Proteome of resistant and susceptible Passiflora species in the interaction with cowpea aphid-borne mosaic virus reveals distinct responses to pathogenesis

Abstract

To better understand plant–pathogen interactions and the activation of defense mechanisms, this study proposes to identify the differentially abundant proteins in an interspecific hybrid of passion fruit and its parents, Passiflora edulis and P. setacea, inoculated with CABMV compared to their non-inoculated counterparts. Leaves from the three populations were inoculated and collected 72 h after inoculation. The experiment was set up as a completely randomized design with three replicates. Data are available via ProteomeXchange with identifier PXD013123. Of the over 500 identified proteins, 100, 290, and 96 were differentially abundant for the hybrid, P. edulis, and P. setacea, respectively, in response to CABMV. In the interspecific hybrid, 41% of the proteins were down-regulated and 59% were up-regulated, compared to control. In the P. setacea, 39% of the protein being down-regulated. The P. edulis, in turn, showed a distinct profile, in which 82% of the protein were down-regulated and only 18% were up-regulated compared to control. It is suggested that CABMV suppresses accumulation of proteins in susceptible species that may have a key function in plant defense response, such as those linked to proteasome regulation and heat shock proteins. At the same time, it should regulate the accumulation of proteins that may impair viral signaling within the host such as glutathione peroxidase. Despite responding to the infection, P. edulis was not capable of stopping the disease establishment. Results suggest that the disease manifests due to a failure in the signaling system of susceptible species.

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References

  1. Abreu S de PM (2011) Cultivo de maracujá-azedo. Cent. Apoio ao Desenvolv. Tecnológico - CDT/UnB

  2. Alfenas-Zerbini P, Maia IG, Fávaro RD et al (2009) Genome-wide analysis of differentially expressed genes during the early stages of tomato infection by a potyvirus. Mol Plant Microbe Interact 22:352–361. https://doi.org/10.1094/MPMI-22-3-0352

    CAS  Article  PubMed  Google Scholar 

  3. Amata R, Otipa M, Waiganjo M et al (2013) Management of dieback disease of passion fruits. Acta Hortic. https://doi.org/10.17660/ActaHortic.2013.1007.40

    Article  Google Scholar 

  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701

    CAS  Article  PubMed  Google Scholar 

  5. Babu M, Gagarinova AG, Brandle JE, Wang A (2008) Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection. J Gen Virol 89:1069–1080. https://doi.org/10.1099/vir.0.83531-0

    CAS  Article  PubMed  Google Scholar 

  6. Boro MC, Beriam LOS, Guzzo SD (2011) Induced resistance against Xanthomonas axonopodis pv. passiflorae in passion fruit plants. Trop Plant Pathol 36:74–80. https://doi.org/10.1590/s1982-56762011000200002

    Article  Google Scholar 

  7. Cerqueira-Silva CB, Conceição LDHCS, Souza AP, Corrêa RX (2014) A history of passion fruit woodiness disease with enphasis on the current situation in Brazil and prospects for Brazilian passion fruit cultivation A history of passion fruit woodiness disease with emphasis on the current situation in Brazil and prospects. Eur J Plant Pathol 139:261–270. https://doi.org/10.1007/s10658-014-0391-z

    Article  Google Scholar 

  8. Chen H, Boutros PC (2011) VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinformatics. https://doi.org/10.1186/1471-2105-12-35

    Article  PubMed  PubMed Central  Google Scholar 

  9. Citovsky V, Zaltsman A, Kozlovsky SV et al (2009) Proteasomal degradation in plant–pathogen interactions. Semin Cell Dev Biol 20:1048–1054. https://doi.org/10.1016/j.semcdb.2009.05.012

    CAS  Article  PubMed  Google Scholar 

  10. Conesa A, Götz S, García-gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610

    CAS  Article  PubMed  Google Scholar 

  11. Cotter TG (2011) Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis 2:e213–e218. https://doi.org/10.1038/cddis.2011.96

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. Damerval C, Vienne D, Zivy M, Thiellemen H (1986) Technical improvements in two-dimensional electro-phoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7(1):52–54

    CAS  Article  Google Scholar 

  13. Di Carli M, Villani ME, Bianco L et al (2010) Proteomic analysis of the plant—virus interaction in cucumber mosaic virus (CMV) resistant transgenic tomato. J Proteome Res 9:5684–5697

    Article  Google Scholar 

  14. Distler U, Kuharev J, Navarro P et al (2014) Drift time-specific collision energies enable independent acquisition proteomics. Nat Methods 11:167–170. https://doi.org/10.1038/nmeth.2767

    CAS  Article  PubMed  Google Scholar 

  15. Dolja VV, Mcbride HJ, Carrington JC (1992) Tagging of plant potyvirus replication and movement by insertion of β-glucuronidase into the viral polyprotein. Proc Natl Acad Sci USA 89:10208–10212

    CAS  Article  Google Scholar 

  16. Eldakak M, Milad SIM, Nawar AI, Rohila JS (2013) Proteomics: a biotechnology tool for crop improvement. Front Plant Sci 4:1–21. https://doi.org/10.3389/fpls.2013.00035

    Article  Google Scholar 

  17. Gonçalves ZS, De Jesus ON, Cerqueira-Silva CB, Diniz RP, Soares TL, de Oliveira EJ (2017) Methodological approaches to assess passion fruit resistance (Passiflora spp.) to passionfruit woodiness disease. Biosci J 33:1441–1451. https://doi.org/10.14393/bj-v33n6a2017-36619

    Article  Google Scholar 

  18. Ha C, Coombs S, Revill PA et al (2008) Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Arch Virol 851495:25–36. https://doi.org/10.1007/s00705-007-1053-7

    CAS  Article  Google Scholar 

  19. Hanley-Bowdoin L, Settlage SB, Robertson D (2004) Reprogramming plant gene expression: a prerequisite to geminivirus DNA replication. Mol Plant Pathol 5:149–156. https://doi.org/10.1111/J.1364-3703.2004.00214.X

    CAS  Article  PubMed  Google Scholar 

  20. Huot B, Yao J, Montgomery BL, Yang S (2014) Growth—defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287. https://doi.org/10.1093/mp/ssu049

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Jockusch H, Wiegand C, Mersch B, Rajes D (2001) Mutants of Tobacco mosaic virus with temperature-sensitive coat proteins induce heat shock response in tobacco leaves. Mol Plant-Microbe Interact 14:914–917

    CAS  Article  Google Scholar 

  22. Jones JDG, Dangl JL (2006) The plant immune system. Nat Publishing Group 444:323–329. https://doi.org/10.1038/nature05286

    CAS  Article  Google Scholar 

  23. Junqueira NTV, Braga MF, Faleiro FG, Peixoto JR, Bernacci LC (2005) Potencial de espécies silvestres de maracujazeiro como fonte de resistência a doenças. In: Maracujá: germoplasma e melhoramento genético, pp 81–108

  24. Kawano Y, Kaneko-Kawano T, Shimamoto K (2014) Rho family GTPase-dependent immunity in plants and animals. Front Plant Sci 5:1–12. https://doi.org/10.3389/fpls.2014.00522

    Article  Google Scholar 

  25. Kuć J, Preisig C (1984) Fungal regulation of disease resistance mechanisms in plants. Mycol Soc Am 76:767–784

    Article  Google Scholar 

  26. Livneh I, Cohen-kaplan V, Cohen-rosenzweig C et al (2016) The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Nat Publishing Group 26:869–885. https://doi.org/10.1038/cr.2016.86

    CAS  Article  Google Scholar 

  27. Mcgregor CE, Miano DW, Labonte DR et al (2009) Differential gene expression of resistant and susceptible sweetpotato plants after infection with the causal agents of sweet potato virus disease. J Am Soc Hortic Sci 134:658–666

    Article  Google Scholar 

  28. Meletti LMM (2011) Avanços na cultura do maracujá no Brasil. Rev Bras Frutic 33:83–91. https://doi.org/10.1590/S0100-29452011000500012

    Article  Google Scholar 

  29. Monteiro ACB de A, Higashi EN, Gonçalvez AN, Rodriguez APM (2000) A novel approach for the definition of the inorganic medium components for micropropagation of yellow passionfruit (Passiflora edulis sims f. flavicarpa Deg.). Vitr Cell Dev Biol 36:527–531

    Article  Google Scholar 

  30. Moshe ADI, Gorovits R, Liu Y, Czosnek H (2016) Tomato plant cell death induced by inhibition of HSP90 is alleviated by tomato yellow leaf curl virus infection. Mol Plant Pathol 17(2):247–260. https://doi.org/10.1111/mpp.12275

    CAS  Article  PubMed  Google Scholar 

  31. Munhoz CF, Santos AA, Arenhart RA et al (2015) Analysis of plant gene expression during passion fruit—Xanthomonas axonopodis interaction implicates lipoxygenase 2 in host defence. Ann Appl Biol 167:135–155. https://doi.org/10.1111/aab.12215

    CAS  Article  Google Scholar 

  32. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:437–497

    Article  Google Scholar 

  33. Nagaraj S, Senthil-kumar M, Ramu VS, Wang K (2016) Plant ribosomal proteins, RPL12 and RPL19, play a role in nonhost disease resistance against bacterial pathogens. Front Plant Sci 6:1–10. https://doi.org/10.3389/fpls.2015.01192

    Article  Google Scholar 

  34. Nanjo Y, Skultety L, Hajduch M, Komatsu S (2012) Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. J Proteome Res 11:372–385

    CAS  Article  Google Scholar 

  35. Navrot N, Collin V, Gualberto J et al (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and and abiotic stresses. Plant Physiol 142:1364–1379. https://doi.org/10.1104/pp.106.089458

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Nicaise V (2017) Boosting innate immunity to sustainably control diseases in crops. Curr Opin Virol 26:112–119. https://doi.org/10.1016/j.coviro.2017.07.030

    CAS  Article  PubMed  Google Scholar 

  37. Paiva ALS, Oliveira JTA, De Souza GA, Vasconcelos IM (2016) Label-free proteomics reveals that cowpea severe mosaic virus transiently suppresses the host leaf protein accumulation during the compatible interaction with Cowpea (Vigna unguiculata [L.] Walp.). J Proteome Res. https://doi.org/10.1021/acs.jproteome.6b00211

    Article  PubMed  Google Scholar 

  38. Park C, Seo Y, Park C (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333

    CAS  Article  Google Scholar 

  39. Passaia G, Margis-Pinheiro M (2015) Glutathione peroxidases as redox sensor proteins in plant cells. Plant Sci 234:22–26. https://doi.org/10.1016/j.plantsci.2015.01.017

    CAS  Article  PubMed  Google Scholar 

  40. Perdizio VA (2016) Abordagem proteômica na investigação dos mecanismos de defesa em maracujá. Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes

    Google Scholar 

  41. Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648

    CAS  Article  Google Scholar 

  42. Pieterse MJ, Van Der Does D, Zamioudis C et al (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:16–45. https://doi.org/10.1146/annurev-cellbio-092910-154055

    CAS  Article  Google Scholar 

  43. Pineda M, Sajnani C, Baro M (2010) Changes induced by the pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana. Photosynth Res 103:31–45. https://doi.org/10.1007/s11120-009-9499-y

    CAS  Article  PubMed  Google Scholar 

  44. Preisigke S da C, Martini FV, Rossi AAB et al (2015) Genetic variability of Passiflora spp. against collar rot disease. Aust J Crop Sci 9:69–74

    CAS  Google Scholar 

  45. Quirino BF, Candido ES, Campos PF et al (2010) Proteomic approaches to study plant–pathogen interactions. Phytochemistry 71:351–362. https://doi.org/10.1016/j.phytochem.2009.11.005

    CAS  Article  PubMed  Google Scholar 

  46. Romeiro R (2008) Indução de resistência em plantas a patógenos. In: Pascholati SF, Leite B, Stangarlin JR, Cia P (eds) Interações planta-patógeno: fisiologia, bioquímica e biologia molecular. Fealq, Piracicaba, pp 411–431

    Google Scholar 

  47. Santos EA, Viana AP, de Oliveira Freitas JC et al (2015) Resistance to cowpea aphid-borne mosaic virus in species and hybrids of Passiflora: advances for the control of the passion fruit woodiness disease in Brazil. Eur J Plant Pathol 143:85–98. https://doi.org/10.1007/s10658-015-0667-y

    CAS  Article  Google Scholar 

  48. Serra-Soriano M, Navarro JA, Genoves A, Pallás V (2015) Comparative proteomic analysis of melon phloem exudates in response to viral infection. J Proteomics 124:11–24. https://doi.org/10.1016/j.jprot.2015.04.008

    CAS  Article  PubMed  Google Scholar 

  49. Shirsekar G, Dai L, Hu Y et al (2010) Role of ubiquitination in plant innate immunity and pathogen virulence. J Plant Biol 53:10–18. https://doi.org/10.1007/s12374-009-9087-x

    CAS  Article  Google Scholar 

  50. Silva JC, Gorenstein MV, Li G et al (2006) Absolute quantification of proteins by LCMS E. Mol Cell Proteomics 5:144–156. https://doi.org/10.1074/mcp.M500230-MCP200

    CAS  Article  PubMed  Google Scholar 

  51. Veal E, Day A (2011) Hydrogen peroxide as a signaling molecule. Antioxid Redox Signal. https://doi.org/10.1089/ars.2011.3968

    Article  PubMed  Google Scholar 

  52. Veal EA, Day AM, Morgan BA (2007) Hydrogen peroxide sensing and signaling. Mol Cell. https://doi.org/10.1016/j.molcel.2007.03.016

    Article  PubMed  Google Scholar 

  53. Viana AP, Higino F, Lima D et al (2016) UENF Rio Dourado: a new passion fruit cultivar with high yield potential. Crop Breed Appl Biotechnol 16:250–253

    Article  Google Scholar 

  54. Warner JR, Mcintosh KB (2009) How common are extraribosomal functions of ribosomal proteins? Mol Cell 34:3–11. https://doi.org/10.1016/j.molcel.2009.03.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:3–7. https://doi.org/10.1038/NMETH.1322

    Article  Google Scholar 

  56. Wu L, Han Z, Wang S et al (2013) Comparative proteomic analysis of the plant–virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. J Proteomics 89:124–140. https://doi.org/10.1016/j.jprot.2013.06.005

    CAS  Article  PubMed  Google Scholar 

  57. Xu Z, Li Z, Chen Y et al (2012) Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses. Int J Mol Sci 13:15706–15723. https://doi.org/10.3390/ijms131215706

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. Yaeno T, Iba K (2008) BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiol 148:1032–1041. https://doi.org/10.1104/pp.108.124529

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors are thankful to Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), to Conselho Nacional de Desenvolvimento Científico e Tecnológico (141066/2016-4 CNPq) and to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the granted scholarships and financial support. We also thank Professor Gustavo Antonio de Souza; from Universidade Federal do Rio Grande do Norte, for his support and contributions in the initial phase of data analysis.

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Carvalho, B.M., Viana, A.P., dos Santos, P.H.D. et al. Proteome of resistant and susceptible Passiflora species in the interaction with cowpea aphid-borne mosaic virus reveals distinct responses to pathogenesis. Euphytica 215, 167 (2019). https://doi.org/10.1007/s10681-019-2491-5

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Keywords

  • Fruit woodiness virus
  • Gel-free proteomics
  • Passiflora edulis
  • Passiflora setacea
  • Virus–plant interaction