Posttranslationally modified small-peptide signals in plants

Annual Review of Plant Biology

Volumn 65, Issue , 2014, Pages 385-413

  Matsubayashi, Yoshikatsu ^a  

^a NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

Author keywords

cell to cell communication; plant hormone; posttranslational modification; proteolytic processing; receptor kinase; secreted peptide

Indexed keywords

PEPTIDE; SIGNAL PEPTIDE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; CARBOHYDRATE ANALYSIS; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PLANT; PLANT DEVELOPMENT; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; CARBOHYDRATE SEQUENCE; MOLECULAR SEQUENCE DATA; PEPTIDES; PLANT DEVELOPMENT; PLANT PROTEINS; PLANTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SORTING SIGNALS; SIGNAL TRANSDUCTION;

EID: 84899751488     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-050312-120122     Document Type: Review

References (152)

1. Aichinger E, Kornet N, Friedrich T, Laux T. 2012. Plant stem cell niches. Annu. Rev. Plant Biol. 63:615-36
2. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, et al. 2004. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109-20
3. Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y. 2007. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl. Acad. Sci. USA 104:18333-38
4. Bleckmann A, Weidtkamp-Peters S, Seidel CA, Simon R. 2010. Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol. 152:166-76
5. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R. 2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617-19
6. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, 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
7. Caetano-Anollés G, Gresshoff PM. 1991. Plant genetic control of nodulation. Annu. Rev. Microbiol. 45:345-82
8. Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu CM, Heidstra R, Scheres B. 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. 13:1435-41
9. Casson SA, Chilley PM, Topping JF, Evans IM, Souter MA, Lindsey K. 2002. The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning. Plant Cell 14:1705-21
10. Chen YC, Siems WF, Pearce G, Ryan CA. 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
11. Chen YF, Matsubayashi Y, Sakagami Y. 2000. Peptide growth factor phytosulfokine-αcontributes to the pollen population effect. Planta 211:752-55
12. Chilley PM, Casson SA, Tarkowski P, Hawkins N, Wang KL, et al. 2006. The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell 18:3058-72
13. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, et al. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105:15629-34
14. Chu H, Qian Q, Liang W, Yin C, Tan H, 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
15. Clark SE, Williams RW, Meyerowitz EM. 1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575-85
16. Cock JM, McCormick S. 2001. A large family of genes that share homology with CLAVATA3. Plant Physiol. 126:939-42
17. Delay C, Imin N, Djordjevic MA. 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
18. Djordjevic MA, Oakes M, Wong CE, Singh M, Bhalla P, 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
19. Egelund J, Obel N, Ulvskov P, Geshi N, Pauly M, 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
20. Ellis M, Egelund J, Schultz CJ, Bacic A. 2010. Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol. 153:403-19
21. Endo S, Shinohara H, Matsubayashi Y, Fukuda H. 2013. A novel pollen-pistil interaction conferring high temperature tolerance during reproduction via CLE45 signaling. Curr. Biol. 23:1670-76
22. Etchells JP, Provost CM, Mishra L, Turner SR. 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
23. Etchells JP, Turner SR. 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
24. Fernandez A, Drozdzecki A, Hoogewijs K, Nguyen A, Beeckman T, 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
25. Fisher K, Turner S. 2007. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 17:1061-66
26. Fiume E, Fletcher JC. 2012. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 24:1000-12
27. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM. 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:1911-14
28. Fletcher JC, Meyerowitz EM. 2000. Cell signaling within the shoot meristem. Curr. Opin. Plant Biol. 3:23-30
29. Fuller RS, Sterne RE, Thorner J. 1988. Enzymes required for yeast prohormone processing. Annu. Rev. Physiol. 50:345-62
30. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, et al. 2007. PLETHORA proteins as dosedependent master regulators of Arabidopsis root development. Nature 449:1053-57
31. Gille S, Hansel U, Ziemann M, Pauly M. 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
32. Green TR, Ryan CA. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776-77
33. Guo Y, Han L, Hymes M, Denver R, Clark SE. 2010. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63:889-900
34. Hanai H, Matsuno T, Yamamoto M, Matsubayashi Y, Kobayashi T, 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
35. Hanai H, Nakayama D, Yang H, Matsubayashi Y, Hirota Y, Sakagami Y. 2000. Existence of a plant tyrosylprotein sulfotransferase: novel plant enzyme catalyzing tyrosine O-sulfation of preprophytosulfokine variants in vitro. FEBS Lett. 470:97-101
36. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. 2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev. 21:1720-25
37. Hartmann J, Stuhrwohldt N, Dahlke RI, Sauter M. 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
38. Hieta R, Myllyharju J. 2002. Cloning and characterization of a low molecular weight prolyl 4-hydroxylase from Arabidopsis thaliana: effective hydroxylation of proline-rich, collagen-like, and hypoxiainducible transcription factor α-like peptides. J. Biol. Chem. 277:23965-71
39. Higashiyama T. 2010. Peptide signaling in pollen-pistil interactions. Plant Cell Physiol. 51:177-89
40. Hirakawa Y, Kondo Y, Fukuda H. 2010. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618-29
41. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, 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
42. Hobe M, Muller R, Grunewald M, Brand U, Simon R. 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
43. Huffaker A, Pearce G, Ryan CA. 2006. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. USA 103:10098-103
44. Igarashi D, Tsuda K, Katagiri F. 2012. The peptide growth factor, phytosulfokine, attenuates patterntriggered immunity. Plant J. 71:194-204
45. Igasaki T, Akashi N, Ujino-Ihara T, Matsubayashi Y, Sakagami Y, Shinohara K. 2003. Phytosulfokine stimulates somatic embryogenesis in Cryptomeria japonica. Plant Cell Physiol. 44:1412-16
46. Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, et al. 2006. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842-45
47. Jeong S, Trotochaud AE, Clark SE. 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
48. Jinn TL, Stone JM, Walker JC. 2000. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev. 14:108-17
49. Jun J, Fiume E, Roeder AH, Meng L, Sharma VK, et al. 2010. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiol. 154:1721-36
50. Kieliszewski MJ, de Zacks R, Leykam JF, Lamport DT. 1992. A repetitive proline-rich protein from the gymnosperm Douglas fir is a hydroxyproline-rich glycoprotein. Plant Physiol. 98:919-26
51. Kieliszewski MJ, Lamport DT. 1994. Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 5:157-72
52. Kieliszewski MJ, Lamport DT, Tan L, Cannon MC. 2010. Hydroxyproline-rich glycoproteins: form and function. Annu. Plant Rev. 41:321-42
53. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, et al. 2010. RPK2 is an essential receptorlike kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911-20
54. Kobayashi T, Eun C, Hanai H, Matsubayashi Y, Sakagami Y, Kamada H. 1999. Phytosulphokine-α, a peptidyl plant growth factor, stimulates somatic embryogenesis in carrot. J. Exp. Bot. 50:1123-28
55. Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y. 2009. Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 106:15067-72
56. Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, et al. 2010. Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol. 51:1-8
57. Kondo T, Nakamura T, Yokomine K, Sakagami Y. 2008. Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides. Biochem. Biophys. Res. Commun. 377:312-16
58. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, et al. 2006. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845-48
59. Krusell L, Madsen LH, Sato S, Aubert G, Genua A, et al. 2002. Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420:422-26
60. Kumpf RP, Shi CL, Larrieu A, Sto IM, Butenko MA, 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
61. Kutschmar A, Rzewuski G, Stuhrwohldt N, Beemster GT, Inze D, Sauter M. 2009. PSK-αpromotes root growth in Arabidopsis. New Phytol. 181:820-31
62. Kwezi L, Ruzvidzo O, Wheeler JI, Govender K, Iacuone S, 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
63. Lim CW, Lee YW, Hwang CH. 2011. Soybean nodule-enhanced CLE peptides in roots act as signals in GmNARK-mediated nodulation suppression. Plant Cell Physiol. 52:1613-27
64. Loivamäki M, Stührwohldt N, Deeken R, Steffens B, Roitsch T, et al. 2010. A role for PSK signaling in wounding and microbial interactions in Arabidopsis. Physiol. Plant. 139:348-57
65. Marshall E, Costa LM, Gutierrez-Marcos J. 2011. Cysteine-rich peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development. J. Exp. Bot. 62:1677-86
66. Márton ML, Cordts S, Broadhvest J, Dresselhaus T. 2005. Micropylar pollen tube guidance by Egg Apparatus 1 of maize. Science 307:573-76
67. Matsubayashi Y. 2011. Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol. 52:5-13
68. Matsubayashi Y. 2011. Small post-translationally modified peptide signals in Arabidopsis. Arabidopsis Book 9:e0150
69. Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y. 2006. Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol. 142:45-53
70. Matsubayashi Y, Ogawa M, Morita A, Sakagami Y. 2002. AnLRRreceptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470-72
71. Matsubayashi Y, Sakagami Y. 1996. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl. Acad. Sci. USA 93:7623-27
72. Matsubayashi Y, Sakagami Y. 2006. Peptide hormones in plants. Annu. Rev. Plant Biol. 57:649-74
73. Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y. 1999. The endogenous sulfated pentapeptide phytosulfokine-α stimulates tracheary element differentiation of isolated mesophyll cells of zinnia. Plant Physiol. 120:1043-48
74. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y. 2010. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329:1065-67
75. Meng L, Buchanan BB, Feldman LJ, Luan S. 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
76. Minami E, Kouchi H, Cohn JR, Ogawa T, Stacey G. 1996. Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J. 10:23-32
77. Mitchum MG, Wang X, Wang J, Davis EL. 2012. Role of nematode peptides and other small molecules in plant parasitism. Annu. Rev. Phytopathol. 50:175-95
78. Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S. 2008. The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 49:1752-57
79. Moore KL. 2003. The biology and enzymology of protein tyrosine O-sulfation. J. Biol. Chem. 278:24243-46
80. Mortier V, Den Herder G, Whitford R, Van de Velde W, Rombauts S, et al. 2010. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 153:222-37
81. Mortier V, Fenta BA, Martens C, Rombauts S, Holsters M, et al. 2011. Search for nodulation-related CLE genes in the genome of Glycine max. J. Exp. Bot. 62:2571-83
82. Mosher S, Seybold H, Rodriguez P, Stahl M, Davies KA, 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
83. Motose H, Iwamoto K, Endo S, Demura T, Sakagami Y, et al. 2009. Involvement of phytosulfokine in the attenuation of stress response during the transdifferentiation of zinniamesophyll cells into tracheary elements. Plant Physiol. 150:437-47
84. Muller R, Bleckmann A, Simon R. 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 20:934-46
85. Murphy E, Smith S, De Smet I. 2012. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24:3198-217
86. Muschietti J, Dircks L, Vancanneyt G, McCormick S. 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
87. Myllyharju J. 2003. Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol. 22:15-24
88. Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, 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
89. Narváez-Vásquez J, Pearce G, Ryan CA. 2005. The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc. Natl. Acad. Sci. USA 102:12974-77
90. Ni J, Clark SE. 2006. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 140:726-33
91. Ni J, Guo Y, Jin H, Hartsell J, Clark SE. 2011. Characterization of a CLE processing activity. Plant Mol. Biol. 75:67-75
92. Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM. 2011. Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol. 21:345-52
93. Nishimura R, Hayashi M, Wu GJ, Kouchi H, Imaizumi-Anraku H, et al. 2002. HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426-29
94. Oelkers K, Goffard N, Weiller GF, Gresshoff PM, Mathesius U, Frickey T. 2008. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 8:1
95. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y. 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294
96. Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y. 2013. Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat. Chem. Biol. 9:726-30
97. Ohyama K, Ogawa M, Matsubayashi Y. 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
98. Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y. 2009. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 5:578-80
99. Oka-Kira E, Kawaguchi M. 2006. Long-distance signaling to control root nodule number. Curr. Opin. Plant Biol. 9:496-502
100. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, et al. 2009. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 50:67-77
101. Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M. 2013. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4:2191
102. Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, et al. 2009. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357-61
103. Pearce G, Bhattacharya R, Chen YC, Barona G, Yamaguchi Y, Ryan CA. 2009. Isolation and characterization of hydroxyproline-rich glycopeptide signals in black nightshade leaves. Plant Physiol. 150:1422-33
104. Pearce G, Moura DS, Stratmann J, Ryan CA. 2001. Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817-20
105. Pearce G, Moura DS, Stratmann J, Ryan CA. 2001. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl. Acad. Sci. USA 98:12843-47
106. Pearce G, Ryan CA. 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
107. Pearce G, Siems WF, Bhattacharya R, Chen YC, Ryan CA. 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
108. Pearce G, Strydom D, Johnson S, Ryan CA. 1991. A polypeptide from tomato leaves induces woundinducible proteinase inhibitor proteins. Science 253:895-97
109. Rehemtulla A, Kaufman RJ. 1992. Protein processing within the secretory pathway. Curr. Opin. Biotechnol. 3:560-65
110. Reid DE, Ferguson BJ, Gresshoff PM. 2011. Inoculation- and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol. Plant-Microbe Interact. 24:606-18
111. Roberts I, Smith S, De Rybel B, Van Den Broeke J, Smet W, et al. 2013. The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. J. Exp. Bot. 64:5371-81
112. Ryan CA. 1990. Proteinase inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28:425-49
113. Ryan CA. 2000. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477:112-21
114. Ryan CA, Huffaker A, Yamaguchi Y. 2007. New insights into innate immunity in Arabidopsis. Cell Microbiol. 9:1902-8
115. Ryan CA, Pearce G, Scheer J, Moura DS. 2002. Polypeptide hormones. Plant Cell 14(Suppl.):S251-64
116. +-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263-72
117. Schnabel EL, Kassaw TK, Smith LS, Marsh JF, Oldroyd GE, 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
118. Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T. 2000. The stem cell population of Arabidopsis shoot meristems ismaintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635-44
119. Schopfer CR, Nasrallah ME, Nasrallah JB. 1999. The male determinant of self-incompatibility in Brassica. Science 286:1697-700
120. Shen Y, Diener AC. 2013. Arabidopsis thaliana RESISTANCE TO FUSARIUM OXYSPORUM 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet. 9:e1003525
121. Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, 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
122. Shimada T, Sugano SS, Hara-Nishimura I. 2011. Positive and negative peptide signals control stomatal density. Cell. Mol. Life Sci. 68:2081-88
123. Shimizu M, Igasaki T, Yamada M, Yuasa K, Hasegawa J, et al. 2005. Experimental determination of proline hydroxylation and hydroxyproline arabinogalactosylation motifs in secretory proteins. Plant J. 42:877-89
124. Shinohara H, Matsubayashi Y. 2013. Chemical synthesis of Arabidopsis CLV3 glycopeptide reveals the impact of hydroxyproline arabinosylation on peptide conformation and activity. Plant Cell Physiol. 54:369-74
125. Shinohara H, Moriyama Y, Ohyama K, Matsubayashi Y. 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
126. Shinohara H, Ogawa M, Sakagami Y, Matsubayashi Y. 2007. Identification of ligand binding site of phytosulfokine receptor by on-column photoaffinity labeling. J. Biol. Chem. 282:124-31
127. Song XF, Guo P, Ren SC, Xu TT, Liu CM. 2013. Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis. Plant Physiol. 161:1076-85
128. Song XF, Yu DL, Xu TT, Ren SC, Guo P, Liu CM. 2012. Contributions of individual amino acid residues to the endogenous CLV3 function in shoot apical meristem maintenance in Arabidopsis. Mol. Plant 5:515-23
129. Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T. 2012. Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science 338:1093-97
130. Srivastava R, Liu JX, Howell SH. 2008. Proteolytic processing of a precursor protein for a growthpromoting peptide by a subtilisin serine protease in Arabidopsis. Plant J. 56:219-27
131. Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp-Peters S, et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23:362-71
132. Stahl Y, Wink RH, Ingram GC, Simon R. 2009. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19:909-14
133. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, 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
134. Stratmann JW. 2003. Long distance run in the wound response-jasmonic acid is pulling ahead. Trends Plant Sci. 8:247-50
135. Stuhrwohldt N, Dahlke RI, Steffens B, Johnson A, Sauter M. 2011. Phytosulfokine-αcontrols hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PLoS ONE 6:e21054
136. Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, et al. 2010. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241-44
137. Suzaki T, Ohneda M, Toriba T, Yoshida A, Hirano HY. 2009. FON2 SPARE1 redundantly regulates floral meristem maintenance with FLORAL ORGAN NUMBER2 in rice. PLoS Genet. 5:e1000693
138. Suzaki T, Toriba T, Fujimoto M, Tsutsumi N, Kitano H, Hirano HY. 2006. Conservation and diversification of meristem maintenance mechanism in Oryza sativa: function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 47:1591-602
139. Suzaki T, Yoshida A, Hirano HY. 2008. Functional diversification of CLAVATA3-related CLE proteins in meristem maintenance in rice. Plant Cell 20:2049-58
140. Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, et al. 2000. The pollen determinant of selfincompatibility in Brassica campestris. Proc. Natl. Acad. Sci. USA 97:1920-25
141. Tamaki T, Betsuyaku S, Fujiwara M, Fukao Y, Fukuda H, et al. 2013. SUPPRESSOR OF LLP1 1-mediated C-terminal processing is critical for CLE19 peptide activity. Plant J. 76:970-81
142. Tiainen P, Myllyharju J, Koivunen P. 2005. Characterization of a second Arabidopsis thaliana prolyl 4-hydroxylase with distinct substrate specificity. J. Biol. Chem. 280:1142-48
143. Velasquez SM, Ricardi MM, Dorosz JG, Fernandez PV, Nadra AD, et al. 2011. O-glycosylated cell wall proteins are essential in root hair growth. Science 332:1401-3
144. Wang X, Mitchum MG, Gao B, Li C, Diab H, 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
145. Wen J, Lease KA, Walker JC. 2004. DVL, a novel class of small polypeptides: overexpression alters Arabidopsis development. Plant J. 37:668-77
146. Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P. 2008. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc. Natl. Acad. Sci. USA 105:18625-30
147. Whitford R, Fernandez A, Tejos R, Pérez AC, Kleine-Vehn J, et al. 2012.GOLVENsecretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev. Cell 22:678-85
148. Yang H, Matsubayashi Y, Nakamura K, Sakagami Y. 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
149. Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, et al. 2003. TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792-804
150. Yuasa K, Toyooka K, Fukuda H, Matsuoka K. 2005. Membrane-anchored prolyl hydroxylase with an export signal from the endoplasmic reticulum. Plant J. 41:81-94
151. Zhou W, Wei L, Xu J, Zhai Q, Jiang H, 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
152. Zhu Y, Wang Y, Li R, Song X, Wang Q, 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