Cryogenian Origin and Subsequent Diversification of the Plant Cell-Wall Enzyme XTH Family

Abstract

All land plants encode large multigene families of xyloglucan endotransglucosylase/hydrolases (XTHs), plant-specific enzymes that cleave and reconnect plant cell-wall polysaccharides. Despite the ubiquity of these enzymes, considerable uncertainty remains regarding the evolutionary history of the XTH family. Phylogenomic and comparative analyses in this study traced the non-plant origins of the XTH family to Alphaproteobacteria ExoKs, bacterial enzymes involved in loosening biofilms, rather than Firmicutes licheninases, plant biomass digesting enzymes, as previously supposed. The relevant horizontal gene transfer (HGT) event was mapped to the divergence of non-swimming charophycean algae in the Cryogenian geological period. This HGT event was the likely origin of charophycean EG16-2s, which are putative intermediates between ExoKs and XTHs. Another HGT event in the Cryogenian may have led from EG16-2s or ExoKs to fungal CRHs, enzymes that cleave and reconnect chitin and glucans in fungal cell walls. This successive transfer of enzyme-encoding genes may have supported the adaptation of plants and fungi to the ancient icy environment by facilitating their sessile lifestyles. Furthermore, several protein evolutionary steps, including coevolution of substrate-interacting residues and putative intra-family gene fusion, occurred in the land plant lineage and drove diversification of the XTH family. At least some of those events correlated with the evolutionary gain of broader substrate specificities, which may have underpinned the expansion of the XTH family by enhancing duplicated gene survival. Together, this study highlights the Precambrian evolution of life and the mode of multigene family expansion in the evolutionary history of the XTH family.

Cryogenian Glacial Habitats as a Plant Terrestrialisation Cradle – The Origin of the Anydrophytes and Zygnematophyceae Split

“…The new time-calibrated phylogenies based on the Viridiplantae ( Su et al, 2021 ) and Eukaryota ( Strassert et al, 2021 ) suggest a likely Cryogenian origin of anydrophytes as well as the split of Zygnematophyceae. This dating was indicated very recently by Shinohara and Nishitani (2021) for Zygnematophyceae and acknowledged as a possibility by Lutzoni et al (2018) and Jiao et al (2020) .…”

“…A fascinating example of the possible convergent evolution of cell wall dynamics regulating xyloglucan endotransglucosylase/hydrolases (XTHs) and related enzymes between Zygnematophyceae and zygomycetous fungi in Cryogenian was shown recently by Shinohara and Nishitani (2021) . Using comparative phylogenomic analyses, they traced the non-plant origins of the XTH family to Alphaproteobacteria, pre-XTH enzymes were integrated into zygnematophycean algae in the Cryogenian via the likely HGT.…”

“…The origin of anydrophytes (and later also the Zygnematophyceae) was linked to several crucial horizontal gene transfers (HGTs)–facilitated by the co-existence of streptophyte algae with different kinds of microbes and fungi on the surfaces of land ( Lutzoni et al, 2018 ; Chen R. et al, 2021 ; Shinohara and Nishitani, 2021 ). Three TF families (GRAS, HDKNOX2, and BBR/BPC), a homolog of the PYR/PYL/RCAR-like ABA receptor and genes involved in 1,4 b-xylan formation (GUX1–5, PARVUS) and galactan/RG I pectin synthesis (GALS1-3), were likely gained in the common anydrophyte ancestor of Zygnematophyceae and Embryophyta ( Cheng et al, 2019 ).…”

“…It is important to note that cryptophytes sensu Edwards ( Edwards et al, 2014 ) are extinct plants producing cryptospores, not to be confused with Cryptophyceae algae. Therefore the very first adaptations of Streptophyta to the dry land occurred much earlier, most probably in the Precambrian ( Hedges et al, 2018 ; Servais et al, 2019 ; Shinohara and Nishitani, 2021 ; Strassert et al, 2021 ; Su et al, 2021 ). The first Silurian flora documented by macrofossils (e.g., Cooksonia, Baragwanathia) suggests an undocumented evolution and diversification of land plants preceding the earliest known fossils ( Pšenička et al, 2021 ).…”

Thidiazuron Promotes Leaf Abscission by Regulating the Crosstalk Complexities between Ethylene, Auxin, and Cytokinin in Cotton

“…During phase three of the abscission process, xyloglucan endotransglucosylase hydrolase (XTH), polygalacturonase (PG), cellulase, pectinesterase, endoglucosidase, ribonuclease, expansin (EXP), and so on, participate in the degradation process of the abscission layer cells [ 10 , 11 ]. XTH is involved in the establishment of the cell wall [ 12 ]. Cellulase participates in the degradation of the cell wall by hydrolyzing cellulose.…”