scholarly journals Recruitment of archaeal DTD is a key event toward the emergence of land plants

2021 ◽  
Vol 7 (6) ◽  
pp. eabe8890
Author(s):  
Mohd Mazeed ◽  
Raghvendra Singh ◽  
Pradeep Kumar ◽  
Ankit Roy ◽  
Bakthisaran Raman ◽  
...  

Streptophyte algae emerged as a land plant with adaptations that eventually led to terrestrialization. Land plants encounter a range of biotic and abiotic stresses that elicit anaerobic stress responses. Here, we show that acetaldehyde, a toxic metabolite of anaerobic stress, targets and generates ethyl adducts on aminoacyl-tRNA, a central component of the translation machinery. However, elongation factor thermo unstable (EF-Tu) safeguards l-aminoacyl-tRNA, but not d-aminoacyl-tRNA, from being modified by acetaldehyde. We identified a unique activity of archaeal-derived chiral proofreading module, d-aminoacyl-tRNA deacylase 2 (DTD2), that removes N-ethyl adducts formed on d-aminoacyl-tRNAs (NEDATs). Thus, the study provides the molecular basis of ethanol and acetaldehyde hypersensitivity in DTD2 knockout plants. We uncovered an important gene transfer event from methanogenic archaea to the ancestor of land plants. While missing in other algal lineages, DTD2 is conserved from streptophyte algae to land plants, suggesting its role toward the emergence and evolution of land plants.

2020 ◽  
Author(s):  
Mohd Mazeed ◽  
Raghvendra Singh ◽  
Pradeep Kumar ◽  
Bakthisaran Raman ◽  
Shobha P. Kruparani ◽  
...  

AbstractLand plant evolution is a major leap in the history of life that took place during the Neoproterozoic Era (∼800 Mya). Charophyceae, a class of rhyzophytic green algae emerged as a land plant with innovations in biochemical, cytological and developmental adaptations and played a crucial role in establishing life on the land1,2. One such striking architectural innovation is “root” that experience harsh environmental assaults such as floods, waterlogging and therefore is the epicentre for anaerobic fermentation, which produces toxic acetaldehyde3. Here, we show that such produced acetaldehyde makes N-ethyl-adducts on a central component of translation machinery aa-tRNA. The Plant kingdom is unique among life forms in possessing two chirality-based proofreading systems represented by D-aminoacyl-tRNA deacylases (DTD1 and DTD2), derived from Bacteria and Archaea4. We identified a unique role of archaeal derived chiral proofreading module DTD2 that selectively deacylates N-ethyl-D-aminoacyl-tRNAs (NEDATs) in plants. NEDAT deacylase function is exclusive to DTD2, as no other proofreading modules with similar substrates like canonical DTD1 and peptidyl-tRNA hydrolase (PTH) can clear NEDATs. Thus, the study elucidates the cause of hypersensitivity of DTD2 knockout plants for both ethanol and acetaldehyde. We further show NEDAT elimination is rooted in Archaea which possess the biosynthesis machinery for ethanol fermentation similar to plants. While absent in other algal branches, DTD2 can be identified in plants from land plant ancestors-Charophytes onwards. DTD2 is the only gene that has only archaeal origin among the genes ascribed for architectural and genomic innovations that happened in the land plant ancestors. The work has uncovered an important gene transfer event from methanogenic archaea to the charophytes in the oldest terrestrial ecosystem bog that contains excess of D-amino acids and deprived of oxygen.


Biomolecules ◽  
2021 ◽  
Vol 11 (8) ◽  
pp. 1207
Author(s):  
José Moya-Cuevas ◽  
Marta-Marina Pérez-Alonso ◽  
Paloma Ortiz-García ◽  
Stephan Pollmann

The diversification of land plants largely relies on their ability to cope with constant environmental fluctuations, which negatively impact their reproductive fitness and trigger adaptive responses to biotic and abiotic stresses. In this limiting landscape, cumulative research attention has centred on deepening the roles of major phytohormones, mostly auxins, together with brassinosteroids, jasmonates, and abscisic acid, despite the signaling networks orchestrating the crosstalk among them are so far only poorly understood. Accordingly, this review focuses on the Arabidopsis Amidase Signature (AS) superfamily members, with the aim of highlighting the hitherto relatively underappreciated functions of AMIDASE1 (AMI1) and FATTY ACID AMIDE HYDROLASE (FAAH), as comparable coordinators of the growth-defense trade-off, by balancing auxin and ABA homeostasis through the conversion of their likely bioactive substrates, indole-3-acetamide and N-acylethanolamine.


Author(s):  
José Moya-Cuevas ◽  
Marta-Marina Pérez-Alonso ◽  
Paloma Ortiz-García ◽  
Stephan Pollmann

The evolutionary success of land plants largely relies on their ability to cope with constant environmental fluctuations, which negatively impact their reproductive fitness and trigger adaptational responses to biotic and abiotic stresses. In this challenging scenario, comprehensive research efforts so far aimed at depicting the roles of well-known phytohormones, mainly auxins, along with brassinosteroids, jasmonates, and abscisic acid, although the signaling networks coordinating the crosstalk among them remains vaguely understood. Accordingly, this review focuses on the Arabidopsis Amidase Signature (AS) superfamily members, highlighting the hitherto relatively underappreciated functions of AMIDASE1 (AMI1) and FATTY ACID AMIDE HYDROLASE (FAAH), as crucial coordinators of the growth-defense response trade-off by modulating auxin and ABA homeostasis.


2020 ◽  
Vol 71 (11) ◽  
pp. 3254-3269 ◽  
Author(s):  
Janine M R Fürst-Jansen ◽  
Sophie de Vries ◽  
Jan de Vries

Abstract Embryophytes (land plants) can be found in almost any habitat on the Earth’s surface. All of this ecologically diverse embryophytic flora arose from algae through a singular evolutionary event. Traits that were, by their nature, indispensable for the singular conquest of land by plants were those that are key for overcoming terrestrial stressors. Not surprisingly, the biology of land plant cells is shaped by a core signaling network that connects environmental cues, such as stressors, to the appropriate responses—which, thus, modulate growth and physiology. When did this network emerge? Was it already present when plant terrestrialization was in its infancy? A comparative approach between land plants and their algal relatives, the streptophyte algae, allows us to tackle such questions and resolve parts of the biology of the earliest land plants. Exploring the biology of the earliest land plants might shed light on exactly how they overcame the challenges of terrestrialization. Here, we outline the approaches and rationale underlying comparative analyses towards inferring the genetic toolkit for the stress response that aided the earliest land plants in their conquest of land.


Plants ◽  
2021 ◽  
Vol 10 (1) ◽  
pp. 178
Author(s):  
Ana L. Villagómez-Aranda ◽  
Luis F. García-Ortega ◽  
Irineo Torres-Pacheco ◽  
Ramón G. Guevara-González

Epigenetic regulation is a key component of stress responses, acclimatization and adaptation processes in plants. DNA methylation is a stable mark plausible for the inheritance of epigenetic traits, such that it is a potential scheme for plant breeding. However, the effect of modulators of stress responses, as hydrogen peroxide (H2O2), in the methylome status has not been elucidated. A transgenic tobacco model to the CchGLP gene displayed high H2O2 endogen levels correlated with biotic and abiotic stresses resistance. The present study aimed to determine the DNA methylation status changes in the transgenic model to obtain more information about the molecular mechanism involved in resistance phenotypes. The Whole-genome bisulfite sequencing analysis revealed a minimal impact of overall levels and distribution of methylation. A total of 9432 differential methylated sites were identified in distinct genome regions, most of them in CHG context, with a trend to hypomethylation. Of these, 1117 sites corresponded to genes, from which 83 were also differentially expressed in the plants. Several genes were associated with respiration, energy, and calcium signaling. The data obtained highlighted the relevance of the H2O2 in the homeostasis of the system in stress conditions, affecting at methylation level and suggesting an association of the H2O2 in the physiological adaptation to stress functional linkages may be regulated in part by DNA methylation.


BMC Genomics ◽  
2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Daniel Restrepo-Montoya ◽  
Phillip E. McClean ◽  
Juan M. Osorno

Abstract Background Legume species are an important plant model because of their protein-rich physiology. The adaptability and productivity of legumes are limited by major biotic and abiotic stresses. Responses to these stresses directly involve plasma membrane receptor proteins known as receptor-like kinases and receptor-like proteins. Evaluating the homology relations among RLK and RLP for seven legume species, and exploring their presence among synteny blocks allow an increased understanding of evolutionary relations, physical position, and chromosomal distribution in related species and their shared roles in stress responses. Results Typically, a high proportion of RLK and RLP legume proteins belong to orthologous clusters, which is confirmed in this study, where between 66 to 90% of the RLKs and RLPs per legume species were classified in orthologous clusters. One-third of the evaluated syntenic blocks had shared RLK/RLP genes among both legumes and non-legumes. Among the legumes, between 75 and 98% of the RLK/RLP were present in syntenic blocks. The distribution of chromosomal segments between Phaseolus vulgaris and Vigna unguiculata, two species that diverged ~ 8 mya, were highly similar. Among the RLK/RLP synteny clusters, seven experimentally validated resistance RLK/RLP genes were identified in syntenic blocks. The RLK resistant genes FLS2, BIR2, ERECTA, IOS1, and AtSERK1 from Arabidopsis and SLSERK1 from Solanum lycopersicum were present in different pairwise syntenic blocks among the legume species. Meanwhile, only the LYM1- RLP resistant gene from Arabidopsis shared a syntenic blocks with Glycine max. Conclusions The orthology analysis of the RLK and RLP suggests a dynamic evolution in the legume family, with between 66 to 85% of RLK and 83 to 88% of RLP belonging to orthologous clusters among the species evaluated. In fact, for the 10-species comparison, a lower number of singleton proteins were reported among RLP compared to RLK, suggesting that RLP positions are more physically conserved compared to RLK. The identification of RLK and RLP genes among the synteny blocks in legumes revealed multiple highly conserved syntenic blocks on multiple chromosomes. Additionally, the analysis suggests that P. vulgaris is an appropriate anchor species for comparative genomics among legumes.


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.


Author(s):  
Isabel Manrique-Gil ◽  
Inmaculada Sánchez-Vicente ◽  
Isabel Torres-Quezada ◽  
Oscar Lorenzo

Abstract Plants are aerobic organisms that have evolved to maintain specific requirements for oxygen (O2), leading to a correct respiratory energy supply during growth and development. There are certain plant developmental cues and biotic or abiotic stress responses where O2 is scarce. This O2 deprivation known as hypoxia may occur in hypoxic niches of plant-specific tissues and during adverse environmental cues such as pathogen attack and flooding. In general, plants respond to hypoxia through a complex reprogramming of their molecular activities with the aim of reducing the impact of stress on their physiological and cellular homeostasis. This review focuses on the fine-tuned regulation of hypoxia triggered by a network of gaseous compounds that includes O2, ethylene, and nitric oxide. In view of recent scientific advances, we summarize the molecular mechanisms mediated by phytoglobins and by the N-degron proteolytic pathway, focusing on embryogenesis, seed imbibition, and germination, and also specific structures, most notably root apical and shoot apical meristems. In addition, those biotic and abiotic stresses that comprise hypoxia are also highlighted.


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.


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