The LOV protein of Xanthomonas citri subsp. citri plays a significant role in the counteraction of plant immune responses during citrus canker

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Kraiselburd, Ivana ^a   Daurelio, Lucas D ^a   Tondo, María Laura ^a   Merelo, Paz ^b   Cortadi, Adriana A ^a   Talón, Manuel ^b   Tadeo, Francisco R ^b   Orellano, Elena G ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b Institut Valencia d'Investigacions Agraries IVIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; VEGETABLE PROTEIN; VISUAL PROTEINS AND PIGMENTS;

GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGY; LIGHT; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; PROTEIN TERTIARY STRUCTURE; SWEET ORANGE; VIRULENCE; XANTHOMONAS;

BACTERIAL PROTEINS; CITRUS SINENSIS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; IMMUNE EVASION; LIGHT; PHOTORECEPTORS, MICROBIAL; PHOTOSYNTHESIS; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; VIRULENCE; XANTHOMONAS;

EID: 84894101571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080930     Document Type: Article

References (62)

1. Mysore KS, Ryu CM (2004) Non-host resistance: how much do we know? Trends Plant Sci 9: 97-104. doi:10.5363/tits.9.7-97. PubMed: 15102376. (Pubitemid 38215139)
2. Bolton MD, van Esse HP, Vossen JH, de JR, Stergiopoulos I et al. (2008) The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol Microbiol 69: 119-136. doi:10.1111/j.1365-2958.2008.06270.x. PubMed: 18452583. (Pubitemid 351832760)
3. Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44: 321-334. doi:10.1023/A:1026592509060. PubMed: 11199391.
4. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814. doi:10.1016/j.cell.2006.02.008. PubMed: 16497589. (Pubitemid 43261453)
5. Van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135-162. doi:10.1146/annurev.phyto.44.070505.143425. PubMed: 16602946. (Pubitemid 44435701)
6. Daurelio LD, Romero MS, Petrocelli S, Merelo P, Cortadi AA et al. (2013) Characterization of Citrus sinensis transcription factors closely associated with the non-host response to Xanthomonas campestris pv. vesicatoria. J Plant Physiol 170: 934-942. doi:10.1016/j.jplph.2013.01.011. PubMed: 23453188.
7. Bolton MD (2009) Primary Metabolism and Plant Defense-Fuel for the Fire. Mol Plant Microbe Interact 22: 487-497. doi:10.1094/MPMI-22-5-0487. PubMed: 19348567.
8. Major IT, Nicole MC, Duplessis S, Séguin A (2010) Photosynthetic and respiratory changes in leaves of poplar elicited by rust infection. Photosynth Res 104: 41-48. doi:10.1007/s11120-009-9507-2. PubMed: 20012201.
9. Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ 35: 441-453. doi:10.1111/j.1365-3040.2011.02399.x. PubMed: 21752032.
10. Roberts MR, Paul ND (2006) Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytol 170: 677-699. doi:10.1111/j.1469-8137. 2006.01707.x. PubMed: 16684231. (Pubitemid 43733631)
11. Avila-Pérez M, Hellingwerf KJ, Kort R (2006) Blue light activates the sigmaB-dependent stress response of Bacillus subtilis via YtvA. J Bacteriol 188: 6411-6414. doi:10.1128/JB.00716-06. PubMed: 16923909. (Pubitemid 44448584)
12. Purcell EB, Siegal-Gaskins D, Rawling DC, Fiebig A, Crosson S (2007) A photosensory two-component system regulates bacterial cell attachment. Proc-Natl-Acad-Sci-U-S-A 104: 18241-18246. PubMed: 17986614.
13. Gomelsky M, Hoff WD (2011) Light helps bacteria make important lifestyle decisions. Trends Microbiol 19: 441-448. doi:10.1016/j.tim.2011.05.002. PubMed: 21664820.
14. Swartz TE, Tseng TS, Frederickson MA, Paris G, Comerci DJ et al. (2007) Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317: 1090-1093. doi:10.1126/science.1144306. PubMed: 17717187. (Pubitemid 47330194)
15. Mussi MA, Gaddy JA, Cabruja M, Arivett BA, Viale AM et al. (2010) The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J Bacteriol 192: 6336-6345. doi:10.1128/JB.00917-10. PubMed: 20889755.
16. Kraiselburd I, Alet AI, Tondo ML, Petrocelli S, Daurelio LD et al. (2012) A LOV protein modulates the physiological attributes of Xanthomonas axonopodis pv. citri relevant for host plant colonization. PLOS-ONE 7: e38226. PubMed: 22675525.
17. van der Horst MA, Hellingwerf KJ (2004) Photoreceptor proteins, "star actors of modern times": a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc Chem Res 37: 13-20. doi:10.1021/ar020219d. PubMed: 14730990.
18. Möglich A, Ayers RA, Moffat K (2009) Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17: 1282-1294. doi:10.1016/j.str. 2009.08.011. PubMed: 19836329.
19. Losi A, Gärtner W (2011) Old chromophores, new photoactivation paradigms, trendy applications: flavins in blue light-sensing photoreceptors(dagger). Photochem Photobiol 87: 491-510. doi:10.1111/j.1751- 1097.2011.00913.x. PubMed: 21352235.
20. Krauss U, Minh BQ, Losi A, Gärtner W, Eggert T et al. (2009) Distribution and phylogeny of light-oxygen-voltage-blue-light-signaling proteins in the three kingdoms of life. J Bacteriol 191: 7234-7242. doi:10.1128/JB. 00923-09. PubMed: 19783626.
21. Brunings AM, Gabriel DW (2003) Xanthomonas citri: breaking the surface. Mol Plant Pathol 4: 141-157. doi:10.1046/j.1364-3703.2003.00163.x. PubMed: 20569374. (Pubitemid 36639406)
22. Graham JH, Gottwald TR, Cubero J, Achor DS (2004) Xanthomonas axonopodis pv. citri: factors affecting successful eradication of citrus canker. Mol Plant Pathol 5: 1-15. doi:10.1046/j.1364-3703.2004.00197.x. PubMed: 20565577. (Pubitemid 38171204)
23. da Silva AC, Ferro JA, Reinach FC, Farah CS, Furlan LR et al. (2002) Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature 417: 459-463. doi:10.1038/417459a. PubMed: 12024217. (Pubitemid 34563540)
24. Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: W64-W70. doi:10.1093/nar/gkq310. PubMed: 20435677.
25. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939. doi:10.1111/j.1365-313X.2004.02016.x. PubMed: 14996223. (Pubitemid 38370342)
26. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS et al. (2002) The phenylpropanoid pathway and plant defence-a genomics perspective. Mol Plant Pathol 3: 371-390. doi:10.1046/j.1364-3703.2002.00131.x. PubMed: 20569344.
27. Xu L, Zhu L, Tu L, Liu L, Yuan D et al. (2011) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 62: 5607-5621. doi:10.1093/jxb/err245. PubMed: 21862479.
28. Shadle GL, Wesley SV, Korth KL, Chen F, Lamb C et al. (2003) Phenylpropanoid compounds and disease resistance in transgenic tobacco with altered expression of L-phenylalanine ammonia-lyase. Phytochemistry 64: 153-161. doi:10.1016/S0031-9422(03)00151-1. PubMed: 12946414. (Pubitemid 37101801)
29. Lauvergeat V, Lacomme C, Lacombe E, Lasserre E, Roby D et al. (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria. Phytochemistry 57: 1187-1195. doi:10.1016/S0031-9422(01)00053-X. PubMed: 11430991. (Pubitemid 32625594)
30. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS et al. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant J 25: 315-323. PubMed: 12566575.
31. Albrecht U, Bowman KD (2012) Transcriptional response of susceptible and tolerant citrus to infection with Candidatus Liberibacter asiaticus. Plant Sci 185-186: 118-130. doi:10.1016/j.plantsci.2011.09.008. PubMed: 22325873.
32. Yamaguchi T, Minami E, Ueki J, Shibuya N (2005) Elicitor-induced activation of phospholipases plays an important role for the induction of defense responses in suspension-cultured rice cells. Plant Cell Physiol 46: 579-587. doi:10.1093/pcp/pci065. PubMed: 15695430. (Pubitemid 40640932)
33. Guidetti-Gonzalez S, Freitas-Astúa J, Morais do Amaral A, Martins NF, Mehta A et al. (2007) Genes associated with hypersensitive response (HR) in the citrus EST database (CitEST). Genet Mol Biol 30(3): 943-956. doi:10.1590/S1415-47572007000500022.
34. Daurelio LD, Tondo ML, Dunger G, Gottig N, Ottado J et al. (2009) Hypersensitive response. In: Sampietro DA, Vattuone MA, Catalan AN, Polyticka B, editors Plant Bioassays Houston, Texas. p. 187-206.
35. Kangasjärvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot 63: 1619-1636. doi:10.1093/jxb/err402. PubMed: 22282535.
36. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89-113. doi:10.1146/annurev.arplant.59.032607. 092759. PubMed: 18444897.
37. Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225: 1-12. doi:10.1007/s00425-006-0303-3. PubMed: 16807755. (Pubitemid 44749601)
38. Krause GH, Weis E (1991) Chlorophyl fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42: 313-349. doi:10.1146/annurev. pp.42.060191.001525.
39. Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C et al. (2008) Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis. Proc Natl Acad Sci U-S-A 105: 18631-18636. doi:10.1073/pnas.0810107105. PubMed: 19015524.
40. Khalaf A, Moore GA, Jones JB, Gmitter FG Jr (2007) New insights into the resistance of Nagami kumquat to canker disease. Physiol Mol Plant Pathol 71: 240-250. doi:10.1016/j.pmpp.2008.03.001.
41. Essmann J, Bones P, Weis E, Scharte J (2008) Leaf carbohydrate metabolism during defense: Intracellular sucrose-cleaving enzymes do not compensate repression of cell wall invertase. Plant Signal Behav 3: 885-887. doi:10.4161/psb.3.10.6501. PubMed: 19704530.
42. Scharte J, Schön H, Tjaden Z, Weis E, von SA (2009) Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants. Proc Natl Acad Sci U-S-A 106: 8061-8066. doi:10.1073/pnas.0812902106. PubMed: 19416911.
43. Berger S, Benediktyová Z, Matous K, Bonfig K, Mueller MJ et al. (2007) Visualization of dynamics of plant-pathogen interaction by novel combination of chlorophyll fluorescence imaging and statistical analysis: differential effects of virulent and avirulent strains of P. syringae and of oxylipins on A. thaliana. J Exp Bot 58: 797-806. PubMed: 17138624. (Pubitemid 46363176)
44. Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ et al. (2003) The monosaccharide transporter gene, AtSTP4, and the cellwall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132: 821-829. doi:10.1104/pp.103.021428. PubMed: 12805612. (Pubitemid 36715081)
45. Nielsen KK, Mikkelsen JD, Kragh KM, Bojsen K (1993) An acidic class III chitinase in sugar beet: induction by Cercospora beticola, characterization, and expression in transgenic tobacco plants. Mol Plant Microbe Interact 6: 495-506. doi:10.1094/MPMI-6-495. PubMed: 8400378.
46. Angelova S, Buchheim M, Frowitter D, Schierhorn A, Roos W (2010) Overproduction of alkaloid phytoalexins in California poppy cells is associated with the co-expression of biosynthetic and stress-protective enzymes. Mol Plants 3: 927-939. doi:10.1093/mp/ssq043. PubMed: 20729473.
47. Lawrence CB, Singh NP, Qiu J, Gardner RG, Tuzun S (2000) Constitutive hydrolytic enzymes are associated with polygenic resistance of tomato to Alternaria solani and may function as an elicitor release mechanism. Physiol Mol Plant Pathol 57: 211-220. doi:10.1006/pmpp.2000.0298. (Pubitemid 32040083)
48. Wang X (1999) The role of phospholipase D in signaling cascades. Plant Physiol 120: 645-652. doi:10.1104/pp.120.3.645. PubMed: 10398699.
49. Paliyath G, Droillard JM (1992) The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol Biochem 30: 789-812.
50. Yan M, Zhang Y, Guo W, Wang X (2012) Soybean endo-betamannanase GmMAN1 is not associated with leaf abscission, but might be involved in the response to wounding. PLOS-ONE 7: e49197. PubMed: 23173047.
51. Esnault R, Chibbar RN, Lee D, van Huystee RB, Ward EWB (1987) Early differences in production of mRNAs for phenylalanine ammonialyase and chalcone synthase in resistant and susceptible cultivars of soybean inoculated with Phytophthora megasperma f. sp. glycinea. Physiol Mol Plant Pathol 30: 293-297. doi:10.1016/0885-5765(87)90042-7.
52. Bell JN, Ryder TB, Wingate VP (1986) Differential accumulation of plant defense gene transcripts in a compatible and an incompatible plant-pathogen interaction. Mol Cell Biol 6: 1615-1623. PubMed: 3785174.
53. Young ND (1996) QTL mapping and quantitative disease resistance in plants. Annu Rev Phytopathol 34: 479-501. doi:10.1146/annurev.phyto.34.1.479. PubMed: 15012553.
54. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory Press.
55. Martinez-Godoy MA, Mauri N, Juarez J, Marques MC, Santiago J et al. (2008) A genome-wide 20 K citrus microarray for gene expression analysis. BMC Genomics 9: 318. doi:10.1186/1471-2164-9-318. PubMed: 18598343.
56. Forment J, Gadea J, Huerta L, Abizanda L, Agusti J et al. (2005) Development of a citrus genome-wide EST collection and cDNA microarray as resources for genomic studies. Plant Mol Biol 57: 375-391. doi:10.1007/s11103- 004-7926-1. PubMed: 15830128. (Pubitemid 40572919)
57. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386. PubMed: 10547847.
58. Karsai A, Müller S, Platz S, Hauser MT (2002) Evaluation of a homemade SYBR green I reaction mixture for real-time PCR quantification of gene expression. BioTechniques 32(4): 790-796. 11962601.
59. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4): 402-408. (Pubitemid 34164012)
60. Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73: 149-156. doi:10.1023/A:1020470224740. PubMed: 16245116.
61. D'Ambrogio de Argüeso A (1986) Manual de técnicas en histología vegetal. Buenos Aires: Editorial Hemisferio Sur S.A.
62. WHO (World Health Organization) (2011) Quality Control Methods for Herbal Materials. Geneva, Switzerland: WHO Press, World Health Organization.