Land Plant Evolution Research Articles

Ancient large-scale gene duplications and diversification in bryophytes illuminate the plant terrestrialization.

Large-scale gene duplications (LSGDs) are crucial for evolutionary adaptation and recurrent in vascular plants. However, the role of ancient LSGDs in the terrestrialization and diversification of bryophytes, the second most species-rich group of land plants, remains largely elusive due to limited sampling in bryophytes. Employing the most extensive nuclear gene dataset in bryophytes to date, we reconstructed a time-calibrated phylogenetic tree from 209 species, covering virtually all key bryophyte lineages, for phylogenomic analyses of LSGDs and diversification. We newly identified two ancient LSGDs: one in the most recent common ancestor (MRCA) of extant bryophytes and another in the MRCA of the majority of Jungermanniales s.lato.Duplicated genes from these two LSGDs show significant enrichment in photosynthesis-related processes and structures. Rhizoid-responsive ROOTHAIR DEFECTIVE SIX-LIKE (RSL) genes from ancient LSGDs are present in rhizoidless bryophytes, challenging assumptions about rhizoid absence mechanisms. We highlighted four major diversification rate upshifts, two of which slightly postdated LSGDs, potentially linked to the flourishing of gymnosperms and angiosperms and explaining over 80% of bryophyte diversity. Our findings, supported by extensive bryophyte sampling, highlight the significance of LSGDs in the early terrestrialization and diversification of bryophytes, offering new insights into land plant evolution.

Assessment of bi-metal paleo-redox proxies in the Bakken Formation black shales, Williston Basin, North Dakota, USA

The influence of paleoredox conditions and water-mass restriction on trace metal (TM) accumulation in the lower (LBS) and upper black shales (UBS) of the Devonian–Mississippian (D–M) Bakken Formation was assessed utilizing V/Cr, V/(V + Ni), Ni/Co, U/Th, and enrichment factors (EF) for Mo vs. U. These assessments were compared to previously published estimates based on degree of pyritization (DOPT), sulfur‑iron and C–S–Fe relationships, and sedimentological data. Bi–metal ratios suggest >80 % of samples were deposited under suboxic to anoxic/euxinic conditions, whereas DOPT results suggest >60 % of samples were deposited under dysoxic (0.42–0.75 DOPT) bottom–water conditions. DOPT results are in good agreement with C–S–Fe and total S vs. Fe assessments of paleoredox conditions and sedimentological evidence. Good agreement is also seen between Mo/TOC and Mo EF/U EF that both suggest the Bakken shales were deposited under a relatively unrestricted water mass conditions resulting in consistent renewal of TMs into the basin. With TM resupply outpacing drawdown, the basin could support enhanced primary productivity as well as high concentrations of TMs. Trace metal concentrations for the Bakken Fm. show considerable range for Co (0–10,324 ppm), Mo (0–2018 ppm), Ni (0–1574 ppm), U (0–1604 ppm), and V (0–3194 ppm), and bi–metal ratios for the Bakken Fm. are up to 5× greater than those reported for other D–M black shale formations. Bivariate and principal component analysis indicate Mo, Ni, U, and V accumulation was more closely associated with the organic fraction than with reducing conditions, thus accumulation of organic matter during deposition and generation, migration, and biodegradation of hydrocarbons during diagenesis may have influenced the accumulation and distribution of these TMs. Furthermore, changes in biogeochemical processes during the D–M transition may have fundamentally altered marine chemistry, with the evolution of vascular land plants and enhanced terrestrial weathering leading to an increased influx of nutrients into marine waters resulting in the Annulata, Dasberg, and Hangenberg black shale events. Factors controlling TM accumulation during time of deposition (e.g., TM availability, bottom-water redox conditions, adsorption onto organic matter) and during diagenesis and catagenesis (e.g., alteration and break down of organic matter, movement of fluid hydrocarbons or other basinal fluids) likely contribute to the lack of agreement between redox proxies, and subsequently, the lack of applicability of bi–metal ratios in assessing bottom–water conditions for the Bakken shales. Therefore, it is suggested that these bi-metal redox proxies are not an effective means to describe bottom-water conditions during the deposition of the Bakken shales.

Ocean oxygenation and ecological restructuring caused by the late Paleozoic evolution of land plants

The dramatic increase in ocean-atmosphere oxygen levels during the Devonian and Mississippian is increasingly linked to the diversification of land plants, yet the timing and extent of this event remain uncertain. This study uses the redox-sensitive rare earth element cerium (cerium anomaly—Ce/Ce*) to investigate ocean redox conditions during the deposition of globally distributed Paleozoic carbonate strata. Our Paleozoic Ce/Ce* record suggests that Cambrian, Ordovician, and Silurian oceans had relatively low O2 levels (mean Ce/Ce* = 0.86 ± 0.10, 0.91 ± 0.14, and 0.91 ± 0.10 [±1σ], respectively). In contrast, short-lived ocean oxygenation events, possibly related to the diversification of small land plants, likely occurred throughout the Early and Middle Devonian (mean Ce/Ce* = 0.80 ± 0.07 and 0.58 ± 0.14, respectively). “Modern” Ce/Ce* values (<0.36) first occurred during the Late Devonian, suggesting that the main phase of Devonian and Mississippian oceanic oxygenation was related to the evolution of large vascular plants and the first forests. Despite this, the significant variability of Ce/Ce* values during this time suggests that shallow marine settings were susceptible to redox instability, possibly caused by upwelling of anoxic deep waters. This redox instability potentially provides evidence of a mechanism for contemporaneous mass extinction and metazoan reef collapse events. Development of strongly oxic conditions during the Late Devonian may have resulted in the demise of many Paleozoic-type organisms, facilitated the radiation of the modern evolutionary fauna, and established the modern oxygenated ocean-atmosphere system.

Geography, altitude, agriculture and hypoxia.

Reduced oxygen availability (hypoxia) represents a key plant abiotic stress in natural and agricultural systems, but conversely it is also an important component of normal growth and development. We review recent advances that demonstrate how genetic adaptations associated with hypoxia impact the known plant oxygen sensing mechanism through the PLANT CYSTEINE OXIDASE (PCO) N-degron pathway. Only three protein substrates of this pathway have been identified, and all adaptations identified to date are associated with the most important of these, the group VII ETHYLENE RESPONSE FACTOR transcription factors (ERFVIIs). We discuss how geography, altitude, and agriculture have all shaped molecular responses to hypoxia, and how these responses have emerged at different taxonomic levels through the evolution of land plants. Understanding how ecological and agricultural genetic variation acts positively to enhance hypoxia tolerance will provide novel tools and concepts to improve the performance of crops in the face of increasing extreme flooding events.

ALOG/LSHs, a novel class of transcription factors: Evolutionarily conserved regulators of plant growth and development.

The ALOG/LSH group of proteins is highly conserved across plant lineage, starting from moss to higher flowering plants, suggesting their crucial role in the evolution and adaptation of land plants. The role of ALOG proteins is highly conserved in various developmental responses, such as vegetative and reproductive developmental programs. Their role in meristem identity, cotyledon development, seedling photomorphogenesis and leaf and shoot development has been relatively well established. Moreover, several key pieces of evidence suggest their role in inflorescence architecture and flower development, including male and female reproductive organs and flower colouration. Recent research has started to explore their role in stress response. Functionally, ALOG proteins have been demonstrated to act as transcriptional regulators and are considered a newly emerging class of transcription factors in plants that regulate diverse developmental and physiological processes. This review aims to stimulate discussion about their role in plant development and their role as transcription factors. It also aims to further unravel the underlying molecular mechanism by which they regulate growth and development throughout the plant lineage.

Aberrant growth and expansion in Penium margaritaceum triggered by disruption of microtubules and the cell wall.

Penium margaritaceum, a unicellular zygnematophyte (Streptophyta), was employed to elucidate changes in cell expansion when cells were challenged with the fungal pectinolytic enzyme, pectate lyase, and/or the microtubule disrupting agent, amiprophos-methyl (APM). Microtubule disruption by APM results in significant swelling at expansion zones. These swollen zones provide an easy marker for the location of expansion zones, particularly in cells with altered cell wall pectin. Short term treatment with pectate lyase shows pectin degradation primarily at the isthmus expansion zone and two satellite bands, corresponding with the location of future expansion in daughter cells. When the homogalacturonan lattice of the cell wall is removed by treatment with pectate lyase during long treatments, cell division is maintained, but daughter cell products are considerably smaller. Treatment of cells with a mixture of both pectate lyase and APM results in a distinct phenotype, consisting of "dumbbell"-shaped cells, as APM-induced swelling occurs at the novel expansion centers exposed by pectate lyase treatment. These cells also possess other curious alterations including an extensive, chloroplast-free cytoplasmic zone at the center of the cell, a septum containing ß-glycan, arabinogalactan and homogalacturonan epitopes, unique stacks of ER, displaced Golgi bodies and an extensive network of vacuoles. These results provide insight into the importance of cell wall integrity in defining the location of cell growth and division in P. margaritaceum. Understanding these processes in a unicellular zygnematophyte may provide insights into steps involved in the evolution of land plants.

Functional and Structural Analysis Reveals Distinct Biological Roles of Plant Synaptotagmins in Response to Environmental Stress.

Endoplasmic reticulum-plasma membrane contact sites (ER-PM CSs) are evolutionarily conserved membrane domains found in all eukaryotes, where the ERclosely interfaces with the PM. This short distance is achieved in plants through the action of tether proteins such as synaptotagmins (SYTs). Arabidopsis comprises five SYT members (SYT1-SYT5), but whether they possess overlapping or distinct biological functions remains elusive. SYT1, the best-characterized member, plays an essential role in the resistance to abiotic stress. This study reveals that the functionally redundant SYT1 and SYT3 genes, but not SYT5, are involved in salt and cold stress resistance. We also show that, unlike SYT5, SYT1 and SYT3 are not required for Pseudomonas syringae resistance. Since SYT1 and SYT5 interact in vivo via their SMP domains, the distinct functions of these proteins cannot be caused by differences in their localization. Interestingly, structural phylogenetic analysis indicates that theSYT1 and SYT5 clades emerged early in the evolution of land plants. We also show that theSYT1 and SYT5 clades exhibit different structural features in their SMP and Ca2+binding of their C2 domains, rationalizing their distinct biological roles.

The BNB-GLID module regulates germline fate determination in Marchantia polymorpha.

Germline fate determination is a critical event in sexual reproduction. Unlike animals, plants specify the germline by reprogramming somatic cells at the late stages of their development. However, the genetic basis of germline fate determination and how it evolved during the land plant evolution are still poorly understood. Here, we report that the plant homeodomain finger protein GERMLINE IDENTITY DETERMINANT (GLID) is a key regulator of the germline specification in liverwort, Marchantia polymorpha. Loss of the MpGLID function causes failure of germline initiation, leading to the absence of sperm and egg cells. Remarkably, the overexpression of MpGLID in M. polymorpha induces the ectopic formation of cells with male germline cell features exclusively in male thalli. We further show that MpBONOBO (BNB), with an evolutionarily conserved function, can induce the formation of male germ cell-like cells through the activation of MpGLID by directly binding to its promoter. The Arabidopsis (Arabidopsis thaliana) MpGLID ortholog, MALE STERILITY1 (AtMS1), fails to replace the germline specification function of MpGLID in M. polymorpha, demonstrating that a derived function of MpGLID orthologs has been restricted to tapetum development in flowering plants. Collectively, our findings suggest the presence of the BNB-GLID module in complex ancestral land plants that has been retained in bryophytes, but rewired in flowering plants for male germline fate determination.

Post-transfer adaptation of HGT-acquired genes and contribution to guanine metabolic diversification in land plants.

Horizontal gene transfer (HGT) is a major driving force in the evolution of prokaryotic and eukaryotic genomes. Despite recent advances in distribution and ecological importance, the extensive pattern, especially in seed plants, and post-transfer adaptation of HGT-acquired genes in land plants remain elusive. We systematically identified 1150 foreign genes in 522 land plant genomes that were likely acquired via at least 322 distinct transfers from nonplant donors and confirmed that recent HGT events were unevenly distributed between seedless and seed plants. HGT-acquired genes evolved to be more similar to native genes in terms of average intron length due to intron gains, and HGT-acquired genes containing introns exhibited higher expression levels than those lacking introns, suggesting that intron gains may be involved in the post-transfer adaptation of HGT in land plants. Functional validation of bacteria-derived gene GuaD in mosses and gymnosperms revealed that the invasion of foreign genes introduced a novel bypass of guanine degradation and resulted in the loss of native pathway genes in some gymnosperms, eventually shaping three major types of guanine metabolism in land plants. We conclude that HGT has played a critical role in land plant evolution.

Doubling down on polyploid discoveries: Global advances in genomics and ecological impacts of polyploidy.

All flowering plants are now recognized as diploidized paleopolyploids (Jiao et al., 2011; One Thousand Plant Transcriptomes Initiative, 2019), and polyploid species comprise approximately 30% of contemporary plant species (Wood et al., 2009; Barker et al., 2016a). A major implication of these discoveries is that, to appreciate the evolution of plant diversity, we need to understand the fundamental biology of polyploids and diploidization. This need is broadly recognized by our community as there is a continued, growing interest in polyploidy as a research topic. Over the past 25 years, the sequencing and analysis of plant genomes has revolutionized our understanding of the importance of polyploid speciation to the evolution of land plants.

MYB-related transcription factors control chloroplast biogenesis

Chloroplast biogenesis is dependent on master regulators from the GOLDEN2-LIKE (GLK) family of transcription factors. However, glk mutants contain residual chlorophyll, indicating that other proteins must be involved. Here, we identify MYB-related transcription factors as regulators of chloroplast biogenesis in the liverwort Marchantia polymorpha and angiosperm Arabidopsis thaliana. In both species, double-mutant alleles in MYB-related genes show very limited chloroplast development, and photosynthesis gene expression is perturbed to a greater extent than in GLK mutants. Genes encoding enzymes of chlorophyll biosynthesis are controlled by MYB-related and GLK proteins, whereas those allowing CO2 fixation, photorespiration, and photosystem assembly and repair require MYB-related proteins. Regulation between the MYB-related and GLK transcription factors appears more extensive in A.thaliana than in M.polymorpha. Thus, MYB-related and GLK genes have overlapping as well as distinct targets. We conclude that MYB-related and GLK transcription factors orchestrate chloroplast development in land plants.

Relationships Among the Bryophytes and Vascular Plants: A Case Study in Deep-Time Reconstruction

Relationships of the three bryophyte lineages (liverworts, mosses, and hornworts) to vascular plants is a pivotal question in the study of the origin and evolution of land plants. In recent decades, this question has been subjected to intense phylogenetic analyses using morphological characters, multigene DNA sequences, and genome structural characters. A tentative consensus, reached ten years ago, suggested that bryophytes are a paraphyletic group, with liverworts being sister to all other land plants and hornworts being sister to vascular plants. However, several more recent nuclear phylogenomic studies have concluded that bryophytes represent a monophyletic group that is sister to vascular plants. A discussion is presented here on strengths and weaknesses of different types of characters (morphological traits, nucleotide sequences, and genome structural arrangements) and their suitability for resolving deep phylogenetic relationships. Moreover, several criteria for credible phylogenetic reconstruction are proposed. Strong statistical support for reconstructed relationships should be derived from high-quality, independent characters selected for suitability to the particular question being addressed. The relationships inferred in a study should be congruent with those from as many other lines of phylogenetic evidence as possible. Any incongruities should be explicable by well-understood biological mechanisms. It is concluded that the relationships of the three bryophyte lineages to vascular plants should currently be viewed as unresolved. This is a difficult phylogenetic problem; the land plants underwent a rapid radiation a long time ago. Yet, further exploration of analytical methods and careful choice of characters should lead to the eventual elucidation of diversification patterns among early land plants.

Phylogenomic data resolved the deep relationships of Gymnogynoideae (Selaginellaceae).

The unresolved phylogenetic framework within the Selaginellaceae subfamily Gymnogynoideae (ca. 130 species) has hindered our comprehension of the diversification and evolution of Selaginellaceae, one of the most important lineages in land plant evolution. Here, based on plastid and nuclear data extracted from genomic sequencing of more than 90% species of all genera except two in Gymnogynoideae, a phylogenomic study focusing on the contentious relationships among the genera in Gymnogynoideae was conducted. Our major results included the following: (1) Only single-copy region (named NR) and only one ribosomal operon was firstly found in Afroselaginella among vascular plants, the plastome structure of Gymnogynoideae is diverse among the six genera, and the direct repeats (DR) type is inferred as the ancestral state in the subfamily; (2) The first strong evidence was found to support Afroselaginella as a sister to Megaloselaginella. Alternative placements of Ericetorum and Gymnogynum were detected, and their relationships were investigated by analyzing the variation of phylogenetic signals; and (3) The most likely genus-level relationships in Gymnogynoideae might be: ((Bryodesma, Lepidoselaginella), (((Megaloselaginella, Afroselaginella), Ericetorum), Gymnogynum)), which was supported by maximum likelihood phylogeny based on plastid datasets, maximum likelihood, and Bayesian inference based on SCG dataset and concatenated nuclear and plastid datasets and the highest proportion of phylogenetic signals of plastid genes.

Ancient origin of acetyltransferases catalyzing O-acetylation of plant cell wall polysaccharides.

Members of the domain of unknown function 231 (DUF231)/trichome birefringence-like (TBL) family have been shown to be O-acetyltransferases catalyzing the acetylation of plant cell wall polysaccharides, including pectins, mannan, xyloglucan and xylan. However, little is known about the origin and evolution of plant cell wall polysaccharide acetyltransferases. Here, we investigated the biochemical functions of TBL homologs from Klebsormidium nitens, a representative of an early divergent class of charophyte green algae that are considered to be the closest living relatives of land plants, and Marchantia polymorpha, a liverwort that is an extant representative of an ancient lineage of land plants. The genomes of K. nitens and M. polymorpha harbor two and six TBL homologs, respectively. Biochemical characterization of their recombinant proteins expressed in human embryonic kidney (HEK) 293 cells demonstrated that the two K. nitens TBLs exhibited acetyltransferase activities acetylating the pectin homogalacturonan (HG) and hence were named KnPOAT1 and KnPOAT2. Among the six M. polymorpha TBLs, five of them (MpPOAT1 to 5) possessed acetyltransferase activities toward pectins and the remaining one (MpMOAT1) catalyzed 2-O- and 3-O-acetylation of mannan. While MpPOAT1,2 specifically acetylated HG, MpPOAT3,4,5 could acetylate both HG and rhamnogalacturonan-I (RG-I). Consistent with the acetyltransferase activities of these TBLs, pectins isolated from K. nitens and both pectins and mannan from M. polymorpha were shown to be acetylated. These findings indicate that the TBL genes were recruited as cell wall polysaccharide O-acetyltransferases as early as in charophyte green algae with activities toward pectins and they underwent expansion and functional diversification to acetylate various cell wall polysaccharides during evolution of land plants.

Metagenome-assembled genome of the glacier alga Ancylonema yields insights into the evolution of streptophyte life on ice and land.

Contemporary glaciers are inhabited by streptophyte algae that balance photosynthesis and growth with tolerance of low temperature, desiccation and UV radiation. These same environmental challenges have been hypothesised as the driving force behind the evolution of land plants from streptophyte algal ancestors in the Cryogenian (720-635 million years ago). We sequenced, assembled and analysed the metagenome-assembled genome of the glacier alga Ancylonema nordenskiöldii to investigate its adaptations to life in ice, and whether this represents a vestige of Cryogenian exaptations. Phylogenetic analysis confirms the placement of glacier algae within the sister lineage to land plants, Zygnematophyceae. The metagenome-assembled genome is characterised by an expansion of genes involved in tolerance of high irradiance and UV light, while lineage-specific diversification is linked to the novel screening pigmentation of glacier algae. We found no support for the hypothesis of a common genomic basis for adaptations to ice and to land in streptophytes. Comparative genomics revealed that the reductive morphological evolution in the ancestor of Zygnematophyceae was accompanied by reductive genome evolution. This first genome-scale data for glacier algae suggests an Ancylonema-specific adaptation to the cryosphere, and sheds light on the genome evolution of land plants and Zygnematophyceae.

Biolistics-mediated transformation of hornworts and its application to study pyrenoid protein localization.

Hornworts are a deeply diverged lineage of bryophytes and a sister lineage to mosses and liverworts. Hornworts have an array of unique features that can be leveraged to illuminate not only the early evolution of land plants, but also alternative paths for nitrogen and carbon assimilation via cyanobacterial symbiosis and a pyrenoid-based CO2-concentrating mechanism (CCM), respectively. Despite this, hornworts are one of the few plant lineages with limited available genetic tools. Here we report an efficient biolistics method for generating transient expression and stable transgenic lines in the model hornwort, Anthoceros agrestis. An average of 569 (±268) cells showed transient expression per bombardment, with green fluorescent protein expression observed within 48-72 h. A total of 81 stably transformed lines were recovered across three separate experiments, averaging six lines per bombardment. We followed the same method to transiently transform nine additional hornwort species, and obtained stable transformants from one. This method was further used to verify the localization of Rubisco and Rubisco activase in pyrenoids, which are central proteins for CCM function. Together, our biolistics approach offers key advantages over existing methods as it enables rapid transient expression and can be applied to widely diverse hornwort species.

Development of a Target Enrichment Probe Set for Conifer (REMcon).

Conifers are an ecologically and economically important seed plant group that can provide significant insights into the evolution of land plants. Molecular phylogenetics has developed as an important approach in evolutionary studies, although there have been relatively few studies of conifers that employ large-scale data sourced from multiple nuclear genes. Target enrichment sequencing (target capture, exon capture, or Hyb-Seq) has developed as a key approach in modern phylogenomic studies. However, until now, there has been no bait set that specifically targets the entire conifer clade. REMcon is a target sequence capture probe set intended for family- and species-level phylogenetic studies of conifers that target c. 100 single-copy nuclear loci. We tested the REMcon probe set using 69 species, including 44 conifer genera across six families and four other gymnosperm taxa, to evaluate the efficiency of target capture to efficiently generate comparable DNA sequence data across conifers. The recovery of target loci was high, with, on average, 94% of the targeted regions recovered across samples with high read coverage. A phylogenetic analysis of these data produced a well-supported topology that is consistent with the current understanding of relationships among conifers. The REMcon bait set will be useful in generating relatively large-scale nuclear data sets consistently for any conifer lineage.

The PLETHORA Homolog in Marchantia polymorpha is Essential for Meristem Maintenance, Developmental Progression, and Redox Homeostasis.

To adapt to a terrestrial habitat, the ancestors of land plants must have made several morphological and physiological modifications, such as a meristem allowing for three-dimensional growth, rhizoids for water and nutrient uptake, air pore complexes or stomata that permit air exchange, and a defense system to cope with oxidative stress that occurs frequently in a terrestrial habitat. To understand how the meristem was determined during land plant evolution, we characterized the function of the closest PLETHORA homolog in the liverwort Marchantia polymorpha, which we named MpPLT. Through a transgenic approach, we showed that MpPLT is expressed not only in the stem cells at the apical notch but also in the proliferation zone of the meristem, as well as in cells that form the air-pore complex and rhizoids. Using the CRISPR method we then created mutants for MpPLT and found that the mutants are not only defective in meristem maintenance but also compromised in air-pore complex and rhizoid development. Strikingly, at later developmental stages, numerous gemma-like structures were formed in Mpplt mutants, suggesting developmental arrest. Further experiments indicated that MpPLT promotes plant growth by regulating MpWOX, which shared a similar expression pattern to MpPLT, and genes involved in auxin and cytokinin signaling pathways. Through transcriptome analyses, we found that MpPLT also has a role in redox homeostasis and that this role is essential for plant growth. Taken together, these results suggest that MpPLT has a crucial role in liverwort growth and development and hence may have played a crucial role in early land plant evolution.

Bona Fide Plant Steroid Receptors are Innovated in Seed Plants and Angiosperms through Successive Whole-Genome Duplication Events.

Whole-genome duplication (WGD) events are widespread in plants and animals, thus their long-term evolutionary contribution has long been speculated, yet a specific contribution is difficult to verify. Here, we show that ɛ-WGD and ζ-WGD contribute to the origin and evolution of bona fide brassinosteroid (BR) signaling through the innovation of active BR biosynthetic enzymes and active BR receptors from their respective ancestors. We found that BR receptors BRI1 (BR INSENSITIVE 1) and BRL1/3 (BRI1-LIKES 1/3) derived by ɛ-WGD and ζ-WGD, which occurred in the common ancestor of angiosperms and seed plants, respectively, while orphan BR receptor BRL2 first appeared in stomatophytes. Additionally, CYP85A enzymes synthesizing the bioactive BRs derived from a common ancestor of seed plants, while its sister enzymes CYP90 synthesizing BR precursors presented in all land plants, implying possible ligand-receptor coevolution. Consistently, the island domains (IDs) responsible for BR perception in BR receptors were most divergent among different receptor branches, supporting ligand-driven evolution. As a result, BRI1 was the most diversified BR receptor in angiosperms. Importantly, relative to the BR biosynthetic DET2 gene presented in all land plants, BRL2, BRL1/3 and BRI1 had high expression in vascular plants ferns, gymnosperms and angiosperms, respectively. Notably, BRI1 is the most diversified BR receptor with the most abundant expression in angiosperms, suggesting potential positive selection. Therefore, WGDs initiate a neofunctionalization process diverged by ligand-perception and transcriptional expression, which might optimize both BR biosynthetic enzymes and BR receptors, likely contributing to the evolution of land plants, especially seed plants and angiosperms.

Stomatal evolution and plant adaptation to future climate.

Global climate change is affecting plant photosynthesis and transpiration processes, as well as increasing weather extremes impacting socio-political and environmental events and decisions for decades to come. One major research challenge in plant biology and ecology is the interaction of photosynthesis with the environment. Stomata control plant gas exchange and their evolution was a crucial innovation that facilitated the earliest land plants to colonize terrestrial environments. Stomata couple homoiohydry, together with cuticles, intercellular gas space, with the endohydric water-conducting system, enabling plants to adapt and diversify across the planet. Plants control stomatal movement in response to environmental change through regulating guard cell turgor mediated by membrane transporters and signaling transduction. However, the origin, evolution, and active control of stomata remain controversial topics. We first review stomatal evolution and diversity, providing fossil and phylogenetic evidence of their origins. We summarize functional evolution of guard cell membrane transporters in the context of climate changes and environmental stresses. Our analyses show that the core signaling elements of stomatal movement are more ancient than stomata, while genes involved in stomatal development co-evolved de novo with the earliest stomata. These results suggest that novel stomatal development-specific genes were acquired during plant evolution, whereas genes regulating stomatal movement, especially cell signaling pathways, were inherited ancestrally and co-opted by dynamic functional differentiation. These two processes reflect the different adaptation strategies during land plant evolution.