Thrips and Tospoviruses benefit from jointly challenging plants
Belliure B 1,2, Janssen A1, Sabelis MW1
1IBED, Institute for Biodiversity and Ecosystem Dynamics, Section Population Biology. University of Amsterdam. PO Box 94084 1090 GB Amsterdam, The Netherlands
2Present address: IVIA, Valencian Institute for Agricultural Research, Entomology Unit. Apartado Oficial, 46113 Moncada (Valencia), Spain.
Correspondence: belliure@ivia.es
Plants are the target of various attackers, such as herbivorous arthropods and plant pathogens. Constitutive defences to these attacks (spines, hard cuticle, etc.) are costly when attackers are not present. Therefore, many plants possess inducible defences that are switched on only upon attack. Induced responses to herbivory are mediated via several metabolic pathways, in particular the Jasmonic Acid (JA) pathway. Defences induced by herbivores involve changes in the quality of attacked plants that affect the fitness of the herbivore (direct defence), and the emission of plant volatiles that attract natural enemies of the herbivore towards attacked plants (indirect defence). As a result, herbivore-induced plants become hosts of inferior quality for herbivorous arthropods, and are therefore less attractive for conspecific or heterospecific herbivores. Pathogens induce anti-pathogen resistance in plants through the Salicylic Acid (SA) pathway. Anti-herbivore and anti-pathogen defensive pathways cross talk in several plant-pathogen systems: up-regulation of the SA pathway results in down-regulation of the JA pathway. This negative cross talk can be exploited by vectors of pathogens, because induction of the anti-pathogen pathway reduces investment of the plant in anti-herbivore defence. In turn, vector-borne pathogens receive a benefit from this cross talk because a pathogen-infected plant with a reduced anti-herbivore defence represents a good host plant for the herbivorous vector of the pathogen. This is the case for Tospoviruses that are vectored by thrips. Thrips induce anti-herbivore defences in the plants that are detrimental for thrips. However, adult thrips are often attracted to tospovirus-infected plants, in spite of these being induced by thrips. Recent research showed that Frankliniella occidentalis actually benefited from attking plants infected with Tomato spotted wilt virus; survival and developmental rates of thrips larvae were as high on virus-induced (and thus also herbivore-induced) plants as on clean, uninduced plants, and higher than on plants with thrips damage. This is in agreement with the described JA/SA cross-talk. The interaction between the two pathways has several ecological implications. We show that spider mites, another herbivorous arthropod that do not vector the virus, can benefit from plants being infected with the virus. However, this benefit is not due to the negative effect of the virus on the defensive response of the plants to thrips damage. Furthermore, we show that the shorter developmental rate of thrips larvae that develop on plants with virus results in reduced vulnerability to attacks by at least some of its natural enemies. We propose that mechanisms to reduce direct and indirect plant defences against vectors may have evolved in vector-borne plant pathogens, thereby promoting spread of the pathogen.
