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      Suppression of microRNA159 impacts multiple agronomic traits in rice ( Oryza sativa L .)

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          Abstract

          Background

          microRNAs (miRNAs) are important regulators in plant growth and development. miR159 is a conserved miRNA among different plant species and has various functions in plants. Studies on miR159 are mostly done on model plant, Arabidopsis thaliana. In rice, studies on miR159 were either based upon genome-wide expression analyses focused upon responses to different nitrogen forms and abiotic stress or upon phenotypic studies of transgenic plants overexpressing its precursor. STTM (Short Tandem Target Mimic) is an effective tool to block the activity of endogenous mature miRNA activity in plant. Therefore, specific roles of miR159 in rice could be explored by down regulating miR159 through STTM.

          Results

          In this study, expression of mature miR159 was successfully suppressed by STTM which resulted in the increased expressions of its two targets genes, OsGAMYB and OsGAMYBL1 (GAMYB-LIKE 1). Overall, STTM159 plants exhibited short stature along with smaller organ size and reduction in stem diameter, length of flag leaf, main panicle, spikelet hulls and grain size. Histological analysis of stem, leaf and mature spikelet hull showed the reduced number of small vascular bundles (SVB), less number of small veins (SV) between two big veins (LV) and less cell number in outer parenchyma. Gene Ontology (GO) enrichment analysis of differentially expressed genes between wild type plants and STTM159 transgenic plants showed that genes involved in cell division, auxin, cytokinin (CK) and brassinosteroids (BRs) biosynthesis and signaling are significantly down-regulated in STTM159 plants.

          Conclusion

          Our data suggests that in rice, miR159 positively regulates organ size, including stem, leaf, and grain size due to the promotion of cell division. Further analysis from the RNA-seq data showed that the decreased cell divisions in STTM159 transgenic plants may result, at least partly from the lower expression of the genes involved in cell cycle and hormone homeostasis, which provides new insights of rice miR159-specific functions.

          Electronic supplementary material

          The online version of this article (10.1186/s12870-017-1171-7) contains supplementary material, which is available to authorized users.

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          Most cited references48

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          Control of grain size, shape and quality by OsSPL16 in rice.

          Grain size and shape are important components of grain yield and quality and have been under selection since cereals were first domesticated. Here, we show that a quantitative trait locus GW8 is synonymous with OsSPL16, which encodes a protein that is a positive regulator of cell proliferation. Higher expression of this gene promotes cell division and grain filling, with positive consequences for grain width and yield in rice. Conversely, a loss-of-function mutation in Basmati rice is associated with the formation of a more slender grain and better quality of appearance. The correlation between grain size and allelic variation at the GW8 locus suggests that mutations within the promoter region were likely selected in rice breeding programs. We also show that a marker-assisted strategy targeted at elite alleles of GS3 and OsSPL16 underlying grain size and shape can be effectively used to simultaneously improve grain quality and yield.
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            The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development.

            The functions of the vast majority of genes encoding R2R3 MYB domain proteins remain unknown. The closely related MYB33 and MYB65 genes of Arabidopsis thaliana have high sequence similarity to the barley (Hordeum vulgare) GAMYB gene. T-DNA insertional mutants were isolated for both genes, and a myb33 myb65 double mutant was defective in anther development. In myb33 myb65 anthers, the tapetum undergoes hypertrophy at the pollen mother cell stage, resulting in premeiotic abortion of pollen development. However, myb33 myb65 sterility was conditional, where fertility increased both under higher light or lower temperature conditions. Thus, MYB33/MYB65 facilitate, but are not essential for, anther development. Neither single mutant displayed a phenotype, implying that MYB33 and MYB65 are functionally redundant. Consistent with functional redundancy, promoter-beta-glucuronidase (GUS) fusions of MYB33 and MYB65 gave identical expression patterns in flowers (sepals, style, receptacle, anther filaments, and connective but not in anthers themselves), shoot apices, and root tips. By contrast, expression of a MYB33:GUS translational fusion in flowers was solely in young anthers (consistent with the male sterile phenotype), and no staining was seen in shoot meristems or root tips. A microRNA target sequence is present in the MYB genes, and mutating this sequence in the MYB33:GUS fusion results in an expanded expression pattern, in tissues similar to that observed in the promoter-GUS lines, implying that the microRNA target sequence is restricting MYB33 expression. Arabidopsis transformed with MYB33 containing the mutated microRNA target had dramatic pleiotrophic developmental defects, suggesting that restricting MYB33 expression, especially in the shoot apices, is essential for proper plant development.
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              Cell cycle regulation in plant development.

              Cell cycle regulation is of pivotal importance for plant growth and development. Although plant cell division shares basic mechanisms with all eukaryotes, plants have evolved novel molecules orchestrating the cell cycle. Some regulatory proteins, such as cyclins and inhibitors of cyclin-dependent kinases, are particularly numerous in plants, possibly reflecting the remarkable ability of plants to modulate their postembryonic development. Many plant cells also can continue DNA replication in the absence of mitosis, a process known as endoreduplication, causing polyploidy. Here, we review the molecular mechanisms that regulate cell division and endoreduplication and we discuss our understanding, albeit very limited, on how the cell cycle is integrated with plant development.
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                Author and article information

                Contributors
                zhaoyafan3701@163.com
                wenhuili1128@126.com
                steotia@mtu.edu
                dumatt@163.com
                zhjing98@126.com
                lijunzhou199899@126.com
                sunhongzheng@foxmail.com
                gtang1@mtu.edu
                lypengting@163.com
                qzzhaoh@126.com
                Journal
                BMC Plant Biol
                BMC Plant Biol
                BMC Plant Biology
                BioMed Central (London )
                1471-2229
                21 November 2017
                21 November 2017
                2017
                : 17
                : 215
                Affiliations
                [1 ]GRID grid.108266.b, Collaborative Innovation Center of Henan Grain Crops, , Henan Agricultural University, ; Zhengzhou, 450002 China
                [2 ]GRID grid.108266.b, Key Laboratory of Rice Biology in Henan Province, Henan Agricultural University, ; Zhengzhou, 450002 China
                [3 ]ISNI 0000 0001 0663 5937, GRID grid.259979.9, Department of Biological Sciences, , Michigan Technological University, ; Houghton, MI 49931 USA
                Article
                1171
                10.1186/s12870-017-1171-7
                5699021
                29162059
                a29c0c9a-b085-494f-815b-2e3467c35d86
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 3 May 2017
                : 10 November 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;
                Award ID: 31501292
                Award Recipient :
                Funded by: Major Science and Technology Project of Henan Province
                Award ID: 141100110600
                Award Recipient :
                Funded by: Support Plan of Science and Technology Innovation Team in Universities of Henan province
                Award ID: 17IRTSTHN015
                Award Recipient :
                Funded by: Key Scientific Research Project in Universities of Henan Province
                Award ID: 16A210009
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Plant science & Botany
                rice,mir159,agronomic traits,cell cycle,plant hormone
                Plant science & Botany
                rice, mir159, agronomic traits, cell cycle, plant hormone

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