Metabolic and transcriptomic study of pennycress natural variation identifies targets for oil improvement

Abstract

SummaryPennycress (Thlaspi arvense L.), a member of the Brassicaceae family, produces seed oil high in erucic acid, suitable for biodiesel and aviation fuel. Although pennycress, a winter annual, could be grown as a dedicated bioenergy crop, an increase in its seed oil content is required to improve its economic competitiveness. The success of crop improvement relies upon finding the right combination of biomarkers and targets, and the best genetic engineering and/or breeding strategies. In this work, we combined biomass composition with metabolomic and transcriptomic studies of developing embryos from 22 pennycress natural variants to identify targets for oil improvement. The selected accession collection presented diverse levels of fatty acids at maturity ranging from 29% to 41%. Pearson correlation analyses, weighted gene co‐expression network analysis and biomarker identifications were used as complementary approaches to detect associations between metabolite level or gene expression and oil content at maturity. The results indicated that improving seed oil content can lead to a concomitant increase in the proportion of erucic acid without affecting the weight of embryos. Processes, such as carbon partitioning towards the chloroplast, lipid metabolism, photosynthesis, and a tight control of nitrogen availability, were found to be key for oil improvement in pennycress. Besides identifying specific targets, our results also provide guidance regarding the best timing for their modification, early or middle maturation. Thus, this work lays out promising strategies, specific for pennycress, to accelerate the successful development of lines with increased seed oil content for biofuel applications.

Transcriptomic and lipidomic analysis of the differential pathway contribution to the incorporation of erucic acid to triacylglycerol during Pennycress seed maturation

“…The RNA-Seq analysis was performed on five different maturation stages, covering the whole seed maturation process. A recent transcriptome analysis was reported in Pennycress in natural variants with differences in seed oil content (Arias et al, 2023). In their study, two early developmental stages that might correspond to our initial G stage and an even earlier stage were used.…”

“…This might be consistent with the loss of chlorophyll with seed maturation as seen in Figure 1A or the decrease in plastid lipids MGDG, DGDG or SQDG observed in Figure 8. In their study with early seed maturation stages, Arias et al (2023) detected genes involved in photosynthesis among the most upregulated ones. Our data are consistent with this observation and suggest an important role of photosynthesis providing carbon and reducing power for fatty acid biosynthesis at the early stages of seed maturation.…”

Pennycress domestication and improvement efforts

“…An in-depth analysis of high-and low-oil-yielding pennycress lines identified differentially expressed genes with crucial roles in oil synthesis pathways (Johnston et al, 2022). More recently, using metabolomic and transcriptomic studies, Arias et al (2023) reported 29%-41% oil content through the analysis of 22 pennycress lines. The carbon portioning and tight nitrogen availability in several mechanisms of oil synthesis were identified to be key to improving pennycress oil traits (Arias et al, 2023).…”

“…More recently, using metabolomic and transcriptomic studies, Arias et al (2023) reported 29%-41% oil content through the analysis of 22 pennycress lines. The carbon portioning and tight nitrogen availability in several mechanisms of oil synthesis were identified to be key to improving pennycress oil traits (Arias et al, 2023). These discoveries open new avenues for utilizing genetic engineering approaches for modeling cross-talk between lipid metabolism and other pathways involving oil production.…”

Research progress on the development of pennycress (Thlaspi arvense L.) as a new seed oil crop: a review

“…The introduction of the acyltransferase ( LPAT and diacylglycerol acyltransferase ) gene and thioesterase ( FatB ) gene of its non-related species Cuphea into pennycress promoted the accumulation of a large amount of medium-chain fatty acids (MCFAs) in seeds without affecting the seed vitality ( Esfahanian et al., 2021 ). According to the metabolomics and transcriptomics analysis of the 22 species of pennycress, improving the oil content of pennycress seeds can be achieved through four effective strategies: chlorophyll carbon allocation, gene modification related to lipid synthesis, enhancement of embryonic photosynthetic efficiency, and strict control of nitrogen utilization ( Arias et al., 2023 ).…”