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      Cyclic nucleotide-gated ion channel 6 mediates thermotolerance in Arabidopsis seedlings by regulating nitric oxide production via cytosolic calcium ions

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          Abstract

          Background

          We previously reported the involvement of nitric oxide (NO) and cyclic nucleotide-gated ion channel 6 (CNGC6) in the responses of plants to heat shock (HS) exposure. To elucidate their relationship with heat tolerance in Arabidopsis thaliana, we examined the effects of HS on several groups of seedlings: wild type, cngc6, and cngc6 complementation and overexpression lines.

          Results

          After HS exposure, the level of NO was lower in cngc6 seedlings than in wild-type seedlings but significantly elevated in the transgenic lines depending on CNGC6 expression level. The treatment of seeds with calcium ions (Ca 2+) enhanced the NO level in Arabidopsis seedlings under HS conditions, whereas treatment with EGTA (a Ca 2+ chelator) reduced it, implicating that CNGC6 stimulates the accumulation of NO depending on an increase in cytosolic Ca 2+ ([Ca 2+] cyt). This idea was proved by phenotypic observations and thermotolerance testing of transgenic plants overexpressing NIA2 and NOA1, respectively, in a cngc6 background. Western blotting indicated that CNGC6 stimulated the accumulation of HS proteins via NO.

          Conclusion

          These data indicate that CNGC6 acts upstream of NO in the HS pathway, which improves our insufficient knowledge of the initiation of plant responses to high temerature.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-019-1974-9) contains supplementary material, which is available to authorized users.

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          Most cited references41

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          Abiotic stress, the field environment and stress combination.

          Farmers and breeders have long known that often it is the simultaneous occurrence of several abiotic stresses, rather than a particular stress condition, that is most lethal to crops. Surprisingly, the co-occurrence of different stresses is rarely addressed by molecular biologists that study plant acclimation. Recent studies have revealed that the response of plants to a combination of two different abiotic stresses is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Tolerance to a combination of different stress conditions, particularly those that mimic the field environment, should be the focus of future research programs aimed at developing transgenic crops and plants with enhanced tolerance to naturally occurring environmental conditions.
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            Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose.

            Reactive oxygen species are believed to perform multiple roles during plant defense responses to microbial attack, acting in the initial defense and possibly as cellular signaling molecules. In animals, nitric oxide (NO) is an important redox-active signaling molecule. Here we show that infection of resistant, but not susceptible, tobacco with tobacco mosaic virus resulted in enhanced NO synthase (NOS) activity. Furthermore, administration of NO donors or recombinant mammalian NOS to tobacco plants or tobacco suspension cells triggered expression of the defense-related genes encoding pathogenesis-related 1 protein and phenylalanine ammonia lyase (PAL). These genes were also induced by cyclic GMP (cGMP) and cyclic ADP-ribose, two molecules that can serve as second messengers for NO signaling in mammals. Consistent with cGMP acting as a second messenger in tobacco, NO treatment induced dramatic and transient increases in endogenous cGMP levels. Furthermore, NO-induced activation of PAL was blocked by 6-anilino-5,8-quinolinedione and 1H-(1,2,4)-oxadiazole[4,3-a]quinoxalin-1-one, two inhibitors of guanylate cyclase. Although 6-anilino-5,8-quinolinedione fully blocked PAL activation, inhibition by 1H-(1,2,4)-oxadiazole[4, 3-a]quinoxalin-1-one was not entirely complete, suggesting the existence of cGMP-independent, as well as cGMP-dependent, NO signaling. We conclude that several critical players of animal NO signaling are also operative in plants.
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              New insights into nitric oxide signaling in plants.

              A decade-long investigation of nitric oxide (NO) functions in plants has led to its characterization as a biological mediator involved in key physiological processes. Despite the wealth of information gathered from the analysis of its functions, until recently little was known about the mechanisms by which NO exerts its effects. In the past few years, part of the gap has been bridged. NO modulates the activity of proteins through nitrosylation and probably tyrosine nitration. Furthermore, NO can act as a Ca(2+)-mobilizing messenger, and researchers are beginning to unravel the mechanisms underlying the cross talk between NO and Ca(2+). Nonetheless, progress in this area of research is hindered by our ignorance of the pathways for NO production in plants. This review summarizes the basic concepts of NO signaling in animals and discusses new insights into NO enzymatic sources and molecular signaling in plants.
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                Author and article information

                Contributors
                86 311 80787530 , zhaolq70@163.com
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                20 August 2019
                20 August 2019
                2019
                : 19
                : 368
                Affiliations
                ISNI 0000 0004 0605 1239, GRID grid.256884.5, College of Life Sciences, , Hebei Normal University, ; Shijiazhuang, 050024 China
                Author information
                http://orcid.org/0000-0001-6718-8130
                Article
                1974
                10.1186/s12870-019-1974-9
                6702746
                31429706
                82a9350e-50af-45d1-a98c-c54d4cf3d390
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 18 April 2019
                : 13 August 2019
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2019

                Plant science & Botany
                arabidopsis,cyclic nucleotide-gated ion channel 6,heat shock,heat shock protein,nitric oxide

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