Combined GWAS and eQTL analysis uncovers a genetic regulatory network orchestrating the initiation of secondary cell wall development in cotton

Authors: LI, ZHONGHUA - Huazhong Agricultural University; WANG, PENGCHENG - Huazhong Agricultural University; YOU, CHUNYUAN - Shihezi University; YU, JIWEN - Cotton Research Institute - China; ZHANG, XIANGNAN - Huazhong Agricultural University; YAN, FEILIN - Huazhong Agricultural University; YE, ZHENGXIU - Huazhong Agricultural University; SHEN, CHAO - Huazhong Agricultural University; LI, BAOQI - Huazhong Agricultural University; GUO, KAI - Huazhong Agricultural University; LIU, NIAN - Huazhong Agricultural University; Thyssen, Gregory; Fang, David; LINDSEY, KEITH - University Of Durham; ZHANG, XIANLONG - Huazhong Agricultural University; WANG, MAOJUN - Huazhong Agricultural University; TU, LILI - Huazhong Agricultural University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/28/2020
Publication Date: 2/28/2020
Citation: Li, Z., Wang, P., You, C., Yu, J., Zhang, X., Yan, F., Ye, Z., Shen, C., Li, B., Guo, K., Liu, N., Thyssen, G.N., Fang, D.D., Lindsey, K., Zhang, X., Wang, M., Tu, L. 2020. Combined GWAS and eQTL analysis uncovers a genetic regulatory network orchestrating the initiation of secondary cell wall development in cotton. New Phytologist. 226:1738-1752. https://doi.org/10.1111/nph.16468.
DOI: https://doi.org/10.1111/nph.16468

Interpretive Summary: Cotton fiber is not only widely used in textile industry, but also serves as an experimental model system for studying how plant cell develops and differentiates. In this research, we performed a genome-wide association study (GWAS) and identified 28 genetic loci associated with fiber quality traits in cotton. To better understand the regulatory roles of these loci, we sequenced fiber RNAs of 251 cotton accessions and identified 15,330 expression quantitative trait loci (eQTLs) involved in the expressional regulation of 9,282 genes. Integrated analysis of local eQTL and GWAS data prioritized 13 causal genes for differential fiber quality in a transcriptome-wide association study. Characterization of distal eQTLs revealed differential genetic regulation patterns between two subgenomes, highlighted by an eQTL hotspot (Hot216) on chromosome D11 that establishes a genome-wide genetic network regulating the expression of 962 genes. The primary regulatory role of Hot216, specifically the prioritized casual gene encoding a KIP-related protein, was found to be transcriptional regulation of genes responsible for cell wall synthesis, which contributes to fiber length via modulating developmental transition from rapid fiber elongation to secondary cell wall synthesis. This study reveals subgenome genetic regulation manipulating staged fiber differentiation and sheds further light on the notion of spatiotemporal modulation of secondary cell wall synthesis for cultivating cotton producing superior fiber.

Technical Abstract: Cotton fiber serves as an experimental system for studying cell differentiation in plants, but the understanding of genetic and transcriptional regulation during staged fiber differentiation remains limited. We performed a genome-wide association study (GWAS) and identified 28 genetic loci associated with fiber quality-related traits in an allotetraploid cotton (Gossypium hirsutum). To interrogate the regulatory roles of these loci, we sequenced fiber transcriptomes of 251 cotton accessions and identified 15,330 expression quantitative trait loci (eQTLs) involved in the transcriptional regulation of 9,282 genes. Integrated analysis of local eQTL and GWAS data prioritized 13 causal genes for differential fiber quality in a transcriptome-wide association study (TWAS). Characterization of distal eQTLs revealed differential genetic regulation patterns between two subgenomes, highlighted by an eQTL hotspot (Hot216) on chromosome D11 that establishes a genome-wide genetic network regulating the expression of 962 genes. The primary regulatory role of Hot216, specifically the prioritized casual gene encoding a KIP-related protein, was found to be transcriptional regulation of genes responsible for cell wall synthesis, which contributes to fiber length via modulating developmental transition of rapid fiber elongation to secondary cell wall synthesis. This study uncovers subgenome genetic regulation manipulating staged fiber differentiation and sheds further light on the notion of spatiotemporal modulation of secondary cell wall synthesis for cultivating cotton producing superior fiber.