Cysteine-Rich Peptides (CRPs) mediate diverse aspects of cell-cell communication in plant reproduction and development

Journal of Experimental Botany

Volumn 62, Issue 5, 2011, Pages 1677-1686

  Marshall, Eleanor ^a   Costa, Liliana M ^b   Gutierrez Marcos, Jose ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Defence; development; nodulation; reproduction; signalling; symbiosis

Indexed keywords

CYSTEINE; PEPTIDE; PHYTOHORMONE; VEGETABLE PROTEIN;

BACTERIUM; CELL COMMUNICATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT; PLANT IMMUNITY; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION; SYMBIOSIS;

BACTERIA; CELL COMMUNICATION; CYSTEINE; GENE EXPRESSION REGULATION, PLANT; PEPTIDES; PLANT GROWTH REGULATORS; PLANT IMMUNITY; PLANT PROTEINS; PLANTS; REPRODUCTION; SIGNAL TRANSDUCTION; SYMBIOSIS;

ANIMALIA;

EID: 79952358199     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err002     Document Type: Review

References (76)

1. Abrash EB, Bergmann DC. 2010. Regional specification of stomatal production by the putative ligand CHALLAH. Development 137, 447-455.
2. Amien S, Kliwer I, Marton ML, Debener T, Geiger D, Becker D, Dresselhaus T. 2010. Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biology 8, e1000388.
3. Balandin M, Royo J, Gomez E, Muniz L, Molina A, Hueros G. 2005. A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region. Plant Molecular Biology 58, 269-282. (Pubitemid 41126001)
4. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U. 2009. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136, 3279-3288.
5. Broekaert WF, Cammue BPA, DeBolle MFC, Thevissen K, DeSamblanx GW, Osborn RW. 1997. Antimicrobial peptides from plants. Critical Reviews in Plant Sciences 16, 297-323. (Pubitemid 127468279)
6. Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM. 2009. Plant peptides in signalling: looking for new partners. Trends in Plant Science 14, 255-263.
7. Chae K, Kieslich CA, Morikis D, Kim SC, Lord EM. 2009. A gain-of-function mutation of Arabidopsis lipid transfer protein 5 disturbs pollen tube tip growth and fertilization. The Plant Cell 21, 3902-3914.
8. De Smet I, Voss U, Jurgens G, Beeckman T. 2009. Receptor-like kinases shape the plant. Nature Cell Biology 11, 1166-1173.
9. Dresselhaus T, Lorz H, Kranz E. 1994. Representative cDNA libraries from few plant cells. The Plant Journal 5, 605-610.
10. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U. 2007. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317, 656-660. (Pubitemid 47229963)
11. Foote HC, Ride JP, Franklin-Tong VE, Walker EA, Lawrence MJ, Franklin FC. 1994. Cloning and expression of a distinctive class of self-incompatibility (S) gene from Papaver rhoeas L. Proceedings of the National Academy of Sciences, USA 91, 2265-2269.
12. Graham MA, Silverstein KAT, Cannon SB, VandenBosch KA. 2004. Computational identification and characterization of novel genes from legumes. Plant Physiology 135, 1179-1197. (Pubitemid 39009369)
13. Gutierrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B, O'Sullivan DM, Wormald M, Perez P, Dickinson HG. 2004. maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. The Plant Cell 16, 1288-1301. (Pubitemid 38641521)
14. Hammami R, Ben Hamida J, Vergoten G, Fliss I. 2009. PhytAMP: a database dedicated to antimicrobial plant peptides. Nucleic Acids Research 37, D963-D968.
15. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T. 2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes and Development 21, 1720-1725. (Pubitemid 47076471)
16. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T. 2009. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant and Cell Physiology 50, 1019-1031.
17. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T. 2001. Pollen tube attraction by the synergid cell. Science 293, 1480-1483. (Pubitemid 32807680)
18. Hunt L, Gray JE. 2009. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curent Biology 19, 864-869.
19. Johnston AJ, Meier P, Gheyselinck J, Wuest SE, Federer M, Schlangenhauf E, Becker JD, Grossniklaus U. 2007. Genetic substraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biology 8, R204.
20. Jones-Rhoades MW, Borevitz JO, Preuss D. 2007. Genome-wide expression profiling of the Arabidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genetics 3, 1848-1861. (Pubitemid 350072051)
21. Kondo T, Kajita R, Miyazaki A, et al. 2010. Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant and Cell Physiology 51, 1-8.
22. Kumhlehn J, Kirik V, Czihal A, Sltschmied L, Matzk F, Lorz H, Baumlein H. 2001. Parthenogenetic egg cells of wheat; cellular and molecular studies. Sexual Plant Reproduction 14, 239-243. (Pubitemid 34018139)
23. Le Q, Gutierrez-Marcos JF, Costa LM, Meyer S, Dickinson HG, Lorz H, Kranz E, Scholten S. 2005. Construction and screening of subtracted cDNA libraries from limited populations of plant cells: a comparative analysis of gene expression between maize egg cells and central cells. The Plant Journal 44, 167-178.
24. Liu JY, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ. 2007. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. The Plant Journal 50, 529-544. (Pubitemid 46634492)
25. Magnard JL, Le Deunff E, Domenech J, Rogowsky PM, Testillano PS, Rougier M, Risueno MC, Vergne P, Dumas C. 2000. Genes normally expressed in the endosperm are expressed at early stages of microspore embryogenesis in maize. Plant Molecular Biology 44, 559-574. (Pubitemid 32060753)
26. Mascarenhas JP. 1993. Molecular mechanisms of pollen-tube growth and differentiation. The Plant Cell 5, 1303-1314. (Pubitemid 2001871)
27. Mergaert P, Nikovics K, Kelemen Z, Maunoury N, Vaubert D, Kondorosi A, Kondorosi E. 2003. A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiology 132, 161-173. (Pubitemid 36590408)
28. Mingossi FB, Matos JL, Rizzato AP, Medeiros AH, Falco MC, Silva-Filho MC, Moura DS. 2010. SacRALF1, a peptide signal from the grass sugarcane (Saccharum spp.), is potentially involved in the regulation of tissue expansion. Plant Molecular Biology 73, 271-281.
29. Miyahara A, Hirani TA, Oakes M, Kereszt A, Kobe B, Djordjevic MA, Gresshoff PM. 2008. Soybean nodule autoregulation receptor kinase phosphorylates two kinase-associated protein phosphatases in vitro. Journal of Biological Chemistry 283, 25381-25391.
30. Mollet JC, Park SY, Nothnagel EA, Lord EM. 2000. A lily stylar pectin is necessary for pollen tube adhesion to an in vitro stylar matrix. The Plant Cell 12, 1737-1750.
31. Murase K, Shiba H, Iwano M, Che FS, Watanabe M, Isogai A, Takayama S. 2004. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303, 1516-1519. (Pubitemid 38314421)
32. Muschietti J, Dircks L, Vancanneyt G, McCormick S. 1994. LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. The Plant Journal 6, 321-338. (Pubitemid 124000387)
33. Nadeau JA, Sack FD. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296, 1697-1700. (Pubitemid 34579170)
34. Okuda S, Tsutsui H, Shiina K, et al. 2009. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458, 357-361.
35. Olsen AN, Mundy J, Skriver K. 2002. Peptomics, identification of novel cationic Arabidopsis peptides with conserved sequence motifs. In Silico Biology 2, 441-451. (Pubitemid 36329186)
36. Palanivelu R, Brass L, Edlund AF, Preuss D. 2003. Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114, 47-59. (Pubitemid 36859840)
37. Park SY, Jauh GY, Mollet JC, Eckard KJ, Nothnagel EA, Walling LL, Lord EM. 2000. A lipid transfer-like protein is necessary for lily pollen tube adhesion to an in vitro stylar matrix. The Plant Cell 12, 151-163. (Pubitemid 30086768)
38. Pearce G, Moura DS, Stratmann J, Ryan CA. 2001a. Production of multiple plant hormones from a single polyprotein precursor. Nature 411, 817-820. (Pubitemid 32588107)
39. Pearce G, Moura DS, Stratmann J, Ryan Jr CA. 2001b. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proceedings of the National Academy of Sciences, USA 98, 12843-12847. (Pubitemid 33020032)
40. Preuss D, Lemieux B, Yen G, Davis RW. 1993. A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes and Development 7, 974-985. (Pubitemid 23170822)
41. Punwani JA, Rabiger DS, Drews GN. 2007. MYB98 positively regulates a battery of synergid-expressed genes encoding filiform apparatus localized proteins. The Plant Cell 19, 2557-2568. (Pubitemid 47583844)
42. Punwani JA, Rabiger DS, Lloyd A, Drews GN. 2008. The MYB98 subcircuit of the synergid gene regulatory network includes genes directly and indirectly regulated by MYB98. The Plant Journal 55, 406-414. (Pubitemid 352033351)
43. Richter HE, Sandal NN, Marcker KA, Sengupta-Gopalan C. 1991. Characterization and genomic organization of a highly expressed late nodulin gene subfamily in soybeans. Molecular and General Genetics 229, 445-452.
44. Scheer JM, Pearce G, Ryan CA. 2005. LeRALF, a plant peptide that regulates root growth and development, specifically binds to 25 and 120 kDa cell surface membrane proteins of Lycopersicon peruvianum. Planta 221, 667-674. (Pubitemid 41003883)
45. Scheres B, Van De Wiel C, Zalensky A, et al. 1990 a. The ENOD12 gene product is involved in the infection process during the pea- Rhizobium interaction. Cell 60, 281-294.
46. Scheres B, van Engelen F, van der Knaap E, van de Wiel C, van Kammen A, Bisseling T. 1990 b. Sequential induction of nodulin gene expression in the developing pea nodule. The Plant Cell 2, 687-700. (Pubitemid 120015477)
47. Schopfer CR, Nasrallah ME, Nasrallah JB. 1999. The male determinant of self-incompatibility in Brassica. Science 286, 1697-1700. (Pubitemid 129515868)
48. Schweizer P. 2008. Tissue-specific expression of a defence-related peroxidase in transgenic wheat potentiates cell death in pathogen-attacked leaf epidermis. Molecular Plant Pathology 9, 45-57. (Pubitemid 350295872)
49. Serna A, Maitz M, O'Connell T, et al. 2001. Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. The Plant Journal 25, 687-698. (Pubitemid 32406382)
50. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. 2005. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309, 290-293. (Pubitemid 40967863)
51. Silverstein KA, Graham MA, Paape TD, VandenBosch KA. 2005. Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiology 138, 600-610. (Pubitemid 43793143)
52. Silverstein KA, Moskal Jr WA, Wu HC, Underwood BA, Graham MA, Town CD, VandenBosch KA. 2007. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. The Plant Journal 51, 262-280. (Pubitemid 47030121)
53. Spelbrink RG, Dilmac N, Allen A, Smith TJ, Shah DM, Hockerman GH. 2004. Differential antifungal and calcium channel-blocking activity among structurally related plant defensins. Plant Physiology 135, 2055-2067. (Pubitemid 39182785)
54. Sprunck S, Baumann U, Edwards K, Langridge P, Dresselhaus T. 2005. The transcript composition of egg cells changes significantly following fertilization in wheat (Triticum aestivum L.). The Plant Journal 41, 660-672. (Pubitemid 40335998)
55. Srivastava R, Liu JX, Guo H, Yin Y, Howell SH. 2009. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. The Plant Journal 59, 930-939.
56. Steffen JG, Kang IH, Macfarlane J, Drews GN. 2007. Identification of genes expressed in the Arabidopsis female gametophyte. The Plant Journal 51, 281-292. (Pubitemid 47030122)
57. Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB. 1991. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proceedings of the National Academy of Sciences, USA 88, 8816-8820. (Pubitemid 21915446)
58. Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I. 2010. Stomagen positively regulates stomatal density in Arabidopsis. Nature 463, 241-244.
59. Suzuki G, Kai N, Hirose T, Fukui K, Nishio T, Takayama S, Isogai A, Watanabe M, Hinata K. 1999. Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S-9 haplotype of Brassica campestris (syn. rapa). Genetics 153, 391-400. (Pubitemid 29434789)
60. Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A. 2001. Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413, 534-538. (Pubitemid 32938753)
61. 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. The Plant Cell 14, 2277-2287.
62. Tang WH, Kelley D, Ezcurra I, Cotter R, McCormick S. 2004. LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. The Plant Journal 39, 343-353. (Pubitemid 39040140)
63. Terras FR, Goderis IJ, Van Leuven F, Vanderleyden J, Cammue BP, Broekaert WF. 1992a. In vitro antifungal activity of a radish (Raphanus sativus L.) seed protein homologous to nonspecific lipid transfer proteins. Plant Physiology 100, 1055-1058.
64. Terras FR, Schoofs HM, De Bolle MF, Van Leuven F, Rees SB, Vanderleyden J, Cammue BP, Broekaert WF. 1992b. Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. Journal of Biological Chemistry 267, 15301-15309.
65. Thevissen K, Ghazi A, De Samblanx GW, Brownlee C, Osborn RW, Broekaert WF. 1996. Fungal membrane responses induced by plant defensins and thionins. Journal of Biological Chemistry 271, 15018-15025. (Pubitemid 26197577)
66. Thomas SG, Franklin-Tong VE. 2004. Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429, 305-309. (Pubitemid 38684816)
67. Thomma BPHJ, Cammue BPA, Thevissen K. 2002. Plant defensins. Planta 216, 193-202. (Pubitemid 36761777)
68. Van de Velde W, Zehirov G, Szatmari A, et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126.
69. Wang D, Griffitts J, Starker C, Fedorova E, Limpens E, Ivanov S, Bisseling T, Long SR. 2010. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327, 1126-1129.
70. Wheeler MJ, de Graaf BH, Hadjiosif N, Perry RM, Poulter NS, Osman K, Vatovec S, Harper A, Franklin FC, Franklin-Tong VE. 2009. Identification of the pollen self-incompatibility determinant in Papaver rhoeas. Nature 459, 992-995.
71. Wheeler MJ, Vatovec S, Franklin-Tong VE. 2010. The pollen S-determinant in Papaver: comparisons with known plant receptors and protein-ligand partners. Journal of Experimental Botany 61, 2015-2025.
72. Whitehouse HLK. 1950. Multiple allelomorph incompatibility of pollen and style in the evolution of angiosperms. Annals of Botany 14, 198-216.
73. Wolters H, Jurgens G. 2009. Survival of the flexible: hormonal growth control and adaptation in plant development. Nature Reviews Genetics 10, 305-317.
74. Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenfuhrer J, von Mering C, Grossniklaus U. 2010. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Current Biology 20, 506-512.
75. Yang H, Kaur N, Kiriakopolos S, McCormick S. 2006. EST generation and analyses towards identifying female gametophyte-specific genes in Zea mays L. Planta 224, 1004-1014. (Pubitemid 44435851)
76. Zhu S, Gao B, Tytgat J. 2005. Phylogenetic distribution, functional epitopes and evolution of the CSalphabeta superfamily. Cell and Molecular Life Sciences 62, 2257-2269. (Pubitemid 41500542)