Comparative transcriptome analysis of Cyperus esculentus and C. rotundus with contrasting oil contents in tubers defines genes and regulatory networks involved in oil accumulation

Abstract

Plant vegetative organs present great potential for lipid storage, with tubers of Cyperus esculentus as a unique example. To investigate the genome and transcriptomic features of C. esculentus and related species, we sequenced and assembled the C. esculentus genome at the contig level. Through a comparative study of high-quality transcriptomes across 36 tissues from high-oil and intermediate-oil C. esculentus and low-oil Cyperus rotundus, we identified potential genes and regulatory networks related to tuber oil accumulation. First, we identified tuber-specific genes in two C. esculentus cultivars. Second, genes involved in fatty acid (FA) biosynthesis, triacylglycerol synthesis, and TAG packaging presented increased activity in the later stages of tuber development. Notably, tubers with high oil contents presented higher levels of these genes than those with intermediate oil contents did, whereas tubers with low oil contents presented minimal gene expression. Notably, a large fragment of the FA biosynthesis rate-limiting enzyme-encoding gene BCCP1 was missing from the C. rotundus transcript, which might be responsible for blocking FA biosynthesis in its tubers. WGCNA pinpointed a gene module linked to tuber oil accumulation, with a coexpression network involving the transcription factors WRI1, MYB4, and bHLH68. The ethylene-related genes in this module suggest a role for ethylene signaling in oil accumulation, which is supported by the finding that ethylene (ETH) treatment increases the oil content in C. esculentus tubers. This study identified potential genes and networks associated with tuber oil accumulation in C. esculentus, highlighting the role of specific genes, transcription factors, and ethylene signaling in this process.