The Leucine-Rich Repeat Receptor-Like Kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 and the Cytochrome P450 PHYTOALEXIN DEFICIENT3 Contribute to Innate Immunity to Aphids in Arabidopsis      

Abstract

The importance of pathogen-associated molecular pattern-triggered immunity (PTI) against microbial pathogens has been recently demonstrated. However, it is currently unclear if this layer of immunity mediated by surface-localized pattern recognition receptors (PRRs) also plays a role in basal resistance to insects, such as aphids. Here, we show that PTI is an important component of plant innate immunity to insects. Extract of the green peach aphid (GPA; Myzus persicae) triggers responses characteristic of PTI in Arabidopsis (Arabidopsis thaliana). Two separate eliciting GPA-derived fractions trigger induced resistance to GPA that is dependent on the leucine-rich repeat receptor-like kinase BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1)/SOMATIC-EMBRYOGENESIS RECEPTOR-LIKE KINASE3, which is a key regulator of several leucine-rich repeat-containing PRRs. BAK1 is required for GPA elicitor-mediated induction of reactive oxygen species and callose deposition. Arabidopsis bak1 mutant plants are also compromised in immunity to the pea aphid (Acyrthosiphon pisum), for which Arabidopsis is normally a nonhost. Aphid-derived elicitors induce expression of PHYTOALEXIN DEFICIENT3 (PAD3), a key cytochrome P450 involved in the biosynthesis of camalexin, which is a major Arabidopsis phytoalexin that is toxic to GPA. PAD3 is also required for induced resistance to GPA, independently of BAK1 and reactive oxygen species production. Our results reveal that plant innate immunity to insects may involve early perception of elicitors by cell surface-localized PRRs, leading to subsequent downstream immune signaling.

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

“…M. persicae fecundity was unaltered on the glr3.3 glr3.6 mutant ( Figure 10A) the tpc1-2 mutant ( Figure 10B) and the 35S:TPC1 5.6 line ( Figure 10C). M. persicae fecundity on the bak1-5 mutant has been assessed previously and is also not significantly different from the wild type (Prince et al, 2014). However, the fou2 mutation resulted in a significant reduction in M. persicae fecundity ( Figure 10D).…”

“…While wounding during herbivory by chewing insects is sufficient to induce Ca 2+ signaling (Maffei et al, 2004;Yang et al, 2012;Kiep et al, 2015), aphids probe only a small number of cells (Will and van Bel, 2006) and thus are more comparable to microbial pathogens. Indeed, BAK1 is an essential component of PTI against microbial pathogens (Chinchilla et al, 2007;Heese et al, 2007) and aphids (Prince et al, 2014;Chaudhary et al, 2014). Several plasma membrane PRRs that interact with BAK1 have been implicated in Ca 2+ release during plant-microbe interactions, including CERK1, FLS2, EFR, and PEPR1 (Miya et al, 2007;Jeworutzki et al, 2010;Qi et al, 2010;Ma et al, 2012).…”

“…Aphid Elicitation of [Ca 2+ ] cyt Is Dependent on BAK1 and GLR3.3/GLR3.6 BAK1 is a defense coreceptor required for PTI against microbes (Chinchilla et al, 2007;Heese et al, 2007) and aphids (Prince et al, 2014;Chaudhary et al, 2014). Thus, to establish whether the aphid-elicited [Ca 2+ ] cyt elevation is a component of PTI, 35S:GCaMP3-expressing plants were crossed with the BAK1 null mutant bak1-5.…”

“…The ability of an aphid to feed successfully on a plant appears to be partly determined during these penetrations, as the pathway phase still occurs with aphid species unable to establish long-term feeding (Chen et al, 1997;Sauge et al, 1998;Jaouannet et al, 2015;Nam and Hardie, 2012). Furthermore, as with microbial pathogens, aphids are detected through a BAK1-dependent mechanism, although the PRRs involved have remained elusive, with FLAGELLIN-SENSITIVE2 (FLS2), EF-TU RECEPTOR (EFR), CHITIN ELICITOR RECEPTOR KINASE1 (CERK1), PEP1 RECEPTOR1 (PEPR1), and PEPR2 not appearing to play a role (Prince et al, 2014;Chaudhary et al, 2014).…”

GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense

“…It was recently shown that pea aphids survived longer on the bak1-5 mutant compared with Arabidopsis Col-0, whereas no effect on green peach aphid survival was detected on bak1-5 plants. This shows that BAK1 contributes to nonhost resistance to aphids (39). BAK1 could be participating in PTI triggered by recognition of a number aphidassociated molecular patterns including GroEL.…”