Skip to main content

Advertisement

Log in

Gene silencing approaches through virus-based vectors: speeding up functional genomics in monocots

  • Review
  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

The design and use of existing VIGS vectors for revealing monocot gene functions are described and potential new vectors are discussed, which may expand their repertoire.

Abstract

Virus induced gene silencing (VIGS) is a method of transient gene silencing in plants, triggered by the use of modified viral vectors. VIGS has found widespread use in deciphering the functions of plant genes, mainly for dicots. In the last decade, however, its use in monocots has increased noticeably, involving not only previously described viruses for monocots, but also those described for dicots. Additional viruses have been modified for VIGS to bring a larger collection of monocots under the ambit of this method. For monocots, new methods of inoculation have been tried to obtain increased silencing efficiency. The issue of insert stability and duration of silencing have also been addressed by various research groups. VIGS has been used to unravel the functions of a fairly large collection of monocot genes. This review summarizes the above developments, bringing out some of the gaps in our understanding and identifies directions to develop this technology further in the coming years.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baulcombe DC (1999) Fast forward genetics based on virus-induced gene silencing. Curr Opin Plant Biol 2:109–113

    Article  CAS  Google Scholar 

  • Benavente LM, Ding XS, Redinbaugh MG, Nelson RS, Balint-Kurti PJ (2012) Virus-induced gene silencing in diverse maize lines using the Brome mosaic virus-based silencing vector. Maydica 57:205–213

    Google Scholar 

  • Bennypaul HS, Mutti JS, Rustgi S, Kumar N, Okubara PA, Gill KS (2012) Virus-induced gene silencing (VIGS) of genes expressed in root, leaf, and meiotic tissues of wheat. Funct Integr Genomics 12:143–156

    Article  CAS  Google Scholar 

  • Beyene G, Chauhan RD, Taylor NJ (2017) A rapid virus-induced gene silencing (VIGS) method for assessing resistance and susceptibility to cassava mosaic disease. Virol J 14:47

    Article  Google Scholar 

  • Bruun-Rasmussen M, Madsen CT, Jessing S, Albrechtsen M (2007) Stability of Barley stripe mosaic virus-induced gene silencing in barley. Mol Plant Microbe Interact 20:1323–1331

    Article  CAS  Google Scholar 

  • Buhrow LM, Clark SM, Loewen MC (2016) Identification of an attenuated Barley stripe mosaic virus for the virus-induced gene silencing of pathogenesis-related wheat genes. Plant Methods 12:12

    Article  Google Scholar 

  • Cakir C, Tor M (2010) Factors influencing Barley stripe mosaic virus-mediated gene silencing in wheat. Physiol Mol Plant Pathol 74:246–253

    Article  CAS  Google Scholar 

  • Cheuk A, Houde M (2017) A rapid and efficient method for uniform gene expression using the Barley stripe mosaic virus. Plant Methods 13:24

    Article  Google Scholar 

  • Ding XS, Schneider WL, Chaluvadi SR, Mian MaR, Nelson RS (2006) Characterization of a Brome mosaic virus strain and its use as a vector for gene silencing in monocotyledonous hosts. Mol Plant Microbe Interact 19:1229–1239

    Article  CAS  Google Scholar 

  • Ding XS, Mannas SW, Bishop BA et al (2017) An improved Brome mosaic virus silencing vector: Greater insert stability and more extensive VIGS. Plant Physiol 176:496–510

    Article  Google Scholar 

  • Duan CG, Wang CH, Guo H-S (2012) Application of RNA silencing to plant disease resistance. Silence 3:5

    Article  CAS  Google Scholar 

  • Eamens A, Wang M-BM-B, Smith NA, Waterhouse PM (2008) RNA silencing in plants: yesterday, today, and tomorrow. Plant Physiol 147:456–468

    Article  CAS  Google Scholar 

  • Edwards MC, Weiland JJ (2010) First infectious clone of the propagatively transmitted Oat blue dwarf virus. Arch Virol 155:463–470

    Article  CAS  Google Scholar 

  • Edwards MC, Weiland JJ, Todd J, Stewart LR (2015) Infectious Maize rayado fino virus from cloned cDNA. Phytopathology 105, 833–839

    Article  CAS  Google Scholar 

  • Eftekhariyan Ghamsari MR, Karimi F, Gargari M, Hosseini Tafreshi SL, Salami SA, S.A (2014) Assessing the Tobacco rattle virus-based vectors system as an efficient gene silencing technique in Datura stramonium (Solanaceae). Virus Genes 49:512–516

    Article  CAS  Google Scholar 

  • Groszyk J, Kowalczyk M, Yanushevska Y, Stochmal A, Rakoczy-Trojanowska M, Orczyk W (2017) Identification and VIGS-based characterization of Bx1 ortholog in rye (Secale cereale L.). PLoS ONE 12:1–21

    Article  Google Scholar 

  • Gunupuru LR, Perochon A, Ali SS, Scofield SR, Doohan FM (2019) Virus-induced gene silencing (VIGS) for functional characterization of disease resistance genes in barley seedlings. In: Harwood W (ed) Barley. Methods in molecular biology. Humana Press, New York, 1900, 95–114

    Google Scholar 

  • Holzberg S, Brosio P, Gross C, Pogue GP (2002) Barley stripe mosaic virus-induced gene silencing in a monocot plant. Plant J 30:315–327

    Article  CAS  Google Scholar 

  • Hsieh MH, Lu HC, Pan ZJ, Yeh HH, Wang SS, Chen WH, Chen HH (2013a) Optimizing virus-induced gene silencing efficiency with Cymbidium mosaic virus in Phalaenopsis flower. Plant Sci 201–202:25–41

    Article  Google Scholar 

  • Hsieh MH, Pan ZJ, Lai PH, Lu HC, Yeh HH, Hsu CC, Wu WL, Chung MC, Wang SS, Chen WH, Chen HH (2013b) Virus-induced gene silencing unravels multiple transcription factors involved in floral growth and development in Phalaenopsis orchids. J Exp Bot 64:3869–3884

    Article  CAS  Google Scholar 

  • Jarugula S, Charlesworth SR, Qu F, Stewart LR (2016) Soil-borne wheat mosaic virus infectious clone and manipulation for gene-carrying capacity. Arch Virol 161:2291–2297

    Article  CAS  Google Scholar 

  • Jarugula S, Willie K, Stewart LR (2018) Barley stripe mosaic virus (BSMV) as a virus-induced gene silencing vector in maize seedlings. Virus Genes 54:616–620

    Article  CAS  Google Scholar 

  • Kant R, Dasgupta I (2017) Phenotyping of VIGS-mediated gene silencing in rice using a vector derived from a DNA virus. Plant Cell Rep 36:1159–1170

    Article  CAS  Google Scholar 

  • Lacomme C, Hrubikova K, Hein I (2003) Enhancement of virus-induced gene silencing through viral-based production of inverted-repeats. Plant J 34:543–553

    Article  CAS  Google Scholar 

  • Lee WS, Hammond-Kosack KE, Kanyuka K (2012) Barley stripe mosaic virus-mediated tools for investigating gene function in cereal plants and their pathogens: virus-induced gene silencing, host-mediated gene silencing, and virus-mediated overexpression of heterologous protein. Plant Physiol 160:582–590

    Article  CAS  Google Scholar 

  • Lee W-S, Rudd JJ, Kanyuka K (2015a) Virus induced gene silencing (VIGS) for functional analysis of wheat genes involved in Zymoseptoria tritici susceptibility and resistance. Fungal Genet Biol 79:84–88

    Article  CAS  Google Scholar 

  • Lee WS, Hammond-Kosack KE, Kanyuka K (2015b) In planta transient expression systems for monocots. In: Azhakanandam K et al (eds), Recent advancements in gene expression and enabling technologies in crop plants pp. 391–422

  • Liou MR, Huang YW, Hu CC, Lin NS, Hsu YH (2014) A dual gene-silencing vector system for monocot and dicot plants. Plant Biotechnol J 12:330–343

    Article  CAS  Google Scholar 

  • Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  CAS  Google Scholar 

  • Liu N, Xie K, Jia Q, Zhao J, Chen T, Li H, Wei X, Diao X, Hong Y, Liu Y (2016a) Foxtail mosaic virus-induced gene silencing in monocot plants. Plant Physiol 171:1801–1807

    Article  CAS  Google Scholar 

  • Liu G, Wu Y, Xu M, Gao T, Wang P, Wang L, Guo T, Kang G (2016b) Virus-induced gene silencing identifies an important role of the TaRSR1 transcription factor in starch synthesis in bread wheat. Int J Mol Sci 17

  • Liu-ming G, Jing H, Jing L, Jian-ping C, Heng-mu Z (2018) Chinese wheat mosaic virus: a long-term threat to wheat in China. J Integr Agric 17:60345–60347

    Google Scholar 

  • Lu H, Chen H, Tsai W, Chen W, Su H, Chang DC, Yeh H (2007) Strategies for functional validation of genes involved in reproductive stages of orchids. Plant Physiol 143:558–569

    Article  CAS  Google Scholar 

  • Ma M, Yan Y, Huang L, Chen M, Zhao H (2012) Virus-induced gene-silencing in wheat spikes and grains and its application in functional analysis of HMW-GS-encoding genes. BMC Plant Biol 12:141

    Article  CAS  Google Scholar 

  • Ma M, Zhao H, Li Z, Hu S, Song W, Liu X (2016) TaCYP78A5 regulates seed size in wheat (Triticum aestivum). J Exp Bot 67:1397–1410

    Article  CAS  Google Scholar 

  • Mei Y, Zhang C, Kernodle BM, Hill JH, Whitham SA (2016) A Foxtail mosaic virus vector for virus-induced gene silencing in maize. Plant Physiol 171:760–772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pacak A, Geisler K, Jørgensen B, Barciszewska-Pacak M, Nilsson L, Nielsen TH, Johansen E, Grønlund M, Jakobsen I, Albrechtsen M (2010) Investigations of Barley stripe mosaic virus as a gene silencing vector in barley roots and in Brachypodium distachyon and oat. Plant Methods 6:26

    Article  CAS  Google Scholar 

  • Pan ZJ, Chen YY, Du JS, Chen YY, Chung MC, Tsai WC, Wang CN, Chen HH (2014) Flower development of Phalaenopsis orchid involves functionally divergent SEPALLATA-like genes. New Phytol 202:1024–1042

    Article  CAS  Google Scholar 

  • Purkayastha A, Dasgupta I (2009) Virus-induced gene silencing: a versatile tool for discovery of gene functions in plants. Plant Physiol Biochem 47:967–976

    Article  CAS  Google Scholar 

  • Purkayastha A, Mathur S, Verma V, Sharma S, Dasgupta I (2010) Virus-induced gene silencing in rice using a vector derived from a DNA virus. Planta 232:1531–1540

    Article  CAS  Google Scholar 

  • Ramanna H, Ding XS, Nelson RS (2013) Rationale for developing new virus vectors to analyze gene function in grasses through virus-induced gene silencing. Methods Mol Biol 975:15–32

    Article  CAS  Google Scholar 

  • Ramegowda V, Mysore KS, Senthil-Kumar M (2014) Virus-induced gene silencing is a versatile tool for unraveling the functional relevance of multiple abiotic-stress-responsive genes in crop plants. Front Plant Sci 5:323

    Article  Google Scholar 

  • Redinbaugh MG, Louie R, Ngwira P, Edema R, Gordon DT, Bisaro DM (2001) Transmission of viral RNA and DNA to maize kernels by vascular puncture inoculation. J Virol Methods 98:135–143

    Article  CAS  Google Scholar 

  • Robertson D (2004) VIGS vectors for gene silencing: Many targets, many tools. Annu Rev Plant Biol 55:495–519

    Article  CAS  Google Scholar 

  • Sasaki S, Yamagishi N, Yoshikawa N (2011) Efficient virus-induced gene silencing in apple, pear and Japanese pear using Apple latent spherical virus vectors. Plant Methods 7:15

    Article  CAS  Google Scholar 

  • Scofield SR, Nelson RS (2009) Resources for virus-induced gene silencing in the grasses. Plant Physiol 149:152–157

    Article  CAS  Google Scholar 

  • Scofield SR, Huang L, Brandt AS, Gill BS (2005) Development of a virus-induced gene-silencing system for hexaploid wheat and its use in functional analysis of the Lr21-mediated leaf rust resistance pathway. Plant Physiol 138:2165–2173

    Article  CAS  Google Scholar 

  • Senthil-Kumar M, Mysore KS (2011) New dimensions for VIGS in plant functional genomics. Trends Plant Sci 16:656–665

    Article  CAS  Google Scholar 

  • Stewart LR, Bouchard R, Redinbaugh MG, Meulia T (2012) Complete sequence and development of a full-length infectious clone of an Ohio isolate of Maize dwarf mosaic virus (MDMV). Virus Res 165:219–224

    Article  CAS  Google Scholar 

  • Van Der Linde K, Kastner C, Kumlehn J, Kahmann R, Doehlemann G (2011) Systemic virus-induced gene silencing allows functional characterization of maize genes during biotrophic interaction with Ustilago maydis. New Phytol 189:471–483

    Article  Google Scholar 

  • Vance V, Vaucheret H (2001) RNA silencing in plants—defense and counter-defense. Science 292:2277–2280

    Article  CAS  Google Scholar 

  • Walter S, Kahla A, Arunachalam C, Perochon A, Khan MR, Scofield SR, Doohan FM (2015) A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. J Exp Bot 66:2583–2593

    Article  CAS  Google Scholar 

  • Wang Y, Yu B, Zhao J, Guo J, Li Y, Han S, Huang L, Du Y, Hong Y, Tang D, Liu Y (2013) Autophagy contributes to leaf starch degradation. The Plant Cell 25:1383–1399

    Article  CAS  Google Scholar 

  • Wang R, Yang X, Wang N, Liu X, Nelson RS, Li W, Fan Z, Zhou T (2016) An efficient virus-induced gene silencing vector for maize functional genomics research. Plant J 86:102–115

    Article  CAS  Google Scholar 

  • Weiland JJ, Edwards MC (1996) A single nucleotide substitution in the alpha a gene confers oat pathogenicity to Barley stripe mosaic virus strain ND18. Mol Plant-Microbe Interact 9:62–67

    Article  CAS  Google Scholar 

  • Yang J, Zhang F, Xie L, Song XJ, Li J, Chen JP, Zhang HM (2016) Functional identification of two minor capsid proteins from Chinese wheat mosaic virus using its infectious full-length cDNA clones. J Gen Virol 97, 2441–2450

    Article  CAS  Google Scholar 

  • Yang J, Zhang TY, Liao QS et al (2018) Chinese wheat mosaic virus-induced gene silencing in monocots and dicots at low temperature. Front Plant Sci 9:1627

    Article  Google Scholar 

  • Yuan C, Li C, Yan L, Jackson AO, Liu Z, Han C, Yu J, Li D (2011) A high throughput Barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PloS ONE 6, e26468

  • Zhang C, Ghabrial SA (2006) Development of Bean pod mottle virus-based vectors for stable protein expression and sequence-specific virus-induced gene silencing in soybean. Virology 344:401–411

    Article  CAS  Google Scholar 

  • Zhang B, Shi JA, Chen JB et al (2016) Efficient virus-induced gene silencing in Cynodon dactylon and Zoysia japonica using Rice tungro bacilliform virus vectors. Sci Hortic. (Amsterdam) 207, 97–103

    Article  CAS  Google Scholar 

  • Zhang J, Yu D, Zhang Y, Liu K, Xu K, Zhang F, Wang J, Tan G, Nie X, Ji Q, Zhao L, Li C (2017) Vacuum and co-cultivation agroinfiltration of (germinated) seeds results in Tobacco rattle virus (TRV) mediated whole-plant virus-induced gene silencing (VIGS) in wheat and maize. Front Plant Sci 8:1–12

    Google Scholar 

  • Zhu M, Chen Y, Ding XS, Webb SL, Zhou T, Nelson RS, Fan Z (2014) Maize Elongin C interacts with the viral genome-linked protein, VPg, of Sugarcane mosaic virus and facilitates virus infection. New Phytol 203:1291–1304

    Article  CAS  Google Scholar 

  • Zhu X, Lu C, Du L, Ye X, Liu X, Coules A, Zhang Z (2017) The wheat NB-LRR gene TaRCR1 is required for host defence response to the necrotrophic fungal pathogen Rhizoctonia cerealis. Plant Biotechnol J 15:674–687

    Article  CAS  Google Scholar 

Download references

Acknowledgements

RK acknowledges the research fellowship from Indian Council of Medical Research, New Delhi. ID acknowledges the financial support from Department of Biotechnology, Government of India (Grant No. BT/AB/FG-1(PH-II)/2009), J. C. Bose Fellowship, University of Delhi R&D Grant, PURSE Grant and FIST infrastructure grant.

Author information

Authors and Affiliations

Authors

Contributions

RK and ID conceived the review, both RK and ID wrote the revised review. Both RK and ID approved the final version.

Corresponding author

Correspondence to Indranil Dasgupta.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest associated with this review.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kant, R., Dasgupta, I. Gene silencing approaches through virus-based vectors: speeding up functional genomics in monocots. Plant Mol Biol 100, 3–18 (2019). https://doi.org/10.1007/s11103-019-00854-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00854-6

Keywords

Navigation