Pectin digestion in herbivorous beetles: Impact of pseudoenzymes exceeds that of their active counterparts

Abstract

Many protein families harbor pseudoenzymes that have lost the catalytic function of their enzymatically active counterparts. Assigning alternative function and importance to these proteins is challenging [1]. Because the evolution towards pseudoenzymes is driven by gene duplication, they often accumulate in multigene families. Plant cell wall-degrading enzymes (PCWDEs) are prominent examples of expanded gene families. The pectolytic glycoside hydrolase family 28 (GH28) allows herbivorous insects to break down the PCW polysaccharide pectin. GH28 in the Phytophaga clade of beetles contains many active enzymes but also many inactive counterparts. Using functional characterization, gene silencing, global transcriptome analyses and recordings of life history traits, we found that not only catalytically active but also inactive GH28 proteins are part of the same pectin-digesting pathway. The robustness and plasticity of this pathway and thus its importance for the beetle is supported by extremely high steady-state expression levels and counter-regulatory mechanisms. Unexpectedly, the impact of pseudoenzymes on the pectin-digesting pathway in Phytophaga beetles exceeds even the influence of their active counterparts, such as a lowered efficiency of food-to-energy conversion and a prolongation of the developmental period.

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

“…Therefore, PGIP composition seems to affect the gene expression level of GH28s encoding active PG enzymes as well as inactive PG pseudoenzymes. This work on the PGIP composition of the food plant further supports previous data, indicating that these pseudoenzymes, despite being catalytically inactive, nonetheless contribute somehow to pectin digestion in leaf beetles (Kirsch et al, 2019).…”

“…GH28‐1 is a highly expressed, active PG enzyme in P . cochleariae, and its silencing considerably reduces gut PG activity (Kirsch et al, 2014; Kirsch, Kunert, Vogel, & Pauchet, 2019). Although GH28‐1 was expressed more highly in larvae that fed on wt plants, PG activity was the same or even lower compared with larvae that fed on AtPGIP mutants.…”