The Sequenced Genomes of Non-Flowering Land Plants Reveal the (R)Evolutionary History of Peptide Signaling

Abstract

An understanding of land plant evolution is a prerequisite for in-depth knowledge of plant biology. Here we illustrate how to extract and explore information hidden in the increasing number of sequenced plant genomes, from bryophytes to angiosperms, to elucidate a specific biological question – how peptide signaling evolved. To conquer land and cope with changing environmental conditions, plants have gone through profound transformations that must have required a revolution in cell-to-cell communication. Peptides can act as signals of endogenous and exogenous changes, and interactions with leucine-rich repeat receptor-like kinases activate intracellular molecular signaling. Signaling peptides are typically active in organs like flowers and seeds, vascular tissue, root and shoot meristems, which are absent in the most primitive land plants. However, putative orthologues for several peptide-receptor pairs have been identified in non-seed land plants. These discoveries and elucidation of co-evolution of such ligands and their receptors, have profound implications for the understanding of evolution and diversity of cell-to-cell communication, as de novo interactions in peptide signaling pathways may have contributed to generate novel traits in land plants. Phylogenetic analyses, genomic, structural and functional data can guide us to reveal evolutionary steps that laid the foundation for a wealth of diversified terrestrial plants.

Land plant peptide signaling: What we know—and don't know—about its evolution

“…In bryophytes, while the RGF peptide family is highly conserved in liverworts, RGF‐like sequences are found only in early‐diverging lineages in mosses and are absent in P. patens and the hornwort species that have been examined. Consistently, RGF receptor homologs are present in M. polymorpha but absent in P. patens and A. agrestis , supporting the hypothesis that bryophyte RGF peptides signal through homologs of known RGF receptors (Furumizu et al, 2021). The effect of heterologous expression of M. polymorpha RGF in A. thaliana suggested that signaling activities are conserved in the liverwort RGF (Furumizu and Sawa, 2021b).…”

“…The effect of heterologous expression of M. polymorpha RGF in A. thaliana suggested that T A B L E 1 Representative PTMP sequences and the number of genes encoding PTMPs. (Whitford et al, 2012); 20, (Gully et al, 2019); 21, (Hou et al, 2021); 22, (Furumizu et al, 2021); 23, ; 24, (Zhang et al, 2020a); 25, (Whitewoods et al, 2018); and 26, (Bowman et al, 2017). *The following Arabidopsis thaliana sequences are shown: CEP1 (At1g47485), CIF1 (At2g16385), CLE9 (At1g26600), CLE41 (At3g24770), CTNIP1 (At1g06135), IDA (At1g68765), PEP1 (At5g64900), PIPL3/TOLS2 (At4g37295), PSK1 (At1g13590), PSY1 (At5g58650), RGF1 (At5g60810), SCOOP1 (At5g44565).…”

“…In answering the second question, the IDA family peptides are widely conserved beyond seed plants and thus are strong candidates for the ligands. Notably, in the moss P. patens , IDA‐like peptides were not found, but LRR‐RLKs homologous to the HAE clade receptors are present (Figure 1A) (Bowman et al, 2017; Furumizu et al, 2021). It is both important and interesting to characterize the moss HAE‐like LRR‐RLKs and identify their ligands.…”

TPST-dependent and -independent regulation of root development and signaling by PSK LRR receptor kinases in Arabidopsis

“…In case that a receptor and a ligand did not strictly co-evolve, it is conceivable that residual ligand-independent receptor signaling is retained. It is conceivable that ligand and PSK receptors evolved independently early in land plant evolution and that residual ligand-independent signaling was retained (Furumizu et al , 2020). A recently characterized temperature-sensitive mutation in the FERONIA (FER) receptor that recognizes rapid alkalinization factor (RALF), is point-mutated in a conserved Gly outside the ligand binding site in ectodomain of the receptor (Kim et al , 2021).…”

Rhizobiales commensal bacteria promoteArabidopsis thalianaroot growth via host sulfated peptide pathway

“…This suggests the presence of unidentified cognate receptors or yet another class of sulfated peptides. Receptors for extracellular peptides are typically a member of the leucine-rich repeat receptor-like kinase (LRR-RLK) superfamily, which has been immensely diversified in land plant lineages (Shiu et al, 2004;Furumizu et al, 2021). To date, only a handful of LRR-RLKs have been functionally characterized, while the physiological function of many members, including their cognate ligands, remain unknown.…”