Identification of Key Genes for the Ultrahigh Yield of Rice Using Dynamic Cross-Tissue Network Analysis

Abstract

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 .

OsSPL9 Regulates Grain Number and Grain Yield in Rice

“…There are 19 putative SPL genes in rice ( Xie et al, 2006 ), and 14 genes have been identified to be involved in various biological processes during rice growth and development, such as regulating tiller, panicle branches, grain size, the development of crown root, ligule, auricle and trichome, and stress response ( Lee et al, 2007 ; Jiao et al, 2010 ; Luo et al, 2012 ; Wang et al, 2012 , 2015 ; Si et al, 2016 ; Yue et al, 2017 ; Zhang et al, 2017 ; Dai et al, 2018 ; Lan et al, 2019 ; Shao et al, 2019 ; Yuan et al, 2019 ; Hu et al, 2020 ). OsSPL9 was proven to regulate Cu uptake and distribution by directly activating the expression of Cu transporter genes in rice ( Tang et al, 2016 ), and an OsSPL9 -miR528 pathway was involved in the regulation of plant resistance to rice stripe virus and rice flowering under long-day conditions ( Yang et al, 2019 ; Yao et al, 2019 ).…”

“…To date, 14 genes have been identified to be involved in different regulatory pathways. For example, several SPL genes, such as OsSPL2 , OsSPL4 , OsSPL7 , OsSPL13 , OsSPL14 , OsSPL16 , OsSPL17 , and OsSPL18 , directly regulate yield-related traits, including tiller, panicle branches, grain size, and grain shape ( Jiao et al, 2010 ; Luo et al, 2012 ; Wang et al, 2012 , 2015 ; Si et al, 2016 ; Yue et al, 2017 ; Zhang et al, 2017 ; Dai et al, 2018 ; Yuan et al, 2019 ; Hu et al, 2020 ). In addition, OsSPL3 and OsSPL12 regulate crown root development in rice ( Shao et al, 2019 ).…”

The Elite Alleles of OsSPL4 Regulate Grain Size and Increase Grain Yield in Rice

“…To date, many rice yield-related genes, such as RFL , OsGIF1 , RGG2 , DEP2 , LAC , TGW3 , and GL7/SLG7 have been reported to play essential roles in controlling the panicle architecture and grain size (Hu et al 2020 ; Miao et al 2019 ). In our study, we found that many of these yield-related genes had been differentially expressed in the spl4-d3 lines (Additional file 1 : Table S5).…”

“…In Arabidopsis , the OsSPL4 homologue genes, AtSPL2 , AtSPL10 and AtSPL11 have been reported to control the development of lateral organs associated with shoot maturation in the reproductive phase (Shikata et al 2009 ). Lately, systematic biology analysis revealed that OsSPL4 might affect panicle development and grain weight to enhance yield in rice (Hu et al, 2020 ; Jiang et al, 2020 ). However, the biological function, artificial selection and evolution of OsSPL4 in rice have not been well characterized.…”

Structural, pasting and sensory properties of rice from main and ratoon crops

“…Breeding green varieties that require less resource input and have high-yield potential is an ideal strategy, which has achieved considerable success in recent decades. [7,8] Crop management practices can also be optimized to enhance the production of rice. [9,10] In recent years, there has been growing interest in using ratoon crops to produce rice grains.…”