Common Ancestor Of Vascular Plants Research Articles

Identification of genes differentially expressed between prostrate shoots and erect shoots in the lycophyte Selaginella nipponica using an RNA-seq approach.

Lycophytes are the earliest vascular plants and Selaginella is the most studied genus among them. Prostrate shoots are produced during early growth and erect shoots emerge later in S. nipponica, thus providing an opportunity for exploring the evolution of the mechanism underlying the transition between growth phases. Six libraries were sequenced for the prostrate and the erect shoots, and a total of 206 768 genes were identified. Some genes were differentially expressed in prostate and erect shoot, with relatively high expression in the prostate shoots being related to hormone responses and defence reactions, while higher expression in the erect shoots was related to spore formation and shoot development. Some SPL genes possessed a miR156 binding site and were highly expressed in the erect shoots, while AP2-like genes were more highly expressed in the prostrate shoots but simultaneously lacked any miR172 binding site. MiR156 was detected at a higher concentration in the prostrate shoots. Thus, the mechanism for the vegetative to reproductive transition of sporophytes probably originated in the common ancestor of vascular plants and must have experienced stepwise development during evolution.

Mysteries of the bryophyte-tracheophyte transition revealed: enter the eophytes.

This article is a Commentary on Edwards et al. (2022a,b), 233: 1440–1455 and 1456–1465.

The RGF/GLV/CLEL Family of Short Peptides Evolved Through Lineage-Specific Losses and Diversification and Yet Conserves Its Signaling Role Between Vascular Plants and Bryophytes.

Short secreted plant peptides act as key signaling molecules and control a plethora of developmental and physiological processes. The ROOT GROWTH FACTOR (RGF)/GOLVEN (GLV)/CLE-Like (CLEL) family of peptides was discovered to be involved in root development in Arabidopsis thaliana. In contrast to active research efforts, which have been revealing receptors and downstream signaling components, little attention has been paid to evolutionary processes that shaped the RGF signaling system as we know it in angiosperms today. As a first step toward understanding how RGF signaling emerged and evolved, this study aimed to elucidate the phylogenetic distribution and functional conservation of RGF-like sequences. Using publicly available, genome and transcriptome data, RGF-like sequences were searched in 27 liverworts, 22 mosses, 8 hornworts, 23 lycophytes, 23 ferns, 38 gymnosperms, and 8 angiosperms. This led to the identification of more than four hundreds of RGF-like sequences in all major extant land plant lineages except for hornworts. Sequence comparisons within and between taxonomic groups identified lineage-specific characters. Notably, one of the two major RGF subgroups, represented by A. thaliana RGF6/GLV1/CLEL6, was found only in vascular plants. This subgroup, therefore, likely emerged in a common ancestor of vascular plants after its divergence from bryophytes. In bryophytes, our results infer independent losses of RGF-like sequences in mosses and hornworts. On the other hand, a single, highly similar RGF-like sequence is conserved in liverworts, including Marchantia polymorpha, a genetically tractable model species. When constitutively expressed, the M. polymorpha RGF-like sequence (MpRGF) affected plant development and growth both in A. thaliana and M. polymorpha. This suggests that MpRGF can exert known RGF-like effects and that MpRGF is under transcriptional control so that its potent activities are precisely controlled. These data suggest that RGFs are conserved as signaling molecules in both vascular plants and bryophytes and that lineage-specific diversification has increased sequence variations of RGFs. All together, our findings form a basis for further studies into RGF peptides and their receptors, which will contribute to our understandings of how peptide signaling pathways evolve.

What can lycophytes teach us about plant evolution and development? Modern perspectives on an ancient lineage.

All Evo-Devo studies rely on representative sampling across the tree of interest to elucidate evolutionary trajectories through time. In land plants, genetic resources are well established in model species representing lineages including bryophytes (mosses, liverworts, and hornworts), monilophytes (ferns and allies), and seed plants (gymnosperms and flowering plants), but few resources are available for lycophytes (club mosses, spike mosses, and quillworts). Living lycophytes are a sister group to the euphyllophytes (the fern and seed plant clade), and have retained several ancestral morphological traits despite divergence from a common ancestor of vascular plants around 420 million years ago. This sister relationship offers a unique opportunity to study the conservation of traits such as sporophyte branching, vasculature, and indeterminacy, as well as the convergent evolution of traits such as leaves and roots which have evolved independently in each vascular plant lineage. To elucidate the evolution of vascular development and leaf formation, molecular studies using RNA Seq, quantitative reverse transcription polymerase chain reaction, in situ hybridisation and phylogenetics have revealed the diversification and expression patterns of KNOX, ARP, HD-ZIP, KANADI, and WOX gene families in lycophytes. However, the molecular basis of further trait evolution is not known. Here we describe morphological traits of living lycophytes and their extinct relatives, consider the molecular underpinnings of trait evolution and discuss future research required in lycophytes to understand the key evolutionary innovations enabling the growth and development of all vascular plants.

Bilaterally symmetric axes with rhizoids composed the rooting structure of the common ancestor of vascular plants.

There are two general types of rooting systems in extant land plants: gametophyte rhizoids and sporophyte root axes. These structures carry out the rooting function in the free-living stage of almost all land plant gametophytes and sporophytes, respectively. Extant vascular plants develop a dominant, free-living sporophyte on which roots form, with the exception of a small number of taxa that have secondarily lost roots. However, fossil evidence indicates that early vascular plants did not develop sporophyte roots. We propose that the common ancestor of vascular plants developed a unique rooting system—rhizoidal sporophyte axes. Here we present a synthesis and reinterpretation of the rootless sporophytes of Horneophyton lignieri, Aglaophyton majus, Rhynia gwynne-vaughanii and Nothia aphylla preserved in the Rhynie chert. We show that the sporophyte rooting structures of all four plants comprised regions of plagiotropic (horizontal) axes that developed unicellular rhizoids on their underside. These regions of axes with rhizoids developed bilateral symmetry making them distinct from the other regions which were radially symmetrical. We hypothesize that rhizoidal sporophyte axes constituted the rooting structures in the common ancestor of vascular plants because the phylogenetic positions of these plants span the origin of the vascular lineage.This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.

The Huperzia selago Shoot Tip Transcriptome Sheds New Light on the Evolution of Leaves.

Lycopodiophyta—consisting of three orders, Lycopodiales, Isoetales and Selaginellales, with different types of shoot apical meristems (SAMs)—form the earliest branch among the extant vascular plants. They represent a sister group to all other vascular plants, from which they differ in that their leaves are microphylls—that is, leaves with a single, unbranched vein, emerging from the protostele without a leaf gap—not megaphylls. All leaves represent determinate organs originating on the flanks of indeterminate SAMs. Thus, leaf formation requires the suppression of indeterminacy, that is, of KNOX transcription factors. In seed plants, this is mediated by different groups of transcription factors including ARP and YABBY.We generated a shoot tip transcriptome of Huperzia selago (Lycopodiales) to examine the genes involved in leaf formation. Our H. selago transcriptome does not contain any ARP homolog, although transcriptomes of Selaginella spp. do. Surprisingly, we discovered a YABBY homolog, although these transcription factors were assumed to have evolved only in seed plants.The existence of a YABBY homolog in H. selago suggests that YABBY evolved already in the common ancestor of the vascular plants, and subsequently was lost in some lineages like Selaginellales, whereas ARP may have been lost in Lycopodiales. The presence of YABBY in the common ancestor of vascular plants would also support the hypothesis that this common ancestor had a simplex SAM. Furthermore, a comparison of the expression patterns of ARP in shoot tips of Selaginella kraussiana (Harrison CJ, etal. 2005. Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434(7032):509–514.) and YABBY in shoot tips of H. selago implies that the development of microphylls, unlike megaphylls, does not seem to depend on the combined activities of ARP and YABBY. Altogether, our data show that Lycopodiophyta are a diverse group; so, in order to understand the role of Lycopodiophyta in evolution, representatives of Lycopodiales, Selaginellales, as well as of Isoetales, have to be examined.

Complete mitochondrial genomes from the ferns Ophioglossum californicum and Psilotum nudum are highly repetitive with the largest organellar introns

Currently, complete mitochondrial genomes (mitogenomes) are available from all major land plant lineages except ferns. Sequencing of fern mitogenomes could shed light on the major evolutionary transitions that established mitogenomic diversity among extant lineages. In this study, we generated complete mitogenomes from the adder's tongue fern (Ophioglossum californicum) and the whisk fern (Psilotum nudum). The Psilotum mitogenome (628kb) contains a rich complement of genes and introns, some of which are the largest of any green plant organellar genome. In the Ophioglossum mitogenome (372kb), gene and intron content is slightly reduced, including the loss of all four mitochondrial ccm genes. Transcripts of nuclear Ccm genes also were not detected, suggesting loss of the entire mitochondrial cytochrome c maturation pathway from Ophioglossum. Both fern mitogenomes are highly repetitive, yet they show extremely low levels of active recombination. Transcriptomic sequencing uncovered ˜1000 sites of C-to-U RNA editing in both species, plus a small number (<60) of U-to-C edit sites. Overall, the first mitochondrial genomes of ferns show a mix of features shared with lycophytes and/or seed plants and several novel genomic features, enabling a robust reconstruction of the mitogenome in the common ancestor of vascular plants.

Conserved Gene Expression Programs in Developing Roots from Diverse Plants.

The molecular basis for the origin and diversification of morphological adaptations is a central issue in evolutionary developmental biology. Here, we defined temporal transcript accumulation in developing roots from seven vascular plants, permitting a genome-wide comparative analysis of the molecular programs used by a single organ across diverse species. The resulting gene expression maps uncover significant similarity in the genes employed in roots and their developmental expression profiles. The detailed analysis of a subset of 133 genes known to be associated with root development in Arabidopsis thaliana indicates that most of these are used in all plant species. Strikingly, this was also true for root development in a lycophyte (Selaginella moellendorffii), which forms morphologically different roots and is thought to have evolved roots independently. Thus, despite vast differences in size and anatomy of roots from diverse plants, the basic molecular mechanisms employed during root formation appear to be conserved. This suggests that roots evolved in the two major vascular plant lineages either by parallel recruitment of largely the same developmental program or by elaboration of an existing root program in the common ancestor of vascular plants.

Evolutionary Divergence of Plant Borate Exporters and Critical Amino Acid Residues for the Polar Localization and Boron-Dependent Vacuolar Sorting of AtBOR1.

Boron (B) is an essential micronutrient for plants but is toxic when accumulated in excess. The plant BOR family encodes plasma membrane-localized borate exporters (BORs) that control translocation and homeostasis of B under a wide range of conditions. In this study, we examined the evolutionary divergence of BORs among terrestrial plants and showed that the lycophyte Selaginella moellendorffii and angiosperms have evolved two types of BOR (clades I and II). Clade I includes AtBOR1 and homologs previously shown to be involved in efficient transport of B under conditions of limited B availability. AtBOR1 shows polar localization in the plasma membrane and high-B-induced vacuolar sorting, important features for efficient B transport under low-B conditions, and rapid down-regulation to avoid B toxicity. Clade II includes AtBOR4 and barley Bot1 involved in B exclusion for high-B tolerance. We showed, using yeast complementation and B transport assays, that three genes in S. moellendorffii, SmBOR1 in clade I and SmBOR3 and SmBOR4 in clade II, encode functional BORs. Furthermore, amino acid sequence alignments identified an acidic di-leucine motif unique in clade I BORs. Mutational analysis of AtBOR1 revealed that the acidic di-leucine motif is required for the polarity and high-B-induced vacuolar sorting of AtBOR1. Our data clearly indicated that the common ancestor of vascular plants had already acquired two types of BOR for low- and high-B tolerance, and that the BOR family evolved to establish B tolerance in each lineage by adapting to their environments.

On the phylogeny, expression and targeting of plant nucleoside diphosphate kinases

The plant nucleoside diphosphate kinase (NDPK, EC 2.7.4.6) gene family consists of three groups whose gene products are found in different subcellular locations. In this study we discuss the evolutionary history, localization and expression of the NDPK genes, addressing the question of functional specialization of the different NDPKs. A phylogenetic analysis revealed that the three NDPK isoforms were present already in the last common ancestor of vascular plants and mosses. Our data also imply that the NDPK3 genes possess a higher degree of conservation than the NDPK1 and NDPK2 genes. The expression levels of the different NDPKs in Arabidopsis thaliana inflorescences, leaves and roots were evaluated using quantitative PCR as well as in silico methods. This analysis showed that NDPK1 is the most highly expressed NDPK gene in all the studied tissues. NDPK3a has the second highest NDPK expression, while NDPK3b is expressed to a very low extent. However, expression of NDPK3b is elevated in inflorescence tissue. In situ hybridization experiments performed on inflorescences showed NDPK3a expression in actively dividing cells. NDPK3b expression was observed during later stages of flower development, specifically in the tapetum, ovules and petals. Additionally, we show that an NDPK3 protein is able to direct the green fluorescent protein to both mitochondria and chloroplasts using transient expression in leaf protoplasts. The dual localisation of NDPK3 was confirmed by Western blot, which also demonstrated that the majority of the NDPK3 protein is found in the mitochondria.

Distribution of introns in the mitochondrial gene nad1 in land plants: phylogenetic and molecular evolutionary implications

Forty-six species of diverse land plants were investigated by sequencing for their intron content in the mitochondrial gene nad1. A total of seven introns, all belonging to group II, were found, and two were newly discovered in this study. All 13 liverworts examined contain no intron, the same condition as in green algae. Mosses and hornworts, however, share one intron by themselves and another one with vascular plants. These intron distribution patterns are consistent with the hypothesis that liverworts represent the basal-most land plants and that the two introns were gained in the common ancestor of mosses–hornworts–vascular plants after liverworts had diverged. Hornworts also possess a unique intron of their own. A fourth intron was found only in Equisetum L., Marattiaceae, Ophioglossum L., Osmunda L., Asplenium L., and Adiantum L., and was likely acquired in their common ancestor, which supports the monophyly of moniliformopses. Three introns that were previously characterized in angiosperms and a few pteridophytes are now all extended to lycopods, and were likely gained in the common ancestor of vascular plants. Phylogenetic analyses of the intron sequences recovered topologies mirroring those of the plants, suggesting that the introns have all been vertically inherited. All seven nad1 group II introns show broad phylogenetic distribution patterns, with the narrowest being in moniliformopses and hornworts, lineages that date back to at least the Devonian (345 million years ago) and Silurian (435 million years ago), respectively. Hence, these introns must have invaded the genes via ancient transpositional events during the early stage of land plant evolution. Potentially heavy RNA editing was observed in nad1 of Haplomitrium Dedecek, Takakia Hatt. & Inoue, hornworts, Isoetes L., Ophioglossum, and Asplenium. A new nomenclature is proposed for group II introns.