Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants

Plant Journal

Volumn 51, Issue 2, 2007, Pages 262-280

  Silverstein, Kevin A T ^a   Moskal Jr , William A ^b   Wu, Hank C ^b   Underwood, Beverly A ^b   Graham, Michelle A ^c   Town, Christopher D ^b   VandenBosch, Kathryn A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b J CRAIG VENTER INSTITUTE   (United States)

^c IOWA STATE UNIVERSITY   (United States)

Author keywords

Antimicrobial peptides; Cysteine rich peptides; Defensins; Lipid transfer protein; RALF; Thionin

Indexed keywords

AMINO ACIDS; CROPS; FORESTRY; GENES; LIPIDS; PATHOGENS; PLANTS (BOTANY);

ANTIMICROBIAL PEPTIDES; CYSTEINE-RICH PEPTIDES; DEFENSINS; LIPID TRANSFER PROTEINS; THIONIN;

PEPTIDES;

ANTIINFECTIVE AGENT; CYSTEINE; PEPTIDE; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; RICE;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; ARABIDOPSIS; CLUSTER ANALYSIS; CYSTEINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PEPTIDES; PLANT PROTEINS;

CYSTEINE; LIPIDS; PATHOGENS; PEPTIDES; RICE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; DICOTYLEDONEAE; EUKARYOTA; ORYZA SATIVA;

EID: 34447102400     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2007.03136.x     Document Type: Article

References (106)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389 3402.
2. Alvarez, M.E., Pennell, R.I., Meijer, P.J., Ishikawa, A., Dixon, R.A. Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 92, 773 784.
3. Apweiler, R., Bairoch, A., Wu, C.H. et al. (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res. 32, D115 D119.
4. Aubert, D., Chevillard, M., Dorne, A.M., Arlaud, G. Herzog, M. (1998) Expression patterns of GASA genes in Arabidopsis thaliana: the GASA4 gene is up-regulated by gibberellins in meristematic regions. Plant Mol. Biol. 36, 871 883.
5. Ayele, M., Haas, B.J., Kumar, N., Wu, H., Xiao, Y., Van Aken, S., Utterback, T.R., Wortman, J.R., White, O.R. Town, C.D. (2005) Whole genome shotgun sequencing of Brassica oleracea and its application to gene discovery and annotation in Arabidopsis. Genome Res. 15, 487 495.
6. Bauw, G., Nielsen, H.V., Emmersen, J., Nielsen, K.L., Jorgensen, M. Welinder, K.G. (2006) Patatins, Kunitz protease inhibitors and other major proteins in tuber of potato cv. Kuras. FEBS J. 273, 3569 3584.
7. Bendtsen, J.D., Nielsen, H., von Heijne, G. Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340, 783 795.
8. Berrocal-Lobo, M., Segura, A., Moreno, M., Lopez, G., Garcia-Olmedo, F. Molina, A. (2002) Snakin-2, an antimicrobial peptide from potato whose gene is locally induced by wounding and responds to pathogen infection. Plant Physiol. 128, 951 961.
9. Birk, Y. (1985) The Bowman-Birk inhibitor. Trypsin- and chymo'trypsin-inhibitor from soybeans. Int. J. Pept. Protein Res. 25, 113 131.
10. Bloch, C. Jr. Richardson, M. (1991) A new family of small (5 kDa) protein inhibitors of insect alpha-amylases from seeds or sorghum [Sorghum bicolar (L) Moench] have sequence homologies with wheat gamma-purothionins. FEBS Lett. 279, 101 104.
11. Bloom, J.D., Labthavikul, S.T., Otey, C.R. Arnold, F.H. (2006) Protein stability promotes evolvability. Proc. Natl Acad. Sci. USA, 103, 5869 5874.
12. Boman, H.G. (2003) Antibacterial peptides: basic facts and emerging concepts. J. Intern. Med. 254, 197 215.
13. Brisson, L.F., Tenhaken, R. Lamb, C. (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell, 6, 1703 1712.
14. Broekaert, W.F., Cammue, B.P.A., De Bolle, M.F.C., Thevissen, K., De Samblanx, G.W. Osborn, R.W. (1997) Antimicrobial peptides from plants. Crit. Rev. Plant Sci. 16, 297 323.
15. Bulet, P., Stocklin, R. Menin, L. (2004) Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 198, 169 184.
16. Cano-Delgado, A., Penfield, S., Smith, C., Catley, M. Bevan, M. (2003) Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana. Plant J. 34, 351 362.
17. Cassab, G.I. (1998) Plant cell wall proteins. Annu. Rev. Plant. Physiol. Plant Mol. Biol. 49, 281 309.
18. Chen, K.C., Lin, C.Y., Kuan, C.C., Sung, H.Y. Chen, C.S. (2002) A novel defensin encoded by a mungbean cDNA exhibits insecticidal activity against bruchid. J. Agric. Food Chem. 50, 7258 7263.
19. Clamp, M., Cuff, J., Searle, S. Barton, G.J. (2004) The Jalview Java alignment editor. Bioinformatics, 20, 426 427.
20. Cock, J.M. McCormick, S. (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939 942.
21. Creighton, T.E. (1993) Proteins: structures and molecular properties. 2nd edn. New York, NY : W. H. Freeman and Company.
22. Dangl, J.L. Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826 833.
23. Darvill, A.G. Albersheim, P. (1984) Phytoalexins and their elicitors - a defense against microbial infection in plants. Annu. Rev. Plant Physiol. 35, 243 275.
24. Durbin, R., Eddy, S.R., Krogh, A. Mitchison, G. (1998) Biological sequence analysis: probabilistic models of proteins and nucleic acids. Cambridge, UK : Cambridge University Press.
25. Durrant, W.E. Dong, X. (2004) Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185 209.
26. Endo, Y., Mitsui, K., Motizuki, M. Tsurugi, K. (1987) The mechanism of action of ricin and related toxic lectins on eucaryotic ribosomes. The site and the characterization of the modification in 28S ribosomal RNA caused by the toxins. J. Biol. Chem. 262, 5908 5912.
27. Farmer, E.E. Ryan, C.A. (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc. Natl Acad. Sci. USA, 87, 7713 7716.
28. Florack, D.E. Stiekema, W.J. (1994) Thionins: properties, possible biological roles and mechanisms of action. Plant Mol. Biol. 26, 25 37.
29. Florea, L., Hartzell, G., Zhang, Z., Rubin, G.M. Miller, W. (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res. 8, 967 974.
30. Garcia-Olmedo, F., Carbonerro, P., Hernandez-Lucas, C., Paz-Ares, J., Ponz, F., Vincente, O. Sierra, J.M. (1983) Inhibition of eukaryotic cell-free protein synthesis by thionins from wheat endosperm. Biochim. Biophys. Acta, 740, 52 56.
31. Garcia-Olmedo, F., Rodriquez-Palenzuela, X., Hernandez-Lucas, C., Ponz, F., Marana, C., Carmona, M.J., Lopez-Fando, J.J., Fernandez, J.A. Carbonerro, P. (1989) The thionins: a protein family that includes purothionins, viscotoxins and crambin. In Oxford Surveys of Plant Molecular and Cell Biology. Vol. 6 (Miflin, B.J. ed). Oxford, UK : Oxford University Press, pp. 31 60.
32. Garcia-Olmedo, F., Molina, A., Alamillo, J.M. Rodriguez-Palenzuela, P. (1998) Plant defense peptides. Biopolymers, 47, 479 491.
33. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M.R., Appel, R.D. Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook (Walker, J.M., ed.). Totowa, NJ : Humana Press.
34. Goldman, M.H., Goldberg, R.B. Mariani, C. (1994) Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J. 13, 2976 2984.
35. Graham, M.A., Silverstein, K.A.T., Cannon, S.B. VandenBosch, K.A. (2004) Computational identification and characterization of novel genes from legumes. Plant Physiol. 135, 1179 1197.
36. Greenberg, J.T. Yao, N. (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol. 6, 201 211.
37. Gutierrez-Marcos, J.F., Costa, L.M., Biderre-Petit, C., Khbaya, B., O'Sullivan, D.M., Wormald, M., Perez, P. Dickinson, H.G. (2004) Maternally expressed gene1 Is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell, 16, 1288 1301.
38. Haas, B.J., Delcher, A.L., Mount, S.M. et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654 5666.
39. Haas, B.J., Wortman, J.R., Ronning, C.M. et al. (2005) Complete reannotation of the Arabidopsis genome: methods, tools, protocols and the final release. BMC Biol. 3, 7.
40. Hebsgaard, S.M., Korning, P.G., Tolstrup, N., Engelbrecht, J., Rouze, P. Brunak, S. (1996) Splice site prediction in Arabidopsis thaliana pre-mRNA by combining local and global sequence information. Nucleic Acids Res. 24, 3439 3452.
41. Henrissat, B. Davies, G.J. (2000) Glycoside hydrolases and glycosyltransferases. Families, modules, and implications for genomics. Plant Physiol. 124, 1515 1519.
42. Himly, M., Jahn-Schmid, B., Dedic, A. et al. (2003) Art v 1, the major allergen of mugwort pollen, is a modular glycoprotein with a defensin-like and a hydroxyproline-rich domain. FASEB J. 17, 106 108.
43. Jabs, T., Tschope, M., Colling, C., Hahlbrock, K. Scheel, D. (1997) Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl Acad. Sci. USA, 94, 4800 4805.
44. Kawano, T. (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep. 21, 829 837.
45. Kunkel, B.N. Brooks, D.M. (2002) Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant. Biol. 5, 325 331.
46. Lam, E., Kato, N. Lawton, M. (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature, 411, 848 853.
47. Laskowski, M. Qasim, M.A. (2000) What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes? Biochim. Biophys. Acta, 1477, 324 337.
48. Lay, F.T., Schirra, H.J., Scanlon, M.J., Anderson, M.A. Craik, D.J. (2003) The three-dimensional solution structure of NaD1, a new floral defensin from Nicotiana alata and its application to a homology model of the crop defense protein alfAFP. J. Mol. Biol. 325, 175 188.
49. Mello, M.O., Tanaka, A.S. Silva-Filho, M.C. (2003) Molecular evolution of Bowman-Birk type proteinase inhibitors in flowering plants. Mol. Phylogenet. Evol. 27, 103 112.
50. Melo, F.R., Rigden, D.J., Franco, O.L., Mello, L.V., Ary, M.B., Grossi de Sa, M.F. Bloch, C. Jr. (2002) Inhibition of trypsin by cowpea thionin: characterization, molecular modeling, and docking. Proteins, 48, 311 319.
51. Meyers, B.C., Tej, S.S., Vu, T.H., Haudenschild, C.D., Agrawal, V., Edberg, S.B., Ghazal, H. Decola, S. (2004) The use of MPSS for whole-genome transcriptional analysis in Arabidopsis. Genome Res. 14, 1641 1653.
52. Molina, A., Segura, A. Garcia-Olmedo, F. (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett. 316, 119 122.
53. Moskal, W.A. Jr., Wu, H.C., Underwood, B.A., Wang, W., Town, C.D. Xiao, Y. (2007) Experimental validation of novel genes predicted in the un-annotated regions of the Arabidopsis genome. BMC Genomics, 8, 18.
54. Motose, H., Sugiyama, M. Fukuda, H. (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature, 429, 873 878.
55. Murata, M., Begg, G.S., Lambrou, F., Leslie, B., Simpson, R.J., Freeman, H.C. Morgan, F.J. (1982) Amino acid sequence of a basic blue protein from cucumber seedlings. Proc. Natl Acad. Sci. USA, 79, 6434 6437.
56. Mygind, P.H., Fischer, R.L., Schnorr, K.M. et al. (2005) Plectasin is a peptide antibiotic with therapeutic potential from a saprophytic fungus. Nature, 437, 975 980.
57. Mysore, K.S. Ryu, C.M. (2004) Nonhost resistance: how much do we know? Trends Plant Sci. 9, 97 104.
58. Odani, S., Koide, T. Ono, T. (1983) The complete amino acid sequence of barley trypsin inhibitor. J. Biol. Chem. 258, 7998 8003.
59. Osbourn, A.E. (1996) Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell, 8, 1821 1831.
60. Ouyang, S., Zhu, W., Hamilton, J. et al. (2007) The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res. 35, D883 D887.
61. Pearce, G., Moura, D.S., Stratmann, J. Ryan, C.A. Jr. (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc. Natl Acad. Sci. USA, 98, 12843 12847.
62. Qin, Q., Bergmann, C.W., Rose, J.K., Saladie, M., Kolli, V.S., Albersheim, P., Darvill, A.G. York, W.S. (2003) Characterization of a tomato protein that inhibits a xyloglucan-specific endoglucanase. Plant J. 34, 327 338.
63. Quackenbush, J., Cho, J., Lee, D., Liang, F., Holt, I., Karamycheva, S., Parvizi, B., Pertea, G., Sultana, R. White, J. (2001) The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Res. 29, 159 164.
64. Rawlings, N.D., Tolle, D.P. Barrett, A.J. (2004) Evolutionary families of peptidase inhibitors. Biochem. J. 378, 705 716.
65. van Ree, R. (2002) Clinical importance of non-specific lipid transfer proteins as food allergens. Biochem. Soc. Trans. 30, 910 913.
66. Rhee, S.Y., Beavis, W., Berardini, T.Z. et al. (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res. 31, 224 228.
67. Ride, J.P., Davies, E.M., Franklin, F.C. Marshall, D.F. (1999) Analysis of Arabidopsis genome sequence reveals a large new gene family in plants. Plant Mol. Biol. 39, 927 932.
68. Ross, A.F. (1961) Systemic aquired resistance induced by localized virus infections in plants. Virology, 14, 340 358.
69. Rozen, S. Skaletsky, H. (2000) Primer3 on the WWW for general users and biologist programmers. In Bioinformatics Methods and Protocols (Krawetz, S. Misener, S., eds). Totowa, NJ : Humana Press, pp. 365 386.
70. Ryan, C.A. (1990) Protease inhibitors in plants: genes for improving defenses against insects and pathogens. Annu. Rev. Phytopathol. 28, 425 449.
71. Satoh, S., Sturm, A., Fujii, T. Chrispeels, M.J. (1992) cDNA cloning of an extracellular dermal glycoprotein of carrot and its expression in reponse to wounding. Planta, 188, 432 438.
72. Scheel, D. (1998) Resistance response physiology and signal transduction. Curr. Opin. Plant. Biol. 1, 305 310.
73. Schopfer, C.R., Nasrallah, M.E. Nasrallah, J.B. (1999) The male determinant of self-incompatibility in Brassica. Science, 286, 1697 1700.
74. Segura, A., Moreno, M., Madueno, F., Molina, A. Garcia-Olmedo, F. (1999) Snakin-1, a peptide from potato that is active against plant pathogens. Mol. Plant Microbe Interact. 12, 16 23.
75. Serna, A., Maitz, M., O'Connell, T. et al. (2001) Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J. 25, 687 698.
76. Shai, Y. (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers, 66, 236 248.
77. Siegel, S. (1956) Nonparametric statistics: for the behavioral sciences. New York, NY : McGraw-Hill Book Company.
78. Silverstein, K.A.T., Graham, M.A., Paape, T.D. VandenBosch, K.A. (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol. 138, 600 610.
79. Silverstein, K.A., Graham, M.A. VandenBosch, K.A. (2006) Novel paralogous gene families with potential function in legume nodules and seeds. Curr. Opin. Plant Biol. 9, 142 146.
80. Stec, B., Rao, U. Teeter, M.M. (1995) Refinement of purothionins reveals solute particles important for lattice formation and toxicity. Part 2: structure of beta-purothionin at 1.7 A resolution. Acta Crystallogr. D Biol. Crystallogr. 51, 914 924.
81. Sutton, G.S., White, O., Adams, M.D. Kerlavage, A.R. (1995) TIGR assembler: a new tool for assemblying large shotgun sequencing projects. Genome Sci. Technol. 1, 9 19.
82. Takayama, S., Shiba, H., Iwano, M., Asano, K., Hara, M., Che, F.S., Watanabe, M., Hinata, K. Isogai, A. (2000a) Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen-stigma adhesion. Proc. Natl Acad. Sci. USA, 97, 3765 3770.
83. Takayama, S., Shiba, H., Iwano, M., Shimosato, H., Che, F.S., Kai, N., Watanabe, M., Suzuki, G., Hinata, K. Isogai, A. (2000b) The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl Acad. Sci. USA, 97, 1920 1925.
84. Talyzina, N.M. Ingvarsson, P.K. (2006) Molecular evolution of a small gene family of wound inducible Kunitz trypsin inhibitors in Populus. J. Mol. Evol. 63, 108 119.
85. Terras, F.R.G., Goderis, I.J., Van Leuven, F., Vanderleyden, J., Cammue, B.P.A. Broekaert, W.F. (1992) In vitro anti-fungal activity of a radish (Raogabys satuvys L.) seed protein homologous to nonspecific lipid transfer proteins. Plant Physiol. 100, 1055 1058.
86. The Arabidopsis Genome Intiative. (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796 815.
87. Theis, T. Stahl, U. (2004) Antifungal proteins: targets, mechanisms and prospective applications. Cell. Mol. Life Sci. 61, 437 455.
88. Thevissen, K., Ferket, K.K., Francois, I.E. Cammue, B. (2003) Interactions of antifungal plant defensins with fungal membrane components. Peptides, 24, 1705 1712.
89. Thomma, B., Eggermont, K., Penninckx, I., Mauch-Mani, B., Vogelsang, R., Cammue, B.P.A. Broekaert, W.F. (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in arabidopsis are essential for resistance to distinct microbial pathogens. Proc. Natl Acad. Sci. USA, 95, 15107 15111.
90. Thomma, B.P., Cammue, B.P. Thevissen, K. (2002) Plant defensins. Planta, 216, 193 202.
91. Thompson, J.D., Higgins, D.G. Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673 4680.
92. Underwood, B.A., Vanderhaeghen, R., Whitford, R., Town, C.D. Hilson, P. (2006) Simultaneous high-throughput recombinatorial cloning of open reading frames in closed and open configurations. Plant Biotechnol. J. 4, 317 324.
93. Van Loon, L.C. van Kammen, A. (1970) Polyacrilamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. Samsun and Samsun NN II. Changes in protein constitution after infection with tobacco mosaic virus. Virology, 40, 199 211.
94. Van Loon, L.C. van Strien, E.A. (1999) The families of pathogenesis-related proteins, and their activities, and comparative analysis of PR-1 type proteins. Physiol. Mol. Plant Pathol. 55, 85 97.
95. Vance, C.P., Kirk, T.K. Sherwood, R.T. (1980) Lignification as a mechanism of disease resistance. Annu. Rev. Phytopathol. 18, 259 288.
96. Vanoosthuyse, V., Miege, C., Dumas, C. Cock, J.M. (2001) 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. 46, 17 34.
97. Veronese, P., Ruiz, M.T., Coca, M.A. et al. (2003) In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiol. 131, 1580 1590.
98. Vivanco, J.M., Savary, B.J. Flores, H.E. (1999) Characterization of two novel type I ribosome-inactivating proteins from the storage roots of the andean crop Mirabilis expansa. Plant Physiol. 119, 1447 1456.
99. Watanabe, M., Ito, A., Takada, Y. et al. (2000) Highly divergent sequences of the pollen self-incompatibility (S) gene in class-I S haplotypes of Brassica campestris (syn. rapa) L. FEBS Lett. 473, 139 144.
100. Wortman, J.R., Haas, B.J., Hannick, L.I. et al. (2003) Annotation of the Arabidopsis genome. Plant Physiol. 132, 461 468.
101. Xiao, Y.L., Smith, S.R., Ishmael, N., Redman, J.C., Kumar, N., Monaghan, E.L., Ayele, M., Haas, B.J., Wu, H.C. Town, C.D. (2005) Analysis of the cDNAs of hypothetical genes on Arabidopsis chromosome 2 reveals numerous transcript variants. Plant Physiol. 139, 1323 1337.
102. Yamada, K., Lim, J., Dale, J.M. et al. (2003) Empirical Analysis of transcriptional activity in the Arabidopsis genome. Science, 302, 842 846.
103. Young, N.D., Cannon, S.B., Sato, S., Kim, D., Cook, D.R., Town, C.D., Roe, B.A. Tabata, S. (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiol. 137, 1174 1181.
104. Zhang, S. Klessig, D.F. (2001) MAPK cascades in plant defense signaling. Trends Plant Sci. 6, 520 527.
105. Zhang, K., McKinlay, C., Hocart, C.H. Djordjevic, M.A. (2006) The Medicago truncatula small protein proteome and peptidome. J. Proteome Res. 5, 3355 3367.
106. Zhu, S., Gao, B. Tytgat, J. (2005) Phylogenetic distribution, functional epitopes and evolution of the CSalphabeta superfamily. Cell. Mol. Life Sci. 62, 2257 2269.