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      Short- and Long-Term Effects of UVA on Arabidopsis Are Mediated by a Novel cGMP Phosphodiesterase

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          Summary

          Although UVA radiation (315–400 nm) represents 95% of the UV radiation reaching the earth’s surface, surprisingly little is known about its effects on plants [ 1]. We show that in Arabidopsis, short-term exposure to UVA inhibits the opening of stomata, and this requires a reduction in the cytosolic level of cGMP. This process is independent of UVR8, the UVB receptor. A cGMP-activated phosphodiesterase ( AtCN-PDE1) was responsible for the UVA-induced decrease in cGMP in Arabidopsis. AtCN-PDE1-like proteins form a clade within the large HD-domain/PDEase-like protein superfamily, but no eukaryotic members of this subfamily have been functionally characterized. These genes have been lost from the genomes of metazoans but are otherwise conserved as single-copy genes across the tree of life. In longer-term experiments, UVA radiation increased growth and decreased water-use efficiency. These experiments revealed that PDE1 is also a negative regulator of growth. As the PDE1 gene is ancient and not represented in animal lineages, it is likely that at least one element of cGMP signaling in plants has evolved differently to the system present in metazoans.

          Highlights

          • UVA inhibits stomatal opening, and this requires a reduction in the cytosolic cGMP

          • UVA-induced decrease in cGMP was caused by a cGMP phosphodiesterase ( AtcnPDE1)

          • UVA radiation increased growth and decreased water use efficiency

          • cnPDE1 is ancient and has been lost from animal lineages

          Abstract

          Isner et al. show that UVA radiation inhibits stomatal opening in Arabidopsis. This requires a reduction in cytosolic cGMP, mediated by a cGMP-activated phosphodiesterase ( AtCN-PDE1) that is conserved across the tree of life, except in metazoans, where it has been lost. They also show that UVA increases growth and decreases water use efficiency.

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          Most cited references30

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          UniRef: comprehensive and non-redundant UniProt reference clusters.

          Redundant protein sequences in biological databases hinder sequence similarity searches and make interpretation of search results difficult. Clustering of protein sequence space based on sequence similarity helps organize all sequences into manageable datasets and reduces sampling bias and overrepresentation of sequences. The UniRef (UniProt Reference Clusters) provide clustered sets of sequences from the UniProt Knowledgebase (UniProtKB) and selected UniProt Archive records to obtain complete coverage of sequence space at several resolutions while hiding redundant sequences. Currently covering >4 million source sequences, the UniRef100 database combines identical sequences and subfragments from any source organism into a single UniRef entry. UniRef90 and UniRef50 are built by clustering UniRef100 sequences at the 90 or 50% sequence identity levels. UniRef100, UniRef90 and UniRef50 yield a database size reduction of approximately 10, 40 and 70%, respectively, from the source sequence set. The reduced redundancy increases the speed of similarity searches and improves detection of distant relationships. UniRef entries contain summary cluster and membership information, including the sequence of a representative protein, member count and common taxonomy of the cluster, the accession numbers of all the merged entries and links to rich functional annotation in UniProtKB to facilitate biological discovery. UniRef has already been applied to broad research areas ranging from genome annotation to proteomics data analysis. UniRef is updated biweekly and is available for online search and retrieval at http://www.uniprot.org, as well as for download at ftp://ftp.uniprot.org/pub/databases/uniprot/uniref. Supplementary data are available at Bioinformatics online.
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            The role of stomata in sensing and driving environmental change.

            Stomata, the small pores on the surfaces of leaves and stalks, regulate the flow of gases in and out of leaves and thus plants as a whole. They adapt to local and global changes on all timescales from minutes to millennia. Recent data from diverse fields are establishing their central importance to plant physiology, evolution and global ecology. Stomatal morphology, distribution and behaviour respond to a spectrum of signals, from intracellular signalling to global climatic change. Such concerted adaptation results from a web of control systems, reminiscent of a 'scale-free' network, whose untangling requires integrated approaches beyond those currently used.
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              The timescale of early land plant evolution

              Significance Establishing the timescale of early land plant evolution is essential to testing hypotheses on the coevolution of land plants and Earth’s System. Here, we establish a timescale for early land plant evolution that integrates over competing hypotheses on bryophyte−tracheophyte relationships. We estimate land plants to have emerged in a middle Cambrian–Early Ordovocian interval, and vascular plants to have emerged in the Late Ordovician−Silurian. This timescale implies an early establishment of terrestrial ecosystems by land plants that is in close accord with recent estimates for the origin of terrestrial animal lineages. Biogeochemical models that are constrained by the fossil record of early land plants, or attempt to explain their impact, must consider a much earlier, middle Cambrian–Early Ordovician, origin.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                05 August 2019
                05 August 2019
                : 29
                : 15
                : 2580-2585.e4
                Affiliations
                [1 ]School of Biological Sciences, Life Sciences Building, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TH, UK
                [2 ]Department of Computer Science, Merchant Venturers Building, University of Bristol, Woodland Road, Bristol BS8 1UB, UK
                [3 ]Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK
                [4 ]Department of Biology, University of York, York YO10 5DD, UK
                [5 ]School of Earth and Environmental Sciences, University of Manchester, Simon Building, Oxford Road, Manchester M13 9PL, UK
                [6 ]MRC Laboratory of Molecular Biology, Francis Crick Avenue, Cambridge Biomedical Campus, Cambridge CB2 0QU, UK
                Author notes
                [7]

                Lead Contact

                Article
                S0960-9822(19)30798-5
                10.1016/j.cub.2019.06.071
                6692503
                31353185
                6597696b-0ee2-4611-9dd1-2f61b8c7a307
                © 2019 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 10 February 2019
                : 5 June 2019
                : 24 June 2019
                Categories
                Article

                Life sciences
                uva,guard cell signaling,cgmp,cgmp-phosphodiesterase,light signaling,arabidopsis, evolution,cyclic nucleotides,water-use efficiency

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