RNA-seq analysis reveals the role of red light in resistance against Pseudomonas syringae pv. tomato DC3000 in tomato plants

详细信息    查看全文

• 作者：You-Xin Yang (1) (2)
  Meng-Meng Wang (1) (3)
  Yan-Ling Yin (1) (2)
  Eugen Onac (4)
  Guo-Fu Zhou (4)
  Sheng Peng (3)
  Xiao-Jian Xia (1)
  Kai Shi (1)
  Jing-Quan Yu (1) (2)
  Yan-Hong Zhou (1) (2)
  
  1. Department of Horticulture ; Zijingang Campus ; Zhejiang University ; Yuhangtang Road 866 ; Hangzhou ; 310058 ; P. R. China
  2. Key Laboratory of Horticultural Plants Growth ; Development and Quality Improvement ; Agricultural Ministry of China ; Zijingang Road 866 ; Hangzhou ; 310058 ; P. R. China
  3. Philips Research China ; No. 9 Lane 888 Tian Lin Road ; Shanghai ; 200233 ; P. R. China
  4. Philips Research Europe ; High Tech Campus 34 ; 5656 AE ; Eindhoven ; Netherlands
  
• 刊名：BMC Genomics
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：16
• 期：1
• 全文大小：1,113 KB
• 参考文献：1. Dangl, JL, Jones, JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411: pp. 826-33 CrossRef
  2. Kunkel, BN, Brooks, DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5: pp. 325-31 CrossRef
  3. Durrant, W, Dong, X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: pp. 185-209 CrossRef
  4. Chester, KS (1933) The problem of acquired physiological immunity in plants. Q Rev Biol 8: pp. 275-324 CrossRef
  5. Durner, J, Shah, J, Klessig, DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2: pp. 266-74 CrossRef
  6. Koga, H, Dohi, K, Mori, M (2004) Abscisic acid and low temperatures suppress the whole plant-specific resistance reaction of rice plants to the infection of Magnaporthe grisea. Physiol Mol Plant Pathol 65: pp. 3-9 CrossRef
  7. Yasuda, M, Ishikawa, A, Jikumaru, Y, Seki, M, Umezawa, T, Asami, T (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid鈥搈ediated abiotic stress response in Arabidopsis. Plant Cell 20: pp. 1678-92 CrossRef
  8. 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: pp. 677-99 CrossRef
  9. Griebel, T, Zeier, J (2008) Light regulation and daytime dependency of inducible plant defenses in Arabidopsis: phytochrome signaling controls systemic acquired resistance rather than local defense. Plant Physiol 147: pp. 790-801 CrossRef
  10. Chandra-Shekara, AC, Gupte, M, Navarre, D, Raina, S, Raina, R, Klessig, D (2006) Light-dependent hypersensitive response and resistance signaling against Turnip Crinkle Virus in Arabidopsis. Plant J 45: pp. 320-34 CrossRef
  11. Gyula, P, Sch盲fer, E, Nagy, F (2003) Light perception and signalling in higher plants. Curr Opin Plant Biol 6: pp. 446-52 CrossRef
  12. Genoud, T, Buchala, AJ (2002) Phytochrome signalling modulates the SA-perceptive pathway in Arabidopsis. Plant J 31: pp. 87-95 CrossRef
  13. Wang, W, Barnaby, JY, Tada, Y, Li, H, T枚r, M, Caldelari, D (2011) Timing of plant immune responses by a central circadian regulator. Nature 470: pp. 110-4 CrossRef
  14. Roden, LC, Ingle, RA (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell 21: pp. 2546-52 CrossRef
  15. Gouinguen茅, SP, Turlings, TC (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129: pp. 1296-307 CrossRef
  16. Zeier, J, Pink, B, Mueller, MJ, Berger, S (2004) Light conditions influence specific defence responses in incompatible plant-pathogen interactions: uncoupling systemic resistance from salicylic acid and PR-1 accumulation. Planta 219: pp. 673-83 CrossRef
  17. Soitamo, AJ, Piippo, M, Allahverdiyeva, Y, Battchikova, N, Aro, EM (2008) Light has a specific role in modulating Arabidopsis gene expression at low temperature. BMC Plant Biol 8: pp. 13 CrossRef
  18. Morker, KH, Roberts, MR (2011) Light exerts multiple levels of influence on the Arabidopsis wound response. Plant Cell Environ 34: pp. 717-28 CrossRef
  19. Karpinski, S, Gabrys, H, Mateo, A, Karpinska, B, Mullineaux, PM (2003) Light perception in plant disease defence signalling. Curr Opin Plant Biol 6: pp. 390-6 CrossRef
  20. Wang, H, Jiang, YP, Yu, HJ, Xia, XJ, Shi, K, Zhou, YH (2010) Light quality affects incidence of powdery mildew, expression of defence-related genes and associated metabolism in cucumber plants. Eur J Plant Pathol 127: pp. 125-35 CrossRef
  21. Zhou, J, Xia, XJ, Zhou, YH, Shi, K, Chen, ZX, Yu, JQ (2014) RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato. J Exp Bot 65: pp. 595-607 CrossRef
  22. Katagiri, F, Thilmony, R, He, SY The Arabidopsis thaliana-Pseudomonas syringae interaction. In: Somerville, CR, Meyerowitz, EM eds. (2002) The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, pp. 1-39
  23. Shah, J, Tsui, F, Klessig, DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene. Mol Plant Microbe Interact 10: pp. 69-78 CrossRef
  24. Koch, E, Slusarenko, A (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2: pp. 437-45 CrossRef
  25. Zhou J, Wang J, Shi K, Xia XJ, Zhou YH, Yu JQ. Hydrogen peroxide is involved in the cold acclimation-induced chilling tolerance of tomato plants. Plant Physiol Biochem. 2012;60:141-9.
  26. Lichtenthaler, HK, AR, W (1983) Determinations of total carotenoids and chlorophylls b of leaf extracts in different solvents. Biochem Soc Trans 11: pp. 591-2
  27. Hong, SW, Lee, U, Vierling, E (2003) Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol 132: pp. 757-67 CrossRef
  28. Sgherri, CLM, Navariizzo, F (1995) Sunflower seedlings subjected to increasing water deficit stress: oxidative stress and defense-mechanisms. Physiol Plant 93: pp. 25-30 CrossRef
  29. Storey, JD, Tibshirani, R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: pp. 9440-5 CrossRef
  30. Conesa, A, G枚tz, S, Garc铆a-G贸mez, JM, Terol, J, Tal贸n, M, Robles, M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: pp. 3674-6 CrossRef
  31. Ye, J, Fang, L, Zheng, H, Zhang, Y, Chen, J, Zhang, Z (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34: pp. W293-7 CrossRef
  32. Xia, XJ, Wang, YJ, Zhou, YH, Tao, Y, Mao, WH, Shi, K (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150: pp. 801-14 CrossRef
  33. Livak, KJ, Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-螖螖CT method. Methods 25: pp. 402-8 CrossRef
  34. Bhardwaj, V, Meier, S, Petersen, LN, Ingle, RA, Roden, LC (2011) Defence responses of Arabidopsis thaliana to infection by Pseudomonas syringae are regulated by the circadian clock. PLoS One 6: pp. e26968 CrossRef
  35. Zhang, C, Xie, Q, Anderson, RG, Ng, G, Seitz, NC, Peterson, T (2013) Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog 9: pp. e1003370 CrossRef
  36. Islam, SZ, Babadoost, M, Bekal, S, Lambert, K (2008) Red light-induced systemic disease resistance against root-knot nematode Meloidogyne javanica and Pseudomonas syringae pv. tomato DC 3000. J Phytopathol 156: pp. 708-14 CrossRef
  37. Xie, XZ, Xue, YJ, Zhou, JJ, Zhang, B, Chang, H, Takano, M (2011) Phytochromes regulate SA and JA signaling pathways in rice and are required for developmentally controlled resistance to Magnaporthe grisea. Mol Plant 4: pp. 688-96 CrossRef
  38. Carvalho, RF, Campos, ML, Azevedo, RA (2011) The role of phytochrome in stress tolerance. J Integr Plant Biol 53: pp. 920-9 CrossRef
  39. McClung, CR (2006) Plant circadian rhythms. Plant Cell 18: pp. 792-803 CrossRef
  40. Khanna, R, Kikis, EA, Quail, PH (2003) EARLY FLOWERING 4 functions in phytochrome B-regulated seedling de-etiolation. Plant Physiol 133: pp. 1530-8 CrossRef
  41. Goodspeed, D, Chehab, EW, Covington, MF, Braam, J (2013) Circadian control of jasmonates and salicylates: The clock role in plant defense. Plant Signal Behav 8: pp. e23123 CrossRef
  42. Cao, S, Ye, M, Jiang, S (2005) Involvement of GIGANTEA gene in the regulation of the cold stress response in Arabidopsis. Plant Cell Rep 24: pp. 683-90 CrossRef
  43. Cao, S, Jiang, S, Zhang, R (2006) The role of GIGANTEA gene in mediating the oxidative stress response and in Arabidopsis. Plant Growth Regul 48: pp. 261-70 CrossRef
  44. Kang, K, Lee, K, Park, S, Kim, YS, Back, K (2010) Enhanced production of melatonin by ectopic overexpression of human serotonin N-acetyltransferase plays a role in cold resistance in transgenic rice seedlings. J Pineal Res 49: pp. 176-82
  45. Huang, JL, Gu, M, Lai, ZB, Fan, BF, Shi, K, Zhou, YH (2010) Functional analysis of the Arabidopsis PAL gene family in plant growth, development, and response to environmental stress. Plant Physiol 153: pp. 1526-38 CrossRef
  46. Chen, Z, Silva, H, Klessig, DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: pp. 1883-6 CrossRef
  47. Ryals, JA, Neuenschwander, UH, Willits, MG, Molina, A, Steiner, HY, Hunt, MD (1996) Systemic acquired resistance. Plant Cell 8: pp. 1809 CrossRef
  48. Pieterse, CM, Leon-Reyes, A, Ent, S, Wees, SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5: pp. 308-16 CrossRef
  49. Ithal, N, Recknor, J, Nettleton, D, Maier, T, Baum, TJ, Mitchum, MG (2007) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact 20: pp. 510-25 CrossRef
  50. Kazan, K, Manners, JM (2008) Jasmonate signaling: toward an integrated view. Plant Physiol 146: pp. 1459-68 CrossRef
  51. Cohn, JR, Martin, GB (2005) Pseudomonas syringae pv. tomato type III effectors AvrPto and AvrPtoB promote ethylene鈥恉ependent cell death in tomato. Plant J 44: pp. 139-54 CrossRef
  52. Chaouch, S, Queval, G, Noctor, G (2012) AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis. Plant J 69: pp. 613-27 CrossRef
  53. Steinhorst, L, Kudla, J (2013) Calcium and reactive oxygen species rule the waves of signaling. Plant Physiol 163: pp. 471-85 CrossRef
  54. Mou, Z, Fan, WH, Dong, XN (2003) Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: pp. 935-44 CrossRef
  55. Li, J, Brader, G, Palva, ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16: pp. 319-31 CrossRef
  56. Li, Y, Baldauf, S, Lim, E-K, Bowles, DJ (2001) Phylogenetic analysis of the UDP-glycosyltransferase multigene family of Arabidopsis thaliana. J Biol Chem 276: pp. 4338-43 CrossRef
  57. Vogt, T, Jones, P (2000) Glycosyltransferases in plant natural product synthesis: characterization of a supergene family. Trends Plant Sci 5: pp. 380-6 CrossRef
  58. Langlois-Meurinne, M, Gachon, CM, Saindrenan, P (2005) Pathogen-responsive expression of glycosyltransferase genes UGT73B3 and UGT73B5 is necessary for resistance to Pseudomonas syringae pv tomato in Arabidopsis. Plant Physiol 139: pp. 1890-901 CrossRef
  59. Schaff, JE, Nielsen, DM, Smith, CP, Scholl, EH, Bird, DM (2007) Comprehensive transcriptome profiling in tomato reveals a role for glycosyltransferase in Mi-mediated nematode resistance. Plant Physiol 144: pp. 1079-92 CrossRef
  60. Dodds, PN, Rathjen, JP (2010) Plant immunity: towards an integrated view of plant鈥損athogen interactions. Nat Rev Genet 11: pp. 539-48 CrossRef
  61. Hauck, P, Thilmony, R, He, SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A 100: pp. 8577-82 CrossRef
  62. Rosli, HG, Zheng, Y, Pombo, MA, Zhong, S, Bombarely, A, Fei, ZJ (2013) Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol 14: pp. R139 CrossRef
  
• 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
• 出版者：BioMed Central
• ISSN：1471-2164

文摘

Background Plants attenuate their responses to a variety of bacterial and fungal pathogens, leading to higher incidences of pathogen infection at night. However, little is known about the molecular mechanism responsible for the light-induced defence response; transcriptome data would likely facilitate the elucidation of this mechanism. Results In this study, we observed diurnal changes in tomato resistance to Pseudomonas syringae pv. tomato DC3000 (Pto DC3000), with the greatest susceptibility before midnight. Nightly light treatment, particularly red light treatment, significantly enhanced the resistance; this effect was correlated with increased salicylic acid (SA) accumulation and defence-related gene transcription. RNA-seq analysis revealed that red light induced a set of circadian rhythm-related genes involved in the phytochrome and SA-regulated resistance response. The biosynthesis and signalling pathways of multiple plant hormones (auxin, SA, jasmonate, and ethylene) were co-ordinately regulated following Pto DC3000 infection and red light, and the SA pathway was most significantly affected by red light and Pto DC3000 infection. This result indicates that SA-mediated signalling pathways are involved in red light-induced resistance to pathogens. Importantly, silencing of nonexpressor of pathogensis-related genes 1 (NPR1) partially compromised red light-induced resistance against Pto DC3000. Furthermore, sets of genes involved in redox homeostasis (respiratory burst oxidase homologue, RBOH; glutathione S-transferases, GSTs; glycosyltransferase, GTs), calcium (calmodulin, CAM; calmodulin-binding protein, CBP), and defence (polyphenol oxidase, PPO; nudix hydrolase1, NUDX1) as well as transcription factors (WRKY18, WRKY53, WRKY60, WRKY70) and cellulose synthase were differentially induced at the transcriptional level by red light in response to pathogen challenge. Conclusions Taken together, our results suggest that there is a diurnal change in susceptibility to Pto DC3000 with greatest susceptibility in the evening. The red light induced-resistance to Pto DC3000 at night is associated with enhancement of the SA pathway, cellulose synthase, and reduced redox homeostasis.