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Rice (Oryza sativa L.) is one of the essential staple food crops and tillering, panicle branching and grain filling are three important traits determining the grain yield. Although miRNAs have been reported being regulating yield, no study has systematically investigated how miRNAs differentially function in high and low yield rice, in particular at a network level. This abundance of data from high-throughput sequencing provides an effective solution for systematic identification of regulatory miRNAs using developed algorithms in plants. We here present a novel algorithm, Gene Co-expression Network differential edge-like transformation (GRN-DET), which can identify key regulatory miRNAs in plant development. Based on the small RNA and RNA-seq data, miRNA-gene-TF co-regulation networks were constructed for yield of rice. Using GRN-DET, the key regulatory miRNAs for rice yield were characterized by the differential expression variances of miRNAs and co-variances of miRNA-mRNA, including osa-miR171 and osa-miR1432. Phytohormone cross-talks (auxin and brassinosteroid) were also revealed by these co-expression networks for the yield of rice.

Significantly increasing crop yield is a major and worldwide challenge for food supply and security. It is well-known that rice cultivated at Taoyuan in Yunnan of China can produce the highest yield worldwide. Yet, the gene regulatory mechanism underpinning this ultrahigh yield has been a mystery. Here, we systematically collected the transcriptome data for seven key tissues at different developmental stages using rice cultivated both at Taoyuan as the case group and at another regular rice planting place Jinghong as the control group. We identified the top 24 candidate high-yield genes with their network modules from these well-designed datasets by developing a novel computational systems biology method, i.e. , dynamic cross-tissue (DCT) network analysis. We used one of the candidate genes, OsSPL4 , whose function was previously unknown, for gene editing experimental validation of the high yield, and confirmed that OsSPL4 significantly affects panicle branching and increases the rice yield. This study, which included extensive field phenotyping, cross-tissue systems biology analyses, and functional validation, uncovered the key genes and gene regulatory networks underpinning the ultrahigh yield of rice. The DCT method could be applied to other plant or animal systems if different phenotypes under various environments with the common genome sequences of the examined sample. DCT can be downloaded from https://github.com/ztpub/DCT .

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