scholarly journals The Genome of the Charophyte Alga Penium margaritaceum Bears Footprints of the Evolutionary Origins of Land Plants

2019 ◽  
Author(s):  
Chen Jiao ◽  
Iben Sørensen ◽  
Xuepeng Sun ◽  
Honghe Sun ◽  
Hila Behar ◽  
...  

ABSTRACTThe colonization of land by plants was a pivotal event in the history of the biosphere, and yet the underlying evolutionary features and innovations of the first land plant ancestors are not well understood. Here we present the genome sequence of the unicellular alga Penium margaritaceum, a member of the Zygnematophyceae, the sister lineage to land plants. The P. margaritaceum genome has a high proportion of repeat sequences, which are associated with massive segmental gene duplications, likely facilitating neofunctionalization. Compared with earlier diverging plant lineages, P. margaritaceum has uniquely expanded repertoires of gene families, signaling networks and adaptive responses, supporting its phylogenetic placement and highlighting the evolutionary trajectory towards terrestrialization. These encompass a broad range of physiological processes and cellular structures, such as large families of extracellular polymer biosynthetic and modifying enzymes involved in cell wall assembly and remodeling. Transcriptome profiling of cells exposed to conditions that are common in terrestrial habitats, namely high light and desiccation, further elucidated key adaptations to the semi-aquatic ecosystems that are home to the Zygnematophyceae. Such habitats, in which a simpler body plan would be advantageous, likely provided the evolutionary crucible in which selective pressures shaped the transition to land. Earlier diverging charophyte lineages that are characterized by more complex land plant-like anatomies have either remained exclusively aquatic, or developed alternative life styles that allow periods of desiccation.

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Sumanth K Mutte ◽  
Hirotaka Kato ◽  
Carl Rothfels ◽  
Michael Melkonian ◽  
Gane Ka-Shu Wong ◽  
...  

The small signaling molecule auxin controls numerous developmental processes in land plants, acting mostly by regulating gene expression. Auxin response proteins are represented by large families of diverse functions, but neither their origin nor their evolution is understood. Here, we use a deep phylogenomics approach to reconstruct both the origin and the evolutionary trajectory of all nuclear auxin response protein families. We found that, while all subdomains are ancient, a complete auxin response mechanism is limited to land plants. Functional phylogenomics predicts defined steps in the evolution of response system properties, and comparative transcriptomics across six ancient lineages revealed how these innovations shaped a sophisticated response mechanism. Genetic analysis in a basal land plant revealed unexpected contributions of ancient non-canonical proteins in auxin response as well as auxin-unrelated function of core transcription factors. Our study provides a functional evolutionary framework for understanding diverse functions of the auxin signal.


2017 ◽  
Author(s):  
Sumanth K. Mutte ◽  
Hirotaka Kato ◽  
Carl Rothfels ◽  
Michael Melkonian ◽  
Gane Ka-Shu Wong ◽  
...  

AbstractThe small signaling molecule auxin controls numerous developmental processes in land plants, acting mostly by regulating gene expression. Auxin response proteins are represented by large families of diverse functions, but neither their origin nor their evolution is understood. Here we use a deep phylogenomics approach to reconstruct both the origin and the evolutionary trajectory of all nuclear auxin response protein families. We found that, while all subdomains are ancient, a complete auxin response mechanism is limited to land plants. Functional phylogenomics predicts defined steps in the evolution of response system properties, and comparative transcriptomics across six ancient lineages revealed how these innovations shaped a sophisticated response mechanism. Genetic analysis in a basal land plant revealed unexpected contributions of ancient non-canonical proteins in auxin response as well as auxin-unrelated function of core transcription factors. Our study provides a functional evolutionary framework for understanding diverse functions of the auxin signal.


2021 ◽  
Author(s):  
Sophie de Vries ◽  
Janine MR Fuerst-Jansen ◽  
Iker Irisarri ◽  
Amra Dhabalia Ashok ◽  
Till Ischebeck ◽  
...  

Land plants constantly respond to fluctuations in their environment. Part of their response is the production of a diverse repertoire of specialized metabolites. One of the foremost sources for metabolites relevant to environmental responses is the phenylpropanoid pathway, which was long thought to be a land plant-specific adaptation shaped by selective forces in the terrestrial habitat. Recent data have however revealed that streptophyte algae, the algal relatives of land plants, have candidates for the genetic toolkit for phenylpropanoid biosynthesis and produce phenylpropanoid-derived metabolites. Using phylogenetic and sequence analyses, we here show that the enzyme families that orchestrate pivotal steps in phenylpropanoid biosynthesis have independently undergone pronounced radiations and divergence in multiple lineages of major groups of land plants; sister to many of these radiated gene families are streptophyte algal candidates for these enzymes. These radiations suggest a high evolutionary versatility in the enzyme families involved in the phenylpropanoid-derived metabolism across embryophytes. We suggest that this versatility likely translates into functional divergence and may explain the key to one of the defining traits of embryophytes: a rich specialized metabolism.


Author(s):  
John L. Bowman ◽  
Eduardo Flores Sandoval ◽  
Hirotaka Kato

2016 ◽  
Author(s):  
Florencia Berruezo ◽  
Flavio S. J. de Souza ◽  
Pablo I. Picca ◽  
Sergio I. Nemirovsky ◽  
Leandro Martinez-Tosar ◽  
...  

AbstractMicroRNAs (miRNAs) are short, single stranded RNA molecules that regulate the stability and translation of messenger RNAs in diverse eukaryotic groups. Several miRNA genes are of ancient origin and have been maintained in the genomes of animal and plant taxa for hundreds of millions of years, and functional studies indicate that ancient miRNAs play key roles in development and physiology. In the last decade, genome and small RNA (sRNA) sequencing of several plant species have helped unveil the evolutionary history of land plant miRNAs. Land plants are divided into bryophytes (liverworts, mosses), lycopods (clubmosses and spikemosses), monilophytes (ferns and horsetails), gymnosperms (cycads, conifers and allies) and angiosperms (flowering plants). Among these, the fern group occupies a key phylogenetic position, since it represents the closest extant cousin taxon of seed plants, i.e. gymno- and angiosperms. However, in spite of their evolutionary, economic and ecological importance, no fern genome has been sequenced yet and few genomic resources are available for this group. Here, we sequenced the small RNA fraction of an epiphytic South American fern, Pleopeltis minima (Polypodiaceae), and compared it to plant miRNA databases, allowing for the identification of miRNA families that are shared by all land plants, shared by all vascular plants (tracheophytes) or shared by euphyllophytes (ferns and seed plants) only. Using the recently described transcriptome of another fern, Lygodium japonicum, we also estimated the degree of conservation of fern miRNA targets in relation to other plant groups. Our results pinpoint the origin of several miRNA families in the land plant evolutionary tree with more precision and are a resource for future genomic and functional studies of fern miRNAs.


2021 ◽  
Vol 22 (23) ◽  
pp. 13036
Author(s):  
Normig M. Zoghbi-Rodríguez ◽  
Samuel David Gamboa-Tuz ◽  
Alejandro Pereira-Santana ◽  
Luis C. Rodríguez-Zapata ◽  
Lorenzo Felipe Sánchez-Teyer ◽  
...  

Nitrate transporter 2 (NRT2) and NRT3 or nitrate-assimilation-related 2 (NAR2) proteins families form a two-component, high-affinity nitrate transport system, which is essential for the acquisition of nitrate from soils with low N availability. An extensive phylogenomic analysis across land plants for these families has not been performed. In this study, we performed a microsynteny and orthology analysis on the NRT2 and NRT3 genes families across 132 plants (Sensu lato) to decipher their evolutionary history. We identified significant differences in the number of sequences per taxonomic group and different genomic contexts within the NRT2 family that might have contributed to N acquisition by the plants. We hypothesized that the greater losses of NRT2 sequences correlate with specialized ecological adaptations, such as aquatic, epiphytic, and carnivory lifestyles. We also detected expansion on the NRT2 family in specific lineages that could be a source of key innovations for colonizing contrasting niches in N availability. Microsyntenic analysis on NRT3 family showed a deep conservation on land plants, suggesting a high evolutionary constraint to preserve their function. Our study provides novel information that could be used as guide for functional characterization of these gene families across plant lineages.


2020 ◽  
Vol 71 (11) ◽  
pp. 3270-3278 ◽  
Author(s):  
Burkhard Becker ◽  
Xuehuan Feng ◽  
Yanbin Yin ◽  
Andreas Holzinger

Abstract The present review summarizes the effects of desiccation in streptophyte green algae, as numerous experimental studies have been performed over the past decade particularly in the early branching streptophyte Klebsormidium sp. and the late branching Zygnema circumcarinatum. The latter genus gives its name to the Zygenmatophyceae, the sister group to land plants. For both organisms, transcriptomic investigations of desiccation stress are available, and illustrate a high variability in the stress response depending on the conditions and the strains used. However, overall, the responses of both organisms to desiccation stress are very similar to that of land plants. We highlight the evolution of two highly regulated protein families, the late embryogenesis abundant (LEA) proteins and the major intrinsic protein (MIP) family. Chlorophytes and streptophytes encode LEA4 and LEA5, while LEA2 have so far only been found in streptophyte algae, indicating an evolutionary origin in this group. Within the MIP family, a high transcriptomic regulation of a tonoplast intrinsic protein (TIP) has been found for the first time outside the embryophytes in Z. circumcarinatum. The MIP family became more complex on the way to terrestrialization but simplified afterwards. These observations suggest a key role for water transport proteins in desiccation tolerance of streptophytes.


1986 ◽  
Vol 123 (4) ◽  
pp. 445-454 ◽  
Author(s):  
J. Gray ◽  
J. N. Theron ◽  
A. J. Boucot

AbstractThe first occurrence of Early Paleozoic land plants is reported from South Africa. The plant remains are small, compact tetrahedral spore tetrads. They occur abundantly in the Soom Shale Member of the Cedarberg Formation, Table Mountain Group. Marine? phytoplankton (sphaeromorphs or leiospheres) occur with the spore tetrads in all samples. Rare chitinozoans are found in half the samples. Together with similar spore tetrads from the Paraná Basin (Gray et al. 1985) these are the first well-documented records of Ashgill and/or earlier Llandovery land plants from the Malvinokaffric Realm, and from the African continent south of Libya. These spore tetrads have botanical, evolutionary, and biogeographic significance. Their size in comparison with spore tetrads from stratigraphic sections throughout eastern North America, suggests that an earliest Llandovery age is more probable for the Soom Shale Member, although a latest Ordovician age cannot be discounted. The age of the brachiopods in the overlying Disa Siltstone Member has been in contention for over a decade. Both Ashgillian and Early Llandovery ages have been proposed. The age of the underlying Soom Shale Member based on plant spores and trilobites (earliest Llandovery or latest Ashgillian) suggests that the Disa Siltstone Member is also likely to be of Early Llandovery age, although the distance between the Soom Shale Member spore-bearing locality and rocks to the south yielding abundant invertebrate body fossils at one locality is great enough to permit diachroneity.


2000 ◽  
Vol 355 (1398) ◽  
pp. 769-793 ◽  
Author(s):  
Karen Sue Renzaglia ◽  
R. Joel Duff ◽  
Daniel L. Nickrent ◽  
David J. Garbary

As the oldest extant lineages of land plants, bryophytes provide a living laboratory in which to evaluate morphological adaptations associated with early land existence. In this paper we examine reproductive and structural innovations in the gametophyte and sporophyte generations of hornworts, liverworts, mosses and basal pteridophytes. Reproductive features relating to spermatogenesis and the architecture of motile male gametes are overviewed and evaluated from an evolutionary perspective. Phylogenetic analyses of a data set derived from spermatogenesis and one derived from comprehensive morphogenetic data are compared with a molecular analysis of nuclear and mitochondrial small subunit rDNA sequences. Although relatively small because of a reliance on water for sexual reproduction, gametophytes of bryophytes are the most elaborate of those produced by any land plant. Phenotypic variability in gametophytic habit ranges from leafy to thalloid forms with the greatest diversity exhibited by hepatics. Appendages, including leaves, slime papillae and hairs, predominate in liverworts and mosses, while hornwort gametophytes are strictly thalloid with no organized external structures. Internalization of reproductive and vegetative structures within mucilage–filled spaces is an adaptive strategy exhibited by hornworts. The formative stages of gametangial development are similar in the three bryophyte groups, with the exception that in mosses apical growth is intercalated into early organogenesis, a feature echoed in moss sporophyte ontogeny. A monosporangiate, unbranched sporophyte typifies bryophytes, but developmental and structural innovations suggest the three bryophyte groups diverged prior to elaboration of this generation. Sporophyte morphogenesis in hornworts involves non–synchronized sporogenesis and the continued elongation of the single sporangium, features unique among archegoniates. In hepatics, elongation of the sporophyte seta and archegoniophore is rapid and requires instantaneous wall expandability and hydrostatic support. Unicellular, spiralled elaters and capsule dehiscence through the formation of four regular valves are autapomorphies of liverworts. Sporophytic sophistications in the moss clade include conducting tissue, stomata, an assimilative layer and an elaborate peristome for extended spore dispersal. Characters such as stomata and conducting cells that are shared among sporophytes of mosses, hornworts and pteridophytes are interpreted as parallelisms and not homologies. Our phylogenetic analysis of three different data sets is the most comprehensive to date and points to a single phylogenetic solution for the evolution of basal embryophytes. Hornworts are supported as the earliest divergent embryophyte clade with a moss/liverwort clade sister to tracheophytes. Among pteridophytes, lycophytes are monophyletic and an assemblage containing ferns, Equisetum and psilophytes is sister to seed plants. Congruence between morphological and molecular hypotheses indicates that these data sets are tracking the same phylogenetic signal and reinforces our phylogenetic conclusions. It appears that total evidence approaches are valuable in resolving ancient radiations such as those characterizing the evolution of early embryophytes. More information on land plant phylogeny can be found at: http://www.science.siu.edu/landplants/index.html.


2017 ◽  
Vol 59 (4) ◽  
pp. 240-260 ◽  
Author(s):  
Frances C. Sussmilch ◽  
Timothy J. Brodribb ◽  
Scott A. M. McAdam

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