1932

Abstract

During the past decade, a flurry of research focusing on the role of peptides as short- and long-distance signaling molecules in plant cell communication has been undertaken. Here, we focus on peptides derived from nonfunctional precursors, and we address several key questions regarding peptide signaling. We provide an overview of the regulatory steps involved in producing a biologically active peptide ligand that can bind its corresponding receptor(s) and discuss how this binding and subsequent activation lead to specific cellular outputs. We discuss different experimental approaches that can be used to match peptide ligands with their receptors. Lastly, we explore how peptides evolved from basic signaling units regulating essential processes in plants to more complex signaling systems as new adaptive traits developed and how nonplant organisms exploit this signaling machinery by producing peptide mimics.

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2019-04-29
2024-03-28
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Literature Cited

  1. 1.  Abrash EB, Bergmann DC 2010. Regional specification of stomatal production by the putative ligand CHALLAH. Development 137:447–55
    [Google Scholar]
  2. 2.  Abrash EB, Davies KA, Bergmann DC 2011. Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand–receptor interactions. Plant Cell 23:2864–79
    [Google Scholar]
  3. 3.  Alfonzo-Méndez MA, Carmona-Rosas G, Hernández-Espinosa DA, Romero-Ávila MT, García-Sáinz JA 2018. Different phosphorylation patterns regulate α1D-adrenoceptor signaling and desensitization. Biochim. Biophys. Acta 1865:842–54
    [Google Scholar]
  4. 4.  Anne P, Amiguet-Vercher A, Brandt B, Kalmbach L, Geldner N et al. 2018. CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis. Development 145:dev162354
    [Google Scholar]
  5. 5.  Baldwin JG, Nadler SA, Adams BJ 2004. Evolution of plant parasitism among nematodes. Annu. Rev. Phytopathol. 42:83–105
    [Google Scholar]
  6. 6.  Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332:960–63
    [Google Scholar]
  7. 7.  Bircheneder S, Dresselhaus T 2016. Why cellular communication during plant reproduction is particularly mediated by CRP signalling. J. Exp. Bot. 67:4849–61
    [Google Scholar]
  8. 8.  Bird DM, Jones JT, Opperman CH, Kikuchi T, Danchin EG 2015. Signatures of adaptation to plant parasitism in nematode genomes. Parasitology 142:S71–84
    [Google Scholar]
  9. 9.  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
    [Google Scholar]
  10. 10.  Bobay BG, DiGennaro P, Scholl E, Imin N, Djordjevic MA, McK Bird D 2013. Solution NMR studies of the plant peptide hormone CEP inform function. FEBS Lett 587:3979–85
    [Google Scholar]
  11. 11.  Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M et al. 2009. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–88
    [Google Scholar]
  12. 12.  Bommert P, Lunde C, Nardmann J, Vollbrecht E, Running M et al. 2005. thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase. Development 132:1235–45
    [Google Scholar]
  13. 13.  Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S et al. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304.e15
    [Google Scholar]
  14. 14.  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
    [Google Scholar]
  15. 15.  Bray D, Levin MD, Morton-Firth CJ 1998. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393:85–88
    [Google Scholar]
  16. 16.  Bryan AC, Obaidi A, Wierzba M, Tax FE 2012. XYLEM INTERMIXED WITH PHLOEM1, a leucine-rich repeat receptor-like kinase required for stem growth and vascular development in Arabidopsis thaliana. Planta 235:111–22
    [Google Scholar]
  17. 17.  Bücherl CA, Jarsch IK, Schudoma C, Segonzac C, Mbengue M et al. 2017. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6:e25114
    [Google Scholar]
  18. 18.  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
    [Google Scholar]
  19. 19.  Butenko MA, Wildhagen M, Albert M, Jehle A, Kalbacher H et al. 2014. Tools and strategies to match peptide-ligand receptor pairs. Plant Cell 26:1838–47
    [Google Scholar]
  20. 20.  Campbell L, Turner SR 2017. A comprehensive analysis of RALF proteins in green plants suggests there are two distinct functional groups. Front. Plant Sci. 8:37Extensive phylogenetic analysis of RALF genes in multiple plant species.
    [Google Scholar]
  21. 21.  Cao J, Shi F 2012. Evolution of the RALF gene family in plants: gene duplication and selection patterns. Evol. Bioinform. Online 8:271–92
    [Google Scholar]
  22. 22.  Chen ZH, Chen G, Dai F, Wang Y, Hills A et al. 2017. Molecular evolution of grass stomata. Trends Plant Sci 22:124–39
    [Google Scholar]
  23. 23.  Cheung AY, Wu HM 2016. Plant biology: LURE is bait for multiple receptors. Nature 531:178–80
    [Google Scholar]
  24. 24.  Chien CH, Chow CN, Wu NY, Chiang-Hsieh YF, Hou PF, Chang WC 2015. EXPath: a database of comparative expression analysis inferring metabolic pathways for plants. BMC Genom 16:S6
    [Google Scholar]
  25. 25.  Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500
    [Google Scholar]
  26. 26.  Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL et al. 2008. Regulation of floral organ abscission in Arabidopsis thaliana. PNAS 105:15629–34
    [Google Scholar]
  27. 27.  Clark SE, Running MP, Meyerowitz EM 1995. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–67
    [Google Scholar]
  28. 28.  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
    [Google Scholar]
  29. 29.  Cui Y, Hu C, Zhu Y, Cheng K, Li X et al. 2018. CIK receptor kinases determine cell fate specification during early anther development in Arabidopsis. Plant Cell 30:2383–401
    [Google Scholar]
  30. 30.  Czyzewicz N, Shi CL, Vu LD, Van De Cotte B, Hodgman C et al. 2015. Modulation of Arabidopsis and monocot root architecture by CLAVATA3/EMBRYO SURROUNDING REGION 26 peptide. J. Exp. Bot. 66:5229–43
    [Google Scholar]
  31. 31.  Danchin EG, Rosso MN, Vieira P, de Almeida-Engler J, Coutinho PM et al. 2010. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. PNAS 107:17651–56
    [Google Scholar]
  32. 32.  De Coninck B, De Smet I 2016. Plant peptides: taking them to the next level. J. Exp. Bot. 67:4791–95
    [Google Scholar]
  33. 33.  Delattin N, Brucker K, Cremer K, Cammue BP, Thevissen K 2017. Antimicrobial peptides as a strategy to combat fungal biofilms. Curr. Top. Med. Chem. 17:604–12
    [Google Scholar]
  34. 34.  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
    [Google Scholar]
  35. 35.  Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS 2013. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. PNAS 110:7074–79
    [Google Scholar]
  36. 36.  DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE 2006. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16
    [Google Scholar]
  37. 37.  Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M et al. 2017. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355:280–84
    [Google Scholar]
  38. 38.  Dong J, MacAlister CA, Bergmann DC 2009. BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–30
    [Google Scholar]
  39. 39.  Dresselhaus T, Franklin-Tong N 2013. Male–female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol. Plant 6:1018–36
    [Google Scholar]
  40. 40.  Dresselhaus T, Lausser A, Marton ML 2011. Using maize as a model to study pollen tube growth and guidance, cross-incompatibility and sperm delivery in grasses. Ann. Bot. 108:727–37
    [Google Scholar]
  41. 41.  Du C, Li X, Chen J, Chen W, Li B et al. 2016. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. PNAS 113:E8326–34
    [Google Scholar]
  42. 42.  Duan Q, Kita D, Li C, Cheung AY, Wu HM 2010. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. PNAS 107:17821–26
    [Google Scholar]
  43. 43.  Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J et al. 2007. The FERONIA receptor-like kinase mediates male–female interactions during pollen tube reception. Science 317:656–60
    [Google Scholar]
  44. 44.  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
    [Google Scholar]
  45. 45.  Eves-Van Den Akker S, Lilley CJ, Yusup HB, Jones JT, Urwin PE 2016. Functional C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis. Mol. Plant Pathol 17:1265–75
    [Google Scholar]
  46. 46.  Fan M, Wang M, Bai MY 2016. Diverse roles of SERK family genes in plant growth, development and defense response. Sci. China Life Sci. 59:889–96
    [Google Scholar]
  47. 47.  Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V et al. 2018. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28:666–75.e5
    [Google Scholar]
  48. 48.  Freedman RB, Hirst TR, Tuite MF 1994. Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci. 19:331–36
    [Google Scholar]
  49. 49.  Galindo-Trigo S, Gray JE, Smith LM 2016. Conserved roles of CrRLK1L receptor-like kinases in cell expansion and reproduction from algae to angiosperms. Front. Plant Sci. 7:1269
    [Google Scholar]
  50. 50.  Gao B, Allen R, Maier T, Davis EL, Baum JT, Hussey RS 2003. The parasitome of the phytonematode Heterodera glycines. Mol. Plant Microbe Interact 16:720–26
    [Google Scholar]
  51. 51.  Ge Z, Bergonci T, Zhao Y, Zou Y, Du S et al. 2017. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358:1596–600
    [Google Scholar]
  52. 52.  Ghorbani S, Hoogewijs K, Pecenkova T, Fernandez A, Inze A et al. 2016. The SBT6.1 subtilase processes the GOLVEN1 peptide controlling cell elongation. J. Exp. Bot. 67:4877–87
    [Google Scholar]
  53. 53.  Goad DM, Zhu C, Kellogg EA 2016. Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function. New Phytol 216:605–16Presents evidence about the evolutionary and functional path of CLE peptides.
    [Google Scholar]
  54. 54.  Gorres KL, Raines RT 2010. Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol. 45:106–24
    [Google Scholar]
  55. 55.  Gruber CW, Cemazar M, Clark RJ, Horibe T, Renda RF et al. 2007. A novel plant protein-disulfide isomerase involved in the oxidative folding of cystine knot defense proteins. J. Biol. Chem. 282:20435–46
    [Google Scholar]
  56. 56.  Guo X, Wang J, Gardner M, Fukuda H, Kondo Y et al. 2017. Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation. PLOS Pathog 13:e1006142
    [Google Scholar]
  57. 57.  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
    [Google Scholar]
  58. 58.  Hara K, Yokoo T, Kajita R, Onishi T, Yahata S et al. 2009. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–31
    [Google Scholar]
  59. 59.  Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR 2014. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–11
    [Google Scholar]
  60. 60.  Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. PNAS 104:12217–22
    [Google Scholar]
  61. 61.  Hetherington AJ, Dolan L 2018. Stepwise and independent origins of roots among land plants. Nature 561:235–38
    [Google Scholar]
  62. 62.  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 hypoxia-inducible transcription factor alpha-like peptides. J. Biol. Chem. 277:23965–71
    [Google Scholar]
  63. 63.  Higashiyama T, Takeuchi H 2015. The mechanism and key molecules involved in pollen tube guidance. Annu. Rev. Plant Biol. 66:393–413
    [Google Scholar]
  64. 64.  Hohmann U, Lau K, Hothorn M 2017. The structural basis of ligand perception and signal activation by receptor kinases. Annu. Rev. Plant Biol. 68:109–37
    [Google Scholar]
  65. 65.  Hohmann U, Santiago J, Nicolet J, Olsson V, Spiga FM et al. 2018. Mechanistic basis for the activation of plant membrane receptor kinases by SERK-family coreceptors. PNAS 115:3488–93
    [Google Scholar]
  66. 66.  Holton N, Cano-Delgado A, Harrison K, Montoya T, Chory J, Bishop GJ 2007. Tomato BRASSINO-STEROID INSENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifolium but is not essential for wound signaling. Plant Cell 19:1709–17
    [Google Scholar]
  67. 67.  Honkanen S, Jones VAS, Morieri G, Champion C, Hetherington AJ et al. 2016. The mechanism forming the cell surface of tip-growing rooting cells is conserved among land plants. Curr. Biol. 26:3238–44
    [Google Scholar]
  68. 68.  Hou S, Wang X, Chen D, Yang X, Wang M et al. 2014. The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7. PLOS Pathog 10:e1004331
    [Google Scholar]
  69. 69.  Houston NL, Fan C, Xiang JQ, Schulze JM, Jung R, Boston RS 2005. Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins. Plant Physiol 137:762–78
    [Google Scholar]
  70. 70.  Hu C, Zhu Y, Cui Y, Cheng K, Liang W et al. 2018. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nat. Plants 4:205–11
    [Google Scholar]
  71. 71.  Huck N, Moore JM, Federer M, Grossniklaus U 2003. The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130:2149–59
    [Google Scholar]
  72. 72.  Huffaker A, Ryan CA 2007. Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. PNAS 104:10732–36
    [Google Scholar]
  73. 73.  Hunt L, Bailey KJ, Gray JE 2010. The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol 186:609–14
    [Google Scholar]
  74. 74.  Hunt L, Gray JE 2009. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 19:864–69
    [Google Scholar]
  75. 75.  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
    [Google Scholar]
  76. 76.  Je BI, Gruel J, Lee YK, Bommert P, Arevalo ED et al. 2016. Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits. Nat. Genet. 48:785–91
    [Google Scholar]
  77. 77.  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
    [Google Scholar]
  78. 78.  Jia G, Liu X, Owen HA, Zhao D 2008. Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. PNAS 105:2220–25
    [Google Scholar]
  79. 79.  Kadota Y, Sklenar J, Derbyshire P, Stransfeld L, Asai S et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 54:43–55
    [Google Scholar]
  80. 80.  Kanaoka MM, Kawano N, Matsubara Y, Susaki D, Okuda S et al. 2011. Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor. Ann. Bot 108:739–47
    [Google Scholar]
  81. 81.  Kenrick P, Strullu-Derrien C 2014. The origin and early evolution of roots. Plant Physiol 166:570–80
    [Google Scholar]
  82. 82.  Kim H-J, Wu C-Y, Yu H-M, Sheen J, Lee H 2017. Dual CLAVATA3 peptides in Arabidopsis shoot stem cell signaling. J. Plant Biol. 60:506–12
    [Google Scholar]
  83. 83.  Kim J, Yang R, Chang C, Park Y, Tucker ML 2018. The root-knot nematode Meloidogyne incognita produces a functional mimic of the Arabidopsis INFLORESCENCE DEFICIENT IN ABSCISSION signaling peptide. J. Exp. Bot. 69:3009–21
    [Google Scholar]
  84. 84.  Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S et al. 2010. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–20
    [Google Scholar]
  85. 85.  Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y 2009. Identification of tyrosylprotein sulfotransferase in Arabidopsis. PNAS 106:15067–72
    [Google Scholar]
  86. 86.  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
    [Google Scholar]
  87. 87.  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. PNAS 110:5235–40
    [Google Scholar]
  88. 88.  Lalonde S, Ehrhardt DW, Loque D, Chen J, Rhee SY, Frommer WB 2008. Molecular and cellular approaches for the detection of protein-protein interactions: latest techniques and current limitations. Plant J 53:610–35
    [Google Scholar]
  89. 89.  Lauressergues D, Couzigou JM, Clemente HS, Martinez Y, Dunand C et al. 2015. Primary transcripts of microRNAs encode regulatory peptides. Nature 520:90–93
    [Google Scholar]
  90. 90.  Lease KA, Walker JC 2006. The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol 142:831–38
    [Google Scholar]
  91. 91.  Lee JS, Hnilova M, Maes M, Lin YC, Putarjunan A et al. 2015. Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522:439–43
    [Google Scholar]
  92. 92.  Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM et al. 2012. Direct interaction of ligand–receptor pairs specifying stomatal patterning. Genes Dev 26:126–36
    [Google Scholar]
  93. 93.  Li C, Yeh FL, Cheung AY, Duan Q, Kita D et al. 2015. Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife 4:e06587
    [Google Scholar]
  94. 94.  Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell 110:213–22
    [Google Scholar]
  95. 95.  Li L, Li M, Yu L, Zhou Z, Liang X et al. 2014. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe 15:329–38
    [Google Scholar]
  96. 96.  Liao H, Tang R, Zhang X, Luan S, Yu F 2017. FERONIA receptor kinase at the crossroad of hormone signaling and stress responses. Plant Cell Physiol 58:1143–50
    [Google Scholar]
  97. 97.  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
    [Google Scholar]
  98. 98.  Lin G, Zhang L, Han Z, Yang X, Liu W et al. 2017. A receptor-like protein acts as a specificity switch for the regulation of stomatal development. Genes Dev 31:1–12Structural and biochemical studies showing that the perception of EPF peptides to the ER receptors is dictated by the receptor-like protein TMM.
    [Google Scholar]
  99. 99.  Lu S-W, Chen S, Wang X, Wang J, Yu H et al. 2009. Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol. Plant Microbe Interact 22:1128–42
    [Google Scholar]
  100. 100.  MacAlister CA, Ohashi-Ito K, Bergmann DC 2007. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–40
    [Google Scholar]
  101. 101.  MacAlister CA, Ortiz-Ramirez C, Becker JD, Feijo JA, Lippman ZB 2016. Hydroxyproline O-arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens. Plant J 85:193–208
    [Google Scholar]
  102. 102.  Malinowski R, Higgins R, Luo Y, Piper L, Nazir A et al. 2009. The tomato brassinosteroid receptor BRI1 increases binding of systemin to tobacco plasma membranes, but is not involved in systemin signaling. Plant Mol. Biol. 70:603–16
    [Google Scholar]
  103. 103.  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
    [Google Scholar]
  104. 104.  Masachis S, Segorbe D, Turra D, Leon-Ruiz M, Furst U et al. 2016. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1:16043
    [Google Scholar]
  105. 105.  Matos JL, Lau OS, Hachez C, Cruz-Ramirez A, Scheres B, Bergmann DC 2014. Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module. eLife 3:e03271
    [Google Scholar]
  106. 106.  Matsubayashi Y 2014. Posttranslationally modified small-peptide signals in plants. Annu. Rev. Plant Biol. 65:385–413
    [Google Scholar]
  107. 107.  Matsubayashi Y, Shinohara H, Ogawa M 2006. Identification and functional characterization of phytosulfokine receptor using a ligand-based approach. Chem. Rec. 6:356–64
    [Google Scholar]
  108. 108.  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
    [Google Scholar]
  109. 109.  McElwain JC, Chaloner WG 1995. Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Palaeozoic. Ann. Bot. 76:389–95
    [Google Scholar]
  110. 110.  Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A et al. 2017. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358:1600–3
    [Google Scholar]
  111. 111.  Meng L, Buchanan BB, Feldman LJ, Luan S 2011. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. PNAS 109:1760–65
    [Google Scholar]
  112. 112.  Meng X, Chen X, Mang H, Liu C, Yu X et al. 2015. Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr. Biol. 25:2361–72
    [Google Scholar]
  113. 113.  Meng X, Zhou J, Tang J, Li B, de Oliveira MV et al. 2016. Ligand-induced receptor-like kinase complex regulates floral organ abscission in Arabidopsis. Cell Rep 14:1330–38Genetic and biochemical studies showing the involvement of SERK family members in the positive regulation of floral organ abscission.
    [Google Scholar]
  114. 114.  Morato do Canto A, Ceciliato PH, Ribeiro B, Ortiz Morea FA, Franco Garcia AA et al. 2014. Biological activity of nine recombinant AtRALF peptides: implications for their perception and function in Arabidopsis. Plant Physiol. Biochem 75:45–54
    [Google Scholar]
  115. 115.  Mortier V, De Wever E, Vuylsteke M, Holsters M, Goormachtig S 2012. Nodule numbers are governed by interaction between CLE peptides and cytokinin signaling. Plant J 70:367–76
    [Google Scholar]
  116. 116.  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
    [Google Scholar]
  117. 117.  Mou S, Zhang X, Han Z, Wang J, Gong X, Chai J 2017. CLE42 binding induces PXL2 interaction with SERK2. Protein Cell 8:612–17
    [Google Scholar]
  118. 118.  Müller 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
    [Google Scholar]
  119. 119.  Murphy E, De Smet I 2014. Understanding the RALF family: a tale of many species. Trends Plant Sci 19:664–71
    [Google Scholar]
  120. 120.  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
    [Google Scholar]
  121. 121.  Murphy E, Vu LD, Van den Broeck L, Lin Z, Ramakrishna P et al. 2016. RALFL34 regulates formative cell divisions in Arabidopsis pericycle during lateral root initiation. J. Exp. Bot. 67:4863–75
    [Google Scholar]
  122. 122.  Nakayama T, Shinohara H, Tanaka M, Baba K, Ogawa-Ohnishi M, Matsubayashi Y 2017. A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science 355:284–86Identifies sulfated peptides that are required for the Casparian strip formation.
    [Google Scholar]
  123. 123.  Nam KH, Li J 2002. BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–12
    [Google Scholar]
  124. 124.  Ni J, Guo Y, Jin H, Hartsell J, Clark SE 2011. Characterization of a CLE processing activity. Plant Mol. Biol. 75:67–75
    [Google Scholar]
  125. 125.  Nimchuk ZL 2017. CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop. PLOS Genet 13:e1006681
    [Google Scholar]
  126. 126.  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
    [Google Scholar]
  127. 127.  Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294
    [Google Scholar]
  128. 128.  Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y 2013. Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat. Chem. Biol 9:726–30
    [Google Scholar]
  129. 129.  Ogilvie AH, Imin N, Djordjevic AM 2014. Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes. BMC Genom 15:870
    [Google Scholar]
  130. 130.  Ohashi-Ito K, Bergmann DC 2006. Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18:2493–505
    [Google Scholar]
  131. 131.  Ohki S, Takeuchi M, Mori M 2011. The NMR structure of stomagen reveals the basis of stomatal density regulation by plant peptide hormones. Nat. Commun. 2:512
    [Google Scholar]
  132. 132.  Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y 2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat. Plants 3:17029Molecular identification of long-distance mobile signals important for nitrogen uptake in the roots.
    [Google Scholar]
  133. 133.  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
    [Google Scholar]
  134. 134.  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
    [Google Scholar]
  135. 135.  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
    [Google Scholar]
  136. 136.  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
    [Google Scholar]
  137. 137.  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
    [Google Scholar]
  138. 138.  Olsen AN, Mundy J, Skriver K 2002. Peptomics, identification of novel cationic Arabidopsis peptides with conserved sequence motifs. In Silico Biol 2:441–51
    [Google Scholar]
  139. 139.  Osipova MA, Mortier V, Demchenko KN, Tsyganov VE, Tikhonovich IA et al. 2012. WUSCHEL-RELATED HOMEOBOX5 gene expression and interaction of CLE peptides with components of the systemic control add two pieces to the puzzle of autoregulation of nodulation. Plant Physiol 158:1329–41
    [Google Scholar]
  140. 140.  Owens RJ, Northcote DH 1981. The location of arabinosyl:hydroxyproline transferase in the membrane system of potato tissue culture cells. Biochem. J. 195:661–67
    [Google Scholar]
  141. 141.  Patel N, Mohd-Radzman NA, Corcilius L, Crossett B, Connolly A et al. 2018. Diverse peptide hormones affecting root growth identified in the Medicago truncatula secreted peptidome. Mol. Cell. Proteom. 17:160–74
    [Google Scholar]
  142. 142.  Pearce G, Moura DS, Stratmann J, Ryan CA 2001. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. PNAS 98:12843–47
    [Google Scholar]
  143. 143.  Perraki A, DeFalco TA, Derbyshire P, Avila J, Séré D et al. 2018. Phosphocode-dependent functional dichotomy of a common co-receptor in plant signalling. Nature 561:248–52
    [Google Scholar]
  144. 144.  Peterson BA, Haak DC, Nishimura MT, Teixeira PJ, James SR et al. 2016. Genome-wide assessment of efficiency and specificity in CRISPR/Cas9 mediated multiple site targeting in Arabidopsis. PLOS ONE 11:e0162169
    [Google Scholar]
  145. 145.  Peterson KM, Rychel AL, Torii KU 2010. Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22:296–306
    [Google Scholar]
  146. 146.  Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y et al. 2014. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. eLife 3:e03115
    [Google Scholar]
  147. 147.  Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU 2007. Termination of asymmetric cell division and differentiation of stomata. Nature 445:501–5
    [Google Scholar]
  148. 148.  Pruitt RN, Joe A, Zhang W, Feng W, Stewart V et al. 2017. A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone. New Phytol 215:725–36
    [Google Scholar]
  149. 149.  Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F et al. 2015. The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a Gram-negative bacterium. Sci. Adv. 16:e1500245
    [Google Scholar]
  150. 150.  Qu LJ, Li L, Lan Z, Dresselhaus T 2015. Peptide signalling during the pollen tube journey and double fertilization. J. Exp. Bot. 66:5139–50
    [Google Scholar]
  151. 151.  Raghavan V 2003. Some reflections on double fertilization, from its discovery to the present. New Phytol 159:565–83
    [Google Scholar]
  152. 152.  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
    [Google Scholar]
  153. 153.  Roberts I, Smith S, Stes E, De Rybel B, Staes A et al. 2016. CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. J. Exp. Bot. 67:4889–99
    [Google Scholar]
  154. 154.  Roux M, Schwessinger B, Albrecht C, Chinchilla D, Jones A et al. 2011. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440–55
    [Google Scholar]
  155. 155.  Ruffel S, Gojon A 2017. Systemic nutrient signalling: on the road for nitrate. Nat. Plants 3:17040
    [Google Scholar]
  156. 156.  Rutter WB, Hewezi T, Maier TR, Mitchum MG, Davis EL et al. 2014. Members of the Meloidogyne avirulence protein family contain multiple plant ligand-like motifs. Phytopathology 104:879–85
    [Google Scholar]
  157. 157.  Rychel AL, Peterson KM, Torii KU 2010. Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. J. Plant Res. 123:275–80
    [Google Scholar]
  158. 158.  Santiago J, Brandt B, Wildhagen M, Hohmann U, Hothorn LA et al. 2016. Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. eLife 5:e15075Structural analysis of the IDA-HAESA-SERK1 complex disclosing how the SERK1 coreceptor allows for high-affinity sensing of the IDA peptide positively regulating floral abscission.
    [Google Scholar]
  159. 159.  Santiago J, Henzler C, Hothorn M 2013. Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341:889–92
    [Google Scholar]
  160. 160.  Schardon K, Hohl M, Graff L, Pfannstiel J, Schulze W et al. 2016. Precursor processing for plant peptide hormone maturation by subtilisin-like serine proteinases. Science 354:1594–97
    [Google Scholar]
  161. 161.  Scheer JM, Ryan CA 2002. The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. PNAS 99:9585–90
    [Google Scholar]
  162. 162.  Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J et al. 2006. Fragments of ATP synthase mediate plant perception of insect attack. PNAS 103:8894–99
    [Google Scholar]
  163. 163.  Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J et al. 2011. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLOS Genet 7:e1002046
    [Google Scholar]
  164. 164.  Seago JL, Fernando DD 2013. Anatomical aspects of angiosperm root evolution. Ann. Bot. 112:223–38
    [Google Scholar]
  165. 165.  Shinohara H, Matsubayashi Y 2015. Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand-binding point of view. Plant J 82:328–36
    [Google Scholar]
  166. 166.  Shinohara H, Mori A, Yasue N, Sumida K, Matsubayashi Y 2016. Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis. PNAS 113:3897–902
    [Google Scholar]
  167. 167.  Shiu SH, Bleecker AB 2001. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE 2001:re22
    [Google Scholar]
  168. 168.  Showalter AM, Basu D 2016. Extensin and arabinogalactan-protein biosynthesis: glycosyltransferases, research challenges, and biosensors. Front. Plant Sci. 7:814
    [Google Scholar]
  169. 169.  Somssich M, Je BI, Simon R, Jackson D 2016. CLAVATA-WUSCHEL signaling in the shoot meristem. Development 143:3238–48
    [Google Scholar]
  170. 170.  Somssich M, Ma Q, Weidtkamp-Peters S, Stahl Y, Felekyan S et al. 2015. Real-time dynamics of peptide ligand–dependent receptor complex formation in planta. Sci. Signal 8:ra76
    [Google Scholar]
  171. 171.  Song W, Liu L, Wang J, Wu Z, Zhang H et al. 2016. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res 26:674–85Elegant structural approach where a conserved peptide recognition motif in a receptor family was used to identify peptide–receptor pairs responsible for root meristem growth.
    [Google Scholar]
  172. 172.  Spincemaille P, Alborzinia H, Dekervel J, Windmolders P, van Pelt J et al. 2014. The plant decapeptide OSIP108 can alleviate mitochondrial dysfunction induced by cisplatin in human cells. Molecules 19:15088–102
    [Google Scholar]
  173. 173.  Srivastava R, Liu JX, Guo H, Yin Y, Howell SH 2009. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J 59:930–39
    [Google Scholar]
  174. 174.  Srivastava R, Liu JX, Howell SH 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]
  175. 175.  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
    [Google Scholar]
  176. 176.  Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A et al. 2017. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–89
    [Google Scholar]
  177. 177.  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
    [Google Scholar]
  178. 178.  Stes E, Gevaert K, De Smet I 2015. Phosphoproteomics-based peptide ligand–receptor kinase pairing. Commentary on: “A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion.”. Front. Plant Sci. 6:224
    [Google Scholar]
  179. 179.  Sto IM, Orr RJ, Fooyontphanich K, Jin X, Knutsen JM et al. 2015. Conservation of the abscission signaling peptide IDA during angiosperm evolution: withstanding genome duplications and gain and loss of the receptors HAE/HSL2. Front. Plant Sci. 6:931
    [Google Scholar]
  180. 180.  Strabala TJ, Phillips L, West M, Stanbra L 2014. Bioinformatic and phylogenetic analysis of the CLAVATA3/EMBRYO-SURROUNDING REGION (CLE) and the CLE-LIKE signal peptide genes in the Pinophyta. BMC Plant Biol 14:47
    [Google Scholar]
  181. 181.  Suer S, Agusti J, Sanchez P, Schwarz M, Greb T 2011. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell 23:3247–59
    [Google Scholar]
  182. 182.  Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A et al. 2010. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–44
    [Google Scholar]
  183. 183.  Sun Y, Li L, Macho AP, Han Z, Hu Z et al. 2013. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342:624–28
    [Google Scholar]
  184. 184.  Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46
    [Google Scholar]
  185. 185.  Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y et al. 2018. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–38
    [Google Scholar]
  186. 186.  Takata N, Yokota K, Ohki S, Mori M, Taniguchi T, Kurita M 2013. Evolutionary relationship and structural characterization of the EPF/EPFL gene family. PLOS ONE 8:e65183
    [Google Scholar]
  187. 187.  Takeuchi H, Higashiyama T 2012. A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLOS Biol 10:e1001449
    [Google Scholar]
  188. 188.  Takeuchi H, Higashiyama T 2016. Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:245–48
    [Google Scholar]
  189. 189.  Tamaki T, Betsuyaku S, Fujiwara M, Fukao Y, Fukuda H, Sawa S 2013. SUPPRESSOR OF LLP1 1-mediated C-terminal processing is critical for CLE19 peptide activity. Plant J 76:970–81
    [Google Scholar]
  190. 190.  Tang W, Ezcurra I, Muschietti J, McCormick S 2002. A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14:2277–87
    [Google Scholar]
  191. 191.  Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue BP 2015. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell 27:2095–118Extensive overview of peptides that provides a new classification system.
    [Google Scholar]
  192. 192.  Tena G, Boudsocq M, Sheen J 2011. Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 14:519–29
    [Google Scholar]
  193. 193.  Thynne E, Saur IM, Simbaqueba J, Ogilvie HA, Gonzalez-Cendales Y et al. 2016. Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. Mol. Plant Pathol. 18:811–24
    [Google Scholar]
  194. 194.  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
    [Google Scholar]
  195. 195.  Tucker ML, Yang R 2013. A gene encoding a peptide with similarity to the plant IDA signaling peptide (AtIDA) is expressed most abundantly in the root-knot nematode (Meloidogyne incognita) soon after root infection. Exp. Parasitol. 134:165–70
    [Google Scholar]
  196. 196.  Uchida N, Lee JS, Horst RJ, Lai HH, Kajita R et al. 2012. Regulation of inflorescence architecture by intertissue layer ligand–receptor communication between endodermis and phloem. PNAS 109:6337–42
    [Google Scholar]
  197. 197.  Vanstraelen M, Benkova E 2012. Hormonal interactions in the regulation of plant development. Annu. Rev. Cell Dev. Biol. 28:463–87
    [Google Scholar]
  198. 198.  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
    [Google Scholar]
  199. 199.  Velasquez SM, Ricardi MM, Poulsen CP, Oikawa A, Dilokpimol A et al. 2015. Complex regulation of prolyl-4-hydroxylases impacts root hair expansion. Mol. Plant 8:734–46
    [Google Scholar]
  200. 200.  Vie AK, Najafi J, Liu B, Winge P, Butenko MA et al. 2015. The IDA/IDA-LIKE and PIP/PIP-LIKE gene families in Arabidopsis: phylogenetic relationship, expression patterns, and transcriptional effect of the PIPL3 peptide. J. Exp. Bot. 66:5351–65
    [Google Scholar]
  201. 201.  Vie AK, Najafi J, Winge P, Cattan E, Wrzaczek M et al. 2017. The IDA-LIKE peptides IDL6 and IDL7 are negative modulators of stress responses in Arabidopsis thaliana. J. Exp. Bot 68:3557–71
    [Google Scholar]
  202. 202.  Wang J, Lee C, Replogle A, Joshi S, Korkin D et al. 2010. Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol 187:1003–17
    [Google Scholar]
  203. 203.  Wang J, Li H, Han Z, Zhang H, Wang T et al. 2015. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature 525:265–68
    [Google Scholar]
  204. 204.  Wang L, Einig E, Almeida-Trapp M, Albert M, Fliegmann J et al. 2018. The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nat. Plants 4:152–56
    [Google Scholar]
  205. 205.  Wang T, Liang L, Xue Y, Jia PF, Chen W et al. 2016. A receptor heteromer mediates the male perception of female attractants in plants. Nature 531:241–44
    [Google Scholar]
  206. 206.  Wang X, Baum TJ, Allen R, Ding X, Hussey RS et al. 2001. Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant Microbe Interact 14:536–44
    [Google Scholar]
  207. 207.  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
    [Google Scholar]
  208. 208.  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. PNAS 105:18625–30
    [Google Scholar]
  209. 209.  Whitford R, Fernandez A, Tejos R, Perez AC, Kleine-Vehn J et al. 2012. GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev. Cell 22:678–85
    [Google Scholar]
  210. 210.  Wildhagen M 2016. Signalling module regulating abscission in plants; an in-depth molecular study of early signalling events PhD thesis, Dep. Biosci., Univ. Oslo
  211. 211.  Wubben MJ, Gavilano L, Baum TJ, Davis EL 2015. Sequence and spatiotemporal expression analysis of CLE-motif containing genes from the reniform nematode (Rotylenchulus reniformis Linford & Oliveira). J. Nematol. 47:159–65
    [Google Scholar]
  212. 212.  Xu C, Liberatore KL, MacAlister CA, Huang Z, Chu YH et al. 2015. A cascade of arabinosyltransferases controls shoot meristem size in tomato. Nat. Genet. 47:784–92
    [Google Scholar]
  213. 213.  Xu J, Zhang S 2015. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci 20:56–64
    [Google Scholar]
  214. 214.  Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV 2011. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–30
    [Google Scholar]
  215. 215.  Yamaguchi YL, Ishida T, Yoshimura M, Imamura Y, Shimaoka C, Sawa S 2017. A collection of mutants for CLE-peptide-encoding genes in Arabidopsis generated by CRISPR/Cas9-mediated gene targeting. Plant Cell Physiol 58:1848–56
    [Google Scholar]
  216. 216.  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
    [Google Scholar]
  217. 217.  Zhang H, Han Z, Song W, Chai J 2016. Structural insight into recognition of plant peptide hormones by receptors. Mol. Plant 9:1454–63
    [Google Scholar]
  218. 218.  Zhang H, Hu Z, Lei C, Zheng C, Wang J et al. 2018. A plant phytosulfokine peptide initiates auxin-dependent immunity through cytosolic Ca2+ signaling in tomato. Plant Cell 30:652–67
    [Google Scholar]
  219. 219.  Zhang H, Lin X, Han Z, Qu LJ, Chai J 2016. Crystal structure of PXY–TDIF complex reveals a conserved recognition mechanism among CLE peptide–receptor pairs. Cell Res 26:543–55Structural analysis of the TDIF-CLE complex involved in vascular development and wood formation provides a template that discloses how CLE peptides interact with their receptors.
    [Google Scholar]
  220. 220.  Zhang T, Chen S, Harmon AC 2016. Protein–protein interactions in plant mitogen-activated protein kinase cascades. J. Exp. Bot. 67:607–18
    [Google Scholar]
  221. 221.  Zhang X, Liu W, Nagae TT, Takeuchi H, Zhang H et al. 2017. Structural basis for receptor recognition of pollen tube attraction peptides. Nat. Commun. 8:1331
    [Google Scholar]
  222. 222.  Zhang Y, Wang P, Shao W, Zhu JK, Dong J 2015. The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. Dev. Cell 33:136–49
    [Google Scholar]
  223. 223.  Zhou Y, Yan A, Han H, Li T, Geng Y et al. 2018. HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 361:502–6
    [Google Scholar]
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