Early Land Plants Research Articles

Molecular and phylogenetic evidence of parallel expansion of anion channels in plants.

Aluminum-activated malate transporters (ALMTs) and slow anion channels (SLACs) are important in various physiological processes in plants, including stomatal regulation, nutrient uptake, and in response to abiotic stress such as aluminum toxicity. To understand their evolutionary history and functional divergence, we conducted phylogenetic and expression analyses of ALMTs and SLACs in green plants. Our findings from phylogenetic studies indicate that ALMTs and SLACs may have originated from green algae and red algae, respectively. The ALMTs of early land plants and charophytes formed a monophyletic clade consisting of three subgroups. A single duplication event of ALMTs was identified in vascular plants and subsequent duplications into six clades occurred in angiosperms, including an identified clade, 1-1. The ALMTs experienced gene number losses in clades 1-1 and 2-1 and expansions in clades 1-2 and 2-2b. Interestingly, the expansion of clade 1-2 was also associated with higher expression levels compared to genes in clades that experienced apparent loss. SLACs first diversified in bryophytes, followed by duplication in vascular plants, giving rise to three distinct clades (I, II, and III), and clade II potentially associated with stomatal control in seed plants. SLACs show losses in clades II and III without substantial expansion in clade I. Additionally, ALMT clade 2-2 and SLAC clade III contain genes specifically expressed in reproductive organs and roots in angiosperms, lycophytes, and mosses, indicating neofunctionalization. In summary, our study demonstrates the evolutionary complexity of ALMTs and SLACs, highlighting their crucial role in the adaptation and diversification of vascular plants.

Identification of miRNA858 long-loop precursors in seed plants.

MicroRNAs (miRNAs) are a class of nonprotein-coding short transcripts that provide a layer of post-transcriptional regulation essential to many plant biological processes. MiR858, which targets the transcripts of MYB transcription factors, can affect a range of secondary metabolic processes. Although miR858 and its 187-nt precursor have been well studied in Arabidopsis (Arabidopsis thaliana), a systematic investigation of miR858 precursors and their functions across plant species is lacking due to a problem in identifying the transcripts that generate this subclass. By re-evaluating the transcript of miR858 and relaxing the length cut-off for identifying hairpins, we found in kiwifruit (Actinidia chinensis) that miR858 has long-loop hairpins (1,100 to 2,100 nt), whose intervening sequences between miRNA generating complementary sites were longer than all previously reported miRNA hairpins. Importantly, these precursors of miR858 containing long-loop hairpins (termed MIR858L) are widespread in seed plants including Arabidopsis, varying between 350 and 5,500 nt. Moreover, we showed that MIR858L has a greater impact on proanthocyanidin and flavonol levels in both Arabidopsis and kiwifruit. We suggest that an active MIR858L-MYB regulatory module appeared in the transition of early land plants to large upright flowering plants, making a key contribution to plant secondary metabolism.

Silurian–Devonian construction of active continental margin in the southwestern Paleo-Asian Ocean witnesses the modification of fluvial system by early land plants

In accretionary orogeny, the intra-oceanic subduction-accretion could generate juvenile continental crustal materials and form new continental blocks by their lateral tectonic accretion, and the juvenile continental crust would provide a sialic basement for continental margin arc during the subsequent oceanic-continental subduction-accretion. These two distinct subduction-accretion processes occurred successively in the southwestern part of the Paleo-Asian Ocean during the Neoproterozoic–Late Paleozoic and created a multi-stage evolution of continental crusts in West Junggar. In this study, a Late Silurian landmass in West Junggar is revealed by the detailed geological mapping and comparison of the Late Silurian–Early Devonian angular unconformity in southern and northern West Junggar. This crucial unconformity confines the Middle Silurian termination of Early Paleozoic intra-oceanic subduction-accretion, as evidenced by the pre-Late Silurian emplacement of Cambrian–Ordovician ophiolitic mélanges, the Middle Silurian cessation of Early Paleozoic arc magmatism and the Late Silurian–Early Devonian sedimentary hiatus. The Late Silurian landmass was consequently constructed by amalgamations of island arcs, accretionary complexes and seamounts, and its break-up was marked by the Middle Devonian opening of the Karamay back-arc Ocean in central West Junggar. In contrast with the Early Paleozoic intra-oceanic arc systems, continental margin arcs on the sialic basement of rifted landmass emerged since the Middle Devonian, as suggested by our new chronological data and field observations. We further unravel that the increase in mudstone of Devonian successions on the active continental margin is contemporaneous with the emergence and boom of lycopsid forest in West Junggar, which is in agreement with a global trend in alteration of fluvial systems due to evolution of early land plants. In summary, this paper presents a typical record for two distinguished styles of subduction-accretion systems that developed successively in an accretionary orogeny, and sedimentary successions of the later active continental margin documented the interaction between terrestrial sedimentation and early land plants.

Control of stem cell behavior by CLE-JINGASA signaling in the shoot apical meristem in Marchantia polymorpha

Land plants undergo indeterminate growth by the activity of meristems in both gametophyte (haploid) and sporophyte (diploid) generations. In the sporophyte of the flowering plant Arabidopsis thaliana, the apical meristems are located at the shoot and root tips in which a number of regulatory gene homologs are shared for their development, implying deep evolutionary origins. However, little is known about their functional conservation with gametophytic meristems in distantly related land plants such as bryophytes, even thoughgenomic studies have revealed that the subfamily-level diversity of regulatory genes is mostly conserved throughout land plants. Here, we show that a NAM/ATAF/CUC (NAC) domain transcription factor, JINGASA (MpJIN), acts downstream of CLAVATA3 (CLV3)/ESR-related (CLE) peptide signaling and controls stem cell behavior in the gametophytic shoot apical meristem of the liverwort Marchantia polymorpha. In the meristem, strong MpJIN expression was associated with the periclinal cell division at the periphery of the stem cell zone (SCZ), whereas faint MpJIN expression was found at the center of the SCZ. Time course observation indicates that the MpJIN-negative cells are lost from the SCZ and respecified de novo at two separate positions during the dichotomous branching event. Consistently, the induction of MpJIN results in ectopic periclinal cell division in the SCZ and meristem termination. Based on the comparative expression data, we speculate that the function of JIN/FEZ subfamily genes was shared among the shoot apical meristems in the gametophyte and sporophyte generations in early land plants but was lost in certain lineages, including the flowering plant A.thaliana.

The impact of salt stress on the physiology and the transcriptome of the model streptophyte green alga Chara braunii.

Chara braunii is a model for early land plant evolution and terrestrialization. Salt stress has a profound effect on water and ion transport activities, thereby interacting with many other processes, including inorganic carbon acquisition for photosynthesis. In this study, we analyzed the impact of salt stress (5 practical salt units, PSU) on the physiology and gene expression in C. braunii. Photosynthesis was only slightly affected 6 h after salt addition and returned to control levels after 48 h. Several organic compounds such as proline, glutamate, sucrose, and 2-aminobutyrate accumulated in salt-treated thalli and might contribute to osmotic potential acclimation, whereas the amount of K+ decreased. We quantified transcript levels for 17,387 genes, of which 95 were up-regulated and 44 down-regulated after salt addition. Genes encoding proteins of the functional groups ion/solute transport and cell wall synthesis/modulation were enriched among the up-regulated genes 24-48 h after salt stress, indicating their role in osmotic acclimation. However, a homolog to land plant ERD4 osmosensors was transiently upregulated after 6 h, and phylogenetic analyses suggested that these sensors evolved in Charophyceae. Down-regulated genes were mainly related to photosynthesis and carbon metabolism/fixation, consistent with the observed lowered growth after extended cultivation. The changed expression of genes encoding proteins for inorganic carbon acquisition might be related to the impact of salt on ionic relations and inorganic carbon uptake. The results indicate that C. braunii can tolerate enhanced salt concentrations in a defined acclimation process, including distinct gene expression changes to achieve new metabolic homeostasis.

Deciphering the hidden complexity of early land plant reproduction.

This article is a Commentary on D'Ario et al. (2024), 241: 937–949.

Hidden functional complexity in the flora of an early land ecosystem.

The first land ecosystems were composed of organisms considered simple in nature, yet the morphological diversity of their flora was extraordinary. The biological significance of this diversity remains a mystery largely due to the absence of feasible study approaches. To study the functional biology of Early Devonian flora, we have reconstructed extinct plants from fossilised remains in silico. We explored the morphological diversity of sporangia in relation to their mechanical properties using finite element method. Our approach highlights the impact of sporangia morphology on spore dispersal and adaptation. We discovered previously unidentified innovations among early land plants, discussing how different species might have opted for different spore dispersal strategies. We present examples of convergent evolution for turgor pressure resistance, achieved by homogenisation of stress in spherical sporangia and by torquing force in Tortilicaulis-like specimens. In addition, we show a potential mechanism for stress-assisted sporangium rupture. Our study reveals the deceptive complexity of this seemingly simple group of organisms. We leveraged the quantitative nature of our approach and constructed a fitness landscape to understand the different ecological niches present in the Early Devonian Welsh Borderland flora. By connecting morphology to functional biology, these findings facilitate a deeper understanding of the diversity of early land plants and their place within their ecosystem.

Role of TRDMT1/DNMT2 in stress adaptation and its influence on transcriptome and proteome dynamics under osmotic stress in Physcomitrium patens.

Early land plants such as the moss Physcomitrium patens lack several morphological traits that offer protection to tracheophytes from environmental stresses. These plants instead have evolved several physiological and biochemical mechanisms that facilitate them to adapt to terrestrial stresses such as drought. We have previously shown that loss-of-function mutants of tRNA (cytosine(38)-C(5))-methyltransferase TRDMT1/DNMT2 in P. patens are highly sensitive to oxidative and osmotic stress. To gain insight into the role of PpTRDMT1/PpDNMT2 in modulating genetic networks under osmotic stress, genome-wide transcriptome and proteome studies were undertaken in wild-type and ppdnmt2 plants. Transcriptome analysis revealed 375 genes to be differentially expressed in the ppdnmt2 under stress compared to the WT. Most of these genes are affiliated with carbohydrate metabolic pathways, photosynthesis, cell wall biogenesis, pathways related to isotropic and polarised cell growth and transcription factors among others. Histochemical staining showed elevated levels of reactive oxygen species in ppdnmt2 while transmission electron microscopy revealed no distinct defects in the ultrastructure of chloroplasts. Immunoprecipitation using PpDNMT2-specific antibody coupled with mass spectrometry revealed core proteins of the glycolytic pathway, antioxidant enzymes, proteins of amino acid biosynthetic pathways and photosynthesis-related proteins among others to co-purify with PpTRDMT1/PpDNMT2 under osmotic stress. Yeast two-hybrid assays, protein deletion and α-galactosidase assays showed the cytosol glycolytic protein glyceraldehyde 3-phosphate dehydrogenase to bind to the catalytic motifs in PpTRDMT1/PpDNMT2. Results presented in this study allow us to better understand genetic networks linking enzymes of energy metabolism, epigenetic processes and RNA pol II-mediated transcription during osmotic stress tolerance in P. patens.

Insight into the nodal cells transcriptome of the streptophyte green alga Chara braunii S276.

Charophyceae are the most complex streptophyte algae, possessing tissue-like structures, rhizoids and a cellulose-pectin-based cell wall akin to embryophytes. Together with the Zygnematophyceae and the Coleochaetophycae, the Charophyceae form a grade in which the Zygnematophyceae share a last common ancestor with land plants. The availability of genomic data, its short life cycle, and the ease of non-sterile cultivation in the laboratory have made the species Chara braunii an emerging model system for streptophyte terrestrialization and early land plant evolution. In this study, tissue containing nodal cells was prepared under the stereomicroscope, and an RNA-seq dataset was generated and compared to transcriptome data from whole plantlets. In both samples, transcript coverage was high for genes encoding ribosomal proteins and a homolog of the putative PAX3- and PAX7-binding protein 1. Gene ontology was used to classify the putative functions of the differently expressed genes. In the nodal cell sample, main upregulated molecular functions were related to protein, nucleic acid, ATP- and DNA binding. Looking at specific genes, several signaling-related genes and genes encoding sugar-metabolizing enzymes were found to be expressed at a higher level in the nodal cell sample, while photosynthesis-and chloroplast-related genes were expressed at a comparatively lower level. We detected the transcription of 21 different genes encoding DUF4360-containing cysteine-rich proteins. The data contribute to the growing understanding of Charophyceae developmental biology by providing a first insight into the transcriptome composition of Chara nodal cells.

Immunochemical Identification of the Main Cell Wall Polysaccharides of the Early Land Plant Marchantia polymorpha.

Plant primary cell walls are composite structures surrounding the protoplast and containing pectins, hemicelluloses, and cellulose polysaccharides, as well as proteins. Their composition changed during the evolution of the green lineage from algae to terrestrial plants, i.e., from an aquatic to a terrestrial environment. The constraints of life in terrestrial environments have generated new requirements for the organisms, necessitating adaptations, such as cell wall modifications. We have studied the cell wall polysaccharide composition of thalli of Marchantia polymorpha, a bryophyte belonging to one of the first land plant genera. Using a collection of specific antibodies raised against different cell wall polysaccharide epitopes, we were able to identify in polysaccharide-enriched fractions: pectins, including low-methylesterified homogalacturonans; rhamnogalacturonan I with arabinan side-chains; and hemicelluloses, such as xyloglucans with XXLG and XXXG modules, mannans, including galactomannans, and xylans. We could also show the even distribution of XXLG xyloglucans and galactomannans in the cell walls of thalli by immunocytochemistry. These results are discussed with regard to the cell wall proteome composition and in the context of the evolution of the green lineage. The cell wall polysaccharides of M. polymorpha illustrate the transition from the charophyte ancestors of terrestrial plants containing xyloglucans, xylans and mannans as hemicelluloses, and embryophytes which do not exhibit mannans as major primary cell wall polysaccharides.

Notes on Early Land Plants Today. 91*. Types and original material of liverworts (Marchantiophyta) in Herbarium Haussknecht (JE) collected in Central America

Notes on Early Land Plants Today. 91*. Types and original material of liverworts (Marchantiophyta) in Herbarium Haussknecht (JE) collected in Central America

The first homosporous lycophyte genome revealed the association between the recent dynamic accumulation of LTR-RTs and genome size variation.

The contrasting genome size between homosporous and heterosporous plants is fascinating. Different from the heterosporous seed plants and mainly homosporous ferns, the lycophytes are either heterosporous (Isoetales and Selaginellales) or homosporous (Lycopodiales). Many lycophytes are the resource plants of Huperzine A (HupA) which is invaluable for treating Alzheimer's disease. For the seed-free vascular plants, several high-quality genomes of heterosporous Selaginella, homosporous ferns (maidenhair fern, monkey spider tree fern), and heterosporous ferns (Azolla) have been published and provided important insights into the origin and evolution of early land plants. However, the homosporous lycophyte genome has not been decoded. Here, we assembled the first homosporous lycophyte genome and conducted comparative genomic analyses by applying a reformed pipeline for filtering out non-plant sequences. The obtained genome size of Lycopodium clavatum is 2.30Gb, distinguished in more than 85% repetitive elements of which 62% is long terminal repeat (LTR). This study disclosed a high birth rate and a low death rate of theLTR-RTs inhomosporous lycophytes, but the opposite occurs inheterosporous lycophytes. we proposethat the recent activity of LTR-RT is responsible forthe immense genome sizevariation between homosporous and heterosporous lycophytes. By combing Ks analysis with a phylogenetic approach, we discovered two whole genome duplications (WGD). Morover, we identified all thefive recognized key enzymes for the HupA biosynthetic pathway in the L. clavatum genome, but found this pathwayincompletein other major lineages of land plants. Overall, this study is of great importance for the medicinal utilization of lycophytes and the decoded genome data will be a key cornerstone to elucidate the evolution and biology of early vascular land plants.

Notes on Early Land Plants Today*. 81. Lectotypification of some names in Frullania

Five names in Frullania, F. convoluta Lindenb. et Hampe, F. herzogiana Steph. 1911 (= F. rio-janeirensis (Raddi) Ångstr., syn. nov.), F. herzogiana Steph. 1916 (= F. convoluta), F. convoluta var. ampliata Herzog (= F. convoluta, syn. nov.) and F. piliflora var. appendiculata Herzog (= F. peruviana Gottsche, syn. nov.) are lectotypified.

The effect of geological biases on our perception of early land plant radiation

AbstractThe Silurian–Devonian plant radiation was a critical development in the evolution of early terrestrial ecosystems. Characterizing the diversity dynamics of this radiation has been a focus of numerous studies. However, little is known about the impact of geological bias on our perception of this biodiversification. Here, we use a new, comprehensive compilation of plant occurrences from North America, together with a Macrostrat lithological dataset, to elucidate the relationships between the palaeobotanical and geological records of early land plants. Results show that observed raw diversity patterns at both species and genus rank are significantly correlated with fluctuations of sedimentary rock volume, especially of non‐marine fossiliferous deposits. The lack of terrestrial sedimentary deposits before the Emsian (Early Devonian) makes it difficult to obtain an accurate depiction of the pre‐Emsian plant diversification in North America. However, complementary analyses reveal that sampling‐standardized diversity patterns partially correct the raw trajectories, especially at the genus‐level if enough preserved non‐marine sediments are available for sampling. Our findings highlight that geological incompleteness remains a fundamental bias for describing early plant diversification. This indicates that, even when sampling is extensive, observed diversity patterns potentially reflect the heterogeneity of the rock record, which blurs our understanding of the early history of land vegetation.

Terrestrial surface stabilisation by modern analogues of the earliest land plants: A multi-dimensional imaging study.

The evolution of the first plant-based terrestrial ecosystems in the early Palaeozoic had a profound effect on the development of soils, the architecture of sedimentary systems, and shifts in global biogeochemical cycles. In part, this was due to the evolution of complex below-ground (root-like) anchorage systems in plants, which expanded and promoted plant-mineral interactions, weathering, and resulting surface sediment stabilisation. However, little is understood about how these micro-scale processes occurred, because of a lack of in situ plant fossils in sedimentary rocks/palaeosols that exhibit these interactions. Some modern plants (e.g., liverworts, mosses, lycophytes) share key features with the earliest land plants; these include uni- or multicellular rhizoid-like anchorage systems or simple roots, and the ability to develop below-ground networks through prostrate axes, and intimate associations with fungi, making them suitable analogues. Here, we investigated cryptogamic ground covers in Iceland and New Zealand to better understand these interactions, and how they initiate the sediment stabilisation process. We employed multi-dimensional and multi-scale imaging, including scanning electron microscopy (SEM) and X-ray Computed Tomography (μCT) of non-vascular liverworts (Haplomitriopsida and complex thalloids) and mosses, with additional imaging of vascular lycopods. We find that plants interact with their substrate in multiple ways, including: (1) through the development of extensive surface coverings as mats; (2) entrapment of sediment grains within and between networks of rhizoids; (3) grain entwining and adherence by rhizoids, through mucilage secretions, biofilm-like envelopment of thalli on surface grains; and (4) through grain entrapment within upright 'leafy' structures. Significantly, μCT imaging allows us to ascertain that rhizoids are the main method for entrapment and stabilisation of soil grains in the thalloid liverworts. This information provides us with details of how the earliest land plants may have significantly influenced early Palaeozoic sedimentary system architectures, promoted in situ weathering and proto-soil development, and how these interactions diversified over time with the evolution of new plant organ systems. Further, this study highlights the importance of cryptogamic organisms in the early stages of sediment stabilisation and soil formation today.

Preliminary results on reproductive organs and in situ spores of an early land plant Tichavekia grandis Pšenička et al. from Přídolí (upper Silurian) of the Prague Basin, Czech Republic

Reproductive organs and in situ spores isolated from early land plant Tichavekia grandis from the Kosov, Přídolí, upper Silurian of the Prague Basin are described in detail. Subspherical to reniform sporangia are 2.2–3.0 mm wide and 1.6–2.0 mm long, and are formed by a thick layer of coaly matter showing a marginal rim. Trilete crassitate in situ spores 17–32 µm in diameter have microgranulate, microspinate to rugulate sculpture of proximal surface and are not comparable with any dispersed and in situ Silurian spore taxa and, therefore, it may represent a new spore taxon. Palynological comparison with other cooksonioid taxa is made.

New insights into Silurian–Devonian palaeophytogeography

The Silurian–Devonian plant radiation was an event triggered by the progressive colonization of subaerial habitats. Nevertheless, it is still unclear whether this radiation was globally uniform or whether alternative diversification scenarios emerged depending on the geographical context. Here, we report on early land plant diversity patterns across different previously defined palaeogeographical units (i.e., Laurussia, Siberia, Kazakhstania, NE, NW and South Gondwana). Results reveal apparent diachronous events of diversification and extinction partly resulting from uneven sampling effort, especially in Gondwana. Global diversity patterns are most similar to the Laurussian curve suggesting that the observed global dynamics are mostly controlled by the historically best-sampled continents. Nevertheless, changes in floral composition through time become less prone to sampling biases, and reveal geographical disparities that indicate a non-random distribution of the Silurian–Devonian vegetation. Consequently, we further performed a set of multivariate analyses to revisit the palaeophytogeographical signal through four time-intervals (i.e., Silurian–Lochkovian, Pragian–Emsian, Middle and Late Devonian), which revealed that spatial differentiation of vegetation was mainly controlled by climatic conditions and to a lesser extent geographical barriers. Most importantly, we find the maximum provincialism during cooler periods such as during the Silurian–Lochkovian and Middle Devonian, whilst warmer periods (Pragian–Emsian and Late Devonian) coincided with increased cosmopolitanism among early land plants.

Early land plant remains from the uppermost Ordovician–?lowermost Silurian Cedarberg Formation of South Africa

Early land plant remains from the uppermost Ordovician–?lowermost Silurian Cedarberg Formation of South Africa

An early snapshot of plant-herbivore interactions: Psilophyton diakanthon sp. nov. from the Early Devonian of Gaspé (Quebec, Canada).

Trimerophytes are a plexus of early tracheophytes that form the base of the euphyllophyte clade and, thus, represent the link between the earliest land plants and modern-day ferns, sphenophytes, and seed plants. As the best-characterized trimerophyte, the genus Psilophyton occupies a key position in the euphyllophyte fossil record. We describe a new Psilophyton species that has implications for the evolution of plant-animal interactions. The fossil material is preserved by permineralization in the Lower Devonian (Emsian) Battery Point Formation (Québec, Canada) and was studied in serial sections using the cellulose acetate peel technique. Psilophyton diakanthon sp. nov. differs from other Psilophyton species in possessing fibers that form a discontinuous layer in the inner cortex and two distinct types of spinescent emergences whose anatomy and morphology are consistent with roles in anti-herbivore defense. Psilophyton diakanthon adds another species to an already diverse genus. Its two morphologically distinct types of spinescence suggest that herbivory was rampant in plant-animal interactions and demonstrate that anti-herbivory defenses had reached a previously unrecognized level of sophistication by 400 million years ago, in the Early Devonian.

Prototaxites reinterpreted as mega-rhizomorphs, facilitating nutrient transport in early terrestrial ecosystems.

The enigmatic fossil Prototaxites found in successions ranging from the Middle Ordovician to the Upper Devonian was originally described as having conifer affinity. The current debate, however, suggests that they probably represent gigantic algal-fungal symbioses. Our re-investigation of permineralized Prototaxites specimens from two localities, the Heider quarry in Germany and the Bordeaux quarry in Canada, reveals striking anatomical similarities with modern fungal rhizomorphs Armillaria mellea. We analysed extant fungal rhizomorphs and fossil Prototaxites through light microscopy of their anatomy, Fourier transform infrared spectroscopy, X-ray microscopy, and Raman spectroscopy. Based on these comparisons, we interpret the Prototaxites as fungi. The detailed preservation of cell walls and possible organelles seen in transverse sections of Prototaxites reveal that fossilization initiated while the organism was alive, inhibiting the collapse of delicate cellular structures. Prototaxites has been interpreted to grow vertically by many previous workers. Here we propose an alternative view that Prototaxites represents a complex hyphal aggregation (rhizomorph) that may have grown horizontally similar to modern complex aggregated mycelial growth forms, such as cords and rhizomorphs. Their main function was possibly to redistribute water and nutrition from nutrient-rich to nutrient-poor areas facilitating the expansion for early land plant communities.