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Phytoplasma infection of a tropical root crop triggers bottom-up cascades by favoring generalist over specialist herbivores.

ABSTRACT: Global interest on plant-microbe-insect interactions is rapidly growing, revealing the multiple ways in which microorganisms mediate plant-herbivore interactions. Phytopathogens regularly alter whole repertoires of plant phenotypic traits, and bring about shifts in key chemical or morphological characteristics of plant hosts. Pathogens can also cause cascading effects on higher trophic levels, and eventually shape entire plant-associated arthropod communities. We tested the hypothesis that a Candidatus Phytoplasma causing cassava witches' broom (CWB) on cassava (Manihot esculenta Grantz) is altering species composition of invasive herbivores and their associated parasitic hymenopterans. We conducted observational studies in cassava fields in eastern Cambodia to assess the effect of CWB infection on abundance of specialist and generalist mealybugs (Homoptera: Pseudococcidae), and associated primary and hyper-parasitoid species. CWB infection positively affects overall mealybug abundance and species richness at a plant- and field-level, and disproportionately favors a generalist mealybug over a specialist feeder. CWB phytoplasma infection led to increased parasitoid richness and diversity, with richness of 'comparative' specialist taxa being the most significantly affected. Parasitism rate did not differ among infected and uninfected plants, and mealybug host suppression was not impacted. CWB phytoplasma modifies host plant quality for sap-feeding homopterans, differentially affects success rates of two invasive species, and generates niche opportunities for higher trophic orders. By doing so, a Candidatus phytoplasma affects broader food web structure and functioning, and assumes the role of an ecosystem engineer. Our work unveils key facets of phytoplasma ecology, and sheds light upon complex multi-trophic interactions mediated by an emerging phytopathogen. These findings have further implications for invasion ecology and management.

SUBMITTER: Wyckhuys KAG

PROVIDER: S-EPMC5559091 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Phytoplasma infection of a tropical root crop triggers bottom-up cascades by favoring generalist over specialist herbivores.

Wyckhuys Kris A G KAG Graziosi Ignazio I Burra Dharani Dhar DD Walter Abigail Jan AJ

PloS one 20170816 8

Global interest on plant-microbe-insect interactions is rapidly growing, revealing the multiple ways in which microorganisms mediate plant-herbivore interactions. Phytopathogens regularly alter whole repertoires of plant phenotypic traits, and bring about shifts in key chemical or morphological characteristics of plant hosts. Pathogens can also cause cascading effects on higher trophic levels, and eventually shape entire plant-associated arthropod communities. We tested the hypothesis that a Can ...[more]

PMID: 28813469

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Project description:Through artificial selection, domesticated plants often contain modified levels of primary and secondary metabolites compared to their wild progenitors. It is hypothesized that the changed chemistry of cultivated plants will affect the performance of insects associated with these plants. In this paper, the development of several specialist and generalist herbivores and their endoparasitoids were compared when reared on a wild and cultivated population of cabbage, Brassica oleracea, and a recently established feral Brassica species. Irrespective of insect species or the degree of dietary specialization, herbivores and parasitoids developed most poorly on the wild population. For the specialists, plant population influenced only development time and adult body mass, whereas for the generalists, plant populations also affected egg-to-adult survival. Two parasitoid species, a generalist (Diadegma fenestrale) and a specialist (D. semiclausum), were reared from the same host (Plutella xylostella). Performance of D. semiclausum was closely linked to that of its host, whereas the correlation between survival of D. fenestrale and host performance was less clear. Plants in the Brassicaceae characteristically produce defense-related glucosinolates (GS). Levels of GS in leaves of undamaged plants were significantly higher in plants from the wild population than from the domesticated populations. Moreover, total GS concentrations increased significantly in wild plants after herbivory, but not in domesticated or feral plants. The results of this study reveal that a cabbage cultivar and plants from a wild cabbage population exhibit significant differences in quality in terms of their effects on the growth and development of insect herbivores and their natural enemies. Although cultivated plants have proved to be model systems in agroecology, we argue that some caution should be applied to evolutionary explanations derived from studies on domesticated plants, unless some knowledge exists on the history of the system under investigation.

Project description:BackgroundHerbivore feeding elicits dramatic increases in defenses, most of which require jasmonate (JA) signaling, and against which specialist herbivores are thought to be better adapted than generalist herbivores. Unbiased transcriptional analyses of how neonate larvae cope with these induced plant defenses are lacking.Methodology/principal findingsWe created cDNA microarrays for Manduca sexta and Heliothis virescens separately, by spotting normalized midgut-specific cDNA libraries created from larvae that fed for 24 hours on MeJA-elicited wild-type (WT) Nicotiana attenuata plants. These microarrays were hybridized with labeled probes from neonates that fed for 24 hours on WT and isogenic plants progressively silenced in JA-mediated defenses (N: nicotine; N/PI: N and trypsin protease inhibitors; JA: all JA-mediated defenses). H. virescens neonates regulated 16 times more genes than did M. sexta neonates when they fed on plants silenced in JA-mediated defenses, and for both species, the greater the number of defenses silenced in the host plant (JA > N/PI > N), the greater were the number of transcripts regulated in the larvae. M. sexta larvae tended to down-regulate while H. virescens larvae up- and down-regulated transcripts from the same functional categories of genes. M. sexta larvae regulated transcripts in a diet-specific manner, while H. virescens larvae regulated a similar suite of transcripts across all diet types.Conclusions/significanceThe observations are consistent with the expectation that specialists are better adapted than generalist herbivores to the defense responses elicited in their host plants by their feeding. While M. sexta larvae appear to be better adapted to N. attenuata's defenses, some of the elicited responses remain effective defenses against both herbivore species. The regulated genes provide novel insights into larval adaptations to N. attenuata's induced defenses, and represent potential targets for plant-mediated RNAi to falsify hypotheses about the process of adaptation.

Dataset Information

Phytoplasma infection of a tropical root crop triggers bottom-up cascades by favoring generalist over specialist herbivores.

Publications

Phytoplasma infection of a tropical root crop triggers bottom-up cascades by favoring generalist over specialist herbivores.

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