Arabidopsis thaliana-Myzus persicae interaction: shaping the understanding of plant defense against phloem-feeding aphids - PubMed

Figure 2

Model depicting relationship between genes and mechanisms that influence Arabidopsis interaction with the green peach aphid. Green peach aphid (GPA) salivary secretions contain effectors that promote infestation, as well as elicitors (e.g., Mp10 and Mp42) that are recognized by the host to turn on defense responses. GPA infestation on the shoot results in the induction of LOX5 expression in roots and a concomitant increase in the levels of LOX5-derived oxylipins (e.g., 9-HOD). LOX5 expression is likely induced by a GPA infestation-induced factor that is translocated from the leaves to the roots. The LOX5-derived oxylipins are transported from the roots to the shoots where one or more of these oxylipins stimulate expression of the defense regulatory gene, PAD4. A PAD4-dependent mechanism adversely impacts GPA settling, feeding and fecundity on Arabidopsis. PAD4 expression is further stimulated by the trehalose (Tre) metabolic pathway. GPA infestation results in the elevated expression of TPS11, which encodes an enzyme with Trehalose-6-phosphate (T6P) synthase and T6P phosphatase activities that is required for promoting PAD4 expression in GPA-infested plants. TPS11 also promotes accumulation of starch at the expense of sucrose (Suc), which is a major feeding stimulant, thereby generating a secondary sink that is detrimental to the insect's ability to colonize Arabidopsis. TPS11 and PAD4 are also required for accumulation of an antibiosis factor in the petiole exudates that limits insect fecundity. However, the GPA has evolved mechanisms that over time spent on the plant suppress this TPS11/PAD4-determined antibiosis activity. The GPA has also evolved to utilize one or more of the 9-LOX-derived oxylipins, or products thereof, as cues to stimulate feeding from phloem and xylem, and enhance fecundity. These oxylipins, which are consumed by the insect from the plant, likely induce changes in the GPA gene expression/physiology, thus allowing the insect to overcome and/or bypass plant defenses and adapt to the host plant. Salicylic acid (SA) signaling through NPR1 is also stimulated in GPA-infested plants. In plant-pathogen interaction, the PAD4 protein functions along with its interacting partner EDS1 in an amplification loop that promotes SA synthesis, leading to activation of SA dependent defenses. SA in turn amplifies PAD4 and EDS1 expression, thus resulting in positive amplification of this PAD4/EDS1-SA loop in plant defense against pathogens. Although EDS1 expression and SA signaling are activated in GPA-infested Arabidopsis, genetic studies confirm that SA and EDS1 are not required for controlling GPA infestation on Arabidopsis. Quite to the contrary, SA by antagonizing the jasmonic acid (JA; active form is JA-Isoleucine [JA-Ile]) signaling mechanism likely facilitates GPA infestation. JA, which is synthesized by the 13-LOX pathway, is required for controlling severity of GPA infestation. JA promotes the accumulation of N^δ-acetylornithine, camalexin and indole-glucosinolates, which are detrimental to GPA. Expression of PAD3, which is involved in camalexin synthesis and some genes involved in glucosinolate synthesis (e.g., CYP79B2 and CYP81F2) are negatively regulated by the small RNA gene-silencing mechanism involving DCL1, HYL1, HENT1, HST, SE, and AGO1. Oxylipins synthesized by the α DOX1 pathway and reactive oxygen species (ROS) produced by the NADPH oxidase RBOHD are also involved in controlling GPA infestation. H₂O₂ promotes callose deposition and thus likely contributes to phloem occlusion and plant defense against GPA. ROS's could also impinge on other signaling/defense mechanisms. Ethylene signaling through ETR1 and EIN2 has also been implicated in Arabidopsis defense against GPA. The ethylene inducible MYB44 gene is required for controlling GPA infestation. MYB44 is required for promoting EIN2 expression in response to harpin treatment, which also induces resistance against GPA in Arabidopsis. The ethylene- and harpin-inducible MYB15, MYB51, and MYB73 genes were required for harpin-induced resistance against GPA. By contrast, since mutations in the ethylene- and harpin-inducible MYB30, MYB108, ZFP6, and RAP2.6L genes enhanced the effect of harpin on controlling GPA infestation, these genes are shown as factors that facilitate GPA infestation. The relationship between many of these different pathways/mechanisms remains to be studied. All genes/proteins are in blue and signaling molecules are in yellow boxes. Red lines/arrows indicate steps/mechanisms that facilitate GPA infestation, while black lines indicate steps that contribute to defense. Lines ending with a perpendicular bar are indicative of a repressive effect.