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.
Highlights
As plants are restricted in their mobility, they have evolved sophisticated strategies to adapt to their constantly changing environment
In an unbiased interaction assay, we aimed to first, identify new putative PG inhibitors for beetle PGs and second, test if catalytically inactive pseudoenzymes are still targeted by PG-inhibiting proteins (PGIPs)
We isolated Cell Wall Proteins (CWPs) from B. rapa ssp. pekinensis and, using LC-MS/MS and bioinformatic tools, confirmed that this cell wall proteome correlated with proteomes from previous studies (Ligat et al, 2011; Albenne et al, 2013; Calderan-Rodrigues et al, 2019), making it suitable starting material for our interaction assay (Supplementary Table 4 and Supplementary Figure 3)
Summary
As plants are restricted in their mobility, they have evolved sophisticated strategies to adapt to their constantly changing environment. They contribute to strengthening the mechanical barriers through protein agglutination or crosslinking to cell wall components (Rashid, 2016). Chitinases possess antifungal activity by cleaving fungal cell wall components (Kumar et al, 2018), and lectins impair carbohydrate structures in the insect gut, which has detrimental consequences for the herbivore (Vandenborre et al, 2011). Plants overexpressing inhibitors targeting α-amylases were more resistant than the wild-type plants and drastically decreased the survival of several beetle species (Kaur et al, 2014). Enzymes macerating the plant cell wall are versatile, and inhibiting them enhanced plant resistance to various pathogens (Kalunke et al, 2015; Ma et al, 2017)
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