Peptide Ligands in Plants

Enzymes

Volumn 35, Issue , 2014, Pages 85-112

  Kondo, Yuki ^a   Hirakawa, Yuki ^b   Fukuda, Hiroo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

Ligand; Modification; Peptides; Plants; Processing; Receptor; Signaling

Indexed keywords

EID: 84907999595     PISSN: 18746047     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-801922-1.00004-X     Document Type: Chapter

References (152)

1. Matsubayashi Y. Small post-translationally modified peptide signals in Arabidopsis. Arabidopsis Book 2011, 9:e0150.
2. Czyzewicz N., Yue K., Beeckman T., De Smet I. Message in a bottle: Small signalling peptide outputs during growth and development. J. Exp. Bot. 2013, 64:5281-5296.
3. Matsubayashi Y., Sakagami Y. Peptide hormones in plants. Annu. Rev. Plant Biol. 2006, 57:649-674.
4. Butenko M.A., Vie A.K., Brembu T., Aalen R.B., Bones A.M. Plant peptides in signalling: Looking for new partners. Trends Plant Sci. 2009, 14:255-263.
5. Hirakawa Y., Kondo Y., Fukuda H. Establishment and maintenance of vascular cell communities through local signaling. Curr. Opin. Plant Biol. 2011, 14:17-23.
6. Perales M., Reddy G.V. Stem cell maintenance in shoot apical meristems. Curr. Opin. Plant Biol. 2012, 15:10-16.
7. Shpak E.D. Diverse roles of ERECTA family genes in plant development. J. Integr. Plant Biol. 2013, 55:1238-1250.
8. Endo S., Shinohara H., Matsubayashi Y., Fukuda H. A novel pollen-pistil interaction conferring high-temperature tolerance during reproduction via CLE45 signaling. Curr. Biol. 2013, 23:1670-1676.
9. Okamoto S., Shinohara H., Mori T., Matsubayashi Y., Kawaguchi M. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 2013, 4:2191.
10. Cho H., Ryu H., Rho S., Hill K., Smith S., Audenaert D., Park J., Han S., Beeckman T., Bennett M.J., Hwang D., De Smet I., Hwang I. A secreted peptide acts on BIN2-mediated phosphorylation of ARFs to potentiate auxin response during lateral root development. Nat. Cell Biol. 2014, 16:66-76.
11. Gudesblat G.E., Schneider-Pizon J., Betti C., Mayerhofer J., Vanhoutte I., van Dongen W., Boeren S., Zhiponova M., de Vries S., Jonak C., Russinova E. SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat. Cell Biol. 2012, 14:548-554.
12. Kim T.W., Michniewicz M., Bergmann D.C., Wang Z.Y. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 2012, 482:419-422.
13. Kondo Y., Hirakawa Y., Kieber J.J., Fukuda H. CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol. 2011, 52:37-48.
14. Kondo Y., Ito T., Nakagami H., Hirakawa Y., Saito M., Tamaki T., Shirasu K., Fukuda H. Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling. Nat. Commun. 2014, 5:3504.
15. Tintor N., Ross A., Kanehara K., Yamada K., Fan L., Kemmerling B., Nurnberger T., Tsuda K., Saijo Y. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:6211-6216.
16. Zipfel C. Combined roles of ethylene and endogenous peptides in regulating plant immunity and growth. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:5748-5749.
17. Jun J.H., Fiume E., Fletcher J.C. The CLE family of plant polypeptide signaling molecules. Cell. Mol. Life Sci. 2008, 65:743-755.
18. Oelkers K., Goffard N., Weiller G.F., Gresshoff P.M., Mathesius U., Frickey T. Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol. 2008, 8:1.
19. Cock J.M., McCormick S. A large family of genes that share homology with CLAVATA3. Plant Physiol. 2001, 126:939-942.
20. Rojo E., Sharma V.K., Kovaleva V., Raikhel N.V., Fletcher J.C. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 2002, 14:969-977.
21. Ito Y., Nakanomyo I., Motose H., Iwamoto K., Sawa S., Dohmae N., Fukuda H. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 2006, 313:842-845.
22. Ohyama K., Shinohara H., Ogawa-Ohnishi M., Matsubayashi Y. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat. Chem. Biol. 2009, 5:578-580.
23. Tamaki T., Betsuyaku S., Fujiwara M., Fukao Y., Fukuda H., Sawa S. SUPPRESSOR OF LLP1 1-mediated C-terminal processing is critical for CLE19 peptide activity. Plant J. 2013, 76:970-981.
24. Ogawa-Ohnishi M., Matsushita W., Matsubayashi Y. Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nat. Chem. Biol. 2013, 9:726-730.
25. Gou X., He K., Yang H., Yuan T., Lin H., Clouse S.D., Li J. Genome-wide cloning and sequence analysis of leucine-rich repeat receptor-like protein kinase genes in Arabidopsis thaliana. BMC Genomics 2010, 11:19.
26. Shiu S.H., Karlowski W.M., Pan R.S., Tzeng Y.H., Mayer K.F.X., Li W.H. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004, 16:1220-1234.
27. Betsuyaku S., Sawa S., Yamada M. The function of the CLE peptides in plant development and plant-microbe interactions. Arabidopsis Book 2011, 9:e0149.
28. Clark S.E., Running M.P., Meyerowitz E.M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 1993, 119:397-418.
29. Clark S.E., Running M.P., Meyerowitz E.M. Clavata3 is a specific regulator of shoot and floral meristem development affecting the same processes as Clavata1. Development 1995, 121:2057-2067.
30. Kayes J.M., Clark S.E. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 1998, 125:3843-3851.
31. Fletcher J.C. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 1999, 283:1911-1914.
32. Clark S.E., Williams R.W., Meyerowitz E.M. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 1997, 89:575-585.
33. Jeong S., Trotochaud A.E., Clark S.E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 1999, 11:1925-1933.
34. Ogawa M. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 2008, 319:294.
35. DeYoung B.J., Bickle K.L., Schrage K.J., Muskett P., Patel K., Clark S.E. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 2006, 45:1-16.
36. Kinoshita A., Betsuyaku S., Osakabe Y., Mizuno S., Nagawa S., Stahl Y., Simon R., Yamaguchi-Shinozaki K., Fukuda H., Sawa S. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 2010, 137:3911-3920.
37. Miwa H., Betsuyaku S., Iwamoto K., Kinoshita A., Fukuda H., Sawa S. The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol. 2008, 49:1752-1757.
38. Muller R., Bleckmann A., Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 2008, 20:934-946.
39. Shinohara H., Moriyama Y., Ohyama K., Matsubayashi Y. Biochemical mapping of a ligand-binding domain within Arabidopsis BAM1 reveals diversified ligand recognition mechanisms of plant LRR-RKs. Plant J. 2012, 70:845-854.
40. Brand U., Fletcher J.C., Hobe M., Meyerowitz E.M., Simon R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 2000, 289:617-619.
41. Schoof H., Lenhard M., Haecker A., Mayer K.F.X., Jurgens G., Laux T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 2000, 100:635-644.
42. Stone J.M., Trotochaud A.E., Walker J.C., Clark S.E. Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiol. 1998, 117:1217-1225.
43. Stone J.M., Collinge M.A., Smith R.D., Horn M.A., Walker J.C. Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science 1994, 266:793-795.
44. Williams R.W., Wilson J.M., Meyerowitz E.M. A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:10467-10472.
45. Yu L.P., Miller A.K., Clark S.E. POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Curr. Biol. 2003, 13:179-188.
46. Yu L.P., Simon E.J., Trotochaud A.E., Clark S.E. POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci. Development 2000, 127:1661-1670.
47. Bommert P., Je B.I., Goldshmidt A., Jackson D. The maize Galpha gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 2013, 502:555-558.
48. Ohyama K., Ogawa M., Matsubayashi Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J. 2008, 55:152-160.
49. Hirakawa Y., Shinohara H., Kondo Y., Inoue A., Nakanomyo I., Ogawa M., Sawa S., Ohashi-Ito K., Matsubayashi Y., Fukuda H. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15208-15213.
50. Whitford R., Fernandez A., De Groodt R., Ortega E., Hilson P. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:18625-18630.
51. Fisher K., Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 2007, 17:1061-1066.
52. Hirakawa Y., Kondo Y., Fukuda H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 2010, 22:2618-2629.
53. Stahl Y., Wink R.H., Ingram G.C., Simon R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 2009, 19:909-914.
54. Stahl Y., Grabowski S., Bleckmann A., Kuhnemuth R., Weidtkamp-Peters S., Pinto K.G., Kirschner G.K., Schmid J.B., Wink R.H., Hulsewede A., Felekyan S., Seidel C.A., Simon R. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 2013, 23:362-371.
55. Depuydt S., Rodriguez-Villalon A., Santuari L., Wyser-Rmili C., Ragni L., Hardtke C.S. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:7074-7079.
56. Araya T., Miyamoto M., Wibowo J., Suzuki A., Kojima S., Tsuchiya Y.N., Sawa S., Fukuda H., von Wiren N., Takahashi H. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:2029-2034.
57. Bidadi H., Matsuoka K., Sage-Ono K., Fukushima J., Pitaksaringkarn W., Asahina M., Yamaguchi S., Sawa S., Fukuda H., Matsubayashi Y., Ono M., Satoh S. CLE6 expression recovers gibberellin deficiency to promote shoot growth in Arabidopsis. Plant J. 2014, 78:241-252.
58. Suzaki T., Toriba T., Fujimoto M., Tsutsumi N., Kitano H., Hirano H.Y. Conservation and diversification of meristem maintenance mechanism in Oryza sativa: Function of the FLORAL ORGAN NUMBER2 gene. Plant Cell Physiol. 2006, 47:1591-1602.
59. Ohmori Y., Tanaka W., Kojima M., Sakakibara H., Hirano H.Y. WUSCHEL-RELATED HOMEOBOX4 is involved in meristem maintenance and is negatively regulated by the CLE gene FCP1 in rice. Plant Cell 2013, 25:229-241.
60. Suzaki T., Yoshida A., Hirano H.Y. Functional diversification of CLAVATA3-related CLE proteins in meristem maintenance in rice. Plant Cell 2008, 20:2049-2058.
61. Suzaki T., Ohneda M., Toriba T., Yoshida A., Hirano H.Y. FON2 SPARE1 redundantly regulates floral meristem maintenance with FLORAL ORGAN NUMBER2 in rice. PLoS Genet. 2009, 5:e1000693.
62. Mortier V., Den Herder G., Whitford R., Van de Velde W., Rombauts S., D'Haeseleer K., Holsters M., Goormachtig S. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol. 2010, 153:222-237.
63. Miyazawa H., Oka-Kira E., Sato N., Takahashi H., Wu G.J., Sato S., Hayashi M., Betsuyaku S., Nakazono M., Tabata S., Harada K., Sawa S., Fukuda H., Kawaguchi M. The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development 2010, 137:4317-4325.
64. Okamoto S., Ohnishi E., Sato S., Takahashi H., Nakazono M., Tabata S., Kawaguchi M. Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol. 2009, 50:67-77.
65. Ryan C.A. Assay and biochemical properties of the proteinase inhibitor-inducing factor, a wound hormone. Plant Physiol. 1974, 54:328-332.
66. Pearce G., Strydom D., Johnson S., Ryan C.A. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 1991, 253:895-897.
67. Mcgurl B., Pearce G., Orozcocardenas M., Ryan C.A. Structure, expression, and antisense inhibition of the systemin precursor gene. Science 1992, 255:1570-1573.
68. Li J., Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 1997, 90:929-938.
69. Meindl T., Boller T., Felix G. The plant wound hormone systemin binds with the N-terminal part to its receptor but needs the C-terminal part to activate it. Plant Cell 1998, 10:1561-1570.
70. Wang Z.Y., Seto H., Fujioka S., Yoshida S., Chory J. BRI1 is a critical component of a plasma-membrane receptor for plant. Nature 2001, 410:380-383.
71. Ryan C.A. The systemin signaling pathway: Differential activation of plant defensive genes. Biochim. Biophys. Acta 2000, 1477:112-121.
72. Pearce G., Moura D.S., Stratmann J., Ryan C.A. Production of multiple plant hormones from a single polyprotein precursor. Nature 2001, 411:817-820.
73. Huffaker A., Pearce G., Ryan C.A. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10098-10103.
74. Bartels S., Lori M., Mbengue M., van Verk M., Klauser D., Hander T., Boni R., Robatzek S., Boller T. The family of Peps and their precursors in Arabidopsis: Differential expression and localization but similar induction of pattern-triggered immune responses. J. Exp. Bot. 2013, 64:5309-5321.
75. Huffaker A., Ryan C.A. Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:10732-10736.
76. Yamaguchi Y., Pearce G., Ryan C.A. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10104-10109.
77. Krol E., Mentzel T., Chinchilla D., Boller T., Felix G., Kemmerling B., Postel S., Arents M., Jeworutzki E., Al-Rasheid K.A.S., Becker D., Hedrich R. Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J. Biol. Chem. 2010, 285:13471-13479.
78. Yamaguchi Y., Huffaker A., Bryan A.C., Tax F.E., Ryan C.A. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 2010, 22:508-522.
79. Matsubayashi Y., Sakagami Y. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:7623-7627.
80. Matsubayashi Y., Takagi L., Omura N., Morita A., Sakagami Y. The endogenous sulfated pentapeptide phytosulfokine-alpha stimulates tracheary element differentiation of isolated mesophyll cells of Zinnia. Plant Physiol. 1999, 120:1043-1048.
81. Matsubayashi Y., Ogawa M., Kihara H., Niwa M., Sakagami Y. Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol. 2006, 142:45-53.
82. Srivastava R., Liu J.X., Howell S.H. Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J. 2008, 56:219-227.
83. Komori R., Amano Y., Ogawa-Ohnishi M., Matsubayashi Y. Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:15067-15072.
84. Matsubayashi Y., Ogawa M., Morita A., Sakagami Y. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 2002, 296:1470-1472.
85. Amano Y., Tsubouchi H., Shinohara H., Ogawa M., Matsubayashi Y. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18333-18338.
86. Mosher S., Seybold H., Rodriguez P., Stahl M., Davies K.A., Dayaratne S., Morillo S.A., Wierzba M., Favery B., Keller H., Tax F.E., Kemmerling B. The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J. 2013, 73:469-482.
87. Matsuzaki Y., Ogawa-Ohnishi M., Mori A., Matsubayashi Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 2010, 329:1065-1067.
88. Meng L., Buchanan B.B., Feldman L.J., Luan S. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:1760-1765.
89. Whitford R., Fernandez A., Tejos R., Perez A.C., Kleine-Vehn J., Vanneste S., Drozdzecki A., Leitner J., Abas L., Aerts M., Hoogewijs K., Baster P., De Groodt R., Lin Y.C., Storme V., Van de Peer Y., Beeckman T., Madder A., Devreese B., Luschnig C., Friml J., Hilson P. GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev. Cell 2012, 22:678-685.
90. Butenko M.A., Patterson S.E., Grini P.E., Stenvik G.E., Amundsen S.S., Mandal A., Aalen R.B. Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 2003, 15:2296-2307.
91. Stenvik G.E., Tandstad N.M., Guo Y., Shi C.L., Kristiansen W., Holmgren A., Clark S.E., Aalen R.B., Butenko M.A. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 2008, 20:1805-1817.
92. Cho S.K., Larue C.T., Chevalier D., Wang H., Jinn T.L., Zhang S., Walker J.C. Regulation of floral organ abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15629-15634.
93. Jinn T.L., Stone J.M., Walker J.C. HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev. 2000, 14:108-117.
94. Shiu S.H., Bleecker A.B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10763-10768.
95. Kumpf R.P., Shi C.L., Larrieu A., Sto I.M., Butenko M.A., Peret B., Riiser E.S., Bennett M.J., Aalen R.B. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:5235-5240.
96. Delay C., Imin N., Djordjevic M.A. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. J. Exp. Bot. 2013, 64:5383-5394.
97. Imin N., Mohd-Radzman N.A., Ogilvie H.A., Djordjevic M.A. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. J. Exp. Bot. 2013, 64:5395-5409.
98. Hara K., Kajita R., Torii K.U., Bergmann D.C., Kakimoto T. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev. 2007, 21:1720-1725.
99. Hara K., Yokoo T., Kajita R., Onishi T., Yahata S., Peterson K.M., Torii K.U., Kakimoto T. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol. 2009, 50:1019-1031.
100. Kondo T., Kajita R., Miyazaki A., Hokoyama M., Nakamura-Miura T., Mizuno S., Masuda Y., Irie K., Tanaka Y., Takada S., Kakimoto T., Sakagami Y. Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol. 2010, 51:1-8.
101. Sugano S.S., Shimada T., Imai Y., Okawa K., Tamai A., Mori M., Hara-Nishimura I. Stomagen positively regulates stomatal density in Arabidopsis. Nature 2010, 463:241-244.
102. Ohki S., Takeuchi M., Mori M. The NMR structure of stomagen reveals the basis of stomatal density regulation by plant peptide hormones. Nat. Commun. 2011, 2:512.
103. Hunt L., Gray J.E. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 2009, 19:864-869.
104. Hunt L., Bailey K.J., Gray J.E. The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol. 2010, 186:609-614.
105. Abrash E.B., Bergmann D.C. Regional specification of stomatal production by the putative ligand CHALLAH. Development 2010, 137:447-455.
106. Abrash E.B., Davies K.A., Bergmann D.C. Generation of signaling specificity in Arabidopsis by spatially restricted buffering of ligand-receptor interactions. Plant Cell 2011, 23:2864-2879.
107. Uchida N., Lee J.S., Horst R.J., Lai H.H., Kajita R., Kakimoto T., Tasaka M., Torii K.U. Regulation of inflorescence architecture by intertissue layer ligand-receptor communication between endodermis and phloem. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:6337-6342.
108. Lee J.S., Kuroha T., Hnilova M., Khatayevich D., Kanaoka M.M., McAbee J.M., Sarikaya M., Tamerler C., Torii K.U. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev. 2012, 26:126-136.
109. Bergmann D.C., Lukowitz W., Somerville C.R. Stomatal development and pattern controlled by a MAPKK kinase. Science 2004, 304:1494-1497.
110. Wang H., Ngwenyama N., Liu Y., Walker J.C., Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 2007, 19:63-73.
111. Okuda S., Tsutsui H., Shiina K., Sprunck S., Takeuchi H., Yui R., Kasahara R.D., Hamamura Y., Mizukami A., Susaki D., Kawano N., Sakakibara T., Namiki S., Itoh K., Otsuka K., Matsuzaki M., Nozaki H., Kuroiwa T., Nakano A., Kanaoka M.M., Dresselhaus T., Sasaki N., Higashiyama T. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 2009, 458:357-361.
112. Higashiyama T., Yabe S., Sasaki N., Nishimura Y., Miyagishima S., Kuroiwa H., Kuroiwa T. Pollen tube attraction by the synergid cell. Science 2001, 293:1480-1483.
113. Takeuchi H., Higashiyama T. A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol. 2012, 10:e1001449.
114. Tantikanjana T., Nasrallah M.E., Nasrallah J.B. Complex networks of self-incompatibility signaling in the Brassicaceae. Curr. Opin. Plant Biol. 2010, 13:520-526.
115. Schopfer C.R., Nasrallah M.E., Nasrallah J.B. The male determinant of self-incompatibility in Brassica. Science 1999, 286:1697-1700.
116. Takayama S., Shiba H., Iwano M., Shimosato H., Che F.S., Kai N., Watanabe M., Suzuki G., Hinata K., Isogai A. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:1920-1925.
117. Kachroo A., Schopfer C.R., Nasrallah M.E., Nasrallah J.B. Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 2001, 293:1824-1826.
118. Takayama S., Shimosato H., Shiba H., Funato M., Che F.S., Watanabe M., Iwano M., Isogai A. Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 2001, 413:534-538.
119. Chookajorn T., Kachroo A., Ripoll D.R., Clark A.G., Nasrallah J.B. Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:911-917.
120. Mishima M., Takayama S., Sasaki K., Jee J.G., Kojima C., Isogai A., Shirakawa M. Structure of the male determinant factor for Brassica self-incompatibility. J. Biol. Chem. 2003, 278:36389-36395.
121. Nasrallah J.B., Kao T.H., Chen C.H., Goldberg M.L., Nasrallah M.E. Amino-acid sequence of glycoproteins encoded by 3 alleles of the S-locus of Brassica oleracea. Nature 1987, 326:617-619.
122. Stein J.C., Howlett B., Boyes D.C., Nasrallah M.E., Nasrallah J.B. Molecular-cloning of a putative receptor protein-kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:8816-8820.
123. Takasaki T., Hatakeyama K., Suzuki G., Watanabe M., Isogai A., Hinata K. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 2000, 403:913-916.
124. Takayama S., Isogai A., Tsukamoto C., Ueda Y., Hinata K., Okazaki K., Suzuki A. Sequences of S-glycoproteins, products of the Brassica campestris self-incompatibility locus. Nature 1987, 326:102-105.
125. Dixit R., Nasrallah M.E., Nasrallah J.B. Post-transcriptional maturation of the S receptor kinase of Brassica correlates with co-expression of the S-Locus glycoprotein in the stigmas of two Brassica strains and in transgenic tobacco plants. Plant Physiol. 2000, 124:297-311.
126. Nasrallah M.E., Liu P., Nasrallah J.B. Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A-lyrata. Science 2002, 297:247-249.
127. Nasrallah M.E., Liu P., Sherman-Broyles S., Boggs N.A., Nasrallah J.B. Natural variation in expression of self-incompatibility in Arabidopsis thaliana: Implications for the evolution of selfing. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16070-16074.
128. Kakita M., Murase K., Iwano M., Matsumoto T., Watanabe M., Shiba H., Isogai A., Takayama S. Two distinct forms of M-locus protein kinase localize to the plasma membrane and interact directly with S-Locus receptor kinase to transduce self-incompatibility signaling in Brassica rapa. Plant Cell 2007, 19:3961-3973.
129. Murase K., Shiba H., Iwano M., Che F.S., Watanabe M., Isogai A., Takayama S. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 2004, 303:1516-1519.
130. Stone S.L., Anderson E.M., Mullen R.T., Goring D.R. ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 2003, 15:885-898.
131. Samuel M.A., Chong Y.T., Haasen K.E., Aldea-Brydges M.G., Stone S.L., Goring D.R. Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 2009, 21:2655-2671.
132. Vanoosthuyse V., Miege C., Dumas C., Cock J.M. Two large Arabidopsis thaliana gene families are homologous to the Brassica gene superfamily that encodes pollen coat proteins and the male component of the self-incompatibility response. Plant Mol. Biol. 2001, 46:17-34.
133. Pearce G., Moura D.S., Stratmann J., Ryan C.A. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12843-12847.
134. Pearce G., Yamaguchi Y., Munske G., Ryan C.A. Structure-activity studies of RALF, rapid alkalinization factor, reveal an essential-YISY-Motif. Peptides 2010, 31:1973-1977.
135. Matos J.L., Fiori C.S., Silva-Filho M.C., Moura D.S. A conserved dibasic site is essential for correct processing of the peptide hormone AtRALF1 in Arabidopsis thaliana. FEBS Lett. 2008, 582:3343-3347.
136. Haruta M., Sabat G., Stecker K., Minkoff B.B., Sussman M.R. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 2014, 343:408-411.
137. Escobar-Restrepo J.M., Huck N., Kessler S., Gagliardini V., Gheyselinck J., Yang W.C., Grossniklaus U. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 2007, 317:656-660.
138. 2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: Identification of AtRALF1 peptide. Biochemistry 2008, 47:6311-6321.
139. Cornbier J.P., Kuster H., Journet E.P., Hohnjec N., Gamas P., Niebel A. Evidence for the involvement in nodulation of the two small putative regulatory peptide-encoding genes MtRALFL1 and MtDVL1. Mol. Plant Microbe Interact. 2008, 21:1118-1127.
140. Covey P.A., Subbaiah C.C., Parsons R.L., Pearce G., Lay F.T., Anderson M.A., Ryan C.A., Bedinger P.A. A pollen-specific RALF from tomato that regulates pollen tube elongation. Plant Physiol. 2010, 153:703-715.
141. Duan Q.H., Kita D., Johnson E.A., Aggarwal M., Gates L., Wu H.M., Cheung A.Y. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Commun. 2014, 5:3129.
142. Motose H., Fukuda H., Sugiyama M. Involvement of local intercellular communication in the differentiation of Zinnia mesophyll cells into tracheary elements. Planta 2001, 213:121-131.
143. Motose H., Sugiyama M., Fukuda H. A proteoglycan mediates inductive interaction during plant vascular development. Nature 2004, 429:873-878.
144. Kobayashi Y., Motose H., Iwamoto K., Fukuda H. Expression and genome-wide analysis of the xylogen-type gene family. Plant Cell Physiol. 2011, 52:1095-1106.
145. Yang S.L., Xiea L.F., Mao H.Z., Puah C.S., Yang W.C., Jiang L.X., Sundaresan V., Ye D. TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 2003, 15:2792-2804.
146. Jia G.X., Liu X.D., Owen H.A., Zhao D.Z. Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:2220-2225.
147. Yang S.L., Jiang L.X., Puah C.S., Xie L.F., Zhang X.Q., Chen L.Q., Yang W.C., Ye D. Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS. Plant Physiol. 2005, 139:186-191.
148. Wang C.J.R., Nan G.L., Kelliher T., Timofejeva L., Vernoud V., Golubovskaya I.N., Harper L., Egger R., Walbot V., Cande W.Z. Maize multiple archesporial cells 1 (mac1), an ortholog of rice TDL1A, modulates cell proliferation and identity in early anther development. Development 2012, 139:2594-2603.
149. Canales C., Bhatt A.M., Scott R., Dickinson H. EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr. Biol. 2002, 12:1718-1727.
150. Zhao D.Z., Wang G.F., Speal B., Ma H. The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 2002, 16:2021-2031.
151. Albrecht C., Russinova E., Hecht V., Baaijens E., de Vries S. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 2005, 17:3337-3349.
152. Colcombet J., Boisson-Dernier A., Ros-Palau R., Vera C.E., Schroeder J.I. Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 2005, 17:3350-3361.