Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants

Abstract

Glycerolipid biosynthesis in plants proceeds through two major pathways compartmentalized in the chloroplast and the endoplasmic reticulum (ER). The involvement of glycerolipid pathway interactions in modulating membrane desaturation under temperature stress has been suggested but not fully explored. We profiled glycerolipid changes as well as transcript dynamics under suboptimal temperature conditions in three plant species that are distinctively different in the mode of lipid pathway interactions. In Arabidopsis thaliana, a 16:3 plant, the chloroplast pathway is upregulated in response to low temperature, whereas high temperature promotes the eukaryotic pathway. Operating under a similar mechanistic framework, Atriplex lentiformis at high temperature drastically increases the contribution of the eukaryotic pathway and correspondingly suppresses the prokaryotic pathway, resulting in the switch of lipid profile from 16:3 to 18:3. In wheat (Triticum aestivum), an 18:3 plant, low temperature also influences the channeling of glycerolipids from the ER to chloroplast. Evidence of differential trafficking of diacylglycerol moieties from the ER to chloroplast was uncovered in three plant species as another layer of metabolic adaptation under temperature stress. We propose a model that highlights the predominance and prevalence of lipid pathway interactions in temperature-induced lipid compositional changes.

Genome Wide Analysis of Fatty Acid Desaturation and Its Response to Temperature

“…The PUFA content of Arabidopsis leaf lipids also responds to temperature (Falcone et al, 2004). However, the change reported in leaf PC composition between 10°C and 30°C is very modest (Li et al, 2015) compared with our data in seeds. Sanyal and Linder (2013) also reported that there is no significant relationship between the temperature response of fatty acid composition in seed TAG and leaf phospholipids across 84 Arabidopsis accessions.…”

“…Temperature can influence the degree of microsomal fatty acid desaturation indirectly through its effects on substrate availability (Harris and James, 1969;Browse and Slack, 1983;Rolletschek et al, 2007;Li et al, 2015). However, there also is evidence that FAD2 and FAD3 are regulated directly by temperature (Tang et al, 2005;O'Quin et al, 2010).…”

“…Whether this regulation occurs at the level of gene expression appears to vary depending upon the species, tissue, and gene in question. Several studies have reported a significant up-regulation of FAD2 or FAD3 isogenes at lower temperature (Martz et al, 2006;Kargiotidou et al, 2008;Román et al, 2012;Zhu et al, 2012), while others have reported either down-regulation or no appreciable change (Okuley et al, 1994;Heppard et al, 1996;Horiguchi et al, 2000;Li et al, 2015). In the case of FAD3, evidence also has been provided for translational regulation by temperature (Horiguchi et al, 2000), mediated by the 59 untranslated region (UTR) of the transcript (Wang and Xu, 2010).…”

Transport and transcriptional regulation of oil production in plants

“…[4,42] The mechanism underlying these lipid trafficking processes is not fully understood. [3,4,43] In Arabidopsis and Atriplexlen tiformis, low temperatures up-regulate the chloroplast pathway and channel glycerolipids from the ER to the chloroplast, whereas high temperatures increase the contribution of the eukaryotic pathway but suppress the prokaryotic pathway. [43] Arabidopsis ABC lipid transporters are believed to be involved in the ER-chloroplast phospholipid trafficking consisting of TGD1, 2, and 3, which are located in the inner membrane envelope (Figure 2).…”

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

“…The regulation of glycerolipid pathways also is induced in Arabidopsis, wheat (Triticum aestivum), and saltbush (Atriplex spp.) in response to temperature stress, which results in diacylglycerol trafficking from the endoplasmic reticulum to the chloroplasts (Li et al, 2015). In Arabidopsis, heat, salt, and drought also induce triacylglycerol accumulation in the cytosol, an adaptation that enables structural remodeling of membrane lipids (Mueller et al, 2015).…”