Origins and Stepwise Expansion of R2R3-MYB Transcription Factors for the Terrestrial Adaptation of Plants

Abstract

The R2R3-MYB transcription factors play critical roles in various processes in embryophytes (land plants). Here, we identified genes encoding R2R3-MYB proteins from rhodophytes, glaucophytes, Chromista, chlorophytes, charophytes, and embryophytes. We classified the R2R3-MYB genes into three subgroups (I, II, and III) based on their evolutionary history and gene structure. The subgroup I is the most ancient group that includes members from all plant lineages. The subgroup II was formed before the divergence of charophytes and embryophytes. The subgroup III genes form a monophyletic group and only comprise members from land plants with conserved exon–intron structure. Each subgroup was further divided into multiple clades. The subgroup I can be divided into I-A, I-B, I-C, and I-D. The I-A, I-B, and I-C are the most basal clades that have originated before the divergence of Archaeplastida. The I-D with the II and III subgroups form a monophyletic group, containing only green plants. The II and III subgroups form another monophyletic group with Streptophyta only. Once on land, the subgroup III genes have experienced two rounds of major expansions. The first round occurred before the origin of land plants, and the second round occurred after the divergence of land plants. Due to significant gene expansion, the subgroup III genes have become the predominant group of R2R3-MYBs in land plants. The highly unbalanced pattern of birth and death evolution of R2R3-MYB genes indicates their important roles in the successful adaptation and massive radiation of land plants to occupy a multitude of terrestrial environments.

Genome-Wide Comparative Analysis of R2R3 MYB Gene Family in Populus and Salix and Identification of Male Flower Bud Development-Related Genes

“…Therefore, the comparative analysis of the important gene families of the poplar and willow is helpful to identify the retention and loss of key gene family members after the differentiation of the two species. The MYB transcription factor superfamily is one of the largest gene families in plants, and R2R3 MYB transcription factors participate in plant cell differentiation, growth, metabolism, and various stress responses ( Millard et al, 2019a ; Chang et al, 2020 ). Through comparative analysis of the R2R3 MYB transcription factor family in the poplar and willow, it was found that they have both retained most of the gene members of the ancestral species.…”

Evolution and functional diversification of R2R3-MYB transcription factors in plants

“…Third, the genome sequences for Marchantia polymorpha [ 59 ] and M. viride [ 51 ] have enabled the development of a macroscopic classification regime, resulting in three clades of R2R3-MYBs that correspond to their biological functions. Each clade is correlated with different functions associated with essential developmental processes, from the basic life cycle to specialized metabolism and organismal complexity, corresponding to a very recent classification in 2020 [ 60 ]. In that study, genes encoding R2R3-MYBs from Rhodophytes, Glaucophytes, Chromista, Chlorophytes, Charophytes, and Embryophytes were divided into three major clades (I, II, and III) (named subgroups in the original paper).…”

“…In that study, genes encoding R2R3-MYBs from Rhodophytes, Glaucophytes, Chromista, Chlorophytes, Charophytes, and Embryophytes were divided into three major clades (I, II, and III) (named subgroups in the original paper). Subgroup I is the most ancient group and includes members from all plant lineages, whereas subgroup III has become predominant in land plants [ 60 ]. The former two classification schemes share overlaps and are based on domain conservation, whereas this final classification system provides a macroscopic perspective based on broad evolutionary patterns.…”

“…basic helix–loop–helix proteins (bHLHs) [ 68 ], MADS-Box [ 69 ], and GRAS [ 70 ], we propose an improved nomenclature system from superfamily (MYB) and family (R2R3-MYB) to subfamily. “Subgroup” used by Chang and colleagues should be revised to evolutionary clade/group [ 60 ]. To avoid confusion, in the following sections, we uniformly refer to the lower classifications within the gene family as subfamilies (abbreviated as S1, S2, etc.).…”

“…from algae to land plants), resulting in a gradual increase in number together with an increase in organismal complexity. Accordingly, the number of genes in this family in land plants is large, showing a huge expansion after the divergence of angiosperms from other vascular plants [ 10 , 60 ]. For example, only eight R2R3-MYBs were detected in the single-celled chlorophyte Chlamydomonas reinhardtii , whereas up to 429 R2R3-MYBs were observed in the allotetraploid Brassica napus [ 18 ] ( Fig.…”