Land Plant Evolution Research Articles

Does integument arise de novo or from pre-existing structures? ── Insights from the key regulatory genes controlling integument development.

The origin of seeds is one of the key innovations in land plant evolution. Ovules are the developmental precursors of seeds. The integument is the envelope structure surrounding the nucellus within the ovule and developing into the seed coat when ovules mature upon fertilization. The question of whether the integument arise de novo or evolve from elaboration of pre-existing structures has caused much debate. By exploring the origin and evolution of the key regulatory genes controlling integument development and their functions during both individual and historical developmental processes, we showed the widespread presence of the homologs of ANT, CUC, BEL1, SPL, C3HDZ, INO, ATS, and ETT in seedless plant genomes. All of these genes have undergone duplication-divergence events in their evolutionary history, with most of the descendant paralogous suffering motif gain and/or loss in the coding regions. Expression and functional characterization have shown that these genes are key components of the genetic program that patterns leaf-like lateral organs. Serial homology can thus be postulated between integuments and other lateral organs in terms of the shared master regulatory genes. Given that the genetic program patterning leaf-like lateral organs formed in seedless plants, and was reused during seed origin, the integument is unlikely to arise de novo but evolved from the stem segment-specific modification of pre-existing serially homologous structures. The master 'switches' trigging the modification to specify the integument identity remain unclear. We propose a successive transformation model of integument origin.

Horizontally acquired fungal killer protein genes affect cell development in mosses.

The moss Physcomitrium patens is crucial for studying plant development and evolution. Although the P. patens genome includes genes acquired from bacteria, fungi and viruses, the functions and evolutionary significance of these acquired genes remain largely unclear. Killer protein 4 (KP4) is a toxin secreted by the phytopathogenic fungus Ustilago maydis that inhibits the growth of sensitive target strains by blocking their calcium uptake. Here, we show that KP4 genes in mosses were acquired from fungi through at least three independent events of horizontal gene transfer. Two paralogous copies of KP4 (PpKP4-1 and PpKP4-2) exist in P. patens. Knockout mutants ppkp4-1 and ppkp4-2 showed cell death at the protonemal stage, and ppkp4-2 also exhibited defects in tip growth. We provide experimental evidence indicating that PpKP4-1/2 affects P. patens protonemal cell development by mediating cytoplasmic calcium and that KP4 genes are functionally conserved between P. patens and fungi. The present study provides additional insights into the role of horizontal gene transfer in land plant development and evolution.

Horizontal gene transfer: Driving the evolution and adaptation of plants.

Horizontal gene transfer greatly contributes to the diversification and long-term evolution of green plants. Recent studies suggest that horizontal gene transfer events drove the evolution and adaptation of charophyte green algae and land plants.

Plant (di)terpenoid evolution: from pigments to hormones and beyond.

Covering: up to 2014-2022.Diterpenoid biosynthesis in plants builds on the necessary production of (E,E,E)-geranylgeranyl diphosphate (GGPP) for photosynthetic pigment production, with diterpenoid biosynthesis arising very early in land plant evolution, enabling stockpiling of the extensive arsenal of (di)terpenoid natural products currently observed in this kingdom. This review will build upon that previously published in the Annual Review of Plant Biology, with a stronger focus on enzyme structure-function relationships, as well as additional insights into the evolution of (di)terpenoid metabolism since generated.

Phylogenetic, Structural and Functional Evolution of the LHC Gene Family in Plant Species.

Light-harvesting chlorophyll a/b-binding (LHC) superfamily proteins play a vital role in photosynthesis. Although the physiological and biochemical functions of LHC genes have been well-characterized, the structural evolution and functional differentiation of the products need to be further studied. In this paper, we report the genome-wide identification and phylogenetic analysis of LHC genes in photosynthetic organisms. A total of 1222 non-redundant members of the LHC family were identified from 42 species. According to the phylogenetic clustering of their homologues with Arabidopsis thaliana, they can be divided into four subfamilies. In the subsequent evolution of land plants, a whole-genome replication (WGD) event was the driving force for the evolution and expansion of the LHC superfamily, with its copy numbers rapidly increasing in angiosperms. The selection pressure of photosystem II sub-unit S (PsbS) and ferrochelatase (FCII) families were higher than other subfamilies. In addition, the transcriptional expression profiles of LHC gene family members in different tissues and their expression patterns under exogenous abiotic stress conditions significantly differed, and the LHC genes are highly expressed in mature leaves, which is consistent with the conclusion that LHC is mainly involved in the capture and transmission of light energy in photosynthesis. According to the expression pattern and copy number of LHC genes in land plants, we propose different evolutionary trajectories in this gene family. This study provides a basis for understanding the molecular evolutionary characteristics and evolution patterns of plant LHCs.

An Overview of Molecular Basis and Genetic Modification of Floral Organs Genes: Impact of Next-Generation Sequencing.

In plant development, flowering is the most widely studied process. Floral forms show large diversity in different species due to simple variations in basic architecture. To determine the floral gene expression during the past decade, MADS-box genes have identified as key regulators in both reproductive and vegetative plant development. Traditional genetics and functional genomics tools are now available to elucidate the expression and function of this complex gene family on a much larger scale. Moreover, comparative analysis of the MADS-box genes in diverse flowering and non-flowering plants, boosted by various molecular technologies such as ChIP and next-generation DNA sequencing, contributes to our understanding of how this important gene family has expanded during the evolution of land plants. Likewise, the big data analysis revealed combined activity of transcriptional regulators and floral organ identity factors regulate the flower developmental programs. Thus, with the help of cutting-edge technologies like RNA-Sequencing, sex determination is now better understood in few non-model plants Therefore, the recent advances in next-generation sequencing (NGS) should enable researchers to identify the full range of floral gene functions, which will significantly help to understand plant development and evolution. This review summarizes the floral homeotic genes in model and non-model species to understand the flower development genes and dioecy evolution.

Paleozoic vegetation increased fine sediment in fluvial and tidal channels: Evidence from secular changes to the mudrock content of ancient point bars

Abstract The amount of mudrock preserved globally in alluvium increased in stratigraphic synchrony with the Paleozoic evolution of land plants. This observation has been explained by vegetation promoting both the retention of mud through baffling, stabilization, and flocculation, and the production of mud through chemical weathering. However, the latter explanation has been challenged on the basis that it is perceived to require imbalance in the long-term global carbon cycle. We present a compendium of empirical evidence that is supportive of increased global fine sediment supply, and thus the contention that land plants did, in fact, promote the production of mud on the continents. We refine previous broad-brush analyses of Paleozoic mudrock content by specifically tracking shifts in the mudrock content of regions of alluvial and tidal landscapes that remained locally unvegetated even after the greening of the continents, namely inclined heterolithic stratification (IHS) that records submerged in-channel bars. We show that the Paleozoic mudrock increase was pronounced even within these areas, away from any biomechanical binding and baffling effects of plants. Precambrian and Cambrian IHS are composed almost exclusively of sandstone, whereas Silurian through to Carboniferous examples show a steady increase in total mudrock content. This progressive rise in the mudrock component of channel bars cannot alone be explained by physical retention of mud by vegetation and requires heightened fine sediment concentrations from the hinterland, which suggests that plants increased the volume of mud available at source. The muddying of Earth’s preserved IHS serves as a proxy that suggests evolving Paleozoic land plants triggered a global increase in the production and supply of fine-grained sediment.

Horizontal gene transfer and the evolution of land plants.

Horizontal gene transfer (HGT) is the transfer of genetic material between organisms. It has been known for some time that HGT in eukaryotes is not a rare phenomenon. A recent study by Ma et al. has shown that HGT has played a crucial role in shaping the evolution of land plants.

A potential role of salicylic acid in the evolutionary behavior of Trichoderma as a plant pathogen: from Marchantia polymorpha to Arabidopsis thaliana

Main conclusionRecognition of the interaction of Trichoderma during the evolution of land plants plays a potential key role in the development of the salicylic acid defense pathway and the establishment of a mutualistic relationship.Marchantia polymorpha is a common liverwort considered in recent years as a model plant for evolutionary studies on plant–microorganism interactions. Despite the lack of research, remarkable results have been reported regarding the understanding of metabolic and evolutionary processes of beneficial and/or harmful interactions, owing to a better understanding of the origin and evolution of different plant defense pathways. In this study, we have carried out work on the direct and indirect interactions (exudates and volatiles) of M. polymorpha with different species of the fungal genus Trichoderma. These interactions showed different outcomes, including resistance or even growth promotion and disease. We have analyzed the level of tissue colonization and defense-related gene expression. Furthermore, we have used the pteridophyte Dryopteris affinis and the angiosperm Arabidopsis thaliana, as subsequent steps in plant evolution, together with the plant pathogen Rhizoctonia solani as a control of plant pathogenicity. Trichoderma virens, T. brevicompactum and T. hamatum are pathogens of M. polymorpha, while exudates of T. asperellum are harmful to the plant. The analysis of the expression of several defense genes in M. polymorpha and A. thaliana showed that there is a correlation of the transcriptional activation of SA-related genes with resistance or susceptibility of M. polymorpha to Trichoderma. Moreover, exogenous SA provides resistance to the virulent Trichoderma species. This beneficial fungus may have had an evolutionary period of interaction with plants in which it behaved as a plant pathogen until plants developed a defense system to limit its colonization through a defense response mediated by SA.

Establishment and optimization of a new model organism to study early land plant evolution: Germination, cultivation and oospore variation of Chara braunii Gmelin, 1826.

For studying land plant evolution, the establishment and optimization of model organisms representing streptophytic algae, sister to land plants, is essential. Long-term cultivation experiments with Chara braunii S276 were performed over 8 years, since 4 years (Nov. 2018) under constant conditions. Additionally, short-term experiments for optimization of culture conditions were performed with three strains of C. braunii (S276, NIES-1604 and Lausiger Teiche, LaT-2708). Germination success after application of sterilization agents, addition of gibberellic acid and under different incubation conditions with respect to pre-treatment, irradiance regime and substrate was investigated in order to develop protocols for generative cultivation of at least unialgal cultures. The resulting cultivation protocols for C. braunii S276, allowing maintenance of vegetative as well as generative cultures are presented in detail, including protocols for germination induction and growth of sterilized and unsterilized oospores.

Nearshore environments before the evolution of land plants

The long-term evolution of the biosphere has caused fundamental shifts in environmental conditions and sedimentation at Earth’s surface. While effects of the evolution of terrestrial vegetation on river systems have been explored in detail, facies models and possible shifts in sedimentation in pre-vegetation nearshore marine settings have not been sufficiently explored. The circa 800-million-year-old Burra Group, exposed in the Adelaide Fold Belt of South Australia, is a terrestrial to nearshore transgressive sedimentary succession associated with rifting. The Burra Group provides a record of marginal and shallow marine environments before the evolution of land plants. Environments are interpreted to record deposition in low energy fine-grained tidal flat, lagoon, tidal inlet, and beach-barrier environments (a beach-barrier system). The thick mudflats (up to 30 m) of the studied units indicate that vegetation is not essential for mudflat accumulation, contrary to some models. The fluvial–marine transition and the back-barrier–tidal inlet–beach-barrier transition is highly regular and there is little interbedding of units. The Tonian beach-barriers of the Burra Group do not backstep into the back-barrier region and aggrade much like stable modern systems backed by peat. These observations are suggestive of a stable barrier system in the absence of land plants. The high mud percentage and/or early carbonate cementation (including microbialite and stromatolite deposition during transgression) may have contributed to the stability of this beach-barrier system.

G protein controls stress readiness by modulating transcriptional and metabolic homeostasis in Arabidopsis thaliana and Marchantia polymorpha

The core G protein signaling module, which consists of Gα and extra-large Gα (XLG) subunits coupled with the Gβγ dimer, is a master regulator of various stress responses. In this study, we compared the basal and salt stress-induced transcriptomic, metabolomic and phenotypic profiles in Gα, Gβ, and XLG-null mutants of two plant species, Arabidopsis thaliana and Marchantia polymorpha, and showed that G protein mediates the shift of transcriptional and metabolic homeostasis to stress readiness status. We demonstrated that such stress readiness serves as an intrinsic protection mechanism against further stressors through enhancing the phenylpropanoid pathway and abscisic acid responses. Furthermore, WRKY transcription factors were identified as key intermediates of G protein-mediated homeostatic shifts. Statistical and mathematical model comparisons between A. thaliana and M. polymorpha revealed evolutionary conservation of transcriptional and metabolic networks over land plant evolution, whereas divergence has occurred in the function of plant-specific atypical XLG subunit. Taken together, our results indicate that the shifts in transcriptional and metabolic homeostasis at least partially act as the mechanisms of G protein-coupled stress responses that are conserved between two distantly related plants.

What Can Zircons Tell Us About the Evolution of Plants?

The versatile mineral could contain evidence of the evolution of land plants and their effect on the sedimentary system.

Genome-wide characterization of C2H2 zinc-finger gene family provides insight into the mechanisms and evolution of the dehydration-rehydration responses in Physcomitrium and Arabidopsis.

Dehydration tolerance is a vital factor for land plant evolution and world agricultural production. Numerous studies enlightened that the plant-specific C2H2-type zinc-finger proteins (C2H2-ZFPs) as master regulators played pivotal roles in the abiotic stress responses of plants. However, a comprehensive understanding of the evolution of C2H2-ZFPs in terrestrial plants and its regulatory mechanism in dehydration and rehydration response remains a mystery. In this study, the genome-wide identification of C2H2-ZFP genes revealed 549 homologs in the representatives of terrestrial plant lineages from liverwort to angiosperms. Based on the characteristics of the conserved C2H2-ZF domains, four major C2H2-ZF types (M-, Z-, Q-, and D-type) were identified in the C2H2-ZFPs, with the dominants of M-type in all selected species and followed by Z-type in non-seed plants and Q-type in seed plants, respectively. Phylogenetic analyses of the identified C2H2-ZFPs supported four major groups in the land plant representatives, among which the members from the desiccation-tolerant Physcomitrium patens and the dehydration-sensitive Arabidopsis thaliana displayed different topological relationships in the phylogenies reconstructed for a single species. C2H2-ZFPs clustered in the same subclades shared similar features in their conserved domains and gene structures. Approximately, 81% of the C2H2-ZFP promoters of all 549 identified C2H2-ZFPs harbored the conserved ABA-responsive elements (ABREs) and/or dehydration-responsive elements (DREs). Comparative transcriptomic analyses showed that 50 PpZFPs and 56 AtZFPs significantly changed their transcripts abundance. Interestingly, most of the dehydration- and rehydration-responsive PpZPFs and AtZFPs had been predicted to contain the ABRE and DRE elements in their promoter regions and with over half of which phylogenetically belonging to group III. The differences in the expression patterns of C2H2-ZFPs in responses to dehydration and rehydration between P. patens and A. thaliana reflected their different strategies to adapt to dehydration. The identified candidate PpZFPs were specifically induced by moderate dehydration and reached the peak transcript abundance in severe dehydration. Our study lays the foundations for further functional investigation of C2H2-ZFPs in dehydration responses from an evolutionary perspective in land plants. The findings will provide us with genetic resources and potential targets for drought tolerance breeding in crops and beyond.

Characterization of the ABC Transporter G Subfamily in Pomegranate and Function Analysis of PgrABCG14.

ATP-binding cassette subfamily G (ABCG) proteins play important roles in plant growth and development by transporting metabolites across cell membranes. To date, the genetic characteristics and potential functions of pomegranate ABCG proteins (PgrABCGs) have remained largely unknown. In this study, we found that 47 PgrABCGs were divided into five groups according to a phylogenetic analysis; groups I, II, III, and IV members are half-size proteins, and group V members are full-size proteins. PgrABCG14, PgrABCG21, and PgrABCG47 were highly expressed in the inner seed coat but had very low expression levels in the outer seed coat, and the expression levels of these three PgrABCG genes in the inner seed coats of hard-seeded pomegranate ‘Dabenzi’ were higher than those of soft-seeded pomegranate ‘Tunisia’. In addition, the expression of these three PgrABCG genes was highly correlated with the expression of genes involved in lignin biosynthesis and hormone signaling pathways. The evolution of PgrABCG14 presents a highly similar trend to the origin and evolution of lignin biosynthesis during land plant evolution. Ectopic expression of PgrABCG14 in Arabidopsis promoted plant growth and lignin accumulation compared to wild type plants; meanwhile, the expression levels of lignin biosynthesis-related genes (CAD5, C4H, and Prx71) and cytokinin response marker genes (ARR5 and ARR15) were significantly upregulated in transgenic plants, which suggests the potential role of PgrABCG14 in promoting plant growth and lignin accumulation. Taken together, these findings not only provide insight into the characteristics and evolution of PgrABCGs, but also shed a light on the potential functions of PgrABCGs in seed hardness development.

The single Marchantia polymorpha FERONIA homolog reveals an ancestral role in regulating cellular expansion and integrity.

Plant cells are surrounded by a cell wall, a rigid structure that is not only important for cell and organ shape, but is also crucial for intercellular communication and interactions with the environment. In the flowering plant Arabidopsis thaliana, the 17 members of the Catharanthus roseus RLK1-like (CrRLK1L) receptor kinase family are involved in a multitude of physiological and developmental processes, making it difficult to assess their primary or ancestral function. To reduce genetic complexity, we characterized the single CrRLK1L gene of Marchantia polymorpha, MpFERONIA (MpFER). Plants with reduced MpFER levels show defects in vegetative development, i.e. rhizoid formation and cell expansion, and have reduced male fertility. In contrast, cell integrity and morphogenesis of the gametophyte are severely affected in Mpfer null mutants and MpFER overexpression lines. Thus, we conclude that the CrRLK1L gene family originated from a single gene with an ancestral function in cell expansion and the maintenance of cellular integrity. During land plant evolution, this ancestral gene diversified to fulfill a multitude of specialized physiological and developmental roles in the formation of both gametophytic and sporophytic structures essential to the life cycle of flowering plants.

Petrology and organic geochemistry of the Baishaping and Damaidi Devonian cutinitic liptobioliths, west of the Kangdian Uplift, China

Devonian cutinitic liptobiolith is a special type of coal formed during the early evolutionary stage of land plants. The Baishaping and Damaidi Devonian coals are notable for their distinct papery, sheet-like texture, and unusually high cutinite content (>50%), belonging to typical cutinitic liptobiolith. They are bituminous coals and have a suppressed vitrinite reflectance. Compared with typical type III kerogen, these liptobioliths are characterized by extremely high yields of volatile matter and high hydrogen contents owing to their enhanced cutinite contents. As indicated by pyrolysis and elemental analysis results, the Devonian cutinitic liptobioliths are dominated by type I-II kerogens and have an excellent potential to generate liquid hydrocarbons. The Baishaping cutinitic liptobioliths are mainly composed of ribbon-like thick-walled cutinites, with small amounts of thin-walled type. Vitrinite is only present in trace amounts and is dominated by telinite. Meanwhile, the Damaidi Devonian coals are primarily composed of ribbon-like thin-walled cutinites, followed by collotelinites which are usually sandwiched by cutinites. The different petrological characteristics of the Baishaping and Damaidi liptobioliths might indicate a structural variation in the coal-forming plant cuticles and two distinct coal-forming conditions. The molecular biomarkers in the Devonian coals are mainly composed of C 18 –C 20 tetracyclic diterpenoids, which are assumed to be the dominant soluble constituent of the Devonian land-plant cuticles and might have played an important role in early land plant radiation. Other molecules include aromatic tetracyclic diterpenoids, 3–5 ring polycyclic aromatic hydrocarbons and their methylated counterparts, and C 16 - and C 18 -monocarboxylic acids. n -Alkanes are present only in small amounts. The molecular composition of the cutinite-rich coals is unexpected, because cuticular waxes are one of the most important sources of n -alkanes. In general, the petrology and geochemistry of the Devonian cutinitic liptobiolith indicate a distinct structure and composition for the early land-plant cuticles, which is significantly different from that of the plant cuticles since Carboniferous. Devonian cutinitic liptobioliths are of great interest because of their unique petrography, geochemistry, coal-forming plants, and oil-prone potential. Studies on this unique coal type provide a better understanding of coal-forming plants, paleoenvironment, paleoclimate, and early land-plant evolution in the Devonian.

Functional conservation of an AP2/ERF transcription factor in cuticle formation suggests an important role in the terrestrialization of early land plants.

The formation of a hydrophobic cuticle layer on aerial plant parts was a critical innovation for protection from the terrestrial environment during the evolution of land plants. However, little is known about the molecular mechanisms underlying cuticle biogenesis in early terrestrial plants. Here, we report an APETALA2/Ethylene Response Factor (AP2/ERF) transcriptional activator, PpWIN1, involved in cutin and cuticular wax biosynthesis in Physcomitrium patens and Arabidopsis. The transcript levels of PpWIN1 were 2.5-fold higher in gametophores than in the protonema, and increased by approximately 3- to 4.7-fold in the protonema and gametophores under salt and osmotic stresses. PpWIN1 harbouring transcriptional activation activity is localized in the nucleus of tobacco leaf epidermal cells. Δppwin1 knockout mutants displayed a permeable cuticle, increased water loss, and cutin- and wax-deficient phenotypes. In contrast, increased total cutin and wax loads, and decreased water loss rates were observed in PpWIN1-overexpressing Arabidopsis plants. The transcript levels of genes involved in cutin or wax biosynthesis were significantly up-regulated in PpWIN1-overexpressing Arabidopsis lines, indicating that PpWIN1 acts as a transcriptional activator in cuticle biosynthesis. This study suggests that Arabidopsis WIN1/SHN1 orthologs may be functionally conserved from early to vascular land plants.

The evolution of complex multicellularity in animals

The transition to multicellularity is perhaps the best-studied of the “major evolutionary transitions”. It has occurred independently multiple times within the eukaryotes alone, and multicellular organisms comprise virtually the entirety of Earth’s macrobiota. However, the theoretical framework used to study the major evolutionary transitions does not neatly accommodate the evolution of complex multicellularity as a process distinct from the evolution of multicellularity more generally. Here, I attempt to fill this explanatory gap. I will first give an overview of research on the major evolutionary transitions, focusing on multicellularity, and demonstrate that the theoretical framework so far utilised does not provide us with sufficient conceptual tools to explain crucial phenomena that call for explanation, such as the evolution of organs and organ systems. I will then discuss our current understanding of early metazoan evolution as paradigmatically exemplifying the evolution of complex organisation in a multicellular system, specifically regarding three core processes enabling it, namely modularisation, subfunctionalisation, and integration, allowing the provision of a general account of the evolution of complex from simple multicellularity that is potentially applicable to other such cases such as the evolution of land plants. This paves the way for a revised account of major evolutionary transitions which incorporates the evolution of complex organismal traits following the evolution of minimal autonomous reproducers while marking a shift of emphasis from reproducers to organisms.

MarpolBase Expression: A Web-Based, Comprehensive Platform for Visualization and Analysis of Transcriptomes in the Liverwort Marchantia 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.