A Functional Genomics Approach Identifies Candidate Effectors from the Aphid Species Myzus persicae (Green Peach Aphid)

Abstract

Aphids are amongst the most devastating sap-feeding insects of plants. Like most plant parasites, aphids require intimate associations with their host plants to gain access to nutrients. Aphid feeding induces responses such as clogging of phloem sieve elements and callose formation, which are suppressed by unknown molecules, probably proteins, in aphid saliva. Therefore, it is likely that aphids, like plant pathogens, deliver proteins (effectors) inside their hosts to modulate host cell processes, suppress plant defenses, and promote infestation. We exploited publicly available aphid salivary gland expressed sequence tags (ESTs) to apply a functional genomics approach for identification of candidate effectors from Myzus persicae (green peach aphid), based on common features of plant pathogen effectors. A total of 48 effector candidates were identified, cloned, and subjected to transient overexpression in Nicotiana benthamiana to assay for elicitation of a phenotype, suppression of the Pathogen-Associated Molecular Pattern (PAMP)–mediated oxidative burst, and effects on aphid reproductive performance. We identified one candidate effector, Mp10, which specifically induced chlorosis and local cell death in N. benthamiana and conferred avirulence to recombinant Potato virus X (PVX) expressing Mp10, PVX-Mp10, in N. tabacum, indicating that this protein may trigger plant defenses. The ubiquitin-ligase associated protein SGT1 was required for the Mp10-mediated chlorosis response in N. benthamiana. Mp10 also suppressed the oxidative burst induced by flg22, but not by chitin. Aphid fecundity assays revealed that in planta overexpression of Mp10 and Mp42 reduced aphid fecundity, whereas another effector candidate, MpC002, enhanced aphid fecundity. Thus, these results suggest that, although Mp10 suppresses flg22-triggered immunity, it triggers a defense response, resulting in an overall decrease in aphid performance in the fecundity assays. Overall, we identified aphid salivary proteins that share features with plant pathogen effectors and therefore may function as aphid effectors by perturbing host cellular processes.

Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays

“…Similar induction of salicylic acid-dependent gene expression has been reported in response to feeding by several other aphid species, including green peach aphid, cabbage aphid, greenbug aphid, and potato aphid (Giordanengo et al, 2010;Appel et al, 2014), suggesting that this may be a more general plant response to aphids. Aphids secrete a variety of proteins into the phloem as they are feeding (Elzinga and Jander, 2013), and some of these are known to suppress plant defense responses Bos et al, 2010;Elzinga et al, 2014). However, although it has been proposed that aphids actively induce salicylic acid production to misdirect plant defenses (Walling, 2008), specific salivary effectors involved in this process have not yet been identified.…”

Alteration of plant primary metabolism in response to insect herbivory

“…Several proteomic studies have identified potential effectors in aphid saliva (Harmel et al, 2008;Carolan et al, 2009;Rao et al, 2013), and specific proteins have been reported to affect aphid performance on host plants (Bos et al, 2010;Elzinga et al, 2014). Although there are clearly differences in the salivary proteomes of different aphid species, it is not yet known whether this variation causes differences in plant primary metabolism, such as those that are observed when the specialist cabbage aphid and the generalist green peach aphid are feeding from Arabidopsis (Fig.…”

Effector Biology of Plant-Associated Organisms: Concepts and Perspectives

“…Some common themes are starting to emerge. Effectors from diverse pathogenic species of bacteria, oomycetes, fungi, and insects have been reported to suppress an overlapping set of PTI signaling pathways (Gimenez-Ibanez et al 2009;Bos et al 2010;de Jonge et al 2010;Wang et al 2011). Both bacterial and oomycete plant pathogens target vesicle trafficking pathways to interfere with focal immunity, although the exact mechanisms are yet to emerge Lindeberg et al 2012).…”