The sequenced genomes of nonflowering land plants reveal the innovative evolutionary history of peptide signaling

Abstract

An understanding of land plant evolution is a prerequisite for in-depth knowledge of plant biology. Here we 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 transformations that must have required innovations in cell-to-cell communication. We discuss peptides mediating endogenous and exogenous changes by interaction with receptors activating intracellular molecular signaling. Signaling peptides were discovered in angiosperms and operate in tissues and organs such as flowers, seeds, vasculature, and 3D meristems that are not universally conserved across land plants. Nevertheless, orthologs of angiosperm peptides and receptors have been identified in non-angiosperms. These discoveries provoke questions regarding co-evolution of ligands and their receptors, and whether de novo interactions in peptide signaling pathways may have contributed to generate novel traits in land plants. The answers to such questions will have profound implications for the understanding of the evolution of cell-to-cell communication and the wealth of diversified terrestrial plants. Under this perspective we have generated, analyzed, and reviewed phylogenetic, genomic, structural, and functional data to elucidate the evolution of peptide signaling.

The RGF/GLV/CLEL Family of Short Peptides Evolved Through Lineage-Specific Losses and Diversification and Yet Conserves Its Signaling Role Between Vascular Plants and Bryophytes

“…Searches in the hornwort transcriptomes did not find any RGF-like sequences. Taken together with the previous reports, in which RGF was not identified in the sequenced four genomes of Anthoceros species (Li et al, 2020;Zhang J. et al, 2020;Furumizu et al, 2021), these data suggest that during the hornwort evolution, RGF was possibly lost before extant lineages diversified (Figure 3). It is still yet possible that the low to zero abundance in the transcriptome data did not allow us to identify hornwort RGFs in this study.…”

“…The fifth and ninth P as well as the eighth histidine (H) residues are also highly conserved ( Figure 1A ). All these residues are conserved in the RGF-like sequence found in a liverwort, M. polymorpha , MpRGF ( Furumizu et al, 2021 ; Figure 1A ). A notable difference is the twelfth residue, which is either H or N in AtRGFs but is serine (S) in MpRGF, pointing to RGF sequence diversification between two evolutionary distant lineages.…”

“…Initial BLAST (Basic Local Alignment Search Tool) queries were assembled based on the previously published RGF-like sequences ( Furumizu et al, 2021 ) and used to set up BLASTP or tBLASTn searches. The finalized query file is available as Supplementary Data Sheet 1 .…”

“…These limit our view on how this peptide signaling pathway evolved to play their roles as known today. Meanwhile, increasing availability of complete genome sequences enabled larger-scale bioinformatics analyses and led to the identification of RGF homolog in another vascular plant lineage, ferns ( Furumizu et al, 2021 ). An RGF-like sequence was also found in a non-vascular plant, Marchantia polymorpha (designated as MpRGF for R OOT GROWTH FACTOR/ G OLVEN/CLE-Like- F LAVORED) ( Furumizu et al, 2021 ).…”

“…Meanwhile, increasing availability of complete genome sequences enabled larger-scale bioinformatics analyses and led to the identification of RGF homolog in another vascular plant lineage, ferns ( Furumizu et al, 2021 ). An RGF-like sequence was also found in a non-vascular plant, Marchantia polymorpha (designated as MpRGF for R OOT GROWTH FACTOR/ G OLVEN/CLE-Like- F LAVORED) ( Furumizu et al, 2021 ). These discoveries open up opportunities for studying RGF signaling pathways in different developmental or evolutionary settings.…”