Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)

Nian Liu; Bei Wu; Manish K Pandey; Li Huang; Huaiyong Luo; Yuning Chen; Xiaojing Zhou; Weigang Chen; Dongxin Huai; Bolun Yu; Hao Chen; Jianbin Guo; Yong Lei; Boshou Liao; Rajeev K Varshney; Huifang Jiang

doi:10.3389/fpls.2022.1065267

Gene expression and DNA methylation altering lead to the high oil content in wild allotetraploid peanut (A. monticola)

Front Plant Sci. 2022 Dec 16:13:1065267. doi: 10.3389/fpls.2022.1065267. eCollection 2022.

Authors

Affiliations

¹ Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, Oil Crops Research Institute of the Chinese Academy of Agricultural Sciences, Wuhan, China.
² Center of Excellence in Genomics and Systems Biology (CEGSB), International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, India.
³ Institute of Crop Sciences, Fujian Academy of Agricultural Sciences, Fuzhou, China.

Abstract

Introduction: The wild allotetraploid peanut Arachis monticola contains a higher oil content than the cultivated allotetraploid Arachis hypogaea. Besides the fact that increasing oil content is the most important peanut breeding objective, a proper understanding of its molecular mechanism controlling oil accumulation is still lacking.

Methods: We investigated this aspect by performing comparative transcriptomics from developing seeds between three wild and five cultivated peanut varieties.

Results: The analyses not only showed species-specific grouping transcriptional profiles but also detected two gene clusters with divergent expression patterns between two species enriched in lipid metabolism. Further analysis revealed that expression alteration of lipid metabolic genes with co-expressed transcription factors in wild peanut led to enhanced activity of oil biogenesis and retarded the rate of lipid degradation. In addition, bisulfite sequencing was conducted to characterize the variation of DNA methylation between wild allotetraploid (245, WH 10025) and cultivated allotetraploid (Z16, Zhh 7720) genotypes. CG and CHG context methylation was found to antagonistically correlate with gene expression during seed development. Differentially methylated region analysis and transgenic assay further illustrated that variations of DNA methylation between wild and cultivated peanuts could affect the oil content via altering the expression of peroxisomal acyl transporter protein (Araip.H6S1B).

Discussion: From the results, we deduced that DNA methylation may negatively regulate lipid metabolic genes and transcription factors to subtly affect oil accumulation divergence between wild and cultivated peanuts. Our work provided the first glimpse on the regulatory mechanism of gene expression altering for oil accumulation in wild peanut and gene resources for future breeding applications.

Keywords: Arachis hypogaea; Arachis monticola; DNA methylation; expression profiling; functional genomics; oil biosynthesis.