Subversion of insect resistance: A novel role for a plant viral silencing suppressor
Lead Research Organisation:
University of Cambridge
Department Name: Plant Sciences
Abstract
Cucumber mosaic virus (CMV) is one of the two most important viruses of field-grown and glasshouse horticultural crops in the UK and worldwide, causing considerable economic damage annually. Moreover it attacks more crop and wild-plant species than any other virus. An essential contributor to the success of CMV is a recently discovered factor made by the virus, which is called the 2b protein. Until recently the most important known role for the 2b protein was that it counter-attacks the resistance mechanisms that plants use to defend themselves against virus infection. We have now discovered another remarkable and novel property of the 2b protein: it inhibits plant defences against insects. This is very important because under natural conditions, CMV (like most plant viruses) is transmitted from plant to plant by aphids. Aphids are a group of insects that feed on plants and in doing so cause damage and promote the spread of disease caused by viruses and other disease-causing organisms. We can imagine that it will be in the interests of the virus to inhibit defences against insects so that sufficient aphids will be born on CMV-infected plants to pass on the infection to new host plants. We found that the 2b protein blocks the action of a natural chemical signal, jasmonate, which stimulates anti-insect defences in plants. We also discovered that in plants infected with a mutant strain of CMV that is unable to make the 2b protein, these defences are activated. We will determine whether it is a substance made by the virus itself, or the stress of viral infection, which triggers the anti-insect responses. In addition we will identify the anti-insect materials produced by plants in response to infection with the mutant strain of the virus, and how the 2b protein inhibits this response in plants infected with the naturally-occurring virus.
Technical Summary
We have discovered that a virus can manipulate plant defences to make the host less able to resist the insects that transmit the virus. The cucumber mosaic virus (CMV) 2b protein is a suppressor of virus resistance mediated by RNAi and salicylic acid (SA). We analyzed Affymetrix arrays of gene expression profiles in 2b-transgenic Arabidopsis plants treated with resistance-inducing chemicals. Surprisingly, the most comprehensively inhibited defensive signalling pathway in 2b-transgenic plants was not the SA pathway, but the pathway regulated by jasmonic acid (JA). JA is a key signal in resistance to insects. This is highly significant because CMV, along with 70% of all plant viruses, is transmitted by insect vectors- specifically aphids. In the course of other experiments using CMVdelta2b (a CMV mutant lacking the gene for the 2b protein) it was noted that on plants infected with CMVdelta2b, aphid reproduction was inhibited and aphid mortality was increased. We hypothesize that inhibition of resistance to insects by the 2b protein favours aphid colonisation of CMV-infected plants, which in turn leads to increased numbers of viruliferous aphid vectors, and consequently a higher rate of transmission. To explore this concept further we will determine: 1. Which viral gene product(s) of CMVdelta2b elicit anti-insect responses or if this elicitation requires the presence of a replicating virus; 2. Which anti-insect responses are induced (induction of protease inhibitors or other directly JA-induced gene products or increased biosynthesis of low molecular weight chemicals), and which of these factors are enhancing aphid morbidity and mortality, and 3. How the 2b protein interferes with the induction of these anti-insect defences, in particular by assessing the role of RNAi in this subversion.
Organisations
Publications
Carr JP
(2010)
Natural and engineered resistance to plant viruses, part II. Preface.
in Advances in virus research
Carr JP
(2010)
Signaling in induced resistance.
in Advances in virus research
Chivasa S
(2009)
Extracellular ATP is a regulator of pathogen defence in plants.
in The Plant journal : for cell and molecular biology
Chivasa S
(2010)
The effects of extracellular adenosine 5'-triphosphate on the tobacco proteome.
in Proteomics
Chivasa S
(2009)
Extracellular ATP: a modulator of cell death and pathogen defense in plants.
in Plant signaling & behavior
Hunter LJ
(2016)
RNA-dependent RNA polymerase 1 in potato (Solanum tuberosum) and its relationship to other plant RNA-dependent RNA polymerases.
in Scientific reports
Lewsey MG
(2009)
Effects of DICER-like proteins 2, 3 and 4 on cucumber mosaic virus and tobacco mosaic virus infections in salicylic acid-treated plants.
in The Journal of general virology
Ling R
(2013)
An essential fifth coding ORF in the sobemoviruses.
in Virology
Loebenstein G
(2009)
The very earliest developments in agriculture, and probably even before then, diseases affecting crop plants have posed an ever-present, yet ever changing, threat to human survival. Preface.
in Advances in virus research
Macaulay KM
(2017)
The biochemical properties of the two Arabidopsis thaliana isochorismate synthases.
in The Biochemical journal
Palukaitis P
(2008)
Plant-virus interactions.
in Methods in molecular biology (Clifton, N.J.)
Tungadi T
(2017)
Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco.
in Virology journal
Westwood J
(2012)
Molecular Plant Immunity
Zhou T
(2014)
Domains of the cucumber mosaic virus 2b silencing suppressor protein affecting inhibition of salicylic acid-induced resistance and priming of salicylic acid accumulation during infection.
in The Journal of general virology
Ziebell H
(2010)
Cross-protection: a century of mystery.
in Advances in virus research
Ziebell H
(2009)
Effects of dicer-like endoribonucleases 2 and 4 on infection of Arabidopsis thaliana by cucumber mosaic virus and a mutant virus lacking the 2b counter-defence protein gene.
in The Journal of general virology
Ziebell H
(2011)
Cucumber mosaic virus and its 2b RNA silencing suppressor modify plant-aphid interactions in tobacco.
in Scientific reports
| Description | Work by researchers from the University of Cambridge shows that virus infection alters the biochemistry of plants to make them smell and taste different to insects,including aphids, which results in the insect spreading the virus further. The work has led to additional translational work (SCPRID Programme) aimed at translating this work by seeing how virus-induced changes in aphid behaviour can teach us how to better combat important aphid-transmitted crop diseases. Successful results from the SCPRID grant led to futher funding under GCRF to generate novel field designs to designs to disrupt the dynamics of aphid-mediated virus transmission in Rwanda and Kenya. |
| Exploitation Route | We are currently carrying out collaborative research (with teams in Uganda, Kenya and the UK: Cambridge and Rothamsted) to look at how virus infection shapes the distribution of aphids under natural conditions. In addition the team will use a combination of molecular analyses, mathematical models and further field observations to identify how to select and deploy plants that could act as decoys for aphids by attracting them away from beans and other crops. |
| Sectors | Agriculture, Food and Drink |
| Description | A full report on this grant was provided via JeS more than 2 years ago. |