A ligand-independent origin of abscisic acid perception

Land plants are considered monophyletic, descending from a single successful colonization of land by an aquatic algal ancestor. The ability to survive dehydration to the point of desiccation is a key adaptive trait enabling terrestrialization. In extant land plants, desiccation tolerance depends on the action of the hormone abscisic acid (ABA) that acts through a receptor-signal transduction pathway comprising a PYRABACTIN RESISTANCE 1-like (PYL)–PROTEIN PHOSPHATASE 2C (PP2C)–SNF1-RELATED PROTEIN KINASE 2 (SnRK2) module. Early-diverging aeroterrestrial algae mount a dehydration response that is similar to that of land plants, but that does not depend on ABA: Although ABA synthesis is widespread among algal species, ABA-dependent responses are not detected, and algae lack an ABA-binding PYL homolog. This raises the key question of how ABA signaling arose in the earliest land plants. Here, we systematically characterized ABA receptor-like proteins from major land plant lineages, including a protein found in the algal sister lineage of land plants. We found that the algal PYL-homolog encoded by Zygnema circumcarinatum has basal, ligand-independent activity of PP2C repression, suggesting this to be an ancestral function. Similarly, a liverwort receptor possesses basal activity, but it is further activated by ABA. We propose that co-option of ABA to control a preexisting PP2C-SnRK2-dependent desiccation-tolerance pathway enabled transition from an all-or-nothing survival strategy to a hormone-modulated, competitive strategy by enabling continued growth of anatomically diversifying vascular plants in dehydrative conditions, enabling them to exploit their new environment more efficiently.

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Desiccation tolerance in streptophyte algae and the algae to land plant transition: evolution of LEA and MIP protein families within the Viridiplantae

Journal of Experimental Botany ◽

10.1093/jxb/eraa105 ◽

2020 ◽

Vol 71 (11) ◽

pp. 3270-3278 ◽

Cited By ~ 1

Author(s):

Burkhard Becker ◽

Xuehuan Feng ◽

Yanbin Yin ◽

Andreas Holzinger

Keyword(s):

Desiccation Tolerance ◽

Experimental Studies ◽

Sister Group ◽

Land Plant ◽

Late Embryogenesis Abundant ◽

Land Plants ◽

Desiccation Stress ◽

Protein Families ◽

Intrinsic Protein ◽

Late Embryogenesis

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.

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Genetic analysis of Physcomitrella patens identifies ABSCISIC ACID NON-RESPONSIVE (ANR), a regulator of ABA responses unique to basal land plants and required for desiccation tolerance

The Plant Cell ◽

10.1105/tpc.16.00091 ◽

2016 ◽

pp. tpc.00091.2016 ◽

Cited By ~ 18

Author(s):

Sean Ross Stevenson ◽

Yasuko Kamisugi ◽

Chi H Trinh ◽

Jeremy Schmutz ◽

Jerry W Jenkins ◽

...

Keyword(s):

Abscisic Acid ◽

Genetic Analysis ◽

Desiccation Tolerance ◽

Physcomitrella Patens ◽

Land Plants

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Algal ancestor of land plants was preadapted for symbiosis

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1515426112 ◽

2015 ◽

Vol 112 (43) ◽

pp. 13390-13395 ◽

Cited By ~ 162

Author(s):

Pierre-Marc Delaux ◽

Guru V. Radhakrishnan ◽

Dhileepkumar Jayaraman ◽

Jitender Cheema ◽

Mathilde Malbreil ◽

...

Keyword(s):

Root Colonization ◽

Land Plant ◽

Land Plants ◽

Recent Common Ancestor ◽

Mycorrhizal Symbiosis ◽

Specific Expression ◽

Symbiotic Associations ◽

Most Recent Common Ancestor ◽

Green Algal ◽

Colonization Of Land

Colonization of land by plants was a major transition on Earth, but the developmental and genetic innovations required for this transition remain unknown. Physiological studies and the fossil record strongly suggest that the ability of the first land plants to form symbiotic associations with beneficial fungi was one of these critical innovations. In angiosperms, genes required for the perception and transduction of diffusible fungal signals for root colonization and for nutrient exchange have been characterized. However, the origin of these genes and their potential correlation with land colonization remain elusive. A comprehensive phylogenetic analysis of 259 transcriptomes and 10 green algal and basal land plant genomes, coupled with the characterization of the evolutionary path leading to the appearance of a key regulator, a calcium- and calmodulin-dependent protein kinase, showed that the symbiotic signaling pathway predated the first land plants. In contrast, downstream genes required for root colonization and their specific expression pattern probably appeared subsequent to the colonization of land. We conclude that the most recent common ancestor of extant land plants and green algae was preadapted for symbiotic associations. Subsequent improvement of this precursor stage in early land plants through rounds of gene duplication led to the acquisition of additional pathways and the ability to form a fully functional arbuscular mycorrhizal symbiosis.

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Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification

10.1101/213090 ◽

2017 ◽

Cited By ~ 1

Author(s):

Frida A.A. Feijen ◽

Rutger A. Vos ◽

Jorinde Nuytinck ◽

Vincent S.F.T. Merckx

Keyword(s):

Soil Fungi ◽

Evolutionary Dynamics ◽

State Transition ◽

Land Plant ◽

Land Plants ◽

Mycorrhizal Symbiosis ◽

Large Species ◽

Mycorrhizal Associations ◽

Colonization Of Land ◽

Early Land

Mycorrhizal symbiosis between soil fungi and land plants is one of the most widespread and ecologically important mutualisms on earth. It has long been hypothesized that the Glomeromycotina, the mycorrhizal symbionts of the majority of plants, facilitated colonization of land by plants in the Ordovician. This view was recently challenged by the discovery of mycorrhizal associations with Mucoromycotina in several early diverging lineages of land plants. Utilizing a large, species-level database of plants’ mycorrhizal associations and a Bayesian approach to state transition dynamics we here show that the recruitment of Mucoromycotina is the best supported transition from a non-mycorrhizal state. We further found that transitions between different combinations of either or both of Mucoromycotina and Glomeromycotina occur at high rates and found similar promiscuity among combinations that include either or both of Glomeromycotina and Ascomycota with a nearly fixed association with Basidiomycota. Our results demonstrate that under the most likely scenario symbiosis with Mucoromycotina enabled the establishment of early land plants.

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Acclimation of liverwort Marchantia polymorpha to physiological drought reveals important roles of antioxidant enzymes, proline and abscisic acid in land plant adaptation to osmotic stress

PeerJ ◽

10.7717/peerj.12419 ◽

2021 ◽

Vol 9 ◽

pp. e12419

Author(s):

Totan Kumar Ghosh ◽

Naznin Haque Tompa ◽

Md. Mezanur Rahman ◽

Mohammed Mohi-Ud-Din ◽

S. M. Zubair Al-Meraj ◽

...

Keyword(s):

Oxidative Stress ◽

Antioxidant Enzymes ◽

Abscisic Acid ◽

Drought Tolerance ◽

Osmotic Stress ◽

Photosynthetic Pigment ◽

Land Plant ◽

Land Plants ◽

Marchantia Polymorpha ◽

Key Species

Liverwort Marchantia polymorpha is considered as the key species for addressing a myriad of questions in plant biology. Exploration of drought tolerance mechanism(s) in this group of land plants offers a platform to identify the early adaptive mechanisms involved in drought tolerance. The current study aimed at elucidating the drought acclimation mechanisms in liverwort’s model M. polymorpha. The gemmae, asexual reproductive units of M. polymorpha, were exposed to sucrose (0.2 M), mannitol (0.5 M) and polyethylene glycol (PEG, 10%) for inducing physiological drought to investigate their effects at morphological, physiological and biochemical levels. Our results showed that drought exposure led to extreme growth inhibition, disruption of membrane stability and reduction in photosynthetic pigment contents in M. polymorpha. The increased accumulation of hydrogen peroxide and malondialdehyde, and the rate of electrolyte leakage in the gemmalings of M. polymorpha indicated an evidence of drought-caused oxidative stress. The gemmalings showed significant induction of the activities of key antioxidant enzymes, including superoxide dismutase, catalase, ascorbate peroxidase, dehydroascorbate reductase and glutathione S-transferase, and total antioxidant activity in response to increased oxidative stress under drought. Importantly, to counteract the drought effects, the gemmalings also accumulated a significant amount of proline, which coincided with the evolutionary presence of proline biosynthesis gene Δ1-pyrroline-5-carboxylate synthase 1 (P5CS1) in land plants. Furthermore, the application of exogenous abscisic acid (ABA) reduced drought-induced tissue damage and improved the activities of antioxidant enzymes and accumulation of proline, implying an archetypal role of this phytohormone in M. polymorpha for drought tolerance. We conclude that physiological drought tolerance mechanisms governed by the cellular antioxidants, proline and ABA were adopted in liverwort M. polymorpha, and that these findings have important implications in aiding our understanding of osmotic stress acclimation processes in land plants.

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The evolution of land plants: a perspective from horizontal gene transfer

Acta Societatis Botanicorum Poloniae ◽

10.5586/asbp.2014.043 ◽

2014 ◽

Vol 83 (4) ◽

pp. 363-368 ◽

Cited By ~ 2

Author(s):

Qia Wang ◽

Hang Sun ◽

Jinling Huang

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Land Plant ◽

Plant Evolution ◽

Land Plants ◽

Plant Colonization ◽

Mitochondrial Genome Evolution ◽

Land Plant Evolution ◽

Colonization Of Land

Recent studies suggest that horizontal gene transfer (HGT) played a significant role in the evolution of eukaryotic lineages. We here review the mechanisms of HGT in plants and the importance of HGT in land plant evolution. In particular, we discuss the role of HGT in plant colonization of land, phototropic response, C<sub>4</sub> photosynthesis, and mitochondrial genome evolution.

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Desiccation Tolerance: Avoiding Cellular Damage During Drying and Rehydration

Annual Review of Plant Biology ◽

10.1146/annurev-arplant-071219-105542 ◽

2020 ◽

Vol 71 (1) ◽

pp. 435-460 ◽

Cited By ~ 11

Author(s):

Melvin J. Oliver ◽

Jill M. Farrant ◽

Henk W.M. Hilhorst ◽

Sagadevan Mundree ◽

Brett Williams ◽

...

Keyword(s):

Desiccation Tolerance ◽

Cell Damage ◽

Cellular Responses ◽

Land Plants ◽

Cellular Damage ◽

Cellular Protection ◽

Vegetative Tissues ◽

Tolerant Plants ◽

Core Set ◽

Protection Mechanisms

Desiccation of plants is often lethal but is tolerated by the majority of seeds and by vegetative tissues of only a small number of land plants. Desiccation tolerance is an ancient trait, lost from vegetative tissues following the appearance of tracheids but reappearing in several lineages when selection pressures favored its evolution. Cells of all desiccation-tolerant plants and seeds must possess a core set of mechanisms to protect them from desiccation- and rehydration-induced damage. This review explores how desiccation generates cell damage and how tolerant cells assuage the complex array of mechanical, structural, metabolic, and chemical stresses and survive.Likewise, the stress of rehydration requires appropriate mitigating cellular responses. We also explore what comparative genomics, both structural and responsive, have added to our understanding of cellular protection mechanisms induced by desiccation, and how vegetative desiccation tolerance circumvents destructive, stress-induced cell senescence.

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Group A PP2Cs evolved in land plants as key regulators of intrinsic desiccation tolerance

Nature Communications ◽

10.1038/ncomms3219 ◽

2013 ◽

Vol 4 (1) ◽

Cited By ~ 72

Author(s):

Kenji Komatsu ◽

Norihiro Suzuki ◽

Mayuri Kuwamura ◽

Yuri Nishikawa ◽

Mao Nakatani ◽

...

Keyword(s):

Desiccation Tolerance ◽

Land Plants ◽

Group A

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Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microRNA repertoire in land plants

10.1101/078907 ◽

2016 ◽

Author(s):

Florencia Berruezo ◽

Flavio S. J. de Souza ◽

Pablo I. Picca ◽

Sergio I. Nemirovsky ◽

Leandro Martinez-Tosar ◽

...

Keyword(s):

Small Rna ◽

Land Plant ◽

Land Plants ◽

Phylogenetic Position ◽

Seed Plants ◽

Messenger Rnas ◽

Rna Molecules ◽

Functional Studies ◽

Mirna Genes ◽

Ecological Importance

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.

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