Fortunella margarita Transcriptional Reprogramming Triggered by Xanthomonas citri subsp. citri
Tóm tắt
Citrus canker disease caused by the bacterial pathogen Xanthomonas citri subsp. citri (Xcc) has become endemic in areas where high temperature, rain, humidity, and windy conditions provide a favourable environment for the dissemination of the bacterium. Xcc is pathogenic on many commercial citrus varieties but appears to elicit an incompatible reaction on the citrus relative Fortunella margarita Swing (kumquat), in the form of a very distinct delayed necrotic response. We have developed subtractive libraries enriched in sequences expressed in kumquat leaves during both early and late stages of the disease. The isolated differentially expressed transcripts were subsequently sequenced. Our results demonstrate how the use of microarray expression profiling can help assign roles to previously uncharacterized genes and elucidate plant pathogenesis-response related mechanisms. This can be considered to be a case study in a citrus relative where high throughput technologies were utilized to understand defence mechanisms in Fortunella and citrus at the molecular level. cDNAs from sequenced kumquat libraries (ESTs) made from subtracted RNA populations, healthy vs. infected, were used to make this microarray. Of 2054 selected genes on a customized array, 317 were differentially expressed (P < 0.05) in Xcc challenged kumquat plants compared to mock-inoculated ones. This study identified components of the incompatible interaction such as reactive oxygen species (ROS) and programmed cell death (PCD). Common defence mechanisms and a number of resistance genes were also identified. In addition, there were a considerable number of differentially regulated genes that had no homologues in the databases. This could be an indication of either a specialized set of genes employed by kumquat in response to canker disease or new defence mechanisms in citrus. Functional categorization of kumquat Xcc-responsive genes revealed an enhanced defence-related metabolism as well as a number of resistant response-specific genes in the kumquat transcriptome in response to Xcc inoculation. Gene expression profile(s) were analyzed to assemble a comprehensive and inclusive image of the molecular interaction in the kumquat/Xcc system. This was done in order to elucidate molecular mechanisms associated with the development of the hypersensitive response phenotype in kumquat leaves. These data will be used to perform comparisons among citrus species to evaluate means to enhance the host immune responses against bacterial diseases.
Tài liệu tham khảo
Gottwald TR, Graham JH, Schubert TS: Citrus canker: The pathogen and its impact. Online Plant Health Progress. 2002.
Głowacki S, Macioszek V, Kononowicz A: R proteins as fundamentals of plant innate immunity. Cellular & Molecular Biology Letters. 2010, 1-24.
Jones JD, Dangl JL: The plant immune system. Nature. 2006, 444 (7117): 323-329. 10.1038/nature05286.
Fujikawa T, Ishihara H, Leach JE, Tuyumu S: Suppression of defense response in plants by avrBs3/pthA gene family of Xanthomonas spp. MolPlant-Microbe Interact. 2006, 19: 342-349. 10.1094/MPMI-19-0342.
Yang B, Sugio A, White FF: Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact. 2005, 18 (2): 142-149. 10.1094/MPMI-18-0142.
Alfano JR, Collmer A: The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol. 1997, 179 (18): 5655-5662.
Sanabria N, Goring D, Nurnberger T, Dubery I: Self/nonself perception and recognition mechanisms in plants: a comparison of self-incompatibility and innate immunity. New Phytol. 2008, 178 (3): 503-514. 10.1111/j.1469-8137.2008.02403.x.
Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C, Orellano EG, Ottado J: Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis. Proc Natl Acad Sci USA. 2008, 105 (47): 18631-18636. 10.1073/pnas.0810107105.
Bestwick CS, Brown IR, Bennett MH, Mansfield JW: Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell. 1997, 9 (2): 209-221.
Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA: Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell. 2007, 19 (3): 1081-1095. 10.1105/tpc.106.045096.
Shiotani H, Fujikawa T, Ishihara H, Tsuyumu S, Ozaki K: A pthA homolog from Xanthomonas axonopodis pv. citri responsible for host-specific suppression of virulence. J Bacteriol. 2007, 189 (8): 3271-3279. 10.1128/JB.01790-06.
Brunings AM, Gabriel DW: Xanthomonas citri: breaking the surface. Molecular Plant Pathology. 2003, 4 (3): 141-157. 10.1046/j.1364-3703.2003.00163.x.
Romer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T: Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science. 2007, 318 (5850): 645-648. 10.1126/science.1144958.
Yang B, White FF: Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol Plant Microbe Interact. 2004, 17 (11): 1192-1200. 10.1094/MPMI.2004.17.11.1192.
Duan YP, A C, G Z, G E, Gabriel DW: Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement, and cell death. Molecular Plant-Microbe Interactions. 1999, 12 (6): 556-560. 10.1094/MPMI.1999.12.6.556.
Tasic L, Borin PF, Khater LC, Ramos CH: Cloning and characterization of three hypothetical secretion chaperone proteins from Xanthomonas axonopodis pv. citri. Protein Expr Purif. 2007, 53 (2): 363-369. 10.1016/j.pep.2007.01.011.
White FF, Potnis N, Jones JB, Koebnik R: The type III effectors of Xanthomonas. Mol Plant Pathol. 2009, 10 (6): 749-766. 10.1111/j.1364-3703.2009.00590.x.
Schenk PM, Kazan K, Manners JM, Anderson JP, Simpson RS, Wilson IW, Somerville SC, Maclean DJ: Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol. 2003, 132 (2): 999-1010. 10.1104/pp.103.021683.
Spoel SH, Dong X: Making sense of hormone crosstalk during plant immune responses. Cell Host Microbe. 2008, 3 (6): 348-351. 10.1016/j.chom.2008.05.009.
Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R: ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell. 2003, 15 (1): 165-178. 10.1105/tpc.007468.
Nemhauser JL, Hong F, Chory J: Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006, 126 (3): 467-475. 10.1016/j.cell.2006.05.050.
Glazebrook J: Use of microarray analysis to dissect the plant defense response. Methods Mol Biol. 2007, 354: 121-130.
Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RA, Ritsema T, Pieterse CM: Ethylene Modulates the Role of NPR1 in Cross-Talk Between Salicylate and Jasmonate Signaling. Plant Physiol. 2009.
Khalaf AA, Moore GA, Jones JB, Gmitter FG: New insights into the resistance of Nagami kumquat to canker disease. Physiological and Molecular Plant Pathology. 2007, 71: 240-250. 10.1016/j.pmpp.2008.03.001.
Alfano JR, Collmer A: Bacterial pathogens in plants: Life up against the wall. Plant Cell. 1996, 8 (10): 1683-1698.
Alba R, Fei Z, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D'Ascenzo M, Gordon JS, Rose JK, et al: ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J. 2004, 39 (5): 697-714. 10.1111/j.1365-313X.2004.02178.x.
Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A: High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36 (10): 3420-3435. 10.1093/nar/gkn176.
Talon M, Gmitter FG: Citrus genomics. Int J Plant Genomics. 2008, 2008: 528361.
Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M: Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005, 21 (18): 3674-3676. 10.1093/bioinformatics/bti610.
Cohn JR, Martin GB: Pseudomonas syringae pv. tomato type III effectors AvrPto and AvrPtoB promote ethylene-dependent cell death in tomato. Plant J. 2005, 44 (1): 139-154. 10.1111/j.1365-313X.2005.02516.x.
Desikan R, S AH-M, Hancock JT, Neill SJ: Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiol. 2001, 127 (1): 159-172. 10.1104/pp.127.1.159.
Gang DR, Wang J, Dudareva N, Nam KH, Simon JE, Lewinsohn E, Pichersky E: An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol. 2001, 125 (2): 539-555. 10.1104/pp.125.2.539.
Conesa A, Gotz S: Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics. 2008, 2008: 619832.
Nueda MJ, Conesa A, Westerhuis JA, Hoefsloot HC, Smilde AK, Talon M, Ferrer A: Discovering gene expression patterns in time course microarray experiments by ANOVA-SCA. Bioinformatics. 2007, 23 (14): 1792-1800. 10.1093/bioinformatics/btm251.
Kay S, Hahn S, Marois E, Hause G, Bonas U: A Bacterial Effector Acts as a Plant Transcription Factor and Induces a Cell Size Regulator. Science. 2007, 318 (5850): 648-651. 10.1126/science.1144956.
Cernadas RA, Camillo LR, Benedetti CE: Transcriptional analysis of the sweet orange interaction with the citrus canker pathogens Xanthomonas axonopodis pv. citri and Xanthomonas axonopodis pv. aurantifolii. Mol Plant Pathol. 2008, 9 (5): 609-631. 10.1111/j.1364-3703.2008.00486.x.
Albrecht U, Bowman KD: Transcriptional response of susceptible and tolerant citrus to infection with Candidatus Liberibacter asiaticus. Plant Science. 2011.
Ross J, Li Y, Lim E, Bowles DJ: Higher plant glycosyltransferases. Genome Biol. 2001, 2 (2): Reviews 3004.
Dixon RA: Natural products and plant disease resistance. Nature. 2001, 411 (6839): 843-847. 10.1038/35081178.
Mugford ST, Qi X, Bakht S, Hill L, Wegel E, Hughes RK, Papadopoulou K, Melton R, Philo M, Sainsbury F, et al: A serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats. Plant Cell. 2009, 21 (8): 2473-2484. 10.1105/tpc.109.065870.
Nanda AK, Andrio E, Marino D, Pauly N, Dunand C: Reactive Oxygen Species during plant-microorganism early interactions. Journal of Integrative Plant Biology. 2010, 52 (2): 195-204. 10.1111/j.1744-7909.2010.00933.x.
Torres MA: ROS in biotic interactions. Physiologia Plantarum. 2010, 138 (4): 414-429. 10.1111/j.1399-3054.2009.01326.x.
de Pinto MC, Paradiso A, Leonetti P, De Gara L: Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J. 2006, 48 (5): 784-795. 10.1111/j.1365-313X.2006.02919.x.
Vranova E, Inze D, Van Breusegem F: Signal transduction during oxidative stress. J Exp Bot. 2002, 53 (372): 1227-1236. 10.1093/jexbot/53.372.1227.
Kuzniak E, Sklodowska M: The effect of Botrytis cinerea infection on the antioxidant profile of mitochondria from tomato leaves. J Exp Bot. 2004, 55 (397): 605-612. 10.1093/jxb/erh076.
Halliwell B, Foyer CH: Ascorbic acid, metal ions and the superoxide radical. Biochem J. 1976, 155 (3): 697-700.
Foyer CH, Noctor G: Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell. 2005, 17 (7): 1866-1875. 10.1105/tpc.105.033589.
Trumper S, Follmann H, Haberlein I: A novel-dehydroascorbate reductase from spinach chloroplasts homologous to plant trypsin inhibitor. FEBS Lett. 1994, 352 (2): 159-162. 10.1016/0014-5793(94)00947-3.
Yang C-W, Gonzalez-Lamothe R, Ewan RA, Rowland O, Yoshioka H, Shenton M, Ye H, O'Donnell E, Jones JDG, Sadanandom A: The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and Its functional tobacco Homolog ACRE276 are required for cell death and defense. Plant Cell. 2006, 18 (4): 1084-1098. 10.1105/tpc.105.039198.
Trujillo M, Ichimura K, Casais C, Shirasu K: Negative regulation of PAMP-triggered immunity by an E3 ubiquitin ligase triplet in Arabidopsis. Curr Biol. 2008, 18 (18): 1396-1401. 10.1016/j.cub.2008.07.085.
Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S: Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta. 2006, 225 (1): 1-12. 10.1007/s00425-006-0303-3.
Mysore KS, D'Ascenzo MD, He X, Martin GB: Overexpression of the disease resistance gene Pto in tomato induces gene expression changes similar to immune responses in human and fruitfly. Plant Physiol. 2003, 132 (4): 1901-1912. 10.1104/pp.103.022731.
Quirino BF, Noh YS, Himelblau E, Amasino RM: Molecular aspects of leaf senescence. Trends Plant Sci. 2000, 5 (7): 278-282. 10.1016/S1360-1385(00)01655-1.
Albert M, Werner M, Proksch P, Fry SC, Kaldenhoff R: The cell wall-modifying xyloglucan endotransglycosylase/hydrolase LeXTH1 is expressed during the defence reaction of tomato against the plant parasite Cuscuta reflexa. Plant Biol (Stuttg). 2004, 6 (4): 402-407. 10.1055/s-2004-817959.
Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H: Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol. 2004, 134 (1): 420-431. 10.1104/pp.103.028324.
Lee S, Kim SY, Chung E, Joung YH, Pai HS, Hur CG, Choi D: EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycines). Funct Integr Genomics. 2004, 4 (3): 196-205.
Brunner F, Stintzi A, Fritig B, Legrand M: Substrate specificities of tobacco chitinases. Plant J. 1998, 14 (2): 225-234. 10.1046/j.1365-313X.1998.00116.x.
Kasprzewska A: Plant chitinases--regulation and function. Cell Mol Biol Lett. 2003, 8 (3): 809-824.
Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E: Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J. 1998, 16 (2): 223-233. 10.1046/j.1365-313x.1998.00288.x.
Mitsuhara I, Iwai T, Seo S, Yanagawa Y, Kawahigasi H, Hirose S, Ohkawa Y, Ohashi Y: Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Molecular genetics and genomics: MGG. 2008, 279 (4): 415-427. 10.1007/s00438-008-0322-9.
Campos MA, Rosa DD, Teixeira JÉC, Targon MLPN, Souza AA, Paiva LV, Stach-Machado DR, Machado MA: PR gene families of citrus: their organ specific-biotic and abiotic inducible expression profiles based on ESTs approach. Genetics and Molecular Biology. 2007, 30: 917-930. 10.1590/S1415-47572007000500020.
Li C-W, Su R-C, Cheng C-P, You S-J, Hsieh T-H, Chao T-C, Chan M-T: Tomato RAV Transcription Factor Is a Pivotal Modulator Involved in the AP2/EREBP-Mediated Defense Pathway. Plant Physiology. 2011, 156 (1): 213-227. 10.1104/pp.111.174268.
Dodds PN, Lawrence GJ, Ellis JG: Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell. 2001, 13 (1): 163-178.
Pontier D, Godiard L, Marco Y, Roby D: hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant/pathogen interactions. Plant J. 1994, 5 (4): 507-521. 10.1046/j.1365-313X.1994.5040507.x.
Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK, Bent AF: The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA. 2000, 97 (16): 9323-9328. 10.1073/pnas.150005697.
Green DR, Reed JC: Mitochondria and apoptosis. Science. 1998, 281 (5381): 1309-1312.
Logan DC: The dynamic plant chondriome. Seminars in Cell & Developmental Biology. 2010, 21 (6): 550-557. 10.1016/j.semcdb.2009.12.010.
Martinou J-C, Desagher S, Antonsson B: Cytochrome c release from mitochondria: all or nothing. Nat Cell Biol. 2000, 2 (3): E41-E43. 10.1038/35004069.
Sanchez P, de Torres Zabala M, Grant M: AtBI-1, a plant homologue of Bax inhibitor-1, suppresses Bax-induced cell death in yeast and is rapidly upregulated during wounding and pathogen challenge. Plant J. 2000, 21 (4): 393-399. 10.1046/j.1365-313x.2000.00690.x.
Hoeberichts FA, Woltering EJ: Multiple mediators of plant programmed cell death: Interplay of conserved cell death mechanisms and plant-specific regulators. BioEssays. 2003, 25 (1): 47-57. 10.1002/bies.10175.
Li J, Brader G, Palva ET: Kunitz trypsin inhibitor: an antagonist of cell death triggered by phytopathogens and fumonisin b1 in Arabidopsis. Mol Plant. 2008, 1 (3): 482-495. 10.1093/mp/ssn013.
Xu R, Song F, Zheng Z: OsBISAMT1, a gene encoding S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, is differentially expressed in rice defense responses. Mol Biol Rep. 2006, 33 (3): 223-231. 10.1007/s11033-005-4823-x.
Kumar D, Klessig DF: High-affinity salicylic acid-binding protein 2 is required for plant innate immunity and has salicylic acid-stimulated lipase activity. Proc Natl Acad Sci USA. 2003, 100 (26): 16101-16106. 10.1073/pnas.0307162100.
Gibly A, Bonshtien A, Balaji V, Debbie P, Martin GB, Sessa G: Identification and expression profiling of tomato genes differentially regulated during a resistance response to Xanthomonas campestris pv. vesicatoria. Mol Plant Microbe Interact. 2004, 17 (11): 1212-1222. 10.1094/MPMI.2004.17.11.1212.
Lund ST, Stall RE, Klee HJ: Ethylene regulates the susceptible response to pathogen infection in tomato. Plant Cell. 1998, 10 (3): 371-382.
Heller RA, Schena M, Chai A, Shalon D, Bedilion T, Gilmore J, Woolley DE, Davis RW: Discovery and analysis of inflammatory disease-related genes using cDNA microarrays. Proc Natl Acad Sci USA. 1997, 94 (6): 2150-2155. 10.1073/pnas.94.6.2150.
Smyth GK, (ed): Limma: Linear models for microarray data. New York:Springer; 2005.
Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP: Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 2002, 30 (4): e15-10.1093/nar/30.4.e15.
Conesa A, Nueda MJ, Ferrer A, Talon M: maSigPro: a method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics. 2006, 22 (9): 1096-1102. 10.1093/bioinformatics/btl056.
Nueda MJ, Sebastian P, Tarazona S, Garcia-Garcia F, Dopazo J, Ferrer A, Conesa A: Functional assessment of time course microarray data. BMC Bioinformatics. 2009, 10 (Suppl 6): S9-10.1186/1471-2105-10-S6-S9.