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      Embryophyte stress signaling evolved in the algal progenitors of land plants

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          Significance

          The evolution of land plants from algae is an age-old question in biology. The entire terrestrial flora stems from a grade of algae, the streptophyte algae. Recent phylogenomic studies have pinpointed the Zygnematophyceae as the modern-day streptophyte algal lineage that is most closely related to the algal land plant ancestor. Here, we provide insight into the biology of this ancestor that might have aided in its conquest of land. Specifically, we uncover the existence of stress-signaling pathways and the potential for intimate plastid-nucleus communication. Plastids act as environmental sensors in land plants; our data suggest that this feature was present in a common ancestor they shared with streptophyte algae.

          Abstract

          Streptophytes are unique among photosynthetic eukaryotes in having conquered land. As the ancestors of land plants, streptophyte algae are hypothesized to have possessed exaptations to the environmental stressors encountered during the transition to terrestrial life. Many of these stressors, including high irradiance and drought, are linked to plastid biology. We have investigated global gene expression patterns across all six major streptophyte algal lineages, analyzing a total of around 46,000 genes assembled from a little more than 1.64 billion sequence reads from six organisms under three growth conditions. Our results show that streptophyte algae respond to cold and high light stress via expression of hallmark genes used by land plants (embryophytes) during stress–response signaling and downstream responses. Among the strongest differentially regulated genes were those associated with plastid biology. We observed that among streptophyte algae, those most closely related to land plants, especially Zygnema, invest the largest fraction of their transcriptional budget in plastid-targeted proteins and possess an array of land plant-type plastid-nucleus communication genes. Streptophyte algae more closely related to land plants also appear most similar to land plants in their capacity to respond to plastid stressors. Support for this notion comes from the detection of a canonical abscisic acid receptor of the PYRABACTIN RESISTANCE (PYR/PYL/RCAR) family in Zygnema, the first found outside the land plant lineage. We conclude that a fine-tuned response toward terrestrial plastid stressors was among the exaptations that allowed streptophytes to colonize the terrestrial habitat on a global scale.

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          Most cited references86

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          Regulators of PP2C phosphatase activity function as abscisic acid sensors.

          The plant hormone abscisic acid (ABA) acts as a developmental signal and as an integrator of environmental cues such as drought and cold. Key players in ABA signal transduction include the type 2C protein phosphatases (PP2Cs) ABI1 and ABI2, which act by negatively regulating ABA responses. In this study, we identify interactors of ABI1 and ABI2 which we have named regulatory components of ABA receptor (RCARs). In Arabidopsis, RCARs belong to a family with 14 members that share structural similarity with class 10 pathogen-related proteins. RCAR1 was shown to bind ABA, to mediate ABA-dependent inactivation of ABI1 or ABI2 in vitro, and to antagonize PP2C action in planta. Other RCARs also mediated ABA-dependent regulation of ABI1 and ABI2, consistent with a combinatorial assembly of receptor complexes.
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            Abscisic acid biosynthesis and catabolism.

            The level of abscisic acid (ABA) in any particular tissue in a plant is determined by the rate of biosynthesis and catabolism of the hormone. Therefore, identifying all the genes involved in the metabolism is essential for a complete understanding of how this hormone directs plant growth and development. To date, almost all the biosynthetic genes have been identified through the isolation of auxotrophic mutants. On the other hand, among several ABA catabolic pathways, current genomic approaches revealed that Arabidopsis CYP707A genes encode ABA 8'-hydroxylases, which catalyze the first committed step in the predominant ABA catabolic pathway. Identification of ABA metabolic genes has revealed that multiple metabolic steps are differentially regulated to fine-tune the ABA level at both transcriptional and post-transcriptional levels. Furthermore, recent ongoing studies have given new insights into the regulation and site of ABA metabolism in relation to its physiological roles.
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              THE MOLECULAR BASIS OF DEHYDRATION TOLERANCE IN PLANTS.

              Molecular studies of drought stress in plants use a variety of strategies and include different species subjected to a wide range of water deficits. Initial research has by necessity been largely descriptive, and relevant genes have been identified either by reference to physiological evidence or by differential screening. A large number of genes with a potential role in drought tolerance have been described, and major themes in the molecular response have been established. Particular areas of importance are sugar metabolism and late-embryogenesis-abundant (LEA) proteins. Studies have begun to examine mechanisms that control the gene expression, and putative regulatory pathways have been established. Recent attempts to understand gene function have utilized transgenic plants. These efforts are of clear agronomic importance.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                10 April 2018
                26 March 2018
                26 March 2018
                : 115
                : 15
                : E3471-E3480
                Affiliations
                [1] aDepartment of Biochemistry and Molecular Biology, Dalhousie University , Halifax, NS, Canada B3H 4R2;
                [2] bMolecular Evolution, Heinrich Heine University Düsseldorf , 40225 Düsseldorf, Germany;
                [3] cProgram in Integrated Microbial Biodiversity, Canadian Institute for Advanced Research , Toronto, ON, Canada M5G 1M1
                Author notes
                1To whom correspondence may be addressed. Email: jan.devries@ 123456dal.ca or john.archibald@ 123456dal.ca .

                Edited by Pamela S. Soltis, University of Florida, Gainesville, FL, and approved February 27, 2018 (received for review November 9, 2017)

                Author contributions: J.d.V. and J.M.A. designed research; J.d.V. and B.A.C. performed research; J.d.V. and B.A.C. analyzed data; and J.d.V., S.B.G., and J.M.A. wrote the paper.

                Author information
                http://orcid.org/0000-0003-3507-5195
                http://orcid.org/0000-0002-2038-8474
                Article
                201719230
                10.1073/pnas.1719230115
                5899452
                29581286
                77a00dda-be04-474e-85db-74045787daf6
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG) 501100001659
                Award ID: 132/1-1
                Funded by: Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (NSERC) 501100000038
                Award ID: n/a
                Funded by: Canadian Institute for Advanced Research (CIFAR) 100007631
                Award ID: Senior Fellow
                Award ID: Program in Integrated Microbial Biodiversity
                Categories
                PNAS Plus
                Biological Sciences
                Evolution
                From the Cover
                PNAS Plus

                plant terrestrialization,abscisic acid,plastid-nucleus communication,charophyte algae,stress physiology

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