The transcriptomic signature of developing soybean seeds reveals the genetic basis of seed trait adaptation during domestication

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Cultivated soybean has undergone many transformations during domestication. In this paper we report a comprehensive assessment of the evolution of gene co-expression networks based on the analysis of 40 transcriptomes from developing soybean seeds in cultivated and wild soybean accessions. We identified 2680 genes that are differentially expressed during seed maturation and established two cultivar-specific gene co-expression networks. Through analysis of the two networks and integration with quantitative trait locus data we identified two potential key drivers for seed trait formation,GA20OXandNFYA.GA20OXencodes an enzyme in a rate-limiting step of gibberellin biosynthesis, andNFYAencodes a transcription factor. Overexpression ofGA20OXandNFYAenhanced seed size/weight and oil content, respectively, in seeds of transgenic plants. The two genes showed significantly higher expression in cultivated than in wild soybean, and the increases in expression were associated with genetic variations in the promoter region of each gene. Moreover, the expression ofGA20OXandNFYAin seeds of soybean accessions correlated with seed weight and oil content, respectively. Our study reveals transcriptional adaptation during soybean domestication and may identify a mechanism of selection by expression for seed trait formation, providing strategies for future breeding practice.

Significance Statement

In this work we analyzed 40 transcriptomes from developing seeds of cultivated and wild soybean accessions and assessed gene co-expression networks. We found that promoter variation accounted for the higher expression of a gibberellin biosynthesis gene and of a transcription factor in cultivated soybean, and positively correlated with seed weight and oil content. Such analyses will inform breeding strategies for soybean and/or other crops.

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