CsBZIP40, a BZIP transcription factor in sweet orange, plays a positive regulatory role in citrus bacterial canker response and tolerance

English version

Autoři: Qiang Li ^aff001; Ruirui Jia ^aff002; Wanfu Dou ^aff001; Jingjing Qi ^aff001; Xiujuan Qin ^aff001; Yongyao Fu ^aff003; Yongrui He ^aff001; Shanchun Chen ^aff001
Působiště autorů: Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, Chongqing, China ^aff001; Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, China ^aff002; School of Advanced Agriculture and Bioengineering, Yangtze Normal University, Chongqing, China ^aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223498

Souhrn

Citrus bacterial canker (CBC) caused by Xanthomonas citri subsp. citri (Xcc) is a systemic bacterial disease that affects citrus plantations globally. Biotic stress in plants has been linked to a group of important transcription factors known as Basic Leucine Zippers (BZIPs). In this study, CsBZIP40 was functionally characterized by expression analysis, including induction by Xcc and hormones, subcellular localization, over-expression and RNAi silencing. CsBZIP40 belongs to group D of the CsBZIP family of transcription factors and localizes in the nucleus, potentially serving as a transcriptional regulator. In wild type (WT) plants CsBZIP40 can be induced by plant hormones in addition to infection by Xcc which has given insight into its involvement in CBC. In the present study, over-expression of CsBZIP40 conferred resistance to Xcc while its silencing led to Xcc susceptibility. Both over-expression and RNAi affected salicylic acid (SA) production and expression of the genes involved in the SA synthesis and signaling pathway, in addition to interaction of CsBZIP40 with CsNPR1, as detected by a GST pull-down assay. Taken together, the results of this study confirmed the important role of CsBZIP40 in improving resistance to citrus canker through the SA signaling pathway by the presence of NPR1 to activate PR genes. Our findings are of potential value in the breeding of tolerance to CBC in citrus fruits.

Klíčová slova:

Gene expression – RNA interference – Transcription factors – Genetically modified plants – Arabidopsis thaliana – Transcriptional control – Fruit crops – Citrus

Zdroje

1. Schaad NW, Postnikova E, Lacy GH, Sechler A, Agarkova I, Stromberg PE, et al. Reclassification of Xanthomonas campestris pv. citri (ex Hasse 1915) Dye 1978 forms A, B/C/D, and E as X. smithii subsp. citri (ex Hasse) sp. nov. nom. rev. comb. nov., X. fuscans subsp. aurantifolii (ex Gabriel 1989) sp. nov. nom. rev. comb. nov., and X. alfalfae subsp. citrumelo (ex Riker and Jones) Gabriel et al., 1989 sp. nov. nom. rev. comb. nov.; X. campestris pv malvacearum (ex smith 1901) Dye 1978 as X. smithii subsp. smithii nov. comb. nov. nom. nov.; X. campestris pv. alfalfae (ex Riker and Jones, 1935) dye 1978 as X. alfalfae subsp. alfalfae (ex Riker et al., 1935) sp. nov. nom. rev.; and "var. fuscans" of X. campestris pv. phaseoli (ex Smith, 1987) Dye 1978 as X. fuscans subsp. fuscans sp. nov. Syst Appl Microbiol. 2005;28(6):494–518. doi: 10.1016/j.syapm.2005.03.017 16104350.

2. Brunings AM, Gabriel DW. Xanthomonas citri: breaking the surface. Mol Plant Pathol. 2003;4(3):141–57. doi: 10.1046/j.1364-3703.2003.00163.x 20569374.

3. Gottwald TR, Sun X, Riley T, Graham JH, Ferrandino F, Taylor EL. Geo-referenced spatiotemporal analysis of the urban citrus canker epidemic in Florida. Phytopathology. 2002;92(4):361–77. doi: 10.1094/PHYTO.2002.92.4.361 18942949.

4. Singh S, Rajam MV. Citrus biotechnology: Achievements, limitations and future directions. Physiol Mol Biol Plants. 2009;15(1):3–22. Epub 2009/05/14. doi: 10.1007/s12298-009-0001-2 23572908; PubMed Central PMCID: PMC3550383.

5. Donmez D, Simsek O, Izgu T, Kacar YA, Mendi YY. Genetic transformation in citrus. ScientificWorldJournal. 2013;2013:491207. Epub 2013/07/25. doi: 10.1155/2013/491207 23983635; PubMed Central PMCID: PMC3745968.

6. Liu Y, Zheng W, Zhang W, Chen N, Chen L, Zhou X, et al. Photoaffinity labeling of transcription factors by DNA-templated crosslinking. Chem Sci. 2015;6(1):745–51. Epub 2014/10/01. doi: 10.1039/c4sc01953a 28706637; PubMed Central PMCID: PMC5494549.

7. Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, et al. Genome-wide analysis of bZIP-encoding genes in maize. DNA Res. 2012;19(6):463–76. Epub 2012/10/26. doi: 10.1093/dnares/dss026 23103471; PubMed Central PMCID: PMC3514857.

8. Gamboa-Meléndez H, Huerta AI, Judelson HS. bZIP transcription factors in the oomycete phytophthora infestans with novel DNA-binding domains are involved in defense against oxidative stress. Eukaryot Cell. 2013;12(10):1403–12. Epub 2013/08/23. doi: 10.1128/EC.00141-13 23975888; PubMed Central PMCID: PMC3811335.

9. Jin Z, Xu W, Liu A. Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.). Planta. 2014;239(2):299–312. Epub 2013/10/29. doi: 10.1007/s00425-013-1979-9 24165825.

10. Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, et al. The draft genome of sweet orange (Citrus sinensis). Nat Genet. 2013;45(1):59–66. Epub 2012/11/25. doi: 10.1038/ng.2472 23179022.

11. Nijhawan A, Jain M, Tyagi AK, Khurana JP. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 2008;146(2):333–50. Epub 2007/12/07. doi: 10.1104/pp.107.112821 PubMed Central PMCID: PMC2245831. 18065552

12. Barah P, Jayavelu ND, Mundy J, Bones AM. Genome scale transcriptional response diversity among ten ecotypes of Arabidopsis thaliana during heat stress. Front Plant Sci. 2013;4:532. Epub 2013/12/26. doi: 10.3389/fpls.2013.00532 24409190; PubMed Central PMCID: PMC3872818.

13. Liu J, Chen N, Chen F, Cai B, Dal Santo S, Tornielli GB, et al. Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics. 2014;15:281. Epub 2014/04/13. doi: 10.1186/1471-2164-15-281 24725365; PubMed Central PMCID: PMC4023599.

14. Pourabed E, Ghane Golmohamadi F, Soleymani Monfared P, Razavi SM, Shobbar ZS. Basic leucine zipper family in barley: genome-wide characterization of members and expression analysis. Mol Biotechnol. 2015;57(1):12–26. doi: 10.1007/s12033-014-9797-2 25173685.

15. Bai Y, Zhu W, Hu X, Sun C, Li Y, Wang D, et al. Genome-Wide Analysis of the bZIP Gene Family Identifies Two ABI5-Like bZIP Transcription Factors, BrABI5a and BrABI5b, as Positive Modulators of ABA Signalling in Chinese Cabbage. PLoS One. 2016;11(7):e0158966. Epub 2016/07/14. doi: 10.1371/journal.pone.0158966 27414644; PubMed Central PMCID: PMC4944949.

16. Baloglu MC, Eldem V, Hajyzadeh M, Unver T. Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS One. 2014;9(4):e96014. Epub 2014/04/23. doi: 10.1371/journal.pone.0096014 24760072; PubMed Central PMCID: PMC3997510.

17. Li Q, Yu H, Cao PB, Fawal N, Mathé C, Azar S, et al. Explosive tandem and segmental duplications of multigenic families in Eucalyptus grandis. Genome Biol Evol. 2015;7(4):1068–81. Epub 2015/03/13. doi: 10.1093/gbe/evv048 25769696; PubMed Central PMCID: PMC4419795.

18. Alves MS, Dadalto SP, Gonçalves AB, De Souza GB, Barros VA, Fietto LG. Plant bZIP transcription factors responsive to pathogens: a review. Int J Mol Sci. 2013;14(4):7815–28. Epub 2013/04/10. doi: 10.3390/ijms14047815 23574941; PubMed Central PMCID: PMC3645718.

19. Amorim LLB, da Fonseca Dos Santos R, Neto JPB, Guida-Santos M, Crovella S, Benko-Iseppon AM. Transcription Factors Involved in Plant Resistance to Pathogens. Curr Protein Pept Sci. 2017;18(4):335–51. doi: 10.2174/1389203717666160619185308 27323805.

20. Sato F, Kitajima S, Koyama T, Yamada Y. Ethylene-induced gene expression of osmotin-like protein, a neutral isoform of tobacco PR-5, is mediated by the AGCCGCC cis-sequence. Plant Cell Physiol. 1996;37(3):249–55. doi: 10.1093/oxfordjournals.pcp.a028939 8673338.

21. Mateo A, Mühlenbock P, Rustérucci C, Chang CC, Miszalski Z, Karpinska B, et al. LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol. 2004;136(1):2818–30. Epub 2004/09/03. doi: 10.1104/pp.104.043646 15347794; PubMed Central PMCID: PMC523344.

22. Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, et al. Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol. 2014;32(7):656–62. Epub 2014/06/08. doi: 10.1038/nbt.2906 24908277; PubMed Central PMCID: PMC4113729.

23. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(Database issue):D1178–86. Epub 2011/11/22. doi: 10.1093/nar/gkr944 22110026; PubMed Central PMCID: PMC3245001.

24. Wang J, Chen D, Lei Y, Chang JW, Hao BH, Xing F, et al. Citrus sinensis annotation project (CAP): a comprehensive database for sweet orange genome. PLoS One. 2014;9(1):e87723. Epub 2014/01/28. doi: 10.1371/journal.pone.0087723 24489955; PubMed Central PMCID: PMC3905029.

25. Xu ZY, Kim SY, Hyeon dY, Kim DH, Dong T, Park Y, et al. The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell. 2013;25(11):4708–24. Epub 2013/11/27. doi: 10.1105/tpc.113.119099 24285786; PubMed Central PMCID: PMC3875745.

26. Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, et al. The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res. 2008;36(Database issue):D1009–14. Epub 2007/11/05. doi: 10.1093/nar/gkm965 17986450; PubMed Central PMCID: PMC2238962.

27. Fawal N, Li Q, Mathé C, Dunand C. Automatic multigenic family annotation: risks and solutions. Trends Genet. 2014;30(8):323–5. Epub 2014/07/10. doi: 10.1016/j.tig.2014.06.004 25017189.

28. Voorrips RE. MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002;93(1):77–8. doi: 10.1093/jhered/93.1.77 12011185.

29. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, et al. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003;31(13):3497–500. doi: 10.1093/nar/gkg500 12824352; PubMed Central PMCID: PMC168907.

30. Silva AE, Villanueva WJ, Knidel H, Bonato VC, Reis SF, Von Zuben FJ. A multi-neighbor-joining approach for phylogenetic tree reconstruction and visualization. Genet Mol Res. 2005;4(3):525–34. Epub 2005/09/30. 16342037.

31. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33(7):1870–4. Epub 2016/03/22. doi: 10.1093/molbev/msw054 27004904.

32. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004;14(6):1188–90. doi: 10.1101/gr.849004 15173120; PubMed Central PMCID: PMC419797.

33. Yu CS, Chen YC, Lu CH, Hwang JK. Prediction of protein subcellular localization. Proteins. 2006;64(3):643–51. doi: 10.1002/prot.21018 16752418.

34. Kosugi S, Hasebe M, Tomita M, Yanagawa H. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci U S A. 2009;106(25):10171–6. Epub 2009/06/11. doi: 10.1073/pnas.0900604106 19520826; PubMed Central PMCID: PMC2695404.

35. Peng A, Chen S, Lei T, Xu L, He Y, Wu L, et al. Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J. 2017;15(12):1509–19. Epub 2017/05/03. doi: 10.1111/pbi.12733 28371200; PubMed Central PMCID: PMC5698050.

36. Sendín LN, Orce IG, Gómez RL, Enrique R, Grellet Bournonville CF, Noguera AS, et al. Inducible expression of Bs2 R gene from Capsicum chacoense in sweet orange (Citrus sinensis L. Osbeck) confers enhanced resistance to citrus canker disease. Plant Mol Biol. 2017;93(6):607–21. Epub 2017/02/02. doi: 10.1007/s11103-017-0586-8 28155188.

37. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8. doi: 10.1006/meth.2001.1262 11846609.

38. Ng DW, Abeysinghe JK, Kamali M. Regulating the Regulators: The Control of Transcription Factors in Plant Defense Signaling. Int J Mol Sci. 2018;19(12). Epub 2018/11/24. doi: 10.3390/ijms19123737 30477211.

39. Pieterse CM, Van Loon LC. NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol. 2004;7(4):456–64. doi: 10.1016/j.pbi.2004.05.006 15231270.

40. Zuo W, Chao Q, Zhang N, Ye J, Tan G, Li B, et al. A maize wall-associated kinase confers quantitative resistance to head smut. Nat Genet. 2015;47(2):151–7. Epub 2014/12/22. doi: 10.1038/ng.3170 25531751.

41. Dong X. NPR1, all things considered. Curr Opin Plant Biol. 2004;7(5):547–52. doi: 10.1016/j.pbi.2004.07.005 15337097.

42. Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, et al. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002;7(3):106–11. 11906833.

43. Schütze K, Harter K, Chaban C. Post-translational regulation of plant bZIP factors. Trends Plant Sci. 2008;13(5):247–55. Epub 2008/04/16. doi: 10.1016/j.tplants.2008.03.002 18424222.

44. Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, et al. Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta. 2008;228(2):225–40. Epub 2008/03/26. doi: 10.1007/s00425-008-0731-3 18365246.

45. Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012;28:489–521. Epub 2012/05/03. doi: 10.1146/annurev-cellbio-092910-154055 22559264.

46. Kesarwani M, Yoo J, Dong X. Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol. 2007;144(1):336–46. Epub 2007/03/16. doi: 10.1104/pp.106.095299 17369431; PubMed Central PMCID: PMC1913812.

47. Lee SC, Choi HW, Hwang IS, Choi DS, Hwang BK. Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses. Planta. 2006;224(5):1209–25. Epub 2006/05/23. doi: 10.1007/s00425-006-0302-4 16718483.

48. Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C. Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J. 2005;44(1):100–13. doi: 10.1111/j.1365-313X.2005.02513.x 16167899.

49. Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol. 2004;42:185–209. doi: 10.1146/annurev.phyto.42.040803.140421 15283665.

50. Fobert PR, Després C. Redox control of systemic acquired resistance. Curr Opin Plant Biol. 2005;8(4):378–82. doi: 10.1016/j.pbi.2005.05.003 15922650.

51. Beckers GJ, Spoel SH. Fine-Tuning Plant Defence Signalling: Salicylate versus Jasmonate. Plant Biol (Stuttg). 2006;8(1):1–10. doi: 10.1055/s-2005-872705 16435264.

52. Rochon A, Boyle P, Wignes T, Fobert PR, Després C. The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell. 2006;18(12):3670–85. Epub 2006/12/15. doi: 10.1105/tpc.106.046953 17172357; PubMed Central PMCID: PMC1785396.

CsBZIP40, a BZIP transcription factor in sweet orange, plays a positive regulatory role in citrus bacterial canker response and tolerance

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