Aphid protein effectors promote aphid colonization in a plant species-specific manner.

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Microbial pathogens and pests produce effectors to modulatehost processes. Aphids are phloem-feeding insects,which introduce effectors via saliva into plant cells. However,it is not known if aphid effectors have adapted tomodulate processes in specific plant species. Myzus persicaeis a polyphagous insect that colonizes Arabidopsis thalianaand Nicotiana benthamiana, while the pea aphid Acyrthosiphonpisum specializes on colonizing plant species of thefamily Fabaceae. We found that M. persicae reproductionincreased on transgenic Arabidopsis, producing the M. persicaeeffectors C002, PIntO1 (Mp1), and PIntO2 (Mp2),whereas reproduction of M. persicae did not increase onArabidopsis producing the A. pisum orthologs of these threeproteins. Plant-mediated RNA interference experimentsshowed that c002- and PIntO2-silenced M. persicae produceless progeny on Arabidopsis and N. benthamiana thannonsilenced aphids. Orthologs of c002, PIntO1, and PIntO2were identified in multiple aphid species with dissimilarplant host ranges. We revealed high nonsynonymous versussynonymous nucleotide substitution rates within the effectororthologs, indicating that the effectors are fast evolving.Application of maximum likelihood methods identified specificsites with high probabilities of being under positiveselection in PIntO1, whereas those of C002 and PIntO2may be located in alignment gaps. In support of the latter,a M. persicae c002 mutant without the NDNQGEE repeatregion, which overlaps with an alignment gap in C002,does not promote M. persicae colonization on Arabidopsis.Taken together, these results provide evidence that aphideffectors are under positive selection to promote aphidcolonization on specific plant species.