Cell-to-cell signaling is essential for many processes in plant growth and development, including coordination of cellular responses to developmental and environmental cues. Cumulative studies have demonstrated that peptide signaling plays a greater-than-anticipated role in such intercellular communication. Some peptides act as signals during plant growth and development, whereas others are involved in defense responses or symbiosis. Peptides secreted as signals often undergo posttranslational modification and proteolytic processing to generate smaller peptides composed of approximately 10 amino acid residues. Such posttranslationally modified small-peptide signals constitute one of the largest groups of secreted peptide signals in plants. The location of the modification group incorporated into the peptides by specific modification enzymes and the peptide chain length defined by the processing enzymes are critical for biological function and receptor interaction. This review covers 20 years of research into posttranslationally modified small-peptide signals in plants.


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Literature Cited

  1. Aichinger E, Kornet N, Friedrich T, Laux T. 1.  2012. Plant stem cell niches. Annu. Rev. Plant Biol. 63:615–36 [Google Scholar]
  2. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I. 2.  et al. 2004. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–20 [Google Scholar]
  3. Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y. 3.  2007. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl. Acad. Sci. USA 104:18333–38 [Google Scholar]
  4. Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R. 4.  2010. Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol. 152:166–76 [Google Scholar]
  5. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. 5.  2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–19 [Google Scholar]
  6. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS. 6.  et al. 2003. INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–307 [Google Scholar]
  7. Caetano-Anollés G, Gresshoff PM. 7.  1991. Plant genetic control of nodulation. Annu. Rev. Microbiol. 45:345–82 [Google Scholar]
  8. Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu CM, Heidstra R, Scheres B. 8.  2003. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr. Biol. 131435–41 [Google Scholar]
  9. Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey K. 9.  2002. The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14:1705–21 [Google Scholar]
  10. Chen YC, Siems WF, Pearce G, Ryan CA. 10.  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. 283:11469–76 [Google Scholar]
  11. Chen YF, Matsubayashi Y, Sakagami Y. 11.  2000. Peptide growth factor phytosulfokine-α contributes to the pollen population effect. Planta 211:752–55 [Google Scholar]
  12. Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KL. 12.  et al. 2006. The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18:3058–72 [Google Scholar]
  13. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL. 13.  et al. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105:15629–34 [Google Scholar]
  14. Chu H, Qian Q, Liang W, Yin C, Tan H. 14.  et al. 2006. The FLORAL ORGAN NUMBER4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice. Plant Physiol. 142:1039–52 [Google Scholar]
  15. Clark SE, Williams RW, Meyerowitz EM. 15.  1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–85 [Google Scholar]
  16. Cock JM, McCormick S. 16.  2001. A large family of genes that share homology with CLAVATA3. Plant Physiol. 126:939–42 [Google Scholar]
  17. Delay C, Imin N, Djordjevic MA. 16a.  2013. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants.. J. Exp. Bot. 64:5383–94 [Google Scholar]
  18. Djordjevic MA, Oakes M, Wong CE, Singh M, Bhalla P. 17.  et al. 2011. Border sequences of Medicago truncatula CLE36 are specifically cleaved by endoproteases common to the extracellular fluids of Medicago and soybean. J. Exp. Bot. 62:4649–59 [Google Scholar]
  19. Egelund J, Obel N, Ulvskov P, Geshi N, Pauly M. 18.  et al. 2007. Molecular characterization of two Arabidopsis thaliana glycosyltransferase mutants, rra1 and rra2, which have a reduced residual arabinose content in a polymer tightly associated with the cellulosic wall residue. Plant Mol. Biol. 64:439–51 [Google Scholar]
  20. Ellis M, Egelund J, Schultz CJ, Bacic A. 19.  2010. Arabinogalactan-proteins: key regulators at the cell surface?. Plant Physiol. 153:403–19 [Google Scholar]
  21. Endo S, Shinohara H, Matsubayashi Y, Fukuda H. 20.  2013. A novel pollen–pistil interaction conferring high temperature tolerance during reproduction via CLE45 signaling. Curr. Biol. 23:1670–76 [Google Scholar]
  22. Etchells JP, Provost CM, Mishra L, Turner SR. 21.  2013. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development 140:2224–34 [Google Scholar]
  23. Etchells JP, Turner SR. 22.  2010. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137:767–74 [Google Scholar]
  24. Fernandez A, Drozdzecki A, Hoogewijs K, Nguyen A, Beeckman T. 23.  et al. 2013. Transcriptional and functional classification of the GOLVEN/ROOT GROWTH FACTOR/CLE-like signaling peptides reveals their role in lateral root and hair formation. Plant Physiol. 161:954–70 [Google Scholar]
  25. Fisher K, Turner S. 24.  2007. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17:1061–66 [Google Scholar]
  26. Fiume E, Fletcher JC. 25.  2012. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 24:1000–12 [Google Scholar]
  27. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 26.  1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911–14 [Google Scholar]
  28. Fletcher JC, Meyerowitz EM. 27.  2000. Cell signaling within the shoot meristem. Curr. Opin. Plant Biol. 3:23–30 [Google Scholar]
  29. Fuller RS, Sterne RE, Thorner J. 28.  1988. Enzymes required for yeast prohormone processing. Annu. Rev. Physiol. 50:345–62 [Google Scholar]
  30. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I. 29.  et al. 2007. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–57 [Google Scholar]
  31. Gille S, Hansel U, Ziemann M, Pauly M. 30.  2009. Identification of plant cell wall mutants by means of a forward chemical genetic approach using hydrolases. Proc. Natl. Acad. Sci. USA 106:14699–704 [Google Scholar]
  32. Green TR, Ryan CA. 31.  1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–77 [Google Scholar]
  33. Guo Y, Han L, Hymes M, Denver R, Clark SE. 32.  2010. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63:889–900 [Google Scholar]
  34. Hanai H, Matsuno T, Yamamoto M, Matsubayashi Y, Kobayashi T. 33.  et al. 2000. A secreted peptide growth factor, phytosulfokine, acting as a stimulatory factor of carrot somatic embryo formation. Plant Cell Physiol. 41:27–32 [Google Scholar]
  35. Hanai H, Nakayama D, Yang H, Matsubayashi Y, Hirota Y, Sakagami Y. 34.  2000. Existence of a plant tyrosylprotein sulfotransferase: novel plant enzyme catalyzing tyrosine O-sulfation of preprophytosulfokine variants in vitro. FEBS Lett. 470:97–101 [Google Scholar]
  36. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. 35.  2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev. 21:1720–25 [Google Scholar]
  37. Hartmann J, Stuhrwohldt N, Dahlke RI, Sauter M. 36.  2013. Phytosulfokine control of growth occurs in the epidermis, is likely to be non-cell autonomous and is dependent on brassinosteroids. Plant J. 73:579–90 [Google Scholar]
  38. Hieta R, Myllyharju J. 37.  2002. Cloning and characterization of a low molecular weight prolyl 4-hydroxylase from Arabidopsis thaliana: effective hydroxylation of proline-rich, collagen-like, and hypoxia-inducible transcription factor α-like peptides. J. Biol. Chem. 277:23965–71 [Google Scholar]
  39. Higashiyama T. 38.  2010. Peptide signaling in pollen-pistil interactions. Plant Cell Physiol. 51:177–89 [Google Scholar]
  40. Hirakawa Y, Kondo Y, Fukuda H. 39.  2010. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–29 [Google Scholar]
  41. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I. 40.  et al. 2008. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl. Acad. Sci. USA 105:15208–13 [Google Scholar]
  42. Hobe M, Muller R, Grunewald M, Brand U, Simon R. 41.  2003. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol. 213:371–81 [Google Scholar]
  43. Huffaker A, Pearce G, Ryan CA. 42.  2006. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. USA 103:10098–103 [Google Scholar]
  44. Igarashi D, Tsuda K, Katagiri F. 43.  2012. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J. 71:194–204 [Google Scholar]
  45. Igasaki T, Akashi N, Ujino-Ihara T, Matsubayashi Y, Sakagami Y, Shinohara K. 44.  2003. Phytosulfokine stimulates somatic embryogenesis in Cryptomeria japonica. Plant Cell Physiol. 44:1412–16 [Google Scholar]
  46. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S. 45.  et al. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–45 [Google Scholar]
  47. Jeong S, Trotochaud AE, Clark SE. 46.  1999. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11:1925–34 [Google Scholar]
  48. Jinn TL, Stone JM, Walker JC. 47.  2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev. 14:108–17 [Google Scholar]
  49. Jun J, Fiume E, Roeder AH, Meng L, Sharma VK. 48.  et al. 2010. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol. 154:1721–36 [Google Scholar]
  50. Kieliszewski MJ, de Zacks R, Leykam JF, Lamport DT. 49.  1992. A repetitive proline-rich protein from the gymnosperm Douglas fir is a hydroxyproline-rich glycoprotein. Plant Physiol. 98:919–26 [Google Scholar]
  51. Kieliszewski MJ, Lamport DT. 50.  1994. Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 5:157–72 [Google Scholar]
  52. Kieliszewski MJ, Lamport DT, Tan L, Cannon MC. 51.  2010. Hydroxyproline-rich glycoproteins: form and function. Annu. Plant Rev. 41:321–42 [Google Scholar]
  53. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S. 52.  et al. 2010. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–20 [Google Scholar]
  54. Kobayashi T, Eun C, Hanai H, Matsubayashi Y, Sakagami Y, Kamada H. 53.  1999. Phytosulphokine-α, a peptidyl plant growth factor, stimulates somatic embryogenesis in carrot. J. Exp. Bot. 50:1123–28 [Google Scholar]
  55. Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y. 54.  2009. Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 106:15067–72 [Google Scholar]
  56. Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T. 54a.  et al. 2010. Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol. 51:1–8 [Google Scholar]
  57. Kondo T, Nakamura T, Yokomine K, Sakagami Y. 55.  2008. Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides. Biochem. Biophys. Res. Commun. 377:312–16 [Google Scholar]
  58. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T. 56.  et al. 2006. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–48 [Google Scholar]
  59. Krusell L, Madsen LH, Sato S, Aubert G, Genua A. 57.  et al. 2002. Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422–26 [Google Scholar]
  60. Kumpf RP, Shi CL, Larrieu A, Sto IM, Butenko MA. 58.  et al. 2013. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence.. Proc. Natl. Acad. Sci. USA 110:5235–40 [Google Scholar]
  61. Kutschmar A, Rzewuski G, Stuhrwohldt N, Beemster GT, Inze D, Sauter M. 59.  2009. PSK-α promotes root growth in Arabidopsis. New Phytol. 181:820–31 [Google Scholar]
  62. Kwezi L, Ruzvidzo O, Wheeler JI, Govender K, Iacuone S. 60.  et al. 2011. The phytosulfokine (PSK) receptor is capable of guanylate cyclase activity and enabling cyclic GMP-dependent signaling in plants. J. Biol. Chem. 286:22580–88 [Google Scholar]
  63. Lim CW, Lee YW, Hwang CH. 61.  2011. Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression. Plant Cell Physiol. 52:1613–27 [Google Scholar]
  64. Loivamäki M, Stührwohldt N, Deeken R, Steffens B, Roitsch T. 62.  et al. 2010. A role for PSK signaling in wounding and microbial interactions in Arabidopsis. Physiol. Plant. 139:348–57 [Google Scholar]
  65. Marshall E, Costa LM, Gutierrez-Marcos J. 63.  2011. Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J. Exp. Bot. 62:1677–86 [Google Scholar]
  66. Márton ML, Cordts S, Broadhvest J, Dresselhaus T. 64.  2005. Micropylar pollen tube guidance by Egg Apparatus 1 of maize. Science 307:573–76 [Google Scholar]
  67. Matsubayashi Y. 65.  2011. Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol. 52:5–13 [Google Scholar]
  68. Matsubayashi Y. 66.  2011. Small post-translationally modified peptide signals in Arabidopsis. Arabidopsis Book 9:e0150 [Google Scholar]
  69. Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y. 67.  2006. Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol. 142:45–53 [Google Scholar]
  70. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y. 68.  2002. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–72 [Google Scholar]
  71. Matsubayashi Y, Sakagami Y. 69.  1996. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl. Acad. Sci. USA 93:7623–27 [Google Scholar]
  72. Matsubayashi Y, Sakagami Y. 70.  2006. Peptide hormones in plants. Annu. Rev. Plant Biol. 57:649–74 [Google Scholar]
  73. Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y. 71.  1999. The endogenous sulfated pentapeptide phytosulfokine-α stimulates tracheary element differentiation of isolated mesophyll cells of zinnia.. Plant Physiol. 120:1043–48 [Google Scholar]
  74. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y. 72.  2010. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065–67 [Google Scholar]
  75. Meng L, Buchanan BB, Feldman LJ, Luan S. 73.  2012. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc. Natl. Acad. Sci. USA 109:1760–65 [Google Scholar]
  76. Minami E, Kouchi H, Cohn JR, Ogawa T, Stacey G. 74.  1996. Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J. 10:23–32 [Google Scholar]
  77. Mitchum MG, Wang X, Wang J, Davis EL. 75.  2012. Role of nematode peptides and other small molecules in plant parasitism. Annu. Rev. Phytopathol. 50:175–95 [Google Scholar]
  78. Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S. 76.  2008. The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 49:1752–57 [Google Scholar]
  79. Moore KL. 77.  2003. The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278:24243–46 [Google Scholar]
  80. Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S. 78.  et al. 2010. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 153:222–37 [Google Scholar]
  81. Mortier V, Fenta BA, Martens C, Rombauts S, Holsters M. 79.  et al. 2011. Search for nodulation-related CLE genes in the genome of Glycine max. J. Exp. Bot. 62:2571–83 [Google Scholar]
  82. Mosher S, Seybold H, Rodriguez P, Stahl M, Davies KA. 80.  et al. 2013. The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J. 73:469–82 [Google Scholar]
  83. Motose H, Iwamoto K, Endo S, Demura T, Sakagami Y. 81.  et al. 2009. Involvement of phytosulfokine in the attenuation of stress response during the transdifferentiation of zinnia mesophyll cells into tracheary elements. Plant Physiol. 150:437–47 [Google Scholar]
  84. Muller R, Bleckmann A, Simon R. 82.  2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934–46 [Google Scholar]
  85. Murphy E, Smith S, De Smet I. 83.  2012. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198–217 [Google Scholar]
  86. Muschietti J, Dircks L, Vancanneyt G, McCormick S. 84.  1994. LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 6:321–38 [Google Scholar]
  87. Myllyharju J. 85.  2003. Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol. 22:15–24 [Google Scholar]
  88. Narita NN, Moore S, Horiguchi G, Kubo M, Demura T. 86.  et al. 2004. Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J. 38:699–713 [Google Scholar]
  89. Narváez-Vásquez J, Pearce G, Ryan CA. 87.  2005. The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc. Natl. Acad. Sci. USA 102:12974–77 [Google Scholar]
  90. Ni J, Clark SE. 88.  2006. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 140:726–33 [Google Scholar]
  91. Ni J, Guo Y, Jin H, Hartsell J, Clark SE. 89.  2011. Characterization of a CLE processing activity. Plant Mol. Biol. 75:67–75 [Google Scholar]
  92. Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM. 90.  2011. Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol. 21:345–52 [Google Scholar]
  93. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H. 91.  et al. 2002. HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426–29 [Google Scholar]
  94. Oelkers K, Goffard N, Weiller GF, Gresshoff PM, Mathesius U, Frickey T. 92.  2008. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 8:1 [Google Scholar]
  95. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 93.  2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294 [Google Scholar]
  96. Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y. 94.  2013. Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat. Chem. Biol. 9:726–30 [Google Scholar]
  97. Ohyama K, Ogawa M, Matsubayashi Y. 95.  2008. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J. 55:152–60 [Google Scholar]
  98. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y. 96.  2009. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5:578–80 [Google Scholar]
  99. Oka-Kira E, Kawaguchi M. 97.  2006. Long-distance signaling to control root nodule number. Curr. Opin. Plant Biol. 9:496–502 [Google Scholar]
  100. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M. 98.  et al. 2009. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 50:67–77 [Google Scholar]
  101. Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M. 99.  2013. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4:2191 [Google Scholar]
  102. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H. 100.  et al. 2009. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–61 [Google Scholar]
  103. Pearce G, Bhattacharya R, Chen YC, Barona G, Yamaguchi Y, Ryan CA. 101.  2009. Isolation and characterization of hydroxyproline-rich glycopeptide signals in black nightshade leaves. Plant Physiol. 150:1422–33 [Google Scholar]
  104. Pearce G, Moura DS, Stratmann J, Ryan CA. 102.  2001. Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817–20 [Google Scholar]
  105. Pearce G, Moura DS, Stratmann J, Ryan CA. 103.  2001. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl. Acad. Sci. USA 98:12843–47 [Google Scholar]
  106. Pearce G, Ryan CA. 104.  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. 278:30044–50 [Google Scholar]
  107. Pearce G, Siems WF, Bhattacharya R, Chen YC, Ryan CA. 105.  2007. Three hydroxyproline-rich glycopeptides derived from a single petunia polyprotein precursor activate defensin I, a pathogen defense response gene. J. Biol. Chem. 282:17777–84 [Google Scholar]
  108. Pearce G, Strydom D, Johnson S, Ryan CA. 106.  1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–97 [Google Scholar]
  109. Rehemtulla A, Kaufman RJ. 107.  1992. Protein processing within the secretory pathway. Curr. Opin. Biotechnol. 3:560–65 [Google Scholar]
  110. Reid DE, Ferguson BJ, Gresshoff PM. 108.  2011. Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol. Plant-Microbe Interact. 24:606–18 [Google Scholar]
  111. Roberts I, Smith S, De Rybel B, Van Den Broeke J, Smet W et al.108a.  2013. The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. J. Exp. Bot. 64:5371–81 [Google Scholar]
  112. Ryan CA. 109.  1990. Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425–49 [Google Scholar]
  113. Ryan CA. 110.  2000. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477:112–21 [Google Scholar]
  114. Ryan CA, Huffaker A, Yamaguchi Y. 111.  2007. New insights into innate immunity in Arabidopsis. Cell Microbiol. 9:1902–8 [Google Scholar]
  115. Ryan CA, Pearce G, Scheer J, Moura DS. 112.  2002. Polypeptide hormones. Plant Cell 14:Suppl.S251–64 [Google Scholar]
  116. Schaller A, Oecking C. 113.  1999. Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–72 [Google Scholar]
  117. Schnabel EL, Kassaw TK, Smith LS, Marsh JF, Oldroyd GE. 114.  et al. 2011. The ROOT DETERMINED NODULATION1 gene regulates nodule number in roots of Medicago truncatula and defines a highly conserved, uncharacterized plant gene family. Plant Physiol. 157:328–40 [Google Scholar]
  118. Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T. 115.  2000. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–44 [Google Scholar]
  119. Schopfer CR, Nasrallah ME, Nasrallah JB. 116.  1999. The male determinant of self-incompatibility in Brassica. Science 286:1697–700 [Google Scholar]
  120. Shen Y, Diener AC. 117.  2013. Arabidopsis thaliana RESISTANCE TO FUSARIUM OXYSPORUM 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet. 9:e1003525 [Google Scholar]
  121. Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V. 118.  et al. 2011. Arabidopsis class I KNOTTED-like homeobox proteins act downstream in the IDA-HAE/HSL2 floral abscission signaling pathway. Plant Cell 23:2553–67 [Google Scholar]
  122. Shimada T, Sugano SS, Hara-Nishimura I. 119.  2011. Positive and negative peptide signals control stomatal density. Cell. Mol. Life Sci. 68:2081–88 [Google Scholar]
  123. Shimizu M, Igasaki T, Yamada M, Yuasa K, Hasegawa J. 120.  et al. 2005. Experimental determination of proline hydroxylation and hydroxyproline arabinogalactosylation motifs in secretory proteins. Plant J. 42:877–89 [Google Scholar]
  124. Shinohara H, Matsubayashi Y. 121.  2013. Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity. Plant Cell Physiol. 54:369–74 [Google Scholar]
  125. Shinohara H, Moriyama Y, Ohyama K, Matsubayashi Y. 122.  2012. Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. Plant J. 70:845–54 [Google Scholar]
  126. Shinohara H, Ogawa M, Sakagami Y, Matsubayashi Y. 123.  2007. Identification of ligand binding site of phytosulfokine receptor by on-column photoaffinity labeling. J. Biol. Chem. 282:124–31 [Google Scholar]
  127. Song XF, Guo P, Ren SC, Xu TT, Liu CM. 124.  2013. Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis. Plant Physiol. 161:1076–85 [Google Scholar]
  128. Song XF, Yu DL, Xu TT, Ren SC, Guo P, Liu CM. 125.  2012. Contributions of individual amino acid residues to the endogenous CLV3 function in shoot apical meristem maintenance in Arabidopsis. Mol. Plant 5:515–23 [Google Scholar]
  129. Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T. 126.  2012. Egg cell–secreted EC1 triggers sperm cell activation during double fertilization. Science 338:1093–97 [Google Scholar]
  130. Srivastava R, Liu JX, Howell SH. 127.  2008. Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J. 56:219–27 [Google Scholar]
  131. Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp-Peters S. 128.  et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23:362–71 [Google Scholar]
  132. Stahl Y, Wink RH, Ingram GC, Simon R. 129.  2009. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19:909–14 [Google Scholar]
  133. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W. 130.  et al. 2008. 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 20:1805–17 [Google Scholar]
  134. Stratmann JW. 131.  2003. Long distance run in the wound response—jasmonic acid is pulling ahead. Trends Plant Sci. 8:247–50 [Google Scholar]
  135. Stuhrwohldt N, Dahlke RI, Steffens B, Johnson A, Sauter M. 132.  2011. Phytosulfokine-α controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS ONE 6:e21054 [Google Scholar]
  136. Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A. 133.  et al. 2010. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–44 [Google Scholar]
  137. Suzaki T, Ohneda M, Toriba T, Yoshida A, Hirano HY. 134.  2009. FON2 SPARE1 redundantly regulates floral meristem maintenance with FLORAL ORGAN NUMBER2 in rice. PLoS Genet. 5:e1000693 [Google Scholar]
  138. Suzaki T, Toriba T, Fujimoto M, Tsutsumi N, Kitano H, Hirano HY. 135.  2006. Conservation and diversification of meristem maintenance mechanism in Oryza sativa: function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 47:1591–602 [Google Scholar]
  139. Suzaki T, Yoshida A, Hirano HY. 136.  2008. Functional diversification of CLAVATA3-related CLE proteins in meristem maintenance in rice. Plant Cell 20:2049–58 [Google Scholar]
  140. Takayama S, Shiba H, Iwano M, Shimosato H, Che FS. 137.  et al. 2000. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. USA 97:1920–25 [Google Scholar]
  141. Tamaki T, Betsuyaku S, Fujiwara M, Fukao Y, Fukuda H. 137a.  et al. 2013. SUPPRESSOR OF LLP1 1-mediated C-terminal processing is critical for CLE19 peptide activity. Plant J. 76:970–81 [Google Scholar]
  142. Tiainen P, Myllyharju J, Koivunen P. 138.  2005. Characterization of a second Arabidopsis thaliana prolyl 4-hydroxylase with distinct substrate specificity. J. Biol. Chem. 280:1142–48 [Google Scholar]
  143. Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD. 139.  et al. 2011. O-glycosylated cell wall proteins are essential in root hair growth. Science 332:1401–3 [Google Scholar]
  144. Wang X, Mitchum MG, Gao B, Li C, Diab H. 140.  et al. 2005. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol. Plant Pathol. 6:187–91 [Google Scholar]
  145. Wen J, Lease KA, Walker JC. 141.  2004. DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J. 37:668–77 [Google Scholar]
  146. Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P. 142.  2008. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc. Natl. Acad. Sci. USA 105:18625–30 [Google Scholar]
  147. Whitford R, Fernandez A, Tejos R, Pérez AC, Kleine-Vehn J. 143.  et al. 2012. GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev. Cell 22:678–85 [Google Scholar]
  148. Yang H, Matsubayashi Y, Nakamura K, Sakagami Y. 144.  1999. Oryza sativa PSK gene encodes a precursor of phytosulfokine-α, a sulfated peptide growth factor found in plants. Proc. Natl. Acad. Sci. USA 96:13560–65 [Google Scholar]
  149. Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC. 145.  et al. 2003. TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–804 [Google Scholar]
  150. Yuasa K, Toyooka K, Fukuda H, Matsuoka K. 146.  2005. Membrane-anchored prolyl hydroxylase with an export signal from the endoplasmic reticulum. Plant J. 41:81–94 [Google Scholar]
  151. Zhou W, Wei L, Xu J, Zhai Q, Jiang H. 147.  et al. 2010. Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22:3692–709 [Google Scholar]
  152. Zhu Y, Wang Y, Li R, Song X, Wang Q. 148.  et al. 2010. Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J. 61:223–33 [Google Scholar]

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