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      Small RNAs, emerging regulators critical for the development of horticultural traits

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          Abstract

          Small RNAs (sRNAs) have been recently recognized as key genetic and epigenetic regulators in various organisms, ranging from the modification of DNA and histone methylations to the modulation of the abundance of coding or non-coding RNAs. In plants, major regulatory sRNAs are classified as respective microRNA (miRNA) and small interfering RNA (siRNA) species, with the former primarily engaging in posttranscriptional regulation while the latter in transcriptional one. Many of these characterized sRNAs are involved in regulation of diverse biological programs, processes, and pathways in response to developmental cues, environmental signals/stresses, pathogen infection, and pest attacks. Recently, sRNAs-mediated regulations have also been extensively investigated in horticultural plants, with many novel mechanisms unveiled, which display far more mechanistic complexity and unique regulatory features compared to those studied in model species. Here, we review the recent progress of sRNA research in horticultural plants, with emphasis on mechanistic aspects as well as their relevance to trait regulation. Given that major and pioneered sRNA research has been carried out in the model and other plants, we also discuss ongoing sRNA research on these plants. Because miRNAs and phased siRNAs (phasiRNAs) are the most studied sRNA regulators, this review focuses on their biogenesis, conservation, function, and targeted genes and traits as well as the mechanistic relation between them, aiming at providing readers comprehensive information instrumental for future sRNA research in horticulture crops.

          Genetics: Tiny keys to important traits

          Studying small RNAs in horticultural plants may reveal the genetic mechanisms underlying many unique and valuable traits, and help improve plant breeding programs. Small RNAs, short RNA molecules only 20–24 bases long, switch genes on or off to control many aspects of plant growth, development, and reproduction. They are well-studied in model plants, but are only just being investigated in horticultural species. In a review of small RNA research in horticultural plants, Rui Xia at South China Agricultural University and co-workers report that horticultural plants contain many novel sRNAs that hold the keys to important traits such as juvenile-to-adult transition in fruit trees, fruit size, fruit quality, and disease resistance. Better understanding of these miRNAs may help in engineering varieties with earlier production of tastier fruit, as well as enhanced resistance to disease.

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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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            A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development.

            X. Chen (2004)
            Plant microRNAs (miRNAs) show a high degree of sequence complementarity to, and are believed to guide the cleavage of, their target messenger RNAs. Here, I show that miRNA172, which can base-pair with the messenger RNA of a floral homeotic gene, APETALA2, regulates APETALA2 expression primarily through translational inhibition. Elevated miRNA172 accumulation results in floral organ identity defects similar to those in loss-of-function apetala2 mutants. Elevated levels of mutant APETALA2 RNA with disrupted miRNA172 base pairing, but not wild-type APETALA2 RNA, result in elevated levels of APETALA2 protein and severe floral patterning defects. Therefore, miRNA172 likely acts in cell-fate specification as a translational repressor of APETALA2 in Arabidopsis flower development.
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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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                Author and article information

                Contributors
                (+86)-20-38348652 , rxia@scau.edu.cn
                Journal
                Hortic Res
                Hortic Res
                Horticulture Research
                Nature Publishing Group UK (London )
                2052-7276
                17 September 2018
                17 September 2018
                2018
                : 5
                : 63
                Affiliations
                [1 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, , South China Agricultural University, ; Guangzhou, 510642 China
                [2 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in South China, Ministry of Agriculture, , South China Agricultural University, ; Guangzhou, 510642 China
                [3 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, Guangdong Litchi Engineering Research Center, College of Horticulture, , South China Agricultural University, ; Guangzhou, 510642 China
                [4 ]ISNI 0000 0004 0478 6311, GRID grid.417548.b, Appalachian Fruit Research Station, Agricultural Research Service, , United States Department of Agriculture, ; Kearneysville, WV 25430 USA
                Author information
                http://orcid.org/0000-0003-2409-1181
                Article
                72
                10.1038/s41438-018-0072-8
                6139297
                30245834
                ac7a9c8d-21b4-45e9-a334-830d32133859
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 18 March 2018
                : 23 June 2018
                : 1 July 2018
                Funding
                Funded by: China Thousand Talents Program
                Categories
                Review Article
                Custom metadata
                © The Author(s) 2018

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