Plant cysteine-rich peptides that inhibit pathogen growth and control rhizobial differentiation in legume nodules

Current Opinion in Plant Biology

Volumn 26, Issue , 2015, Pages 57-63

  Maróti, Gergely ^a   Downie, J Allan ^b   Kondorosi, Éva ^a  

^a INSTITUTE OF BIOCHEMISTRY   (Hungary)

^b NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MEDICAGO TRUNCATULA;

CYSTEINE; PEPTIDE;

CHEMISTRY; GENE EXPRESSION REGULATION; METABOLISM; MICROBIOLOGY; NODULATION; PHYSIOLOGY; RHIZOBIUM; SYMBIOSIS;

CYSTEINE; GENE EXPRESSION REGULATION, PLANT; PEPTIDES; RHIZOBIUM; ROOT NODULES, PLANT; SYMBIOSIS;

EID: 84934993109     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2015.05.031     Document Type: Review

References (47)

1. Fan J., Doerner P. Genetic and molecular basis of nonhost disease resistance: complex, yes; silver bullet, no. Curr Opin Plant Biol 2012, 15:400-406.
2. Lacerda A.F., Vasconcelos E.A., Pelegrini P.B., Grossi de Sa M.F. Antifungal defensins and their role in plant defense. Front Microbiol 2014, 5:116.
3. Goyal R.K., Mattoo A.K. Multitasking antimicrobial peptides in plant development and host defense against biotic/abiotic stress. Plant Sci 2014, 228:135-149.
4. Kereszt A., Mergaert P., Maróti G., Kondorosi E. Innate immunity effectors and virulence factors in symbiosis. Curr Opin Microbiol 2011, 14:76-81.
5. Carro L., Pujic P., Alloisio N., Fournier P., Boubakri H., Hay A.E., Poly F., François P., Hocher V., Mergaert P., et al. Alnus peptides modify membrane porosity and induce the release of nitrogen-rich metabolites from nitrogen-fixing Frankia. ISME J 2015, 10.1038/ismej.2014257.
6. Gao A.G., Hakimi S.M., Mittanck C.A., Wu Y., Woerner B.M., Stark D.M., Shah D.M., Liang J., Rommens C.M. Fungal pathogen protection in potato by expression of a plant defensin peptide. Nat Biotechnol 2000, 18:1307-1310.
7. Park H.C., Kang Y.H., Chun H.J., Koo J.C., Cheong Y.H., Kim C.Y., Kim M.C., Chung W.S., Kim J.C., Yoo J.H., et al. Characterization of a stamen-specific cDNA encoding a novel plant defensin in Chinese cabbage. Plant Mol Biol 2002, 50:59-69.
8. Koike M., Okamoto T., Tsuda S., Imai R. A novel plant defensin-like gene of winter wheat is specifically induced during cold acclimation. Biochem Biophys Res Commun 2002, 298:46-53.
9. Segura A., Moreno M., Molina A., Garcia-Olmedo F. Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Lett 1998, 435:159-162.
10. Chen K.C., Lin C.Y., Kuan C.C., Sung H.Y., Chen C.S. A novel defensin encoded by a mungbean cDNA exhibits insecticidal activity against bruchid. J Agric Food Chem 2002, 50:7258-7263.
11. Kanzaki H., Nirasawa S., Saitoh H., Ito M., Nishihara M., Terauchi R., Nakamura I. Overexpression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice. Theor Appl Genet 2002, 105:809-814.
12. Thomma B.P., Cammue B.P., Thevissen K. Plant defensins. Planta 2002, 216:193-202.
13. Lay F.T., Anderson M.A. Defensins, components of the innate immune system in plants. Curr Protein Pept Sci 2005, 6:85-101.
14. Aerts A.M., François I.E., Cammue B.P., Thevissen K. The mode of antifungal action of plant, insect and human defensins. Cell Mol Life Sci 2008, 65:2069-2079.
15. van der Weerden N.L., Bleackley M.R., Anderson M.A. Properties and mechanisms of action of naturally occurring antifungal peptides. Cell Mol Life Sci 2013, 70:3545-3570.
16. Thevissen K., Kristensen H.H., Thomma B.P., Cammue B.P., François I.E. Therapeutic potential of antifungal plant and insect defensins. Drug Discov Today 2007, 12:966-971.
17. Aerts A.M., François I.E., Meert E.M., Li Q.T., Cammue B.P., Thevissen K. The antifungal activity of RsAFP2, a plant defensin from Raphanus sativus, involves the induction of reactive oxygen species in Candida albicans. J Mol Microbiol Biotechnol 2007, 13:243-247.
18. Sagaram U.S., Pandurangi R., Kaur J., Smith T.J., Shah D.M. Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PLoS One 2011, 6:e18550.
19. De Coninck B., Carron D., Tavormina P., Willem L., Craik D.J., Vos C., Thevissen K., Mathys J., Cammue B.P. Mining the genome of Arabidopsis thaliana as a basis for the identification of novel bioactive peptides involved in oxidative stress tolerance. J Exp Bot 2013, 64:5297-5307.
20. Giacomelli L., Nanni V., Lenzi L., Zhuang J., Dalla Serra M., Banfield M.J., Town C.D., Silverstein K.A., Baraldi E., Moser C. Identification and characterization of the defensin-like gene family of grapevine. Mol Plant Microbe Interact 2012, 25:1118-1131.
21. Silverstein K.A.T., Graham M.A., Paape T.D., VandenBosch K.A. Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 2005, 138:600-610.
22. Young N.D., Debellé F., Oldroyd G.E., Geurts R., Cannon S.B., Udvardi M.K., Benedito V.A., Mayer K.F., Gouzy J., Schoof H., et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 2011, 480:520-524.
23. Tesfaye M., Silverstein K.A., Nallu S., Wang L., Botanga C.J., Gomez S.K., Costa L.M., Harrison M.J., Samac D.A., Glazebrook J., et al. Spatio-temporal expression patterns of Arabidopsis thaliana and Medicago truncatula defensin-like genes. PLoS One 2013, 8:e58992.
24. Mergaert P., Nikovics K., Kelemen Z., Maunoury N., Vaubert D., Kondorosi A., Kondorosi E. A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol 2003, 132:161-173.
25. Graham M.A., Silverstein K.A.T., Cannon S.B., VandenBosch K.A. Computational identification and characterization of novel genes from legumes. Plant Physiol 2004, 135:1179-1197.
26. Silverstein K.A.T., Moskal W.A., Wu H.C., Underwood B.A., Graham M.A., Town C.D., VandenBosch K.A. Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 2007, 51:262-280.
27. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A., Tiricz H., et al. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 2010, 327:1122-1126.
28. Hanks J.N., Snyder A.K., Graham M.A., Shah R.K., Blaylock L.A., Harrison M.J., Shah D.M. Defensin gene family in Medicago truncatula: structure, expression and induction by signal molecules. Plant Mol Biol 2005, 58:385-399.
29. Sagaram U.S., El-Mounadi K., Buchko G.W., Berg H.R., Kaur J., Pandurangi R.S., Smith T.J., Shah D.M. Structural and functional studies of a phosphatidic acid-binding antifungal plant defensin mtdef4: identification of an rgfrrr motif governing fungal cell entry. PLoS One 2013, 8:e82485.
30. Munoz A., Chu M., Marris P.I., Sagaram U.S., Kaur J., Shah D.M., Read N.D. Specific domains of plant defensins differentially disrupt colony initiation, cell fusion and calcium homeostasis in Neurospora crassa. Mol Microbiol 2014, 92:1357-1374.
31. Yount N.Y., Yeaman M.R. Multidimensional signatures in antimicrobial peptides. Proc Natl Acad Sci USA 2004, 101:7363-7368.
32. Spelbrink R.G., Dilmac N., Allen A., Smith T.J., Shah D.M., Hockerman G.H. Differential antifungal and calcium channel-blocking activity among structurally related plant defensins. Plant Physiol 2004, 135:2055-2067.
33. Kaur J., Thokala M., Robert-Seilaniantz A., Zhao P., Peyret H., Berg H., Pandey S., Jones J., Shah D. Subcellular targeting of an evolutionarily conserved plant defensin MtDef4.2 determines the outcome of plant-pathogen interaction in transgenic Arabidopsis. Mol Plant Pathol 2012, 13:1032-1046.
34. Nallu S., Silverstein K.A., Zhou P., Young N.D., Vandenbosch K.A. Patterns of divergence of a large family of nodule cysteine-rich peptides in accessions of Medicago truncatula. Plant J 2014, 78:697-705.
35. Kondorosi E., Mergaert P., Kereszt A. A paradigm for endosymbiotic life: cell differentiation of Rhizobium bacteria provoked by host plant factors. Annu Rev Microbiol 2013, 67:611-628.
36. Haag A.F., Kerscher B., Dall'Angelo S., Sani M., Longhi R., Baloban M., Wilson H.M., Mergaert P., Zanda M., Ferguson G.P. Role of cysteine residues and disulfide bonds in the activity of a legume root nodule-specific, cysteine-rich peptide. J Biol Chem 2012, 287:10791-10798.
37. Tiricz H., Szucs A., Farkas A., Pap B., Lima R.M., Maróti G., Kondorosi É., Kereszt A. Antimicrobial nodule-specific cysteine-rich peptides induce membrane depolarization-associated changes in the transcriptome of Sinorhizobium meliloti. Appl Environ Microbiol 2013, 79:6737-6746.
38. Ördögh L., Vörös A., Nagy I., Kondorosi E., Kereszt A. Symbiotic plant peptides eliminate Candida albicans both in vitro and in an epithelial infection model and inhibit the proliferation of immortalized human cells. Biomed Res Int 2014, 2014:320796. 10.1155/2014/320796.
39. Sinharoy S., Torres-Jerez I., Bandyopadhyay K., Kereszt A., Pislariu C.I., Nakashima J., Benedito V.A., Kondorosi E., Udvardi M.K. The C2H2 transcription factor regulator of symbiosome differentiation represses transcription of the secretory pathway gene VAMP721a and promotes symbiosome development in Medicago truncatula. Plant Cell 2013, 25:3584-3601.
40. Mergaert P., Uchiumi T., Alunni B., Evanno G., Cheron A., Catrice O., Mausset A.E., Barloy-Hubler F., Galibert F., Kondorosi A., et al. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc Natl Acad Sci USA 2006, 103:5230-5235.
41. Guefrachi I., Nagymihaly M., Pislariu C.I., Van de Velde W., Ratet P., Mars M., Udvardi M.K., Kondorosi E., Mergaert P., Alunni B. Extreme specificity of NCR gene expression in Medicago truncatula. BMC Genomics 2014, 15:712. 10.1186/1471-2164-15-712.
42. Maunoury N., Redondo-Nieto M., Bourcy M., Van de Velde W., Alunni B., Laporte P., Durand P., Agier N., Marisa L., Vaubert D., et al. Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLoS One 2010, 5:e9519.
43. Roux B., Rodde N., Jardinaud M.F., Timmers T., Sauviac L., Cottret L., Carrère S., Sallet E., Courcelle E., Moreau S., et al. An integrated analysis of plant and bacterial gene expression in symbiotic root nodules using laser-capture microdissection coupled to RNA sequencing. Plant J 2014, 77:817-837.
44. Wang D., Griffitts J., Starker C., Fedorova E., Limpens E., Ivanov S., Bisseling T., Long S. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 2010, 327:1126-1129.
45. Dürgo H., Klement É., Hunyadi-Gulyás É., Szucs A., Kereszt A., Medzihradszky K.F., Kondorosi É Identification of nodule-specific cysteine-rich plant peptides in endosymbiotic bacteria. Proteomics 2015, 10.1002/pmic.201400385.
46. Farkas A., Maróti G., Dürgo H., Györgypál Z., Lima R.M., Medzihradszky K.F., Kereszt A., Mergaert P., Kondorosi É The Medicago truncatula symbiotic peptide NCR247 contributes to bacteroid differentiation through multiple mechanisms. Proc Natl Acad Sci USA 2014, 111:5183-5188.
47. Penterman J., Abo R.P., De Nisco N.J., Arnold M.F., Longhi R., Zanda M., Walker G.C. Host plant peptides elicit a transcriptional response to control the Sinorhizobium meliloti cell cycle during symbiosis. Proc Natl Acad Sci USA 2014, 111:3561-3566.