Comparative transcriptomic analysis provides insights into the genetic networks regulating oil differential production in oil crops

BMC Biol. 2024 May 13;22(1):110. doi: 10.1186/s12915-024-01909-x.

Abstract

Background: Plants differ more than threefold in seed oil contents (SOCs). Soybean (Glycine max), cotton (Gossypium hirsutum), rapeseed (Brassica napus), and sesame (Sesamum indicum) are four important oil crops with markedly different SOCs and fatty acid compositions.

Results: Compared to grain crops like maize and rice, expanded acyl-lipid metabolism genes and relatively higher expression levels of genes involved in seed oil synthesis (SOS) in the oil crops contributed to the oil accumulation in seeds. Here, we conducted comparative transcriptomics on oil crops with two different SOC materials. In common, DIHYDROLIPOAMIDE DEHYDROGENASE, STEAROYL-ACYL CARRIER PROTEIN DESATURASE, PHOSPHOLIPID:DIACYLGLYCEROL ACYLTRANSFERASE, and oil-body protein genes were both differentially expressed between the high- and low-oil materials of each crop. By comparing functional components of SOS networks, we found that the strong correlations between genes in "glycolysis/gluconeogenesis" and "fatty acid synthesis" were conserved in both grain and oil crops, with PYRUVATE KINASE being the common factor affecting starch and lipid accumulation. Network alignment also found a conserved clique among oil crops affecting seed oil accumulation, which has been validated in Arabidopsis. Differently, secondary and protein metabolism affected oil synthesis to different degrees in different crops, and high SOC was due to less competition of the same precursors. The comparison of Arabidopsis mutants and wild type showed that CINNAMYL ALCOHOL DEHYDROGENASE 9, the conserved regulator we identified, was a factor resulting in different relative contents of lignins to oil in seeds. The interconnection of lipids and proteins was common but in different ways among crops, which partly led to differential oil production.

Conclusions: This study goes beyond the observations made in studies of individual species to provide new insights into which genes and networks may be fundamental to seed oil accumulation from a multispecies perspective.

Keywords: Acyl-lipid metabolism; Coexpression networks; Comparative transcriptomic; Different species; Differential expression analysis; Network alignment; Seed oil synthesis; Seed storage.

Publication types

  • Research Support, Non-U.S. Gov't
  • Comparative Study

MeSH terms

  • Crops, Agricultural* / genetics
  • Crops, Agricultural* / metabolism
  • Gene Expression Profiling* / methods
  • Gene Expression Regulation, Plant
  • Gene Regulatory Networks*
  • Plant Oils* / metabolism
  • Seeds / genetics
  • Seeds / metabolism
  • Transcriptome

Substances

  • Plant Oils