Genome-wide association analysis reveals distinct genetic architectures for single and combined stress responses in Arabidopsis thaliana
Davila Olivas, Nelson H. ; Kruijer, Willem ; Gort, Gerrit ; Wijnen, Cris L. ; Loon, Joop J.A. van; Dicke, Marcel - \ 2017
New Phytologist 213 (2017)2. - ISSN 0028-646X - p. 838 - 851.
abiotic stress - biotic stress - combined stresses - genome-wide association - specialist herbivores
Plants are commonly exposed to abiotic and biotic stresses. We used 350 Arabidopsis thaliana accessions grown under controlled conditions. We employed genome-wide association analysis to investigate the genetic architecture and underlying loci involved in genetic variation in resistance to: two specialist insect herbivores, Pieris rapae and Plutella xylostella; and combinations of stresses, i.e. drought followed by P. rapae and infection by the fungal pathogen Botrytis cinerea followed by infestation by P. rapae. We found that genetic variation in resistance to combined stresses by drought plus P. rapae was limited compared with B. cinerea plus P. rapae or P. rapae alone. Resistance to the two caterpillars is controlled by different genetic components. There is limited overlap in the quantitative trait loci (QTLs) underlying resistance to combined stresses by drought plus P. rapae or B. cinerea plus P. rapae and P. rapae alone. Finally, several candidate genes involved in the biosynthesis of aliphatic glucosinolates and proteinase inhibitors were identified to be involved in resistance to P. rapae and P. xylostella, respectively. This study underlines the importance of investigating plant responses to combinations of stresses. The value of this approach for breeding plants for resistance to combinatorial stresses is discussed.
Ozone affects growth and development of Pieris brassicae on the wild host plant Brassica nigra
Khaling, E. ; Papazian, S. ; Poelman, E.H. ; Holopainen, J.K. ; Albrectsen, B.R. ; Blande, J.D. - \ 2015
Environmental Pollution 199 (2015). - ISSN 0269-7491 - p. 119 - 129.
elevated atmospheric co2 - beetle epilachna-varivestis - betula-pendula roth - glucosinolate concentrations - secondary metabolites - feeding preference - oviposition preference - specialist herbivores - plutella-xylostella - leaf beetle
When plants are exposed to ozone they exhibit changes in both primary and secondary metabolism, which may affect their interactions with herbivorous insects. Here we investigated the performance and preferences of the specialist herbivore Pieris brassicae on the wild plant Brassica nigra under elevated ozone conditions. The direct and indirect effects of ozone on the plant-herbivore system were studied. In both cases ozone exposure had a negative effect on P. brassicae development. However, in dual-choice tests larvae preferentially consumed plant material previously fumigated with the highest concentration tested, showing a lack of correlation between larval preference and performance on ozone exposed plants. Metabolomic analysis of leaf material subjected to combinations of ozone and herbivore-feeding, and focussing on known defence metabolites, indicated that P. brassicae behaviour and performance were associated with ozone-induced alterations to glucosinolate and phenolic pools.
A test of genotypic variation in specificity of herbivore-induced responses in Solidago altissima L. (Asteraceae)
Uesugi, A. ; Poelman, E.H. ; Kessler, A. - \ 2013
Oecologia 173 (2013)4. - ISSN 0029-8549 - p. 1387 - 1396.
milkweed asclepias-syriaca - induced plant-responses - induced resistance - nicotiana-attenuata - common milkweed - interspecific interactions - specialist herbivores - phytophagous insects - tall goldenrod - defense
Plant-induced responses to multiple herbivores can mediate ecological interactions among herbivore species, thereby influencing herbivore community composition in nature. Several studies have indicated high specificity of induced responses to different herbivore species. In addition, there may be genetic variation for plant response specificity that can have significant ecological implications, by altering the competitive strength and hierarchical relationships among interacting herbivore species. However, few studies have examined whether plant populations harbor genetic variation for induction specificity. Using three distinct genotypes of Solidago altissima plants, we examined whether specialist herbivore species Dichomeris leuconotella, Microrhopala vittata, and Trirhabda virgata elicit specific induction responses from plants (specificity of elicitation), and whether induction differentially affects these herbivore species (specificity of effect). Results from bioassays and secondary metabolite analyses suggest that there is specificity of both elicitation and effect in the induced responses: D. leuconotella and M. vittata preferred and performed better on leaves damaged by conspecifics than heterospecifics, and induced qualitatively different secondary metabolite profiles. In contrast, T. virgata equally avoided but physiologically tolerated all types of damage. These patterns of specificity suggest that plant-induced responses mediate asymmetric competitive interactions between herbivore species, which potentially intensifies inter-specific relative to intra-specific competition. Plant genotypes widely differed in overall susceptibility to the herbivores and secondary metabolite production, yet we found no genotype-by-treatment interactions in insect performance, preference and plant secondary metabolite production. This lack of genetic variation for induction specificity suggests that competitive interactions between herbivore species on S. altissima are homogeneous across plant genotypes.
Phenotypic plasticity of plant response to herbivore eggs: effects on resistance to caterpillars and plant development
Pashalidou, F.G. ; Lucas-Barbosa, D. ; Loon, J.J.A. van; Dicke, M. ; Fatouros, N.E. - \ 2013
Ecology 94 (2013)3. - ISSN 0012-9658 - p. 702 - 713.
insect herbivores - pieris-brassicae - specialist herbivores - arabidopsis-thaliana - mamestra-brassicae - defense responses - bunias orientalis - chemical defense - pinus-sylvestris - getting ready
Herbivory induces direct resistance responses in plants that negatively affect subsequently colonizing herbivores. Moreover, eggs of herbivorous insects can also activate plant resistance, which in some cases prevents hatching larvae from feeding. Until now, plant-mediated effects of eggs on subsequent herbivory, and the specificity of such responses, have remained poorly understood. We studied the specificity and effects of plant resistance induced by herbivore egg deposition against lepidopteran larvae of species with different dietary breadths, feeding on a wild annual plant, the crucifer Brassica nigra. We examined whether this plant-mediated response affects the growth of caterpillars of a specialist (Pieris brassicae) that feeds on B. nigra leaves and flowers, and a generalist (Mamestra brassicae) that rarely attacks this wild crucifer. We measured growth rates of neonate larvae to the end of their second instar after the larvae had hatched on plants exposed to eggs vs. plants without eggs, under laboratory and semi-field conditions. Moreover, we studied the effects of egg deposition by the two herbivore species on plant height and flowering rate before and after larval hatching. Larvae of both herbivore species that developed on plants previously infested with eggs of the specialist butterfly P. brassicae gained less mass compared with larvae that developed on egg-free plants. Plants exposed to butterfly eggs showed accelerated plant growth and flowering compared to egg-free plants. Egg deposition by the generalist moth M. brassicae, in contrast, had no effect on subsequent performance by either herbivore species, or on plant development. Our results demonstrate that B. nigra plants respond differently to eggs of two herbivore species in terms of plant development and induced resistance to caterpillar attack. For this annual crucifer, the retardation of caterpillar growth in response to deposition of eggs by P. brassicae in combination with enhanced growth and flowering likely result in reproductive assurance, after being exposed to eggs from an herbivore whose larvae rapidly reduce the plant's reproductive potential through florivory.
Dealing with double trouble: consequences of single and double herbivory in Brassica juncea
Mathur, V. ; Tytgat, T.O.G. ; Graaf, R.M. de; Kalia, V. ; Reddy, A.S. ; Vet, L.E.M. ; Dam, N.M. van - \ 2013
Chemoecology 23 (2013)2. - ISSN 0937-7409 - p. 71 - 82.
induced plant-responses - milkweed asclepias-syriaca - plutella-xylostella - specialist herbivores - induced resistance - diamondback moth - wild radish - nicotiana-attenuata - insect resistance - black mustard
In their natural environment, plants are often attacked simultaneously by many insect species. The specificity of induced plant responses that is reported after single herbivore attacks may be compromised under double herbivory and this may influence later arriving herbivores. The present study focuses on the dynamics of induced plant responses induced by single and double herbivory, and their effects on successive herbivores. Morphological (leaf length, area and trichome density) and chemical changes (leaf alkenyl and indole glucosinolates) in Brassica juncea were evaluated 4, 10, 14 and 20 days after damage by the specialist Plutella xylostella alone, or together with the generalist Spodoptera litura. To assess the biological effect of the plant's responses, the preference and performance of both herbivores on previously induced plants were measured. We found that alkenyl glucosinolates were induced 20 days after damage by P. xylostella alone, whereas their levels were elevated as early as 4 days after double herbivory. Trichome density was increased in both treatments, but was higher after double herbivory. Interestingly, there was an overall decrease in indole glucosinolates and an increase in leaf size due to damage by P. xylostella, which was not observed during double damage. S. litura preferred and performed better on undamaged plants, whereas P. xylostella preferred damaged plants and performed better on plants damaged 14 and 10 days after single and double herbivory, respectively. Our results suggest that temporal studies involving single versus multiple attacker situations are necessary to comprehend the role of induced plant responses in plant-herbivore interactions.
Association mapping of plant resistance to insects
Kloth, K.J. ; Thoen, H.P.M. ; Bouwmeester, H.J. ; Jongsma, M.A. ; Dicke, M. - \ 2012
Trends in Plant Science 17 (2012)5. - ISSN 1360-1385 - p. 311 - 319.
genome-wide association - arabidopsis-thaliana - specialist herbivores - complex traits - glucosinolate accumulation - generalist herbivores - signaling pathways - natural variation - systems biology - host-plant
Association mapping is rapidly becoming an important method to explore the genetic architecture of complex traits in plants and offers unique opportunities for studying resistance to insect herbivores. Recent studies indicate that there is a trade-off between resistance against generalist and specialist insects. Most studies, however, use a targeted approach that will easily miss important components of insect resistance. Genome-wide association mapping provides a comprehensive approach to explore the whole array of plant defense mechanisms in the context of the generalist–specialist paradigm. As association mapping involves the screening of large numbers of plant lines, specific and accurate high-throughput phenotyping (HTP) methods are needed. Here, we discuss the prospects of association mapping for insect resistance and HTP requirements.
Herbivore-induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack
Poelman, E.H. ; Loon, J.J.A. van; Dam, N.M. van; Vet, L.E.M. ; Dicke, M. - \ 2010
Ecological Entomology 35 (2010)2. - ISSN 0307-6946 - p. 240 - 247.
arthropod community structure - tritrophic interaction webs - primrose oenothera-biennis - specialist herbivores - interspecific interactions - generalist herbivores - nicotiana-attenuata - insect herbivores - wild radish - performance
2. Here we studied the effect of early-season herbivory by caterpillars of Pieris rapae on the composition of the insect herbivore community on domesticated Brassica oleracea plants. We compared the effect of herbivory on two cultivars that differ in the degree of susceptibility to herbivores to analyse whether induced plant responses supersede differences caused by constitutive resistance. 3. Early-season herbivory affected the herbivore community, having contrasting effects on different herbivore species, while these effects were similar on the two cultivars. Generalist insect herbivores avoided plants that had been induced, whereas these plants were colonised preferentially by specialist herbivores belonging to both leaf-chewing and sap-sucking guilds. 4. Our results show that community-wide effects of early-season herbivory may prevail over effects of constitutive plant resistance. Induced responses triggered by prior herbivory may lead to an increase in susceptibility to the dominant specialists in the herbivorous insect community. The outcome of the balance between contrasting responses of herbivorous community members to induced plants therefore determines whether induced plant responses result in enhanced plant resistance.
Disruption of plant carotenoid biosynthesis through virus-induced gene silencing affects oviposition behaviour of the butterfly Pieris rapae
Zheng, S.J. ; Snoeren, T.A.L. ; Hogewoning, S.W. ; Loon, J.J.A. van; Dicke, M. - \ 2010
New Phytologist 186 (2010)3. - ISSN 0028-646X - p. 733 - 745.
tobacco rattle virus - specialist herbivores - nicotiana-benthamiana - arabidopsis-thaliana - leaf variegation - resistance - chloroplast - insects - vector - color
Optical plant characteristics are important cues to plant-feeding insects. In this article, we demonstrate for the first time that silencing the phytoene desaturase (PDS) gene, encoding a key enzyme in plant carotenoid biosynthesis, affects insect oviposition site selection behaviour. Virus-induced gene silencing employing tobacco rattle virus was used to knock down endogenous PDS expression in three plant species (Arabidopsis thaliana, Brassica nigra and Nicotiana benthamiana) by its heterologous gene sequence from Brassica oleracea. We investigated the consequences of the silencing of PDS on oviposition behaviour by Pieris rapae butterflies on Arabidopsis and Brassica plants; first landing of the butterflies on Arabidopsis plants (to eliminate an effect of contact cues); first landing on Arabidopsis plants enclosed in containers (to eliminate an effect of volatiles); and caterpillar growth on Arabidopsis plants. Our results show unambiguously that P. rapae has an innate ability to visually discriminate between green and variegated green-whitish plants. Caterpillar growth was significantly lower on PDS-silenced than on empty vector control plants. This study presents the first analysis of PDS function in the interaction with an herbivorous insect. We conclude that virus-induced gene silencing is a powerful tool for investigating insect–plant interactions in model and nonmodel plants
Consequences of variation in plant defense for biodiversity at higher trophic levels
Poelman, E.H. ; Loon, J.J.A. van; Dicke, M. - \ 2008
Trends in Plant Science 13 (2008)10. - ISSN 1360-1385 - p. 534 - 541.
arthropod community structure - primrose oenothera-biennis - genetic similarity rule - induced resistance - interspecific interactions - specialist herbivores - phytophagous insects - natural enemies - nicotiana-attenuata - beneficial insects
Antagonistic interactions between insect herbivores and plants impose selection on plants to defend themselves against these attackers. Although selection on plant defense traits has typically been studied for pairwise plant¿attacker interactions, other community members of plant-based food webs are unavoidably affected by these traits as well. A plant trait might, for example, affect parasitoids and predators feeding on the herbivore. Consequently, defensive plant traits structure the diversity and composition of the complex community associated with the plant, and communities as a whole also feed back to selection on plant traits. Here, we review recent developments in our understanding of how plant defense traits structure insect communities and discuss how molecular mechanisms might drive community-wide effects.