogle Scholar
- Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat Commun. 2013;4:2191.View ArticlePubMedGoogle Scholar
- Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S, Tsuchiya YN, Sawa S, et al. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci U S A. 2014;111(5):2029–34.View ArticlePubMedPubMed CentralGoogle Scholar
- Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M, Jackson D, et al. thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development. 2005;132(6):1235–45.View ArticlePubMedGoogle Scholar
- Je BI, Gruel J, Lee YK, Bommert P, Arevalo ED, Eveland AL, Wu Q, et al. Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits. Nat Genet. 2016. doi:10.1038/ng.3567.PubMedGoogle Scholar