Alterations in the leaf lipidome of Brassica carinata under high-temperature stress

Abstract

Background Brassica carinata (A) Braun has recently gained increased attention across the world as a sustainable biofuel crop. B. carinata is grown as a summer crop in many regions where high temperature is a significant stress during the growing season. However, little research has been conducted to understand the mechanisms through which this crop responds to high temperatures. Understanding traits that improve the high-temperature adaption of this crop is essential for developing heat-tolerant varieties. This study investigated lipid remodeling in B. carinata in response to high-temperature stress. A commercial cultivar, Avanza 641, was grown under sunlit-controlled environmental conditions in Soil-Plant-Atmosphere-Research (SPAR) chambers under optimal temperature (OT; 23/15°C) conditions. At eight days after sowing, plants were exposed to one of the three temperature treatments [OT, high-temperature treatment-1 (HT-1; 33/25°C), and high-temperature treatment-2 (HT-2; 38/30°C)]. The temperature treatment period lasted until the final harvest at 84 days after sowing. Leaf samples were collected at 74 days after sowing to profile lipids using electrospray-ionization triple quadrupole mass spectrometry. Results Temperature treatment significantly affected the growth and development of Avanza 641. Both high-temperature treatments caused alterations in the leaf lipidome. The alterations were primarily manifested in terms of decreases in unsaturation levels of membrane lipids, which was a cumulative effect of lipid remodeling. The decline in unsaturation index was driven by (a) decreases in lipids that contain the highly unsaturated linolenic (18:3) acid and (b) increases in lipids containing less unsaturated fatty acids such as oleic (18:1) and linoleic (18:2) acids and/or saturated fatty acids such as palmitic (16:0) acid. A third mechanism that likely contributed to lowering unsaturation levels, particularly for chloroplast membrane lipids, is a shift toward lipids made by the eukaryotic pathway and the channeling of eukaryotic pathway-derived glycerolipids that are composed of less unsaturated fatty acids into chloroplasts. Conclusions The lipid alterations appear to be acclimation mechanisms to maintain optimal membrane fluidity under high-temperature conditions. The lipid-related mechanisms contributing to heat stress response as identified in this study could be utilized to develop biomarkers for heat tolerance and ultimately heat-tolerant varieties.

High Temperature Alters Leaf Lipid Membrane Composition Associated with Photochemistry of PSII and Membrane Thermostability in Rice Seedlings

“…A decrease in unsaturation or increase in saturation of fatty acids in membrane lipids was known to help maintain appropriate membrane fluidity at high temperature [ 9 ]. Similar to our results, HT treatment in Brassica carinata resulted in remodelling of leaf lipidome manifested by decreases in unsaturated levels of membrane lipids, especially C18:3, and increases in saturated fatty acids such as C16:0 [ 29 ]. These authors proposed that plants can modulate the level of unsaturation of membrane lipids by decreasing the activity of FAD3, FAD7 and FAD8, which catalyse the formation of C18:3, or by increasing the activity of FAD2 and fatty acid synthase (FAS), which catalyse the formation of C18:2 or C16:0, respectively.…”

“…Similarly, Brassica carinata cv. Avanza 641 responded to HT by decreasing the level of unsaturation in membrane lipid, especially in unsaturated linolenic acid (18:3) to maintain optimal membrane fluidity [ 29 ]. Moreover, soybean [ 30 ] and peanut [ 31 ] also responded to HT by decreasing lipid unsaturation levels to maintain membrane fluidity, and the magnitudes of reduction were greater for heat-tolerant than for heat-sensitive genotypes.…”

Lipidomics-Assisted GWAS (lGWAS) Approach for Improving High-Temperature Stress Tolerance of Crops

“…Data about such complex lipid alterations can be recorded with high-throughput mass-spectrometry-based analytical platforms. Several studies have employed MS-based lipidomics to profile changes in plant membrane lipids [ 4 , 5 , 7 , 8 , 9 , 10 ]. The ultimate goal of lipidomics is to determine the relative or absolute abundance of one, several, or all lipid species present in the sample [ 66 , 67 ].…”

“…Lipid compositional variation in response to HT stress has been recorded in several plants such as Arabidopsis thaliana [ 6 ], wheat [ 7 , 8 ], soybean [ 9 ], and Ethiopian mustard ( Brassica carinata ) [ 10 ]. Djanaguiraman et al [ 7 ] have reported that in wheat, the decrease in photosynthetic rate under HT stress is due to thylakoid membrane damage, lipid composition alterations, and oxidative damage of organelles.…”

Low- and High-Temperature Phenotypic Diversity of Brassica carinata Genotypes for Early-Season Growth and Development

“…These studies identified morpho-physiological traits enabling the selection of superior stress-tolerant genotypes at the early growth stage in rice ( Kakar et al, 2019 ; Reddy et al, 2021 ), corn ( Zea mays ) ( Wijewardana et al, 2015 ), sweet potato ( Ipomoea batatas ) ( Ramamoorthy et al, 2022 ), and cotton ( Brand et al, 2016 ). Likewise, variations in stress tolerance among carinata genotypes have been reported ( Angadi et al, 2000 ; Gesch et al, 2019 ; Zoong Lwe et al, 2021 ). There is limited information on carinata response to different temperature ranges during the early season.…”