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      Tapetum-Dependent Male Meiosis Progression in Plants: Increasing Evidence Emerges

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          Abstract

          In higher plants, male meiosis is a key process during microsporogenesis and is crucial for male fertility and seed set. Meiosis involves a highly dynamic organization of chromosomes and cytoskeleton and specifically takes place within sexual cells. However, studies in multiple plant species have suggested that the normal development of tapetum, the somatic cell layer surrounding the developing male meiocytes, is indispensable for the completion of the male meiotic cell cycle. Disrupted tapetum development causes alterations in the expression of a large range of genes involved in male reproduction. Moreover, recent experiments suggest that small RNAs (sRNAs) present in the anthers, including microRNAs (miRNAs) and phased, secondary, small interfering RNAs (phasiRNAs), play a potential but important role in controlling male meiosis, either by influencing the expression of meiotic genes in the meiocytes or through other unclear mechanisms, supporting the hypothesis that male meiosis is non-cell autonomously regulated. In this mini review, we summarize the recorded meiotic defects that occur in plants with defective tapetum development in both Arabidopsis and crops. Thereafter, we outline the latest understanding on the molecular mechanisms that potentially underpin the tapetum-dependent regulation of male meiosis, and we especially discuss the regulatory role of sRNAs. At the end, we propose several outstanding questions that should be addressed in future studies.

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          The expanding world of small RNAs in plants.

          Plant genomes encode various small RNAs that function in distinct, yet overlapping, genetic and epigenetic silencing pathways. However, the abundance and diversity of small-RNA classes varies among plant species, suggesting coevolution between environmental adaptations and gene-silencing mechanisms. Biogenesis of small RNAs in plants is well understood, but we are just beginning to uncover their intricate regulation and activity. Here, we discuss the biogenesis of plant small RNAs, such as microRNAs, secondary siRNAs and heterochromatic siRNAs, and their diverse cellular and developmental functions, including in reproductive transitions, genomic imprinting and paramutation. We also discuss the diversification of small-RNA-directed silencing pathways through the expansion of RNA-dependent RNA polymerases, DICER proteins and ARGONAUTE proteins.
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            Classification and comparison of small RNAs from plants.

            Regulatory small RNAs, which range in size from 20 to 24 nucleotides, are ubiquitous components of endogenous plant transcriptomes, as well as common responses to exogenous viral infections and introduced double-stranded RNA (dsRNA). Endogenous small RNAs derive from the processing of helical RNA precursors and can be categorized into several groups based on differences in biogenesis and function. A major distinction can be observed between small RNAs derived from single-stranded precursors with a hairpin structure [referred to here as hairpin RNAs (hpRNAs)] and those derived from dsRNA precursors [small interfering RNAs (siRNAs)]. hpRNAs in plants can be divided into two secondary groups: microRNAs and those that are not microRNAs. The currently known siRNAs fall mostly into one of three secondary groups: heterochromatic siRNAs, secondary siRNAs, and natural antisense transcript siRNAs. Tertiary subdivisions can be identified within many of the secondary classifications as well. Comparisons between the different classes of plant small RNAs help to illuminate key goals for future research.
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              Methylation as a crucial step in plant microRNA biogenesis.

              Methylation on the base or the ribose is prevalent in eukaryotic ribosomal RNAs (rRNAs) and is thought to be crucial for ribosome biogenesis and function. Artificially introduced 2'-O-methyl groups in small interfering RNAs (siRNAs) can stabilize siRNAs in serum without affecting their activities in RNA interference in mammalian cells. Here, we show that plant microRNAs (miRNAs) have a naturally occurring methyl group on the ribose of the last nucleotide. Whereas methylation of rRNAs depends on guide RNAs, the methyltransferase protein HEN1 is sufficient to methylate miRNA/miRNA* duplexes. Our studies uncover a new and crucial step in plant miRNA biogenesis and have profound implications in the function of miRNAs.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                16 January 2020
                2019
                : 10
                : 1667
                Affiliations
                [1] 1School of Public Health, Key Lab of Public Health Safety of the Ministry of Education and NHC Key Laboratory of Health Technology Assessment, Fudan University , Shanghai, China
                [2] 2Hubei Provincial Key Laboratory for Protection and Application of Special Plants in Wuling Area of China, College of Life Sciences, South-Central University for Nationalities , Wuhan, China
                [3] 3Key Laboratory for Biotechnology of the State Ethnic Affairs Commission, College of Life Sciences, South-Central University for Nationalities , Wuhan, China
                Author notes

                Edited by: Patrick H. Masson, University of Wisconsin-Madison, United States

                Reviewed by: Wanqi Liang, Shanghai Jiao Tong University, China; Yingxiang Wang, Fudan University, China; Stefanie Dukowic-Schulze, University of Regensburg, Germany

                *Correspondence: Bing Liu, bl472@ 123456scuec.edu.cn

                This article was submitted to Plant Physiology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.01667
                6979054
                32010157
                966288c8-1aa9-4369-a7c2-5d129404410d
                Copyright © 2020 Lei and Liu

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 21 June 2019
                : 27 November 2019
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 137, Pages: 10, Words: 4847
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                male meiosis,tapetal cell specification,tapetum pcd,gene expression,srnas
                Plant science & Botany
                male meiosis, tapetal cell specification, tapetum pcd, gene expression, srnas

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