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      Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana

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          Abstract

          Correct developmental timing is essential for plant fitness and reproductive success. Two important transitions in shoot development—the juvenile-to-adult vegetative transition and the vegetative-to-reproductive transition—are mediated by a group of genes targeted by miR156, SQUAMOSA PROMOTER BINDING PROTEIN (SBP) genes. To determine the developmental functions of these genes in Arabidopsis thaliana, we characterized their expression patterns, and their gain-of-function and loss-of-function phenotypes. Our results reveal that SBP-LIKE ( SPL) genes in Arabidopsis can be divided into three functionally distinct groups: 1) SPL2, SPL9, SPL10, SPL11, SPL13 and SPL15 contribute to both the juvenile-to-adult vegetative transition and the vegetative-to-reproductive transition, with SPL9, SP13 and SPL15 being more important for these processes than SPL2, SPL10 and SPL11; 2) SPL3, SPL4 and SPL5 do not play a major role in vegetative phase change or floral induction, but promote the floral meristem identity transition; 3) SPL6 does not have a major function in shoot morphogenesis, but may be important for certain physiological processes. We also found that miR156-regulated SPL genes repress adventitious root development, providing an explanation for the observation that the capacity for adventitious root production declines as the shoot ages. miR156 is expressed at very high levels in young seedlings, and declines in abundance as the shoot develops. It completely blocks the expression of its SPL targets in the first two leaves of the rosette, and represses these genes to different degrees at later stages of development, primarily by promoting their translational repression. These results provide a framework for future studies of this multifunctional family of transcription factors, and offer new insights into the role of miR156 in Arabidopsis development.

          Author Summary

          In Arabidopsis, miR156 acts by repressing the expression of 10 SQUAMOSA PROMOTOR BINDING PROTEIN-LIKE ( SPL) genes. The phenotype of plants over-expressing miR156 demonstrates that these genes control many aspects of plant development and physiology, but the functions of individual miR156-regulated SPL genes, and how their expression is regulated by miR156, are largely unknown. We addressed these questions by determining the phenotypes of loss-of-function mutations in these genes individually and in combination, and by comparing the expression patterns and the phenotypes of miR156-sensitive and miR156-resistant reporters for these genes. Our results reveal the unique and shared functions of the members of this gene family, and demonstrate that miR156 plays different roles in the regulation of SPL gene expression at different times in development.

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          Most cited references73

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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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            miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana.

            The FT gene integrates several external and endogenous cues controlling flowering, including information on day length. A complex of the mobile FT protein and the bZIP transcription factor FD in turn has a central role in activating genes that execute the switch from vegetative to reproductive development. Here we reveal that microRNA156-targeted SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes not only act downstream of FT/FD, but also define a separate endogenous flowering pathway. High levels of miR156 in young plants prevent precocious flowering. A subsequent day length-independent decline in miR156 abundance provides a permissive environment for flowering and is paralleled by a rise in SPL levels. At the shoot apex, FT/FD and SPLs converge on an overlapping set of targets, with SPLs directly activating flower-promoting MADS box genes, providing a molecular substrate for both the redundant activities and the feed-forward action of the miR156/SPL and FT/FD modules in flowering control.
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              Widespread translational inhibition by plant miRNAs and siRNAs.

              High complementarity between plant microRNAs (miRNAs) and their messenger RNA targets is thought to cause silencing, prevalently by endonucleolytic cleavage. We have isolated Arabidopsis mutants defective in miRNA action. Their analysis provides evidence that plant miRNA-guided silencing has a widespread translational inhibitory component that is genetically separable from endonucleolytic cleavage. We further show that the same is true of silencing mediated by small interfering RNA (siRNA) populations. Translational repression is effected in part by the ARGONAUTE proteins AGO1 and AGO10. It also requires the activity of the microtubule-severing enzyme katanin, implicating cytoskeleton dynamics in miRNA action, as recently suggested from animal studies. Also as in animals, the decapping component VARICOSE (VCS)/Ge-1 is required for translational repression by miRNAs, which suggests that the underlying mechanisms in the two kingdoms are related.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                19 August 2016
                August 2016
                : 12
                : 8
                : e1006263
                Affiliations
                [001]Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania, United States of America
                Max Planck, GERMANY
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: RSP.

                • Formal analysis: MX.

                • Funding acquisition: RSP.

                • Investigation: MX TH JZ MYP KWE GW LY RSP.

                • Methodology: MX JZ TH MYP GW LY.

                • Project administration: RSP.

                • Resources: MX TH JZ MYP KWE GW.

                • Supervision: RSP.

                • Validation: MX TH.

                • Visualization: MX RSP.

                • Writing - original draft: MX RSP.

                • Writing - review & editing: MX RSP JZ.

                Author information
                http://orcid.org/0000-0001-7997-573X
                http://orcid.org/0000-0002-7684-9575
                http://orcid.org/0000-0001-6592-5862
                Article
                PGENETICS-D-16-00651
                10.1371/journal.pgen.1006263
                4991793
                27541584
                3b92b6de-19bf-4051-892e-4364267783db
                © 2016 Xu et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 March 2016
                : 27 July 2016
                Page count
                Figures: 9, Tables: 1, Pages: 29
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: GM51893
                Award Recipient :
                This work was supported by the National Institutes of Health GM51893, RSP https://www.nih.gov. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Genetics
                Phenotypes
                Biology and Life Sciences
                Organisms
                Plants
                Brassica
                Arabidopsis Thaliana
                Research and Analysis Methods
                Model Organisms
                Plant and Algal Models
                Arabidopsis Thaliana
                Biology and Life Sciences
                Genetics
                Gene Expression
                Biology and Life Sciences
                Plant Science
                Plant Physiology
                Meristems
                Floral Meristem
                Biology and Life Sciences
                Organisms
                Plants
                Flowering Plants
                Biology and Life Sciences
                Genetics
                Mutation
                Biology and Life Sciences
                Genetics
                Gene Expression
                Gene Regulation
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Genetics
                Genetics

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