Skip to main content

Advertisement

SpringerLink
Log in

Virus tolerance and recovery from viral induced-symptoms in plants are associated with transcriptome reprograming

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Plant recovery from viral infection is characterized by initial severe systemic symptoms which progressively decrease, leading to reduced symptoms or symptomless leaves at the apices. A key feature to plant recovery from invading nucleic acids such as viruses is the degree of the host’s initial basal immunity response. We review current links between RNA silencing, recovery and tolerance, and present a model in which, in addition to regulation of resistance (R) and other defence-related genes by RNA silencing, viral infections incite perturbations of the host physiological state that trigger reprogramming of host responses to by-pass severe symptom development, leading to partial or complete recovery. Recovery, in particular in perennial hosts, may trigger tolerance or virus accommodation. We discuss evidence suggesting that plant viruses can avoid total clearance but persistently replicate at low levels, thereby modulating the host transcriptome response which minimizes fitness cost and triggers recovery from viral-symptoms. In some cases a susceptible host may fail to recover from initial viral systemic symptoms, yet, accommodates the persistent virus throughout the life span, a phenomenon herein referred to as non-recovery accommodation, which differs from tolerance in that there is no distinct recovery phase, and differs from susceptibility in that the host is not killed. Recent advances in plant recovery from virus-induced symptoms involving host transcriptome reprogramming are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agudelo-Romero IP, Carbonell P, De la Iglesia F, Carrera J, Rodrigo G, Jaramillo A, Amador MAP, Elena SF (2008) Changes in the gene expression profile of Arabidopsis thaliana after infection with Tobacco etch virus. Virol J 5:92

    Article  PubMed Central  PubMed  Google Scholar 

  • Al-Kaff NS, Covey SN, Kreike MM, Page AM, Pinder R, Dale PJ (1998) Transcriptional and post-transcriptional plant gene silencing in response to a pathogen. Science 279:2113–2115

    Article  CAS  PubMed  Google Scholar 

  • Allie F, Pierce EJ, Okoniewski MJ, Rey MEC (2014) Transcriptional analysis of South African cassava mosaic virus-infected susceptible and tolerant landraces of cassava highlights differences in resistance, basal defense and cell wall associated genes during infection. BMC Genom 15:1006

    Article  Google Scholar 

  • Blevins T, Rajeswaran R, Aregger M, Borah BK, Schepetilnikov M, Baerlocher L, Farinelli L, Meins Jr-F, Hohn T, Pooggin MM (2011) Massive production of small RNAs from a non-coding region of Cauliflower mosaic virus in plant defense and viral counter-defense. Nucleic Acids Res 39:5003–5014

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Butterbach P, Verlaan MG, Dullemans A, Lohuis D, Visser RGF, Bai Y, Kormelink R (2014) Tomato yellow leaf curl virus resistance by Ty-1 involves increased cytosine methylation of viral genomes and is compromised by Cucumber mosaic virus infection. Proc Natl Acad Sci USA 111(35):12942–12947. doi:10.1073/pnas.1400894111

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Calo S, Nicolás FE, Vila A, Torres-Martínez S, Ruiz-Vázquez RM (2012) Two distinct RNA-dependent RNA polymerases are required for initiation and amplification of RNA silencing in the basal fungus Mucor circinelloides. Mol Microbiol 83(2):379–394

    Article  CAS  PubMed  Google Scholar 

  • Chellappan R, Vanitharani R, Fauquet CM (2004) Short interfering RNA accumulation correlates with host recovery in DNA virus-infected hosts, and gene silencing targets specific viral sequences. J Virol 78:7465–7477

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Covey SN, Al-Kaff NS, Langara A, Turner DS (1997) Plants combat infection by gene silencing. Nature 385:781–782

    Article  CAS  Google Scholar 

  • Dunoyer P, Schoot G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O (2014) Small duplexes function as mobile silencing signals between plant cells. Science 328:912

    Article  Google Scholar 

  • Fargette D, Colon LT, Bouveau D, Fauquet C (1996) Components of resistance of cassava to African cassava mosaic virus. Eur J Plant Pathol 102:645–654

    Article  Google Scholar 

  • Fondong VN, Thresh JM, Fauquet C (2000) Field experiments in Cameroon on cassava mosaic virus disease and the reversion phenomenon in susceptible and resistant cultivars. Int J Pest Manag 4:211–217

    Article  Google Scholar 

  • Fraile A, García-Arenal F (2010) The coevolution of plants and viruses: resistance and pathogenicity. Adv Virus Res 76:1–32

    Article  CAS  PubMed  Google Scholar 

  • Fukuzawa N, Itchoda N, Goto K, Masuta C, Matsumura T (2010) HC-pro, a potyvirus RNA silencing suppressor, cancels cycling of Cucumber mosaic virus in Nicotiana benthamiana plants. Virus Gene 40(3):440–2446

    Article  CAS  Google Scholar 

  • Gasura E (2008) Mechanisms associated with sweet potato virus disease resistance in Ugandan sweet potato genotypes. MSc. Thesis. Makerere University. Kampala, Uganda. P.58

  • Gasura E, Mukasa SB (2009) Prevalence and implications of sweet potato recovery from Sweet potato virus disease in Uganda. Afr Crop Sci J 18:195–205

    Google Scholar 

  • Gasura E, Mashingaidze AB, Mukasa SB (2010) Genetic variability for tuber yield, quality, and virus disease complex traits in Uganda sweet potato germplasm. Afr Crop Sci J 16(2):147–160

    Google Scholar 

  • Ghoshal B, Sanfaçon H (2014) Temperature-dependent symptom recovery in Nicotiana benthamiana plants infected with tomato ringspot virus is associated with reduced translation of viral RNA2 and requires ARGONAUTE 1. Virology 456–457:188–197

    Article  PubMed  Google Scholar 

  • Ghoshal B, Sanfaçon H (2015) Symptom recovery in virus-infected plants: revisiting the role of RNA silencing mechanisms. Virology 479–480:167–179

    Article  PubMed  Google Scholar 

  • Gibson RW, Otim-Nape GW (1997) Factors determining recovery and reversion in mosaic-affected affecting cassava mosaic virus resistant cassava. Ann Appl Biol 131:259–271

    Article  Google Scholar 

  • Goic B, Saleh M-C (2012) Living with the enemy: viral persistent infections from a friendly viewpoint. Curr Opin Microbiol 15:531–537

    Article  PubMed  Google Scholar 

  • Góngora-Castillo E, Ibarra-Laclette E, Trejo-Saavedra DL, Rivera-Bustamante RF (2012) Transcriptome analysis of symptomatic and recovered leaves of geminivirus-infected pepper (Capsicum annuum). Virol J 9:295

    Article  PubMed Central  PubMed  Google Scholar 

  • Hagen C, Rojas MR, Kon T, Gilbertson RL (2008) Recovery from Cucurbit leaf crumple virus (Family Geminiviridae, Genus Begomovirus) infection is an adaptive antiviral response associated with changes in viral small RNAs. Phytopathology 98:1029–1037

    Article  CAS  PubMed  Google Scholar 

  • Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor H (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nature Rev Microbiol 11:777–788

    Article  CAS  Google Scholar 

  • Hanssen IM, Peter van Esse H, Ballester AR, Hogewoning SW, Parra NO, Lievens A, Bovy AG, Thomma BP (2011) Differential tomato transcriptomics responses induced by pepino mosaic virus isolates with differential aggressiveness. Plant Physiol 156:301–318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hulo C, de Castro E, Masson P, Bougueleret L, Bairoch A, Xenarios I, Mercier LP (2011) ViralZone: acknowledge resource understand virus diversity. Nucleic Acids Res . doi:10.1093/nar/gkq901 (Database issue)

    Google Scholar 

  • Jovel J, Walker M, Sanfaçon H (2007) Recovery of Nicotiana bethamiana plants from a necrotic response induced by a nepovirus is associated with RNA silencing but not with reduced virus titer. J Virol 81:12285

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karran RA, Sanfacon H (2014) Tomato ringspot virus coat protein binds to ARGONAUTE 1 and suppresses the translation repression of a reporter gene. Mol Plant Microbe Interact 27:933–943

    Article  CAS  PubMed  Google Scholar 

  • Lecoq H, Moury B, Desbiez C, Palloix A, Pitrat M (2004) Durable virus resistance in plants through conventional approaches: a challenge. Virus Res 100:31–39

    Article  CAS  PubMed  Google Scholar 

  • Little TJ, Shuker DM, Colegrave N, Day N, Graham AL (2010) The coevolution of virulence: tolerance in perspective. PLoS Pathog 6:e1001006

    Article  PubMed Central  PubMed  Google Scholar 

  • Liu J, Yang J, Bi H, Zhang P (2014) Why mosaic? Gene expression profiling of African cassava mosaic virus-infected cassava reveals the effect of chlorophyll degradation on symptom development. JIPB 56(2):122–132

    CAS  PubMed  Google Scholar 

  • Loebenstein G, Cohen J, Shabtai S, Coutts RHA, Wood KR (1977) Distribution of Cucumber mosaic virus in systemically infected tobacco leaves. Virology 81:117–125

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Du Z-X, Kong J, Chen L-N, Qiu Y-H, Li G-F, Meng X-H, Zhu S-F (2012) Transcriptome analysis of Nicotiana tabacum infected by Cucumber mosaic virus during systemic symptom development. PLoS ONE 7:e43447

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ma X, Nicole M-C, Meteignier L-V, Hong N, Wang G, Moffett P (2014) Different roles for RNA silencing and RNA processing components in of virus recovery and virus-induced gene silencing in plants. J Exp Bot 65(1):311–322. doi:10.1093/jxb/eru447

    Article  PubMed Central  PubMed  Google Scholar 

  • Mahajan VS, Drake A, Chen J (2009) Virus-specific host miRNAs: antiviral defenses or promoters of persistent infection? Trends Immunol 30:1–7

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nature Genet 26:403–410

    Article  CAS  PubMed  Google Scholar 

  • Matthews REF (1991) Plant Virology, 3rd edn. Academic Press Inc., Harcourt Brace Jovanovich Publishers, San Diego

    Google Scholar 

  • Mette MF, Aufsatz W, Van der Winden J, Matzke MA, Matzke AJM (2000) Transcriptional silencing and promoter methylation triggered by double stranded RNA. EMBO J 19:5194–5201

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mourrain P, Beclin C, Elmayan T, Feuerbach F, Godon C, Morel J, Jouette D, Lacombe A, Nikic S, Picault N, Remoue K, Sanial M, Vo T, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for post-transcriptional gene silencing and natural virus resistance. Cell 101:533–542

    Article  CAS  PubMed  Google Scholar 

  • Nie X, Molen TA (2015) Host recovery and reduced virus level in the upper leaves after Potato virus y infection occur in tobacco and tomato but not in potato plants. Viruses 7:680–698

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pagán I, Alonso-Blanco C, García-Arenal F (2008) Host responses in life-history traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathog 4:e1000124

    Article  PubMed Central  PubMed  Google Scholar 

  • Pagán I, Montes N, Milgroom MG, García-Arenal F (2014) Vertical transmission selects for reduced virulence in a plant virus and increased resistance in the host. PloS Pathog 10:e1004293

    Article  PubMed Central  PubMed  Google Scholar 

  • Palukaitis P (2011) The road to RNA silencing is paved with plant-virus interactions. Plant Pathol J 27(3):197–206

    Article  CAS  Google Scholar 

  • Patil BL, Fauquet CM (2015) Light intensity and temperature affect systemic spread of silencing signal in transient agroinfiltration studies. Mol Plant Pathol 16(5):48–494. doi:10.1111/mpp.12205

    Article  Google Scholar 

  • Pooggin MM (2013) How can plant DNA viruses evade siRNA-directed DNA methylation and silencing? Int J Mol Sci 14:15233–15259

    Article  PubMed Central  PubMed  Google Scholar 

  • Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nature Rev Microbiol 11:745–760

    Article  CAS  Google Scholar 

  • Quintero A, Perez-Quintero AL, Lopez C (2013) Identification of ta-siRNAs and cis-nat-siRNAs in cassava and their roles in response to cassava bacterial blight. GPB 11(3):172–181. doi:10.1016/j.gpb.2013.03.001

    PubMed Central  CAS  PubMed  Google Scholar 

  • Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812–814

    Article  PubMed  Google Scholar 

  • Raja P, Sanville BC, Buchmann Bisaro DM (2008) Viral genome methylation as an epigenetic defense against geminiviruses. J Virol 82:8997–9007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ramesh SV, Ratnaparkhe MB, Gupta GK, Husain SM (2014) Plant miRNAome and antiviral resistance: a retrospective view and prospective challenges. Virus Genes 48:1–14

    Article  CAS  PubMed  Google Scholar 

  • Ratcliff FG, MacFarlane SG, Baulcombe DC (1999) Gene silencing without DNA: RNA mediated cross-protection between viruses. Plant Cell 11:1207–1215

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodrigo G, Carrera J, Ruiz-Ferrer V, del Toro FJ, Llave C, Voinnet O, Elena SF (2012) A meta-analysis reveals the commonalities and differences in Arabidopsis thaliana response to different viral pathogens. PLoS ONE 7(7):e40526

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rodriquez-Negrete E, Lozano-Duran R, Piedra-Aguilera A, Cruzado L, Bejarano ER, Castillo AG (2013) Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol 199:464–475

    Article  Google Scholar 

  • Rodríquez-Negrete EA, Carrillo-Tripp J, Rivera-Bustamante RF (2009) RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J Virol 83:1332–1340

    Article  Google Scholar 

  • Sahu PP, Rai NK, Chakraborty S, Singh M, Chandrappa PH, Ramesh B, Chattopadhyay D, Prasad M (2010) Tomato cultivar tolerant to Tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defense-associated host gene expression. Mol Plant Pathol 11:531–544

    Article  CAS  PubMed  Google Scholar 

  • Salomon R (1999) The evolutionary advantage of breeding for tolerance over resistance against viral plant disease. Isr J Plant Sci 47:I35–I39

    Article  Google Scholar 

  • Shaw J, Love AJ, Makarova SS, Kalinima NO, Harrison BD, Taliansky ME (2014) Coilin, the signature protein of cajal bodies, differentially modulates the interactions of plants with viruses in widely different taxa. Nucleus 5(1):85–94

    Article  PubMed Central  PubMed  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos ACM, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine rich repeats and other mRNAs. Plant Cell 24:859–874

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Swevers L, Broeck JV, Smagghe G (2013) The possibible impact of persistent virus infection on the function of the RNAi machinery in insects: hypothesis. Front Physiol 4 319:1–15

    Google Scholar 

  • Szittya G, Silhavy D, Molnár A, Havelda Z, Lovas A, Lakatos L, Bánfalvi Z, Burgyán J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22(3):633–640

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thresh JM, Otim-Nape GW, Jennings DL (1994) Exploiting resistance to African cassava mosaic virus. Asp Appl Biol 39:51–60

    Google Scholar 

  • Tiwari M, Sharma D, Trivedi PK (2014) Artificial microRNA mediated gene silencing in plants: progress and perspectives. Plant Mol Biol 86:1–18

    Article  CAS  PubMed  Google Scholar 

  • Wang XB, Wu Q, Ito T, Cillo F, Li WX, Chen X, Yu JL, Ding SW (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proc Natl Acad Sci USA 107(1):484–489

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhai J, Jeong D-H, De Paoli E, Park S, Rosen BD, Li Y, González JA, Yan Z, Kitto LS, Grusak AM, Jackson SA, Stacey G, Cook DR, Green JP, Sherrier JD, Meyers CB (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased trans-acting siRNAs. Genes Dev 25(23):2540–2553

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to apologize to all authors whose valuable work was not mentioned within this review article due to space constraint. We thank the peer-reviewers for all the comments they made leading to the final version of the article. L. Bengyella was supported by URC post-doctoral funding from the School of Molecular and Cell Biology (CSM: 13203), University of the Witwatersrand, Johannesburg, South Africa.

Author information

Authors and Affiliations

  1. School of Molecular and Cell Biology, University of the Witwatersrand, 1, Jan Smuts 6, Ave, Johannesburg, Braamfontein, 2000, South Africa

    Louis Bengyella, Farhahna Allie & Chrissie Rey

  2. Centre of Advanced Study in Life Sciences, Manipur University, Imphal, Manipur, 795003, India

    Sayanika D. Waikhom

  3. School of Basic and Biomedical Science, University of Health and Allied Sciences, PMB 31, Ho, Volta Region, Ghana

    Sayanika D. Waikhom

Authors
  1. Louis Bengyella
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sayanika D. Waikhom
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Farhahna Allie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chrissie Rey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chrissie Rey.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bengyella, L., Waikhom, S.D., Allie, F. et al. Virus tolerance and recovery from viral induced-symptoms in plants are associated with transcriptome reprograming. Plant Mol Biol 89, 243–252 (2015). https://doi.org/10.1007/s11103-015-0362-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-015-0362-6

Keywords

Search

Navigation