Multiple horizontal gene transfer events have shaped plant glycosyl hydrolase diversity and function

Abstract

Summary Plant glycosyl hydrolases (GHs) play a crucial role in selectively breaking down carbohydrates and glycoconjugates during various cellular processes, such as reserve mobilization, pathogen defense, and modification/disassembly of the cell wall. In this study, we examined the distribution of GH genes in the Archaeplastida supergroup, which encompasses red algae, glaucophytes, and green plants. We identified that the GH repertoire expanded from a few tens of genes in early archaeplastidians to over 400 genes in modern angiosperms, spanning 40 GH families in land plants. Our findings reveal that major evolutionary transitions were accompanied by significant changes in the GH repertoire. Specifically, we identified at least 23 GH families acquired by green plants through multiple horizontal gene transfer events, primarily from bacteria and fungi. We found a significant shift in the subcellular localization of GH activity during green plant evolution, with a marked increase in extracellular‐targeted GH proteins associated with the diversification of plant cell wall polysaccharides and defense mechanisms against pathogens. In conclusion, our study sheds light on the macroevolutionary processes that have shaped the GH repertoire in plants, highlighting the acquisition of GH families through horizontal transfer and the role of GHs in plant adaptation and defense mechanisms.

Horizontally transferred glycoside hydrolase 26 may aid hemipteran insects in plant tissue digestion

“…There are over 150 known families of glycoside hydrolases, and there is a wide range of substrate specificity across the families (Garron and Henrissat, 2019; Henrissat, 1991). Glycoside hydrolases are important metabolizers in plants, as complex carbohydrates make up a substantial portion of the plant cell wall, so many glycoside hydrolases are necessary for normal plant growth and elongation (Kfoury et al, 2024; Nazipova et al, 2022). Alternatively, glycoside hydrolases encoded in the genomes of other organisms can be used to break down plant cell walls and access nutrients inside plant cells (He et al, 2022; Rafiei et al, 2021).…”

“…There have been many instances of glycoside hydrolase genes being incorporated into the genomes of insects, fungi, and plants via HGT (Acuña et al, 2012; Da Lage et al, 2013; Kfoury et al, 2024; Kirsch et al, 2014; Pauchet and Heckel, 2013; Shelomi et al, 2014; Shen et al, 2003; Shin et al, 2023; Wheeler et al, 2013; Wybouw et al, 2016). In this study, we characterize an HGT event of a gene encoding for a glycoside hydrolase family 26 (GH26) protein, which are enzymes that break down carbohydrates present in plant cell walls, specifically mannans and galactomannans (Braithwaite et al, 1995; Gao et al, 2023; Patel et al, 2016; Zhang et al, 2014).…”