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MicroRNAs meet with quantitative trait loci: Small powerful players in regulating quantitative yield traits in rice

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Abstract MicroRNAs (miRNAs) are small noncoding RNAs which regulate various functions related to growth, development, and stress responses in plants and animals. Rice, Oryza sativa, is one of the most important food crops of the world. In rice, a number of quantitative trait loci (QTL) controlling yield‐related traits have been identified. Some of them are actually controlled by miRNAs, which control various yield‐related quantitative traits in rice. On one hand, many of these miRNAs are found to regulate more than one yield‐related traits, such as tillering, grain size, and branch number of a panicle. On the other hand, a rice yield‐related trait is usually controlled by multiple miRNAs, for example, grain size being controlled by miR156, miR167, miR396, miR397, and miR1432. In rare case, a single miRNA may specifically regulate only one yield‐related trait, such as, miR444 regulating rice tillering. In this review, we focus on the functions of miRNAs in controlling yield‐related quantitative traits in rice, including panicle grain number, grain weight/size, panicle length and branching, tiller number per plant, spikelet number, seed setting rate, and leaf inclination, and discuss how to modulate the expression of these miRNAs using modern molecular biology tools to promote grain yield. This article is categorized under: RNA in Disease and Development > RNA in Development
A summary of the miRNAs (highlighted in light blue) and their target genes (highlighted in purple) controlling rice yield‐related agronomic traits, including grain number, grain weight, tiller number, fertility, and leaf inclination. The miRNAs marked in red color are those controlling just one of the above mentioned five traits, based on the recent publications. The arrow and nail shape indicate positive and negative regulation, respectively. ACOT13, Acyl‐CoA thioesterase 13; AP2, APETALA2; ARF, AUXIN RESPONSE FACTOR; CSD, Cu or Zn superoxide dismutases; CYP51G3, OBTUSIFOLIOL 1,4‐Α‐DEMETHYLASE; GAMYBL, GAMYB‐like; GRF, GROWTH REGULATING FACTOR; HB4, HOMEODOMAIN CONTAINING PROTEIN 4; LAC: LACCASE; LC4, LEAF INCLINATION 4; MADS57, MADS‐box transcription factor 57; NAC2, NAC (NAM, ATAF, and CUC) transcription factors 2; PDIL1;1, protein disulfide isomerase like 1;1 SPL, SQUAMOSA PROMOTER‐BINDING PROTEIN‐LIKE; TIR1/AFB2, TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F‐BOX 2; UCL8, UCLACYANIN‐LIKE PROTEIN 8
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The methods to manipulate expression of the yield‐related miRNAs. During miRNA biogenesis, a mature miRNA is generated by the cellular Dicer‐like (DCL) enzymes from the primary stem‐looped precursors. (a) Overexpression of any yield‐related miRNA can be achieved by expressing miRNA genes by constitutive, endosperm‐specific or inducible promoters. Silencing of such miRNAs can be achieved through editing of miRNA genes through CRISPR/Cas9 system (b) or of miRNA transcripts through CRISPR/Cas13 system (c). STTMs (d) and MIMs (e) can be used to deactivate any mature miRNA through sequestration and/or cleavage. Finally, to modulate any miRNA‐regulated pathway, the miRNA target gene DNA can also be edited through CRISPR/Cas9 or the target gene mRNA can be silenced through RNAi. AGO1: ARGONAUTE 1; CRISPR/Cas: clusters of regularly interspaced short palindromic repeats/CRISPR‐associated proteins; MIM: target mimic; SDN: small RNA degrading nuclease; STTM: short tandem target mimic
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The possible pathway of miR167 regulating rice grain filling process. The trend of the line showed in the figure represents the level of gene expression, auxin content, and grain filling rate dynamic changes during rice grain filling. In this model, rice grain filling rate is shown to be positively correlated with the expression of ARFs and auxin content, but negatively correlated with miR167's expression. In addition, miR167‐OsILL1 (encodes an IAA‐amino acid hydrolase ILR1‐like 1, conserved with Arabidopsis IAA‐Ala Resistant 3)‐auxin pathway may also have roles in controlling rice grain filling, subsequently determining the rice grain weight. OsARF, auxin response factor
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The transcriptional levels of OsSPL13, OsSPL14, and OsSPL16 are fine adjusted by miR156, miR529, and miR535 during rice seed development. (a) Transcriptional levels of OsSPL13, OsSPL14 and OsSPL16 may be regulated by miR156a‐j, miR156d,f,h,j.2, miR529a‐5p, miR529b, and miR535 posttranscriptionally. The blue, green, and red line refer to the possible cleavage sites of miR529b,a‐5p, miR156a‐j,535, and miR156d,f,h,j.2, respectively. (b) Heatmap shows the expressional level values [log2(normalized miRNA’ expression assayed by high through‐put sequencing)] of different miRNAs, including miR156a‐j, miR156d,f,h,j.2, miR529a‐5p, miR529b, and miR535 during rice seed development (expression data was collected from our published papers Peng et al., , ; unpublished data). DAF, days after flowering
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