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      The miRNA–mRNA Networks Involving Abnormal Energy and Hormone Metabolisms Restrict Tillering in a Wheat Mutant dmc

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          Abstract

          Tillers not only determine plant architecture but also influence crop yield. To explore the miRNA regulatory network restraining tiller development in a dwarf-monoculm wheat mutant ( dmc) derived from Guomai 301 (wild type, WT), we employed miRNome and transcriptome integrative analysis, real-time qRT-PCR, histochemistry, and determinations of the key metabolites and photosynthesis parameters. A total of 91 differentially expressed miRNAs (DEMs) were identified between dmc and WT. Among them, 40 key DEMs targeted 45 differentially expressed genes (DEGs) including the key DEGs encode growth-regulating factors (GRF), auxin response factors (ARF), and other proteins involved in the metabolisms of hormones and carbohydrates, etc. Compared with WT, both the chlorophyll contents and the photosynthesis rate were lower in dmc. The contents of glucose, sucrose, fructose, and maltose were lower in dmc. The contents of auxin (IAA) and zeatin (ZA) were significantly lower, but gibberellin (GA) was significantly higher in the tiller tissues of dmc. This research demonstrated that the DEMs regulating hormone and carbohydrate metabolisms were important causes for dmc to not tiller. A primary miRNA–mRNA regulatory model for dmc tillering was established. The lower photosynthesis rate, insufficient energy, and abnormal hormone metabolisms restrict tillering in dmc.

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          Most cited references56

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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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            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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              High-Throughput Sequencing of Arabidopsis microRNAs: Evidence for Frequent Birth and Death of MIRNA Genes

              In plants, microRNAs (miRNAs) comprise one of two classes of small RNAs that function primarily as negative regulators at the posttranscriptional level. Several MIRNA genes in the plant kingdom are ancient, with conservation extending between angiosperms and the mosses, whereas many others are more recently evolved. Here, we use deep sequencing and computational methods to identify, profile and analyze non-conserved MIRNA genes in Arabidopsis thaliana. 48 non-conserved MIRNA families, nearly all of which were represented by single genes, were identified. Sequence similarity analyses of miRNA precursor foldback arms revealed evidence for recent evolutionary origin of 16 MIRNA loci through inverted duplication events from protein-coding gene sequences. Interestingly, these recently evolved MIRNA genes have taken distinct paths. Whereas some non-conserved miRNAs interact with and regulate target transcripts from gene families that donated parental sequences, others have drifted to the point of non-interaction with parental gene family transcripts. Some young MIRNA loci clearly originated from one gene family but form miRNAs that target transcripts in another family. We suggest that MIRNA genes are undergoing relatively frequent birth and death, with only a subset being stabilized by integration into regulatory networks.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                17 September 2019
                September 2019
                : 20
                : 18
                : 4586
                Affiliations
                [1 ]National Centre of Engineering and Technological Research for Wheat/Key Laboratory of Physiological Ecology and Genetic Improvement of Food Crops in Henan Province, Henan Agricultural University, Zhengzhou 450046, China; jhan68@ 123456163.com (J.A.); nxyjym@ 123456henau.edu.cn (Y.J.); 13253817312@ 123456stu.henau.edu.cn (Y.Z.); guomai301@ 123456163.com (R.H.); chang_top@ 123456163.com (J.L.); zxjiao2018@ 123456163.com (Z.J.); jzhang1023@ 123456126.com (J.Z.); lhj19960901@ 123456163.com (H.L.); liqiaoyun@ 123456henau.edu.cn (Q.L.)
                [2 ]Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang 455000, China; m15927306510@ 123456163.com
                [3 ]Shangqiu Academy of Agricultural and Forestry Sciences, Shangqiu 476000, China; nyj317@ 123456163.com
                Author notes
                [* ]Correspondence: jsniu@ 123456263.net
                Author information
                https://orcid.org/0000-0001-5077-3691
                https://orcid.org/0000-0001-6212-1279
                https://orcid.org/0000-0002-7233-0442
                Article
                ijms-20-04586
                10.3390/ijms20184586
                6770018
                31533225
                65f0aff0-aec3-4e2c-acd3-337bdd4a46a6
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 31 July 2019
                : 15 September 2019
                Categories
                Article

                Molecular biology
                wheat (triticum aestivum l.),dmc mutant,tillering,mirna,mrna,photosynthesis,carbohydrate,phytohormone

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