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      Strigolactone regulates shoot development through a core signalling pathway

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          ABSTRACT

          Strigolactones are a recently identified class of hormone that regulate multiple aspects of plant development. The DWARF14 (D14) α/β fold protein has been identified as a strigolactone receptor, which can act through the SCF MAX2 ubiquitin ligase, but the universality of this mechanism is not clear. Multiple proteins have been suggested as targets for strigolactone signalling, including both direct proteolytic targets of SCF MAX2, and downstream targets. However, the relevance and importance of these proteins to strigolactone signalling in many cases has not been fully established. Here we assess the contribution of these targets to strigolactone signalling in adult shoot developmental responses. We find that all examined strigolactone responses are regulated by SCF MAX2 and D14, and not by other D14-like proteins. We further show that all examined strigolactone responses likely depend on degradation of SMXL proteins in the SMXL6 clade, and not on the other proposed proteolytic targets BES1 or DELLAs. Taken together, our results suggest that in the adult shoot, the dominant mode of strigolactone signalling is D14-initiated, MAX2-mediated degradation of SMXL6-related proteins. We confirm that the BRANCHED1 transcription factor and the PIN-FORMED1 auxin efflux carrier are plausible downstream targets of this pathway in the regulation of shoot branching, and show that BRC1 likely acts in parallel to PIN1.

          Abstract

          Summary: Strigolactones signal through D14 to regulate shoot development by targeting SMXL6-clade proteins, but not BES1 or DELLA proteins, for degradation. BRC1 and PIN1 plausibly act downstream to regulate branching.

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          Most cited references60

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          Strigolactone inhibition of shoot branching.

          A carotenoid-derived hormonal signal that inhibits shoot branching in plants has long escaped identification. Strigolactones are compounds thought to be derived from carotenoids and are known to trigger the germination of parasitic plant seeds and stimulate symbiotic fungi. Here we present evidence that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigolactone application restores the wild-type branching phenotype to ccd8 mutants. Moreover, we show that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack strigolactone response, and are not deficient in strigolactones. These responses are conserved in Arabidopsis. In agreement with the expected properties of the hormonal signal, exogenous strigolactone can be transported in shoots and act at low concentrations. We suggest that endogenous strigolactones or related compounds inhibit shoot branching in plants. Furthermore, ccd8 mutants demonstrate the diverse effects of strigolactones in shoot branching, mycorrhizal symbiosis and parasitic weed interaction.
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            Inhibition of shoot branching by new terpenoid plant hormones.

            Shoot branching is a major determinant of plant architecture and is highly regulated by endogenous and environmental cues. Two classes of hormones, auxin and cytokinin, have long been known to have an important involvement in controlling shoot branching. Previous studies using a series of mutants with enhanced shoot branching suggested the existence of a third class of hormone(s) that is derived from carotenoids, but its chemical identity has been unknown. Here we show that levels of strigolactones, a group of terpenoid lactones, are significantly reduced in some of the branching mutants. Furthermore, application of strigolactones inhibits shoot branching in these mutants. Strigolactones were previously found in root exudates acting as communication chemicals with parasitic weeds and symbiotic arbuscular mycorrhizal fungi. Thus, we propose that strigolactones act as a new hormone class-or their biosynthetic precursors-in regulating above-ground plant architecture, and also have a function in underground communication with other neighbouring organisms.
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              Specific effects of microRNAs on the plant transcriptome.

              Most plant microRNAs (miRNAs) have perfect or near-perfect complementarity with their targets. This is consistent with their primary mode of action being cleavage of target mRNAs, similar to that induced by perfectly complementary small interfering RNAs (siRNAs). However, there are natural targets with up to five mismatches. Furthermore, artificial siRNAs can have substantial effects on so-called off-targets, to which they have only limited complementarity. By analyzing the transcriptome of plants overexpressing different miRNAs, we have deduced a set of empirical parameters for target recognition. Compared to artificial siRNAs, authentic plant miRNAs appear to have much higher specificity, which may reflect their coevolution with the remainder of the transcriptome. We also demonstrate that miR172, previously thought to act primarily by translational repression, can efficiently guide mRNA cleavage, although the effects on steady-state levels of target transcripts are obscured by strong feedback regulation. This finding unifies the view of plant miRNA action.
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                Author and article information

                Journal
                Biol Open
                Biol Open
                bio
                biolopen
                Biology Open
                The Company of Biologists Ltd
                2046-6390
                15 December 2016
                8 November 2016
                8 November 2016
                : 5
                : 12
                : 1806-1820
                Affiliations
                [1 ]Sainsbury Laboratory, University of Cambridge , Bateman Street, Cambridge CB2 1LR, UK
                [2 ]Department of Biology, University of York , York YO10 5DD, UK
                Author notes
                [*]

                Present address: School of Biology, University of Leeds, Leeds LS2 9JT, UK.

                [‡]

                Present address: Institute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3BF, UK.

                [§ ]Author for correspondence ( ol235@ 123456cam.ac.uk )
                Author information
                http://orcid.org/0000-0003-1612-4019
                http://orcid.org/0000-0002-7427-1028
                http://orcid.org/0000-0002-8924-3943
                http://orcid.org/0000-0002-5520-1331
                http://orcid.org/0000-0003-2161-3829
                Article
                BIO021402
                10.1242/bio.021402
                5200909
                27793831
                16ebca9b-866c-4e04-b8ad-3874cbb21efc
                © 2016. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 24 August 2016
                : 25 October 2016
                Funding
                Funded by: European Research Council, http://dx.doi.org/10.13039/501100000781;
                Award ID: 294514
                Funded by: Gatsby Charitable Foundation, http://dx.doi.org/10.13039/501100000324;
                Award ID: GAT3272C
                Funded by: Biotechnology and Biological Sciences Research Council, http://dx.doi.org/10.13039/501100000268;
                Award ID: R1039101
                Funded by: Chinese Scholarship Council PhD Program;
                Funded by: Sichuan Agricultural University, http://dx.doi.org/10.13039/501100008363;
                Categories
                Research Article

                Life sciences
                shoot branching,signal transduction,strigolactone
                Life sciences
                shoot branching, signal transduction, strigolactone

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