Peptide signaling in plant development

Current Biology

Volumn 21, Issue 9, 2011, Pages

  Katsir, Leron ^a   Davies, Kelli A ^b   Bergmann, Dominique C ^b   Laux, Thomas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CLV3 PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; EPF1 PROTEIN, ARABIDOPSIS; SIGNAL PEPTIDE; TRANSCRIPTION FACTOR;

BIOLOGICAL MODEL; CELL COMMUNICATION; CELL DIFFERENTIATION; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MERISTEM; MULTIGENE FAMILY; PHYSIOLOGY; PLANT; PLANT ROOT; PLANT STOMA; REVIEW; SIGNAL TRANSDUCTION;

ARABIDOPSIS PROTEINS; BIOLOGICAL EVOLUTION; CELL COMMUNICATION; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; MERISTEM; MODELS, BIOLOGICAL; MULTIGENE FAMILY; PLANT ROOTS; PLANT STOMATA; PLANTS; PROTEIN SORTING SIGNALS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 79955652217     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2011.03.012     Document Type: Review

References (79)

1. H.G. Dohlman, and J.W. Thorner Regulation of G protein-initiated signal transduction in yeast: paradigms and principles Annu. Rev. Biochem. 70 2001 703 754 (Pubitemid 32662223)
2. C.A. Ryan, G. Pearce, J. Scheer, and D.S. Moura Polypeptide hormones Plant Cell 14 Suppl 2002 S251 S264
3. S. Takayama, and A. Isogai Self-incompatibility in plants Annu. Rev. Plant Biol. 56 2005 467 489 (Pubitemid 40802418)
4. M.A. Butenko, A.K. Vie, T. Brembu, R.B. Aalen, and A.M. Bones Plant peptides in signalling: looking for new partners Trends Plant Sci. 14 2009 255 263
5. M.H. Rowe, and D.C. Bergmann Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development Curr. Opin. Plant Biol. 13 2010 548 555
6. H. Shinohara, and Y. Matsubayashi Arabinosylated glycopeptide hormones: new insights into CLAVATA3 structure Curr. Opin. Plant Biol. 13 2010 515 519
7. M. Koornneef, J. Van Eden, C.J. Hanhart, P. Stam, F.J. Braaksma, and W.J. Feenstra Linkage map of Arabidopsis thaliana J. Hered. 74 1983 265 272
8. H.M.O. Leyser, and I.J. Furner Characterization of three shoot apical meristem mutants of Arabidopsis thaliana Development 116 1992 397 403
9. U. Brand, J.C. Fletcher, M. Hobe, E.M. Meyerowitz, and R. Simon Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity Science 289 2000 617 619 (Pubitemid 30622065)
10. S.E. Clark, R.W. Williams, and E.M. Meyerowitz The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis Cell 89 1997 575 585 (Pubitemid 27511768)
11. H. Schoof, M. Lenhard, A. Haecker, K.F. Mayer, G. Jurgens, and T. Laux The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes Cell 100 2000 635 644
12. J.M. Kayes, and S.E. Clark CLAVATA2, a regulator of meristem and organ development in Arabidopsis Development 125 1998 3843 3851 (Pubitemid 28488359)
13. J.C. Fletcher, U. Brand, M.P. Running, R. Simon, and E.M. Meyerowitz Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems Science 283 1999 1911 1914
14. S. Jeong, A.E. Trotochaud, and S.E. Clark The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase Plant Cell 11 1999 1925 1934
15. J.M. Cock, and S. McCormick A large family of genes that share homology with CLAVATA3 Plant Physiol. 126 2001 939 942 (Pubitemid 32656781)
16. K. Oelkers, N. Goffard, G.F. Weiller, P.M. Gresshoff, U. Mathesius, and T. Frickey Bioinformatic analysis of the CLE signaling peptide family BMC Plant Biol. 8 2008 1
17. M. Fiers, E. Golemiec, R. van der Schors, L. van der Geest, K.W. Li, W.J. Stiekema, and C.M. Liu The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences Plant Physiol. 141 2006 1284 1292 (Pubitemid 44223281)
18. Y. Ito, I. Nakanomyo, H. Motose, K. Iwamoto, S. Sawa, N. Dohmae, and H. Fukuda Dodeca-CLE peptides as suppressors of plant stem cell differentiation Science 313 2006 842 845 (Pubitemid 44223354)
19. T. Kondo, S. Sawa, A. Kinoshita, S. Mizuno, T. Kakimoto, H. Fukuda, and Y. Sakagami A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis Science 313 2006 845 848 (Pubitemid 44223355)
20. K. Ohyama, H. Shinohara, M. Ogawa-Ohnishi, and Y. Matsubayashi A glycopeptide regulating stem cell fate in Arabidopsis thaliana Nat. Chem. Biol. 5 2009 578 580
21. J. Ni, and S.E. Clark Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain Plant Physiol. 140 2006 726 733 (Pubitemid 43956291)
22. J. Ni, Y. Guo, H. Jin, J. Hartsell, and S.E. Clark Characterization of a CLE processing activity Plant Mol. Biol. 75 2010 67 75
23. J. Jun, E. Fiume, A.H. Roeder, L. Meng, V.K. Sharma, K.S. Osmont, C. Baker, C.M. Ha, E.M. Meyerowitz, and L.J. Feldman Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis Plant Physiol. 154 2010 1721 1736
24. R. Whitford, A. Fernandez, R. De Groodt, E. Ortega, and P. Hilson Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells Proc. Natl. Acad. Sci. USA 105 2008 18625 18630
25. T.J. Strabala, P.J. O'Donnell, A.M. Smit, C. Ampomah-Dwamena, E.J. Martin, N. Netzler, N.J. Nieuwenhuizen, B.D. Quinn, H.C. Foote, and K.R. Hudson Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain Plant Physiol. 140 2006 1331 1344 (Pubitemid 43956218)
26. A. Kinoshita, Y. Nakamura, E. Sasaki, J. Kyozuka, H. Fukuda, and S. Sawa Gain-of-function phenotypes of chemically synthetic CLAVATA3/ESR-related (CLE) peptides in Arabidopsis thaliana and Oryza sativa Plant Cell Physiol. 48 2007 1821 1825 (Pubitemid 350262244)
27. L. Meng, and L.J. Feldman CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis Planta 232 2010 1061 1074
28. T. Kondo, T. Nakamura, K. Yokomine, and Y. Sakagami Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides Biochem. Biophys. Res. Commun. 377 2008 312 316
29. Y. Hirakawa, H. Shinohara, Y. Kondo, A. Inoue, I. Nakanomyo, M. Ogawa, S. Sawa, K. Ohashi-Ito, Y. Matsubayashi, and H. Fukuda Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system Proc. Natl. Acad. Sci. USA 105 2008 15208 15213
30. A. Leibfried, J.P. To, W. Busch, S. Stehling, A. Kehle, M. Demar, J.J. Kieber, and J.U. Lohmann WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators Nature 438 2005 1172 1175 (Pubitemid 41831688)
31. R.K. Yadav, M. Tavakkoli, and G.V. Reddy WUSCHEL mediates stem cell homeostasis by regulating stem cell number and patterns of cell division and differentiation of stem cell progenitors Development 137 2010 3581 3589
32. G.V. Reddy, and E.M. Meyerowitz Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex Science 310 2005 663 667 (Pubitemid 41528156)
33. M. Lenhard, and T. Laux Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1 Development 130 2003 3163 3173 (Pubitemid 36926954)
34. R. Muller, L. Borghi, D. Kwiatkowska, P. Laufs, and R. Simon Dynamic and compensatory responses of Arabidopsis shoot and floral meristems to CLV3 signaling Plant Cell 18 2006 1188 1198 (Pubitemid 43956125)
35. Z.L. Nimchuk, P.T. Tarr, C. Ohno, X. Qu, and E.M. Meyerowitz Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase Curr. Biol. 21 2011 1 8
36. M. Hobe, R. Muller, M. Grunewald, U. Brand, and R. Simon Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis Dev. Genes Evol. 213 2003 371 381 (Pubitemid 37080676)
37. R. Muller, A. Bleckmann, and R. Simon The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1 Plant Cell 20 2008 934 946 (Pubitemid 352843971)
38. Y. Guo, L. Han, M. Hymes, R. Denver, and S.E. Clark CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification Plant J. 63 2010 889 900
39. A. Bleckmann, S. Weidtkamp-Peters, C.A. Seidel, and R. Simon Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane Plant Physiol. 152 2010 166 176
40. Y. Zhu, Y. Wang, R. Li, X. Song, Q. Wang, S. Huang, J.B. Jin, C.M. Liu, and J. Lin Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis Plant J. 61 2010 223 233
41. B.J. DeYoung, K.L. Bickle, K.J. Schrage, P. Muskett, K. Patel, and S.E. Clark The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis Plant J. 45 2006 1 16 (Pubitemid 43373728)
42. A. Kinoshita, S. Betsuyaku, Y. Osakabe, S. Mizuno, S. Nagawa, Y. Stahl, R. Simon, K. Yamaguchi-Shinozaki, H. Fukuda, and S. Sawa RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis Development 137 2010 3911 3920
43. S. Betsuyaku, F. Takahashi, A. Kinoshita, H. Miwa, K. Shinozaki, H. Fukuda, and S. Sawa Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis Plant Cell Physiol. 52 2011 14 29
44. L.P. Yu, E.J. Simon, A.E. Trotochaud, and S.E. Clark POLTERGEIST functions to regulate meristem development downstream of the CLAVATA loci Development 127 2000 1661 1670 (Pubitemid 30234923)
45. L.P. Yu, A.K. Miller, and S.E. Clark POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems Curr. Biol. 13 2003 179 188 (Pubitemid 36178295)
46. A.E. Trotochaud, T. Hao, G. Wu, Z. Yang, and S.E. Clark The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein Plant Cell 11 1999 393 406
47. R.W. Williams, J.M. Wilson, and E.M. Meyerowitz A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway Proc. Natl. Acad. Sci. USA 94 1997 10467 10472 (Pubitemid 27407065)
48. S.K. Song, M.M. Lee, and S.E. Clark POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells Development 133 2006 4691 4698 (Pubitemid 46063081)
49. S.K. Song, H. Hofhuis, M.M. Lee, and S.E. Clark Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis Dev. Cell 15 2008 98 109 (Pubitemid 351895603)
50. K. Shah, E. Russinova, T.W. Gadella Jr.; J. Willemse, and S.C. De Vries The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1 Genes Dev. 16 2002 1707 1720 (Pubitemid 34743330)
51. Y. Stahl, R.H. Wink, G.C. Ingram, and R. Simon A signaling module controlling the stem cell niche in Arabidopsis root meristems Curr. Biol. 19 2009 909 914
52. A.K. Sarkar, M. Luijten, S. Miyashima, M. Lenhard, T. Hashimoto, K. Nakajima, B. Scheres, R. Heidstra, and T. Laux Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers Nature 446 2007 811 814 (Pubitemid 46582034)
53. I. De Smet, V. Vassileva, B. De Rybel, M.P. Levesque, W. Grunewald, D. Van Damme, G. Van Noorden, M. Naudts, G. Van Isterdael, and R. De Clercq Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root Science 322 2008 594 597
54. Y. Hirakawa, Y. Kondo, and H. Fukuda Regulation of vascular development by CLE peptide-receptor systems J. Integr. Plant Biol. 52 2010 8 16
55. S.H. Shiu, and A.B. Bleecker Plant receptor-like kinase gene family: diversity, function, and signaling Sci STKE 2001 2001 re22
56. K. Fisher, and S. Turner PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development Curr. Biol. 17 2007 1061 1066 (Pubitemid 46899541)
57. J.P. Etchells, and S.R. Turner The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division Development 137 2010 767 774
58. Y. Hirakawa, Y. Kondo, and H. Fukuda TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis Plant Cell 22 2010 2618 2629
59. K. Hara, R. Kajita, K.U. Torii, D.C. Bergmann, and T. Kakimoto The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule Genes Dev. 21 2007 1720 1725 (Pubitemid 47076471)
60. K. Hara, T. Yokoo, R. Kajita, T. Onishi, S. Yahata, K.M. Peterson, K.U. Torii, and T. Kakimoto Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis Leaves Plant Cell Physiol. 50 2009 1019 1031
61. L. Hunt, and J.E. Gray The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development Curr. Biol. 19 2009 864 869
62. T. Kondo, R. Kajita, A. Miyazaki, M. Hokoyama, T. Nakamura-Miura, S. Mizuno, Y. Masuda, K. Irie, Y. Tanaka, and S. Takada Stomatal density is controlled by a mesophyll-derived signaling molecule Plant Cell Physiol. 51 2010 1 8
63. L. Hunt, K.J. Bailey, and J.E. Gray The signalling peptide EPFL9 is a positive regulator of stomatal development New Phytol. 186 2010 609 614
64. S.S. Sugano, T. Shimada, Y. Imai, K. Okawa, A. Tamai, M. Mori, and I. Hara-Nishimura Stomagen positively regulates stomatal density in Arabidopsis Nature 463 2010 241 244
65. D. Berger, and T. Altmann A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana Genes Dev. 14 2000 1119 1131 (Pubitemid 30324425)
66. E.B. Abrash, and D.C. Bergmann Regional specification of stomatal production by the putative ligand CHALLAH Development 137 2010 447 455
67. J.A. Nadeau, and F.D. Sack Control of stomatal distribution on the Arabidopsis leaf surface Science 296 2002 1697 1700 (Pubitemid 34579170)
68. E.D. Shpak, J.M. McAbee, L.J. Pillitteri, and K.U. Torii Stomatal patterning and differentiation by synergistic interactions of receptor kinases Science 309 2005 290 293 (Pubitemid 40967863)
69. E.D. Shpak, C.T. Berthiaume, E.J. Hill, and K.U. Torii Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation Development 131 2004 1491 1501 (Pubitemid 38559277)
70. C.A. MacAlister, K. Ohashi-Ito, and D.C. Bergmann Transcription factor control of asymmetric cell divisions that establish the stomatal lineage Nature 445 2007 537 540 (Pubitemid 46197633)
71. L.J. Pillitteri, D.B. Sloan, N.L. Bogenschutz, and K.U. Torii Termination of asymmetric cell division and differentiation of stomata Nature 445 2007 501 505 (Pubitemid 46197625)
72. H. Miwa, T. Tamaki, H. Fukuda, and S. Sawa Evolution of CLE signaling: origins of the CLV1 and SOL2/CRN receptor diversity. Plant Signal Behav. 4 2009 477 481
73. H. Chu, Q. Qian, W. Liang, C. Yin, H. Tan, X. Yao, Z. Yuan, J. Yang, H. Huang, and D. Luo The floral organ number4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice Plant Physiol. 142 2006 1039 1052 (Pubitemid 44764630)
74. S. Sawa, A. Kinoshita, S. Betsuyaku, and H. Fukuda A large family of genes that share homology with CLE domain in Arabidopsis and rice Plant Signal Behav. 3 2008 337 339 (Pubitemid 351651947)
75. E. van der Graaff, T. Laux, and S.A. Rensing The WUS homeobox-containing (WOX) protein family Genome Biol. 10 2009 248
76. A.L. Rychel, K.M. Peterson, and K.U. Torii Plant twitter: ligands under 140 amino acids enforcing stomatal patterning J. Plant Res. 123 2010 275 280
77. K.M. Peterson, A.L. Rychel, and K.U. Torii Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development Plant Cell 22 2010 296 306
78. M.D. Lehti-Shiu, C. Zou, K. Hanada, and S.H. Shiu Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes Plant Physiol. 150 2009 12 26
79. K. Ohyama, M. Ogawa, and Y. Matsubayashi 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 2008 152 160 (Pubitemid 351994177)