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      Analysis of the Maize dicer-like1 Mutant, fuzzy tassel, Implicates MicroRNAs in Anther Maturation and Dehiscence

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          Abstract

          Sexual reproduction in plants requires development of haploid gametophytes from somatic tissues. Pollen is the male gametophyte and develops within the stamen; defects in the somatic tissues of the stamen and in the male gametophyte itself can result in male sterility. The maize fuzzy tassel ( fzt) mutant has a mutation in dicer-like1 (dcl1), which encodes a key enzyme required for microRNA (miRNA) biogenesis. Many miRNAs are reduced in fzt, and fzt mutants exhibit a broad range of developmental defects, including male sterility. To gain further insight into the roles of miRNAs in maize stamen development, we conducted a detailed analysis of the male sterility defects in fzt mutants. Early development was normal in fzt mutant anthers, however fzt anthers arrested in late stages of anther maturation and did not dehisce. A minority of locules in fzt anthers also exhibited anther wall defects. At maturity, very little pollen in fzt anthers was viable or able to germinate. Normal pollen is tricellular at maturity; pollen from fzt anthers included a mixture of unicellular, bicellular, and tricellular pollen. Pollen from normal anthers is loaded with starch before dehiscence, however pollen from fzt anthers failed to accumulate starch. Our results indicate an absolute requirement for miRNAs in the final stages of anther and pollen maturation in maize. Anther wall defects also suggest that miRNAs have key roles earlier in anther development. We discuss candidate miRNAs and pathways that might underlie fzt anther defects, and also note that male sterility in fzt resembles water deficit-induced male sterility, highlighting a possible link between development and stress responses in plants.

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          Origin, biogenesis, and activity of plant microRNAs.

          MicroRNAs (miRNAs) are key posttranscriptional regulators of eukaryotic gene expression. Plants use highly conserved as well as more recently evolved, species-specific miRNAs to control a vast array of biological processes. This Review discusses current advances in our understanding of the origin, biogenesis, and mode of action of plant miRNAs and draws comparisons with their metazoan counterparts.
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            Hormone balance and abiotic stress tolerance in crop plants.

            Plant hormones play central roles in the ability of plants to adapt to changing environments, by mediating growth, development, nutrient allocation, and source/sink transitions. Although ABA is the most studied stress-responsive hormone, the role of cytokinins, brassinosteroids, and auxins during environmental stress is emerging. Recent evidence indicated that plant hormones are involved in multiple processes. Cross-talk between the different plant hormones results in synergetic or antagonic interactions that play crucial roles in response of plants to abiotic stress. The characterization of the molecular mechanisms regulating hormone synthesis, signaling, and action are facilitating the modification of hormone biosynthetic pathways for the generation of transgenic crop plants with enhanced abiotic stress tolerance. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Biogenesis, turnover, and mode of action of plant microRNAs.

              MicroRNAs (miRNAs) are small RNAs that control gene expression through silencing of target mRNAs. Mature miRNAs are processed from primary miRNA transcripts by the endonuclease activity of the DICER-LIKE1 (DCL1) protein complex. Mechanisms exist that allow the DCL1 complex to precisely excise the miRNA from its precursor. Our understanding of miRNA biogenesis, particularly its intersection with transcription and other aspects of RNA metabolism such as splicing, is still evolving. Mature miRNAs are incorporated into an ARGONAUTE (AGO) effector complex competent for target gene silencing but are also subjected to turnover through a degradation mechanism that is beginning to be understood. The mechanisms of miRNA target silencing in plants are no longer limited to AGO-catalyzed slicing, and the contribution of translational inhibition is increasingly appreciated. Here, we review the mechanisms underlying the biogenesis, turnover, and activities of plant miRNAs.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                8 January 2016
                2016
                : 11
                : 1
                : e0146534
                Affiliations
                [001]Department of Biology, East Carolina University, Greenville, North Carolina, 27858, United States of America
                USDA Agricultural Research Service, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SF BT. Performed the experiments: SF. Analyzed the data: SF BT. Wrote the paper: SF BT.

                Article
                PONE-D-15-45587
                10.1371/journal.pone.0146534
                4706427
                26745722
                fce8b327-6ba0-4750-b011-913096648b5a
                © 2016 Field, Thompson

                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
                : 16 October 2015
                : 18 December 2015
                Page count
                Figures: 5, Tables: 4, Pages: 14
                Funding
                This work was supported by National Science Foundation grant IOS-1148971 to BT. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its supporting information files.

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