The liverwort Marchantia polymorpha has been utilized as a model for biological studies since the 18th century. In the past few decades, there has been a Renaissance in its utilization in genomic and genetic approaches to investigating physiological, developmental, and evolutionary aspects of land plant biology. The reasons for its adoption are similar to those of other genetic models, e.g. simple cultivation, ready access via its worldwide distribution, ease of crossing, facile genetics, and more recently, efficient transformation, genome editing, and genomic resources. The haploid gametophyte dominant life cycle of M. polymorpha is conducive to forward genetic approaches. The lack of ancient whole-genome duplications within liverworts facilitates reverse genetic approaches, and possibly related to this genomic stability, liverworts possess sex chromosomes that evolved in the ancestral liverwort. As a representative of one of the three bryophyte lineages, its phylogenetic position allows comparative approaches to provide insights into ancestral land plants. Given the karyotype and genome stability within liverworts, the resources developed for M. polymorpha have facilitated the development of related species as models for biological processes lacking in M. polymorpha.

The liverwort Marchantia polymorpha is equipped with a wide range of molecular and genetic tools and resources that have led to its wide use to explore the evo-devo aspects of land plants. Although its diverse transcriptome data are rapidly accumulating, there is no extensive yet user-friendly tool to exploit such a compilation of data and to summarize results with the latest annotations. Here, we have developed a web-based suite of tools, MarpolBase Expression (MBEX, https://marchantia.info/mbex/), where users can visualize gene expression profiles, identify differentially expressed genes, perform co-expression and functional enrichment analyses and summarize their comprehensive output in various portable formats. Using oil body biogenesis as an example, we demonstrated that the results generated by MBEX were consistent with the published experimental evidence and also revealed a novel transcriptional network in this process. MBEX should facilitate the exploration and discovery of the genetic and functional networks behind various biological processes in M. polymorpha and promote our understanding of the evolution of land plants.

Summary: Transcription factors (TFs) are key components of the transcriptional regulation machinery. In plants, they accompanied the evolution from unicellular aquatic algae to complex flowering plants that dominate the land environment. The adaptations of the body plan and physiological responses required changes in the biological functions of TFs. Some ancestral gene regulatory networks are highly conserved, while others evolved more recently and only exist in particular lineages. The recent emergence of novel model organisms provided the opportunity for comparative studies, producing new insights to infer these evolutionary trajectories. In this review, we comprehensively revisit the recent literature on TFs of nonseed plants and algae, focusing on the molecular mechanisms driving their functional evolution. We discuss the particular contribution of changes in DNA‐binding specificity, protein–protein interactions and cis‐regulatory elements to gene regulatory networks. Current advances have shown that these evolutionary processes were shaped by changes in TF expression pattern, not through great innovation in TF protein sequences. We propose that the role of TFs associated with environmental and developmental regulation was unevenly conserved during land plant evolution.

We performed differential gene expression (DGE) and co-expression analyses with genes encoding components of hormonal signaling pathways and the ∼400 annotated transcription factors (TFs) of M. polymorpha across multiple developmental stages of the life cycle. We identify a putative auxin-related co-expression module that has significant overlap with transcripts induced in auxin-treated tissues. Consistent with phylogenetic and functional studies, the class C ARF, MpARF3, is not part of the auxin-related co-expression module and instead is associated with transcripts enriched in gamete-producing gametangiophores. We analyze the Mparf3 and MpmiR160 mutant transcriptomes in the context of coexpression to suggest that MpARF3 may antagonize the reproductive transition via activating the MpMIR11671 and MpMIR529c precursors whose encoded microRNAs target SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) transcripts of MpSPL1 and MpSPL2. Both MpSPL genes are part of the MpARF3 co-expression group corroborating their functional significance. We provide evidence of the independence of MpARF3 from the auxin-signaling module and provide new testable hypotheses on the role of auxin-related genes in patterning meristems and differentiation events in liverworts.

Summary: Plant transition to land required several regulatory adaptations. The mechanisms behind these changes remain unknown. Since the evolution of transcription factors (TFs) families accompanied this transition, we studied the HOMEODOMAIN LEUCINE ZIPPER (HDZ) TF family known to control key developmental and environmental responses. We performed a phylogenetic and bioinformatics analysis of HDZ genes using transcriptomic and genomic datasets from a wide range of Viridiplantae species. We found evidence for the existence of HDZ genes in chlorophytes and early‐divergent charophytes identifying several HDZ members belonging to the four known classes (I–IV). Furthermore, we inferred a progressive incorporation of auxiliary motifs. Interestingly, most of the structural features were already present in ancient lineages. Our phylogenetic analysis inferred that the origin of classes I, III, and IV is monophyletic in land plants in respect to charophytes. However, class IIHDZ genes have two conserved lineages in charophytes and mosses that differ in the CPSCE motif. Our results indicate that the HDZ family was already present in green algae. Later, the HDZ family expanded accompanying critical plant traits. Once on land, the HDZ family experienced multiple duplication events that promoted fundamental neo‐ and subfunctionalizations for terrestrial life.