Characterization of shade tolerance gene network in soybean revealed by forward integrated reverse genetic studies

Abstract

Shade tolerance is a key trait for cultivars in inter/relay-cropped soybeans in maize fields. Our previous genome-wide association study (GWAS) results on southern China soybean germplasm revealed that the shade tolerance was conferred by a complex of genes with multiple alleles. To complete our understanding of the shade tolerance gene system, GWAS with gene-allele sequences as markers (designated GASM-RTM-GWAS) was conducted in a recombinant inbred line (RIL) population between two extreme parents using the shade tolerance index (STI) and relative pith cell length (RCL) as indicators. Altogether, 211 genes, comprising 99 and 119 genes (seven shared) for STI and RCL, respectively, were identified and then annotated into a similar set of five biological categories. Furthermore, transcriptome analysis detected 7837 differentially expressed genes (DEGs), indicating plentiful DEGs involved in the expression of regulatory/causal GWAS genes. Protein-protein interaction (PPI) analysis and gene functional analysis for both GWAS genes and DEGs showed a group of interrelated causal genes and a group of interrelated DEGs; the former were included in the latter and their functions were interconnected as a gene network. For further understanding of the response of soybean to shade stress in a sequential connection, six chronological gene modules were grouped as signal activation and transport, signal-transduction, signal amplification, gene expression, regulated metabolites, and material transport. From the modules, 12 key genes were selected as entry points for further analysis. Our study provides an overview of the shade tolerance gene network as a new insight into a complex-trait genetic system, rather than the usual way of starting from a hand-picked single gene.

Acknowledgements

This work was financially supported by the grants from the National Key Research and Development Program of China (2021YFF1001204, 2021YFD1201602), the MOE 111 Project (B08025), the MOA CARS-04 program, the Zhongshan Biological Breeding Laboratory program (ZSBBL-KY2023-03), the Core Technology Development for Breeding Program of Jiangsu Province (JBGS-2021-014), the Guangxi Scientific Research and Technology Development Plan (14125008-2-16), and the Guidance Foundation of Sanya Institute of NAU (NAUSY-ZZ02, NAUSY-MS05). The funders had no role in work design, data collection and analysis, and preparation and publication of the manuscript. We thank the Sugarcane Research Institute, Guangxi Academy of Agricultural Sciences, for providing the light microscope facilities.

Author contributions

J.G. and Z.S. conceived and designed the study. Y.S., W.Z., Z.L., Z.Z., L.S., N.L., W.W., and J.Z. performed the field experiments. Y.S., Y.P., P.G., X.H., S.G., J.H., and G.X. performed the laboratory work and analyzed the data. J.G. and Y.S. drafted, revised, and finalized the manuscript.

Data availability

All relevant data in this study are provided in the article and its supplementary figure and table files.

Conflict of interest statement

The authors declare no competing interests.

Supplementary data

Supplementary data are available at Horticulture Research online.

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