Plants use identical inhibitors to protect their cell wall pectin against microbes and insects

Abstract

As fundamentally different as phytopathogenic microbes and herbivorous insects are, they enjoy plant‐based diets. Hence, they encounter similar challenges to acquire nutrients. Both microbes and beetles possess polygalacturonases (PGs) that hydrolyze the plant cell wall polysaccharide pectin. Countering these threats, plant proteins inhibit PGs of microbes, thereby lowering their infection rate. Whether PG‐inhibiting proteins (PGIPs) play a role in defense against herbivorous beetles is unknown. To investigate the significance of PGIPs in insect–plant interactions, feeding assays with the leaf beetle Phaedon cochleariae on Arabidopsis thaliana pgip mutants were performed. Fitness was increased when larvae were fed on mutant plants compared to wild‐type plants. Moreover, PG activity was higher, although PG genes were downregulated in larvae fed on PGIP‐deficient plants, strongly suggesting that PGIPs impair PG activity. As low PG activity resulted in delayed larval growth, our data provide the first in vivo correlative evidence that PGIPs act as defense against insects.

Direct evidence for a new mode of plant defense against insects via a novel polygalacturonase-inhibiting protein expression strategy

“…In mung bean (Vigna radiata), resistance to seed beetles (Callosobruchus spp.) was associated withgenes encoding putative PGIPs (76,77).Feeding assaysonA.thalianarevealedthefirstecological relevance of PGIPs for herbivorous beetles, as the fitness of P. cochleariaecorrelatedwiththePGIP compositionofthediet (78).…”

“…gain was reduced if two instead of only one AtPGIP were present in the food plant (78). Thus, PGIPs are not only important in defending plants against phytopathogenic bacteria and fungi, but may also play a role in the protection against herbivorous beetles.…”

“…Despite the impact of PGIPs that our study and Kirsch et al (78) demonstrated, the gut content of P. cochleariae feeding on B. rapa ssp. pekinensis as well as A. thaliana still retains some residual PG activity (35,60,78). This suggests that P. cochleariae has adapted to the PG-inhibiting defenses of its food plants in vivo.…”

A Survey on Cell wall Proteins of C. Sinensis Leaf by Combining Cell Wall Proteomic and N-Glycoproteomic Strategy

“…PMEIs that inhibited partly the activity of PMEs, adjust the degree of pectin methyl-esteri cation. PGIPs (polygalacturonase inhibitorlike) speci cally bind with polygalacturonases (GH28), thereby they can inhibit the hydrolyzation of pectin and then regulate pectin degradation, which can trigger defense against microbes and insects [100]. In summary, two couple of PMEIs and PME, PGIPs and PG occurred coincidentally and modulate precisely pectin metabolism.…”

New Players in the Interaction Between Beetle Polygalacturonases and Plant Polygalacturonase-Inhibiting Proteins: Insights From Proteomics and Gene Expression Analyses

“…Additionally, PGIPs can protect pectin by binding to and thus shielding the substrate from degradation (Spadoni et al, 2006;Protsenko et al, 2008). Some PGIPs are constitutively expressed, whereas others are induced in response to various environmental cues such as wounding, the presence of oligogalacturonides, pathogen infection or herbivory (Li et al, 2003;D'Ovidio et al, 2004b;Hwang et al, 2010;Kirsch et al, 2020). PGIPs have been studied best and extensively reviewed in the context of plant-microbe interactions (De Lorenzo et al, 2001;Kalunke et al, 2015;Rathinam et al, 2020).…”