1887

Abstract

Plants are simultaneously exposed to a variety of biotic and abiotic stresses, such as infections by viruses and bacteria, or drought. This study aimed to improve our understanding of interactions between viral and bacterial pathogens and the environment in the incompatible host and the susceptible host , and the contribution of viral virulence proteins to these responses. Infection by the (PVX)/ (PPV) pathosystem induced resistance to (Pst) and to drought in both compatible and incompatible bacteria–host interactions, once a threshold level of defence responses was triggered by the virulence proteins P25 of PVX and the helper component proteinase of PPV. Virus-induced resistance to Pst was compromised in salicylic acid and jasmonic acid signalling-deficient but not in lines. Elevated temperature and CO levels, parameters associated with climate change, negatively affected resistance to Pst and to drought induced by virus infection, and this correlated with diminished HO production, decreased expression of defence genes and a drop in virus titres. Thus, diminished virulence should be considered as a potential factor limiting the outcome of beneficial trade-offs in the response of virus-infected plants to drought or bacterial pathogens under a climate change scenario.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001353
2019-11-15
2019-12-09
Loading full text...

Full text loading...

References

  1. Ramegowda V, Senthil-Kumar M. The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J Plant Physiol 2015;176:47–54 [CrossRef]
    [Google Scholar]
  2. Prasch CM, Sonnewald U. Signaling events in plants: stress factors in combination change the picture. Environ Exp Bot 2015;114:4–14 [CrossRef]
    [Google Scholar]
  3. Aguilar E, Cutrona C, Del Toro FJ, Vallarino JG, Osorio S et al. Virulence determines beneficial trade-offs in the response of virus-infected plants to drought via induction of salicylic acid. Plant Cell Environ 2017;40:2909–2930 [CrossRef]
    [Google Scholar]
  4. Fernández-Calvino L, Osorio S, Hernández ML, Hamada IB, del Toro FJ et al. Virus-Induced alterations in primary metabolism modulate susceptibility to tobacco rattle virus in Arabidopsis. Plant Physiol 2014;166:1821–1838 [CrossRef]
    [Google Scholar]
  5. Westwood JH, Mccann L, Naish M, Dixon H, Murphy AM et al. A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana. Mol Plant Pathol 2013;14:158–170 [CrossRef]
    [Google Scholar]
  6. Xu P, Chen F, Mannas JP, Feldman T, Sumner LW et al. Virus infection improves drought tolerance. New Phytol 2008;180:911–921 [CrossRef]
    [Google Scholar]
  7. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ et al. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 2005;18:923–937 [CrossRef]
    [Google Scholar]
  8. Lewsey M, Palukaitis P, Carr JP. Plant-virus interactions: defence and counter-defence (Chapter 6). Annu Plant Rev Vol 34 Mol Asp Plant Dis Resist J Park (Ed) 2009;134–176
    [Google Scholar]
  9. Whitham SA, Yang C, Goodin MM. Global impact: elucidating plant responses to viral infection. Mol Plant Microbe Interact 2006;19:1207–1215 [CrossRef]
    [Google Scholar]
  10. Lamichhane JR, Venturi V. Synergisms between microbial pathogens in plant disease complexes: a growing trend. Front Plant Sci 2015;06:1–12 [CrossRef]
    [Google Scholar]
  11. Moore M, Jaykus L-A. Virus–bacteria interactions: implications and potential for the applied and agricultural sciences. Viruses 2018;10:61–15 [CrossRef]
    [Google Scholar]
  12. Ramamoorthy V, Viswanathan R, Raguchander T, Prakasam V, Samiyappan R. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot 2001;20:1–11 [CrossRef]
    [Google Scholar]
  13. Zvereva AS, Golyaev V, Turco S, Gubaeva EG, Rajeswaran R et al. Viral protein suppresses oxidative burst and salicylic acid-dependent autophagy and facilitates bacterial growth on virus-infected plants. New Phytol 2016;211:1020–1034 [CrossRef]
    [Google Scholar]
  14. Tollenaere C, Lacombe S, Wonni I, Barro M, Ndougonna C et al. Virus-bacteria rice co-infection in Africa: field estimation, reciprocal effects, molecular mechanisms, and evolutionary implications. Front Plant Sci 2017;8:1–13 [CrossRef]
    [Google Scholar]
  15. Sasu MA, Ferrari MJ, Du D, Winsor JA, Stephenson AG. Indirect costs of a nontarget pathogen mitigate the direct benefits of a virus-resistant transgene in wild Cucurbita. Proc Natl Acad Sci U S A 2009;106:19067–19071 [CrossRef]
    [Google Scholar]
  16. IPCC Summary for Policymakers Cambridge, United Kingdom and New York, NY, USA: Cambridge University Press,; 2013
    [Google Scholar]
  17. Eastburn DM, McElrone AJ, Bilgin DD. Influence of atmospheric and climatic change on plant-pathogen interactions. Plant Pathol 2011;60:54–69 [CrossRef]
    [Google Scholar]
  18. Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 2012;63:3523–3543 [CrossRef]
    [Google Scholar]
  19. Fu X, Ye L, Kang L, Ge F. Elevated CO2 shifts the focus of tobacco plant defences from cucumber mosaic virus to the green peach aphid. Plant Cell Environ 2010;33:2056–2064 [CrossRef]
    [Google Scholar]
  20. Jones R, Barbetti MJ. Influence of climate change on plant disease infections and epidemics caused by viruses and bacteria. CAB Rev Perspect Agric Vet Sci Nutr Nat Resour 2012;7:1–31 [CrossRef]
    [Google Scholar]
  21. Vance VB, Berger PH, Carrington JC, Hunt AG, Shi XM. 5' proximal potyviral sequences mediate potato virus X/potyviral synergistic disease in transgenic tobacco. Virology 1995;206:583–590 [CrossRef]
    [Google Scholar]
  22. García-Marcos A, Pacheco R, Martiáñez J, González-Jara P, Díaz-Ruíz JR et al. Transcriptional changes and oxidative stress associated with the synergistic interaction between Potato virus X and Potato virus Y and their relationship with symptom expression. Mol Plant-Microbe Interac 2009;22:1431–1444 [CrossRef]
    [Google Scholar]
  23. Aguilar E, Del Toro FJ, Brosseau C, Moffett P, Canto T et al. Cell death triggered by the p25 protein in potato virus X-associated synergisms results from endoplasmic reticulum stress in Nicotiana benthamiana. Mol Plant Pathol 2019;20:194–210 [CrossRef]
    [Google Scholar]
  24. Aguilar E, Almendral D, Allende L, Pacheco R, Chung BN et al. The p25 protein of potato virus X (PVX) is the main pathogenicity determinant responsible for systemic necrosis in PVX-associated synergisms. J Virol 2015;89:2090–2103 [CrossRef]
    [Google Scholar]
  25. González-Jara P, Atencio FA, Martínez-García B, Barajas D, Tenllado F et al. A single amino acid mutation in the Plum pox virus helper component-proteinase gene abolishes both synergistic and RNA silencing suppression activities. Phytopathology 2005;95:894–901 [CrossRef]
    [Google Scholar]
  26. Xin X-F, He SY. Pseudomonas syringae pv. tomato DC3000: a model pathogen for probing disease susceptibility and hormone signaling in plants. Annu Rev Phytopathol 2013;51:473–498 [CrossRef]
    [Google Scholar]
  27. Brooks DM, Bender CL, Kunkel BN. The Pseudomonas syringae phytotoxin coronatine promotes virulence by overcoming salicylic acid-dependent defences in Arabidopsis thaliana. Mol Plant Pathol 2005;6:629–639 [CrossRef]
    [Google Scholar]
  28. Cao B, Liu J, Qin G, Tian S. Oxidative stress acts on special membrane proteins to reduce the viability of Pseudomonas syringae pv tomato. J Proteome Res 2012;11:4927–4938 [CrossRef]
    [Google Scholar]
  29. Ying X-B, Dong L, Zhu H, Duan C-G, Du Q-S et al. Rna-Dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell 2010;22:1358–1372 [CrossRef]
    [Google Scholar]
  30. García-Marcos A, Pacheco R, Manzano A, Aguilar E, Tenllado F. Oxylipin biosynthesis genes positively regulate programmed cell death during compatible infections with the synergistic pair potato virus X-Potato virus Y and tomato spotted wilt virus. J Virol 2013;87:5769–5783 [CrossRef]
    [Google Scholar]
  31. Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S et al. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 1995;8:863–870 [CrossRef]
    [Google Scholar]
  32. Feys BJF, Benedetti CE, Penfold CN, Turner JG. Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 1994;6:751–759 [CrossRef]
    [Google Scholar]
  33. Aguilar E, Allende L, Del Toro FJ, Chung B-N, Canto T et al. Effects of elevated CO₂and temperature on pathogenicity determinants and virulence of potato virus X/Potyvirus-Associated synergism. Mol Plant Microbe Interact 2015;28:1364–1373 [CrossRef]
    [Google Scholar]
  34. Tenllado F, Díaz-Ruíz JR. Double-Stranded RNA-mediated interference with plant virus infection. J Virol 2001;75:12288–12297 [CrossRef]
    [Google Scholar]
  35. Pasin F, Simón-Mateo C, García JA. The hypervariable amino-terminus of P1 protease modulates potyviral replication and host defense responses. PLoS Pathog 2014;10:e1003985 [CrossRef]
    [Google Scholar]
  36. Del Toro F, Tenllado F, Chung B-N, Canto T. A procedure for the transient expression of genes by agroinfiltration above the permissive threshold to study temperature-sensitive processes in plant-pathogen interactions. Mol Plant Pathol 2014;15:848–857 [CrossRef]
    [Google Scholar]
  37. Pacheco R, García-Marcos A, Manzano A, de Lacoba MG, Camañes G et al. Comparative analysis of transcriptomic and hormonal responses to compatible and incompatible plant-virus interactions that lead to cell death. Mol Plant Microbe Interact 2012;25:709–723 [CrossRef]
    [Google Scholar]
  38. Li W, Xu Y-P, Zhang Z-X, Cao W-Y, Li F et al. Identification of genes required for nonhost resistance to Xanthomonas oryzae pv. oryzae reveals novel signaling components. PLoS One 2012;7:e42796 [CrossRef]
    [Google Scholar]
  39. Wang K, Uppalapati SR, Zhu X, Dinesh-Kumar SP, Mysore KS. Sgt1 positively regulates the process of plant cell death during both compatible and incompatible plant-pathogen interactions. Mol Plant Pathol 2010;11:597–611 [CrossRef]
    [Google Scholar]
  40. Ishiga Y, Ishiga T, Uppalapati SR, Mysore KS. Arabidopsis seedling flood-inoculation technique: a rapid and reliable assay for studying plant-bacterial interactions. Plant Methods 2011;7:32–11 [CrossRef]
    [Google Scholar]
  41. Miura K, Okamoto H, Okuma E, Shiba H, Kamada H et al. SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 2013;73:91–104 [CrossRef]
    [Google Scholar]
  42. Melotto M, Underwood W, He SY. Role of stomata in plant innate immunity and foliar bacterial diseases. Annu Rev Phytopathol 2008;46:101–122 [CrossRef]
    [Google Scholar]
  43. Rajput NA, Zhang M, Shen D, Liu T, Zhang Q et al. Overexpression of a Phytophthora cytoplasmic CRN Effector confers resistance to disease, salinity and drought in Nicotiana benthamiana. Plant Cell Physiol 2015;56:2423–2435 [CrossRef]
    [Google Scholar]
  44. van Molken T, de Caluwe H, Hordijk CA, Leon-Reyes A, Snoeren TAL et al. Virus infection decreases the attractiveness of white clover plants for a non-vectoring herbivore. Oecologia 2012;170:433–444 [CrossRef]
    [Google Scholar]
  45. Mascia T, Gallitelli D. Synergies and antagonisms in virus interactions. Plant Sci 2016;252:176–192 [CrossRef]
    [Google Scholar]
  46. Groen SC, Jiang S, Murphy AM, Cunniffe NJ, Westwood JH et al. Virus infection of plants alters pollinator preference: a payback for susceptible hosts?. PLoS Pathog 2016;12:e1005790 [CrossRef]
    [Google Scholar]
  47. Pruss GJ, Lawrence CB, Bass T, Li QQ, Bowman LH et al. The potyviral suppressor of RNA silencing confers enhanced resistance to multiple pathogens. Virology 2004;320:107–120 [CrossRef]
    [Google Scholar]
  48. Navarro L, Jay F, Nomura K, He SY, Voinnet O. Suppression of the microRNA pathway by bacterial effector proteins. Science 2008;321:964–967 [CrossRef]
    [Google Scholar]
  49. Murray RR, Emblow MSM, Hetherington AM, Foster GD. Plant virus infections control stomatal development. Sci Rep 2016;6:1–7 [CrossRef]
    [Google Scholar]
  50. Truman W, Bennett MH, Kubigsteltig I, Turnbull C, Grant M. Arabidopsis systemic immunity uses conserved defense signaling pathways and is mediated by jasmonates. Proc Natl Acad Sci U S A 2007;104:1075–1080 [CrossRef]
    [Google Scholar]
  51. Munemasa S, Oda K, Watanabe-Sugimoto M, Nakamura Y, Shimoishi Y et al. The coronatine-insensitive 1 mutation reveals the hormonal signaling interaction between abscisic acid and methyl jasmonate in Arabidopsis guard cells. specific impairment of ion channel activation and second messenger production. Plant Physiol 2007;143:1398–1407 [CrossRef]
    [Google Scholar]
  52. Fang Y, Xiong L. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 2015;72:673–689 [CrossRef]
    [Google Scholar]
  53. Del Toro FJ, Aguilar E, Hernández-Walias FJ, Tenllado F, Chung B-N et al. High temperature, high ambient CO2 affect the interactions between three Positive-Sense RNA viruses and a compatible host differentially, but not their silencing suppression efficiencies. PLoS One 2015;10:e0136062 [CrossRef]
    [Google Scholar]
  54. Szittya G et al. Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 2003;22:633–640 [CrossRef]
    [Google Scholar]
  55. Huang L, Ren Q, Sun Y, Ye L, Cao H et al. Lower incidence and severity of tomato virus in elevated CO(2) is accompanied by modulated plant induced defence in tomato. Plant Biol 2012;14:905–913 [CrossRef]
    [Google Scholar]
  56. Zhang S, Li X, Sun Z, Shao S, Hu L et al. Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. J Exp Bot 2015;66:1951–1963 [CrossRef]
    [Google Scholar]
  57. Roossinck MJ. The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 2011;9:99–108 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001353
Loading
/content/journal/jgv/10.1099/jgv.0.001353
Loading

Data & Media loading...

Supplements

Supplementary material 2

EXCEL

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error