Aphid Protein Effectors Promote Aphid Colonization in a Plant Species-Specific Manner

Abstract

Microbial pathogens and pests produce effectors to modulate host processes. Aphids are phloem-feeding insects, which introduce effectors via saliva into plant cells. However, it is not known if aphid effectors have adapted to modulate processes in specific plant species. Myzus persicae is a polyphagous insect that colonizes Arabidopsis thaliana and Nicotiana benthamiana, while the pea aphid Acyrthosiphon pisum specializes on colonizing plant species of the family Fabaceae. We found that M. persicae reproduction increased on transgenic Arabidopsis, producing the M. persicae effectors C002, PIntO1 (Mp1), and PIntO2 (Mp2), whereas reproduction of M. persicae did not increase on Arabidopsis producing the A. pisum orthologs of these three proteins. Plant-mediated RNA interference experiments showed that c002- and PIntO2-silenced M. persicae produce less progeny on Arabidopsis and N. benthamiana than nonsilenced aphids. Orthologs of c002, PIntO1, and PIntO2 were identified in multiple aphid species with dissimilar plant host ranges. We revealed high nonsynonymous versus synonymous nucleotide substitution rates within the effector orthologs, indicating that the effectors are fast evolving. Application of maximum likelihood methods identified specific sites with high probabilities of being under positive selection in PIntO1, whereas those of C002 and PIntO2 may be located in alignment gaps. In support of the latter, a M. persicae c002 mutant without the NDNQGEE repeat region, which overlaps with an alignment gap in C002, does not promote M. persicae colonization on Arabidopsis. Taken together, these results provide evidence that aphid effectors are under positive selection to promote aphid colonization on specific plant species.

Interplay of Plasma Membrane and Vacuolar Ion Channels, Together with BAK1, Elicits Rapid Cytosolic Calcium Elevations in Arabidopsis during Aphid Feeding

“…As a result, there is no capacity to increase plant susceptibility to the aphid by disrupting Ca 2+ signaling. The suppression of Arabidopsis defense by aphids is achieved via effector proteins (Bos et al, 2010;Hogenhout and Bos, 2011;Pitino and Hogenhout, 2013;Atamian et al, 2013;Elzinga et al, 2014;Naessens et al, 2015;Wang et al, 2015;Kettles and Kaloshian, 2016) that are injected into epidermal and mesophyll cells during feeding (Martín et al, 1997;Moreno et al, 2011;Mugford et al, 2016). These effectors may actively suppress the feeding site [Ca 2+ ] cyt elevations, as aphid saliva contains Ca 2+ binding proteins Carolan et al, 2009;Rao et al, 2013).…”

“…Indeed, aphid saliva contains Ca 2+ binding proteins Carolan et al, 2009;Rao et al, 2013), and application of saliva to legume phloemplugging proteins results in their contraction . Aphid saliva also contains effector molecules that suppress plant defense (Bos et al, 2010;Pitino and Hogenhout, 2013;Atamian et al, 2013;Naessens et al, 2015;Wang et al, 2015;Kettles and Kaloshian, 2016), as observed with microbial pathogens (Jones and Dangl, 2006;Galán et al, 2014) and chewing insects (Musser et al, 2002).…”

OXI1 kinase plays a key role in resistance of Arabidopsis towards aphids (Myzus persicae)

“…The plant-aphid interaction is complex and highly dynamic, subject to continual change (Mello and Silva-Filho 2002). Recently, studies have shown that aphids secrete effectors that modulate plant defence responses (Bos et al 2010;Atamian et al 2013;Pitino and Hogenhout 2013) pointing to parallels between plant-pathogen and plant-insect interactions (Jaouannet et al 2014). It has been suggested that two different processes are involved in the elicitation of plant defence.…”

Transient Expression of Whitefly Effectors in Nicotiana benthamiana Leaves Activates Systemic Immunity Against the Leaf Pathogen Pseudomonas syringae and Soil-Borne Pathogen Ralstonia solanacearum

“…Plants have developed a sophisticated immune system against insect herbivory. Compared with our understanding of plant defensive responses against chewing insects, little is known about plant responses to phloem-feeding insects in the order Hemiptera (Van Oosten et al, 2008;Walling, 2008;Rodriguez-Medina et al, 2011;van Dam and Heil, 2011;Louis and Shah, 2013;Pitino and Hogenhout, 2013;Rao et al, 2013;VanDoorn et al, 2015). The detailed mechanisms of plant responses to this group of insects, such as aphids and whitefly (Bemisia tabaci Genn.…”

“…The detailed mechanisms of plant responses to this group of insects, such as aphids and whitefly (Bemisia tabaci Genn. ), have only recently begun to be uncovered due to the small size and limited genetic and physiological information about these insects (Louis and Shah, 2013;Pitino and Hogenhout, 2013;VanDoorn et al, 2015).…”