Transcriptome analysis of Actinidia chinensis in response to Botryosphaeria dothidea infection


Autoři: Yuanxiu Wang aff001;  Guihong Xiong aff001;  Zhe He aff001;  Mingfeng Yan aff001;  Manfei Zou aff001;  Junxi Jiang aff001
Působiště autorů: College of Agronomy, Jiangxi Agricultural University, Nanchang, China aff001;  College of Bioscience and Bioengineering, Jiangxi Agricultural University, Nanchang, China aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227303

Souhrn

Ripe rot caused by Botryosphaeria dothidea causes extensive production losses in kiwifruit (Actinidia chinensis Planch.). Our previous study showed that kiwifruit variety “Jinyan” is resistant to B. dothidea while “Hongyang” is susceptible. For a comparative analysis of the response of these varieties to B. dothidea infection, we performed a transcriptome analysis by RNA sequencing. A total of 305.24 Gb of clean bases were generated from 36 libraries of which 175.76 Gb was from the resistant variety and 129.48 Gb from the susceptible variety. From the libraries generated, we identified 44,656 genes including 39,041 reference genes, 5,615 novel transcripts, and 13,898 differentially expressed genes (DEGs). Among these, 2,373 potentially defense-related genes linked to calcium signaling, mitogen-activated protein kinase (MAPK), cell wall modification, phytoalexin synthesis, transcription factors, pattern-recognition receptors, and pathogenesis-related proteins may regulate kiwifruit resistance to B. dothidea. DEGs involved in calcium signaling, MAPK, and cell wall modification in the resistant variety were induced at an earlier stage and at higher levels compared with the susceptible variety. Thirty DEGs involved in plant defense response were strongly induced in the resistant variety at all three time points. This study allowed the first comprehensive understanding of kiwifruit transcriptome in response to B. dothidea and may help identify key genes required for ripe rot resistance in kiwifruit.

Klíčová slova:

Arabidopsis thaliana – Calcium signaling – Fruits – Gene expression – MAPK signaling cascades – Plant cell walls – RNA sequencing – Kiwifruit


Zdroje

1. Everett KR, Taylor RK, Romberg MK, Rees-George J, Fullerton RA, Vanneste JL, et al. First report of Pseudomonas syringae pv. actinidiae causing kiwifruit bacterial canker in New Zealand. Australas. Plant Pathol. 2011; 6(1): 67–71. https://doi.org/10.1007/s13314-011-0023-9.

2. Li C, Jiang JX, Leng JH, Li BM, Yu Q, Tu GQ. Isolation and identification of pathogenic fungi causing fruit rot of kiwifruit in fengxin county. Jiangxi Nongye Daxue Xuebao. 2012; 34(2): 259–263.

3. Koh YJ, Hur JS, Jung JS. Postharvest fruit rots of kiwifruit (Actinidia deliciosa) in Korea. N. Z. J. Crop Hortic. Sci. 2005; 33(3): 303–310. https://doi.org/10.1080/01140671. 2005.9514363.

4. Pennycook SR, Samuels GJ. Botryosphaeria and Fusicoccum species associated with ripe fruit rot of Actinidia deliciosa (Kiwifruit) in New Zealand. Mycotaxon. 1985; 24: 445–458.

5. Li C, Wang L, Jiang JX, Wang YX, Zhao SG, Li BM,et al. Biological characteristics of the main pathogenic fungi causing fruit ripe rot of kiwifruit and disease resistance of kiwifruit cultivars. Jiangxi Nongye Daxue Xuebao. 2014; 36(5): 1061–1065. doi: 10.1093/nar/19.2.303.2014169

6. Jurick WM, Ii, Vico I, Gaskins VL, Janisiewicz WJ, Peter KA. First report of Botryosphaeria dothidea causing white rot on apple fruit in Maryland. Plant Dis. 2013; 97(7): 999. https://doi.org/10.1094/PDIS-01-13-0053-PDN 30722551

7. Garibaldi A, Bertetti D, Poli A, Gullino ML. First report of fruit rot in pear caused by Botryosphaeria dothidea in Italy. Plant Dis. 2012; 96(6): 910. doi: 10.1094/PDIS-02-12-0130-PDN 30727390

8. Wunderlich N, Costa SS, Tpoi RP, Ash GJ. First report of Botryosphaeria dothidea causing shoot blight and cankers of pistachio in Australia. Australas. Plant Dis. Notes. 2012; 7(1): 47–49. doi: 10.1007/s13314-012-0045-y

9. Choi IY. First report of bark dieback on blueberry caused by Botryosphaeria dothidea in Korea. Plant Dis. 2011; 95(2): 227. doi: 10.1094/PDIS-05-10-0371 30743439

10. Bai SH, Dong CH, Li BH, Dai HY. A PR-4 gene identified from Malus domestica is involved in the defense responses against Botryosphaeria dothidea. Plant Physiol Biochem. 2013; 62(1): 23–32. doi: 10.1016/j.plaphy.2012.10.016 23178481

11. Bai SH, Dong CH, Zhu J, Zhang YG, Dai HY. Identification of a xyloglucan-specific endo-(1–4)-beta- d-glucanase inhibitor protein from apple (Malus × domestica Borkh.) as a potential defense gene against Botryosphaeria dothidea. Plant Sci. 2015; 231: 11–9. doi: 10.1016/j.plantsci.2014.11.003 25575987

12. Zhang WW, Dong CH, Zhang YG, Zhu J, Dai HY, Bai SH. An apple cyclic nucleotide-gated ion channel gene highly responsive to Botryosphaeria dothidea infection enhances the susceptibility of Nicotiana benthamiana to bacterial and fungal pathogens. Plant Sci. 2018; 269: 94–105. doi: 10.1016/j.plantsci.2018.01.009 29606221

13. Li CY, Deng GM, Yang J, Viljoen A, Jin Y, Kuang RB, et al. Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculation with Fusarium oxysporum f. sp. cubense tropical race 4. BMC Genomics. 2012; 13(1): 374. doi: 10.1186/1471-2164-13-374 22863187

14. Zhang SP, Xiao YN, Zhao JR, Wang FG, Zheng YL. Digital gene expression analysis of early root infection resistance to Sporisorium reilianum f. sp. zeae in maize. Mol Genet Genomics. 2013; 288(1–2): 21–37. doi: 10.1007/s00438-012-0727-3 23196693

15. Hosseini S, Elfstrand M, Heyman F, Dan FJ, Karlsson M. Deciphering common and specific transcriptional immune responses in pea towards the oomycete pathogens Aphanomyces euteiches and Phytophthora pisi. BMC Genomics. 2015; 16(1): 1–18. doi: 10.1186/s12864-015-1829-1 26293353

16. Xu L, Zhu LF, Tu LL, Liu LL, Yuan DJ, Jin L, et al. 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. 2011; 62(15): 5607–5621. doi: 10.1093/jxb/err245 21862479

17. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25(9):1105–1111. doi: 10.1093/bioinformatics/btp120 19289445

18. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7(3): 562–578. doi: 10.1038/nprot.2012.016 22383036

19. Anders S, Pyl PT, Huber W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics. 2015; 31(2): 166–169. doi: 10.1093/bioinformatics/btu638 25260700

20. Anders S, and Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010; 11(10):R106. doi: 10.1186/gb-2010-11-10-r106 20979621

21. Benjamini Y, Hochberg Y. Controlling the false discovery rate—a practical and powerful approach to multiple testing. Appl Stat. 1995; 57(1): 289–300. https://doi.org/10.2307/2346101

22. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010, 11(2): R14. doi: 10.1186/gb-2010-11-2-r14 20132535

23. Mao X, Cai T, Olyarchuk JG, Wei L. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics. 2005; 21(19): 3787–93. doi: 10.1093/bioinformatics/bti430 15817693

24. Jain M, Nijhawan A, Tyagi AK, Khurana JP. Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun. 2006; 345(2): 646–651. doi: 10.1016/j.bbrc.2006.04.140 16690022

25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001; 25(4): 402–408. doi: 10.1006/meth.2001.1262 11846609

26. Kangasjarvi S, Neukermans J, Li SC, Aro EM, Noctor G. Photosynthesis, photorespiration, and light signalling in defence responses. J Exp Bot. 2012; 63(4): 1619–1636. doi: 10.1093/jxb/err402 22282535

27. Jones JD, Dangl JL. The plant immune system. Nature. 2006; 444(7117): 323–329. doi: 10.1038/nature05286 17108957

28. Kishimoto K, Kouzai Y, Kaku H, Shibuya N, Minami E, Nishizawa Y. Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. The Plant Journal. 2010; 64(2): 343–354. doi: 10.1111/j.1365-313X.2010.04328.x 21070413.

29. Pathak RK, Taj G, Pandey D, Kumar A, Arora S. Modeling of the MAPK machinery activation in response to various abiotic and biotic stresses in plants by a system biology approach. Bioinformation. 2013; 9(9): 443–449. doi: 10.6026/97320630009443 23847397

30. Meng XZ, Zhang SQ. MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol. 2013; 51(1): 245–266. doi: 10.1146/annurev-phyto-082712-102314 23663002

31. Ren DT, Liu YD, Yang Kwang-Y, Han L, Mao GH, Glazebrook J, et al. A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proceedings of the National Academy of Sciences. 2008; 105(14): 5638–5643. doi: 10.1073/pnas.0711301105 18378893

32. Dodd AN, Kudla J, Sanders D. The language of calcium signaling. Annu Rev Plant Biol. 2010; 61(1): 593–620. doi: 10.1146/annurev-arplant-070109-104628 20192754

33. Lecourieux D, Ranjeva R, Pugin A. Calcium in plant defence-signalling pathways. New Phytol. 2006; 171(2): 249–69. doi: 10.1111/j.1469-8137.2006.01777.x 16866934

34. Reddy VS, Ali GS, Reddy ASN. Characterization of a pathogen-induced calmodulin-binding protein: mapping of four Ca2+-dependent calmodulin-binding domains. Plant Mol Biol. 2003; 52(1): 143–159. doi: 10.1023/a:1023993713849 12825696

35. Allen GJ, Chu SP, Schumacher K, Shimazaki CT, Vafeados D, Kemper A, et al. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant. Science. 2000; 289(5488): 2338–2342. doi: 10.1126/science.289.5488.2338 11009417

36. Moscatiello R, Mariani PD, Sanders D, Maathuis FJM. Transcriptional analysis of calcium-dependent and calcium-independent signalling pathways induced by oligogalacturonides. J Exp Bot. 2006; 57(11): 2847–2865. doi: 10.1093/jxb/erl043 16868046

37. Eulgen T. Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 2005; 10(2): 71–78. doi: 10.1016/j.tplants.2004.12.006 15708344

38. Zheng ZY, Qamar SA, Chen ZX, Mengiste T. Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant Journal. 2010; 48(4): 592–605. doi: 10.1111/j.1365-313X.2006.02901.x 17059405

39. Nagano Y, Furuhashi H, Inaba T, Sasaki Y. A novel class of plant-specific zinc-dependent DNA-binding protein that binds to A/T-rich DNA sequences. Nucleic Acids Res. 2001; 29(20): 4097–4105. doi: 10.1093/nar/29.20.4097 11600698

40. Bonthala VS, Mayes K, Moreton J, Blythe M, Wright V, May ST, et al. Identification of gene modules associated with low temperatures response in bambara groundnut by network-based analysis. PLoS One. 2016; 11(2): e0148771. doi: 10.1371/journal.pone.0148771 26859686

41. Hudson D, Guevara D, Yaish MW, Hannam C, Long N, Clarke JD, et al. GNC and CGA1 modulate chlorophyll biosynthesis and glutamate synthase (GLU1/Fd-GOGAT) expression in Arabidopsis. PLoS One. 2011; 6(11): e26765. doi: 10.1371/journal.pone.0026765 22102866

42. So HA, Choi SJ, Chung E, Lee JH. Molecular characterization of stress-inducible PLATZ. Plant Omics Journal. 2015; 8(6): 479–484.

43. Bari R, Jones JDG. Role of plant hormones in plant defence responses. Plant Mol Biol. 2009; 69(4): 473–488. doi: 10.1007/s11103-008-9435-0 19083153

44. Mauch-Mani B, Mauch F. The role of abscisic acid in plant-pathogen interactions. Curr Opin Plant Biol. 2005; 8(4): 409–414. doi: 10.1016/j.pbi.2005.05.015 15939661

45. Wang WM, Ma XF, Zhang Y, Luo MC, Wang GL, Bellizzi M, et al. PAPP2C interacts with the atypical disease resistance protein RPW8.2 and negatively regulates salicylic acid-dependent defense responses in Arabidopsis. Mol Plant. 2012; 5(5): 1125–1137. doi: 10.1093/mp/sss008 22334594

46. Duarte KE, de Souza WR, Santiaqo TR, Sampaio BL, Ribeiro AP, Cotta MG, et al. Identification and characterization of core abscisic acid (ABA) signaling components and their gene expression profile in response to abiotic stresses in Setaria viridis. Sci Rep. 2019; 9:4028. doi: 10.1038/s41598-019-40623-5 30858491

47. Seo JK, Kwon SJ, Cho WK, Choi HS, Kim KH. Type 2C protein phosphatase is a key regulator of antiviral extreme resistance limiting virus spread. Sci Rep. 2014; 4:5905. doi: 10.1038/srep05905 25082428

48. Wang D, Pajerowska-Mukhtar K, Culler AH, Dong XN. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Current Biology. 2007; 17(20): 1784–1790. doi: 10.1016/j.cub.2007.09.025 17919906

49. Llorente F, Muskett P, Sanchez-Vallet A, Lopez G, Ramos B, Sanchez-Rodriguez C, et al. Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol Plant. 2008; 1(3): 496–509. doi: 10.1093/mp/ssn025 19825556

50. Eshraghi L, Anderson JP, Aryamanesh N, Mccomb JA, Shearer B, Hardy GS. Suppression of the auxin response pathway enhances susceptibility to Phytophthora cinnamomi while phosphite-mediated resistance stimulates the auxin signalling pathway. BMC Plant Biol. 2014; 14(1): 68. doi: 10.1186/1471-2229-14-68 24649892

51. Veylder LD, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, et al. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell. 2001; 13(7): 1653–1667. doi: 10.1105/TPC.010087 11449057

52. Hamdoun S, Zhang C, Gill M, Kumar N, Churchman M, Larkin JC, et al. Differential roles of two homologous cyclin-dependent kinase inhibitor genes in regulating cell cycle and innate immunity in Arabidopsis. Plant Physiol. 2016; 170(1): 515–527. doi: 10.1104/pp.15.01466 26561564

53. Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol. 2005; 6(11): 850–861. doi: 10.1038/nrm1746 16261190

54. Liu J, Sui Y, Chen H, Liu Y, Liu Y. Proteomic Analysis of Kiwifruit in Response to the Postharvest Pathogen, Botrytis cinerea. Front Plant Sci. 2018; 9: 158. doi: 10.3389/fpls.2018.00158 29497428

55. Eva M, Lorences EP. The implication of xyloglucan endotransglucosylase/hydrolase (XTHs) in tomato fruit infection by Penicillium expansum Link. A. J Agric Food Chem. 2007; 55(22): 9021–9026. doi: 10.1021/jf0718244 17960871

56. Todd J, Post-Beittenmiller D, Jaworski JG. KCS1 encodes a fatty acid elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana. Plant J. 2010; 17(2): 119–130. doi: 10.1046/j.1365-313x.1999.00352.x 10074711

57. Raffaele S, Leger A, Roby D. Very long chain fatty acid and lipid signaling in the response of plants to pathogens. Plant Signal Behav. 2009; 4(2): 94–99. doi: 10.4161/psb.4.2.7580 19649180

58. Wei G, Shirsat AH. Extensin over-expression in Arabidopsis limits pathogen invasiveness. Mol Plant Pathol. 2010; 7(6): 579–592. doi: 10.1111/j.1364-3703.2006.00363.x 20507471

59. Li YH, Qian Q, Z YH, Yan MX, Sun L, Zhang M, et al. BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell. 2003; 15(9): 2020–2031. doi: 10.1105/tpc.011775 12953108

60. Lü GY, Guo SG, Zhang HY, Geng LH, Song FM, Fei ZJ. Transcriptional profiling of watermelon during its incompatible interaction with Fusarium oxysporum f. sp. niveum. Eur J Plant Pathol. 2011; 131(4): 585–601. https://doi.org/10.1007/s10658-011-9833-z

61. Ramírez V, García-Andrade J, Vera P. Enhanced disease resistance to Botrytis cinerea in myb46 Arabidopsis plants is associated to an early downregulation of CesA genes. Plant Signal Behav. 2011; 6(6): 911–913. doi: 10.4161/psb.6.6.15354 21617373

62. Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J, et al. Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell. 2012; 24(7): 3106–3121. doi: 10.1105/tpc.112.099796 PMID: 22805434

63. Kwon SJ, Jin HC, Lee S, Nam MH, Chung JH, Kwon S, et al. GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant J. 2009; 58(2): 235–245. doi: 10.1111/j.1365-313X.2008.03772.x 19077166


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