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

Abstract

Plants possess various defense strategies to counter attacks from microorganisms or herbivores. For example, plants reduce the cell-wall-macerating activity of pathogen- or insect-derived polygalacturonases (PGs) by expressing PG-inhibiting proteins (PGIPs). PGs and PGIPs belong to multi-gene families believed to have been shaped by an evolutionary arms race. The mustard leaf beetle Phaedon cochleariae expresses both active PGs and catalytically inactive PG pseudoenzymes. Previous studies demonstrated that (i) PGIPs target beetle PGs and (ii) the role of PG pseudoenzymes remains elusive, despite having been linked to the pectin degradation pathway. For further insight into the interaction between plant PGIPs and beetle PG family members, we combined affinity purification with proteomics and gene expression analyses, and identified novel inhibitors of beetle PGs from Chinese cabbage (Brassica rapa ssp. pekinensis). A beetle PG pseudoenzyme was not targeted by PGIPs, but instead interacted with PGIP-like proteins. Phylogenetic analysis revealed that PGIP-like proteins clustered apart from “classical” PGIPs but together with proteins, which have been involved in developmental processes. Our results indicate that PGIP-like proteins represent not only interesting novel PG inhibitor candidates in addition to “classical” PGIPs, but also fascinating new players in the arms race between herbivorous beetles and plant defenses.

High-quality chromosome-level scaffolds of the plant bug Pachypeltis micranthus provide insights into the availability of Mikania micrantha control

“…PG has been widely described in fungi, bacteria, nematodes, and plants [ 102 ]. In insects, PGs have been reported in many orders with piercing-sucking and chewing mouthparts, beetles (Coleoptera, mainly of the Phytophaga clade) are included and notably common in mirid bugs (Hemiptera) [ 103 – 105 ]. Mirid PGs can cause much larger lesions than superficial mechanical damage or feeding by other sap-sucking insects [ 102 ].…”

Unraveling the genomic reorganization of polygalacturonase-inhibiting proteins in chickpea

“…However, PGIPs from V. radiata, VrPGIP1, and VrPGIP2 ( Kaewwongwal et al, 2017 ; Zhang et al, 2021 ) and Brassica rapa ssp. pekinensis BrPGIPs ( Haeger et al, 2021 ) have shown to inhibit insects and P. sativum PsPGIP inhibited nematodes ( Veronico et al, 2011 ).…”

A plant mechanism of hijacking pathogen virulence factors to trigger innate immunity

“…Pathogens secret various cell wall-degrading enzymes (CWDEs), such as polygalacturonases, to depolymerize cell wall polysaccharides and subsequently compromise cell wall integrity (1). Polygalacturonases are produced by various pathogens, and their involvement in pathogenesis has been wellestablished (2)(3)(4)(5)(6). Pathogenic and certain plant-derived polygalacturonases belong to endo-glycoside hydrolase 28 family (endopolygalacturonases).…”