Functional characterization of cotton genes responsive to Verticillium dahliae through bioinformatics and reverse genetics strategies

Journal of Experimental Botany

Volumn 65, Issue 22, 2014, Pages 6679-6692

  Xu, Lian ^a   Zhang, Wenwen ^a   He, Xin ^a   Liu, Min ^a   Zhang, Kun ^a   Shaban, Muhammad ^a   Sun, Longqing ^a   Zhu, Jiachen ^a   Luo, Yijing ^a   Yuan, Daojun ^a   Zhang, Xianlong ^a   Zhu, Longfu ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Arabidopsis; data mining; Gossypium hirsutum; innate immune response; Verticillium dahliae; virus induced gene silencing

Indexed keywords

ARABIDOPSIS; GOSSYPIUM HIRSUTUM; NICOTIANA TABACUM; VERTICILLIUM DAHLIAE;

PLANT PROTEIN; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID; TRANSCRIPTOME;

ARABIDOPSIS; BIOLOGY; DISEASE RESISTANCE; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETIC SCREENING; GENETICS; GOSSYPIUM; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PROCEDURES; REVERSE GENETICS; TOBACCO; VERTICILLIUM;

ARABIDOPSIS; COMPUTATIONAL BIOLOGY; DISEASE RESISTANCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC ASSOCIATION STUDIES; GENETIC TESTING; GOSSYPIUM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT DISEASES; PLANT PROTEINS; REACTIVE OXYGEN SPECIES; REVERSE GENETICS; SALICYLIC ACID; TOBACCO; TRANSCRIPTOME; VERTICILLIUM;

EID: 84922469403     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru393     Document Type: Article

References (63)

1. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J. 2002. MAP kinase signalling cascaDe in Arabidopsis innate immunity. Nature 415, 977-983
2. Atkinson NJ, Lilley CJ, Urwin PE. 2013. IDentification of genes involved in the response of Arabidopsis thaliana to simultaneous biotic and abiotic stresses. Plant Physiology 162, 2028-2041
3. Attaran E, Zeier TE, Griebel T, Zeier J. 2009. Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. The Plant Cell 21, 954-971
4. Bai W, Chern M, Ruan D, Canlas PE, Sze-to WH, Ronald PC. 2011. Enhanced disease resistance and hypersensitivity to BTH by introduction of an NH1/OsNPR1 paralog. Plant Biotechnology Journal 9, 205-215
5. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bauto RJ, Parker JE. 2006. Salicylic acid-inDepenDent enhanced disease susceptibility ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell Death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. The Plant Cell 18, 1038-1051
6. Bednarek P, Pilewska-Bednarek M, Svato A, et al. 2009. A glucosinolate metabolism pathway in living plant cells mediates broadspectrum antifungal Defense. Science 323, 101-106
7. Boudsocq M, Willmann MR, Mccormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J. 2010. Differential innate immune signalling via Ca2+ sensor protein kinases. Nature 464, 418-422
8. Bouwmeester K, Han M, Blanco-Portales R, Song W, WeiDe R, Guo LY, Van Der Vossen EA, Govers F. 2014. The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnology Journal 12, 10-16
9. Brutus A, He SY. 2010. Broad-spectrum Defense against plant pathogens. Nature Biotechnology 28, 330-331
10. Conesa A, Gtz S. 2008. Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics 2008, 1-12
11. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS, Wang L. 2002. The phenylpropanoid pathway and plant Defence-A genomics perspective. Molecular Plant Pathology 3, 371-390
12. Dubouzet JG, Maeda S, Sugano S, et al. 2011. Screening for resistance against Pseudomonas syringae in rice-FOX Arabidopsis lines iDentified a putative receptor-like cytoplasmic kinase gene that confers resistance to major bacterial and fungal pathogens in Arabidopsis and rice. Plant Biotechnology Journal 9, 466-485
13. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 11, 539-548
14. Fradin EF, Abd-El-Haliem A, Masini L, Van Den Berg GC, Joosten MH, Thomma BP. 2011. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiology 156, 2255-2265
15. Fradin EF, Zhang Z, Ayala JCJ, CastroverDe CD, Nazar RN, Robb J, Liu CM, Thomma BP. 2009. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiology 150, 320-332
16. Frickey T, Benedito VA, Udvardi M, Weiller G. 2008. AffyTrees: facilitating comparative analysis of Affymetrix plant microarray chips. Plant Physiology 146, 377-386
17. Gao W, Long L, Zhu LF, Xu L, Gao WH, Sun LQ, Liu LL, Zhang XL. 2013. Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. MCP 12, 3690-3703
18. Gao X, Wheeler T, Li Z, Kenerley CM, He P, Shan L. 2011. Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant Journal 66, 293-305
19. Geisler K, Hughes RK, Sainsbury F, et al. 2013. Biochemical analysis of a multifunctional cytochrome P450 (CYP51) enzyme required for synthesis of antimicrobial triterpenes in plants. Proceedings of the National AcaDemy of Sciences, USA 110, E3360-E3367
20. Helliwell CA, Wesley SV, Wielopolska AJ, Waterhouse PM. 2002. High-throughput vectors for efficient gene silencing in plants. Functional Plant Biology 29, 1217-1225
21. Helliwell EE, Wang Q, Yang Y. 2013. Transgenic rice with inducible ethylene production exhibits broad-spectrum disease resistance to the fungal pathogens Magnaporthe oryzae and Rhizoctonia solani. Plant Biotechnology Journal 11, 33-42
22. Horsch R, Fry J, Hoffmann N, Eichholtz D, Rogers SA, Fraley R. 1985. A simple and general method for transferring genes into plants. Science 227, 1229-1231
23. Jansen L, HollunDer J, Roberts I, Forestan C, Fonteyne P, Quickenborne C, Zhen RG, Mckersie B, Parizot B, Beeckman T. 2013. Comparative transcriptomics as a tool for the iDentification of root branching genes in maize. Plant Biotechnology Journal 11, 1092-1102
24. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444, 323-329
25. Kawchuk L, Hachey J, Lynch DR, et al. 2001. Tomato Ve disease resistance genes encoDe cell surface-like receptors. Proceedings of the National AcaDemy of Sciences, USA 98, 6511-6515
26. Knig S, Feussner K, Kaever A, LanDesfeind M, Thurow C, Karlovsky P, Gatz C, Polle A, Feussner I. 2014. Soluble phenylpropanoids are involved in the Defense response of Arabidopsis against Verticillium longisporum. New Phytologist 202, 823-837
27. Kumar D, Gustafsson C, Klessig DF. 2006. Validation of RNAi silencing specificity using synthetic genes: salicylic acid-binding protein 2 is required for innate immunity in plants. The Plant Journal 45, 863-868
28. Lacombe S, Rougon-Cardoso A, Sherwood E, et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnology 28, 365-369
29. Lee SC, Hwang BK. 2005. Induction of some Defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221, 790-800
30. Leto TL, Geiszt M. 2006. Role of Nox family NADPH oxidases in host Defense. Antioxidants and Redox Signalling 8, 1549-1561
31. Liu C, Wang T, Zhang W, Li X. 2008. Computational iDentification and analysis of immune-Associated nucleotiDe gene family in Arabidopsis thaliana. Journal of Plant Physiology 165, 777-787
32. Liu F, Jiang H, Ye S, et al. 2010. The Arabidopsis P450 protein CYP82C2 modulates jasmonate-induced root growth inhibition, Defense gene expression and indole glucosinolate biosynthesis. Cell Research 20, 539-552
33. Liu LL, Zhang WW, Zhou Y, Miao Y, Xu L, Liu M, Zhang K, Zhang XL, Zhu LF. 2014. The resistance of cotton and tomato to Verticillium dahliae from cotton is inDepenDent on Ve1. Scientia Sinica Vitae 44, 803-814
34. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. 2002. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399-403
35. Mishina TE, Zeier J. 2006. The Arabidopsis flavin-DepenDent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiology 141, 1666-1675
36. Mishina TE, Zeier J. 2007. Pathogen-Associated molecular pattern recognition rather than Development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. The Plant Journal 50, 500-513
37. Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A. 2009. Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiology and Biochemistry 47, 785-795
38. Nogueira FTS, Sassaki FT, Maia IG. 2011. Arabidopsis thaliana uncoupling proteins (AtUCPs): insights into gene expression during Development and stress response and epigenetic regulation. Journal of Bioenergetics and Biomembranes 43, 71-79
39. Palma K, Zhao Q, Cheng YT, Bi D, Monaghan J, Cheng W, Zhang Y, Li X. 2007. Regulation of plant innate immunity by three proteins in a complex conserved across the plant and animal kingdoms. Genes and Development 21, 1484-1493
40. Paterson AH, WenDel JF, Gundlach H, et al. 2012. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492, 423-427
41. Peng M, Bi YM, Zhu T, Rothstein SJ. 2007. Genome-wiDe analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Molecular Biology 65, 775-797
42. Pieterse CM, Leon-Reyes A, Van Der Ent S, Van Wees SC. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308-316
43. Reymond P, Farmer EE. 1998. Jasmonate and salicylate as global signals for Defense gene expression. Current Opinion in Plant Biology 1, 404-411
44. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101-1108
45. Spoel SH, Koornneef A, Claessens SM, et al. 2003. NPR1 modulates cross-talk between salicylate-And jasmonate-DepenDent Defense pathways through a novel function in the cytosol. The Plant Cell 15, 760-770
46. Thaler JS, Owen B, Higgins VJ. 2004. The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiology 135, 530-538
47. Tsuda K, Mine A, Bethke G, Igarashi D, Botanga C J, Tsuda Y, Glazebrook J, Sato M, Katagiri F. 2013. Dual regulation of gene expression mediated by extenDed MAPK activation and salicylic acid contributes to robust innate immunity in Arabidopsis thaliana. PLoS Genetics 9, e1004015
48. Tu LL, Zhang XL, Liu DQ, Jin SX. Cao JL, Zhu LF, Deng FL, Tan JF, Zhang CB. 2007. Suitable internal control genes for qRT-PCR normalization in cotton fiber Development and somatic embryogenesis. Chinese Science Bulletin 52, 3110-3117
49. Van Wees SC, De Swart EA, Van Pelt JA, Van Loon LC, Pieterse CM. 2000. Enhancement of induced disease resistance by simultaneous activation of salicylate-And jasmonate-DepenDent Defense pathways in Arabidopsis thaliana. Proceedings of the National AcaDemy of Sciences, USA 97, 8711-8716
50. Vlot AC, Klessig DF, Park SW. 2008. Systemic acquired resistance: the elusive signal(s). Current Opinion in Plant Biology 11, 436-442
51. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. The Plant Cell 20, 471-481
52. Wang K, Senthil-Kumar M, Ryu CM, Kang L, Mysore KS. 2012a. Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant Physiology 158, 1789-1802
53. Wang K, Wang Z, Li F, et al. 2012b. The draft genome of a diploid cotton Gossypium raimondii. Nature Genetics 44, 1098-1108
54. Xu F, Yang L, Zhang J, Guo X, Zhang X, Li G. 2012a. Prevalence of the Defoliating pathotype of Verticillium dahliae on cotton in central china and virulence on selected cotton cultivars. Journal of Phytopathology 160, 369-376
55. Xu L, Zhu LF, Tu LL, Guo X, Long L, Sun LQ, Gao W, Zhang XL. 2011a. Differential gene expression in cotton Defence response to Verticillium dahliae by SSH. Journal of Phytopathology 159, 606-615
56. Xu L, Zhu LF, Tu LL, Liu LL, Yuan DJ, Jin L, Long L, Zhang XL. 2011b. 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. Journal of Experimental Botany 62, 5607-5621
57. Xu L, Jin L, Long L, Liu LL, He X, Gao W, Zhu LF, Zhang XL. 2012b. Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis. Plant Cell Reports 31, 2177-2188
58. Zhang Y, Wang XF, Ding ZG, Ma Q, Zhang GR, Zhang SL, Li ZK, Wu LQ, Zhang GY, Ma ZY. 2013. Transcriptome profiling of Gossypium barbaDense inoculated with Verticillium dahliae proviDes a resource for cotton improvement. BMC Genomics 14, 637
59. Zhang Y, Wang X, Yang S, Chi J, Zhang G, Ma Z. 2011. Cloning and characterization of a Verticillium wilt resistance gene from Gossypium barbaDense and functional analysis in Arabidopsis thaliana. Plant Cell Reports 30, 2085-2096
60. Zhang B, Yang Y, Chen T, Yu W, Liu T, Li H, Fan X, Ren Y, Shen D, Liu L. 2012. Island cotton Gbve1 gene encoding a receptor-like protein confers resistance to both Defoliating and non-Defoliating isolates of Verticillium dahliae. PloS One 7, e51091
61. Zhu LF, Tu LL, Zeng FC, Liu DQ, Zhang XL. 2005. An improved simple protocol for isolation of high quality RNA from Gossypium spp. suitable for cDNA library construction. Acta Agronomica Sinica 31, 1657-1659
62. Zimmermann P, Hennig L, Gruissem W. 2005. Gene-expression analysis and network discovery using Genevestigator. Trends in Plant Science 10, 407-409
63. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764-767