Plasticity and constraints on fatty acid composition in the phospholipids and triacylglycerols of Arabidopsis accessions grown at different temperatures

Anushree Sanyal,Craig Randal Linder

doi:10.1186/1471-2229-13-63

Anushree Sanyal, Craig Randal Linder

Open Access

https://doi.org/10.1186/1471-2229-13-63

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Abstract

BackgroundNatural selection acts on multiple traits in an organism, and the final outcome of adaptive evolution may be constrained by the interaction of physiological and functional integration of those traits. Fatty acid composition is an important determinant of seed oil quality. In plants the relative proportions of unsaturated fatty acids in phospholipids and seed triacylglycerols often increases adaptively in response to lower growing temperatures to increase fitness. Previous work produced evidence of genetic constraints between phospholipids and triacylglycerols in the widely studied Arabidopsis lines Col and Ler, but because these lines are highly inbred, the correlations might be spurious. In this study, we grew 84 wild Arabidopsis accessions at two temperatures to show that genetic correlation between the fatty acids of the two lipid types is not expected and one should not influence the other and seed oil evolution and also tested for the adaptive response of fatty acids to latitude and temperature.ResultsAs expected no significant correlations between the two lipids classes at either growing temperature were observed. The saturated fatty acids and erucic acid of triacylglycerols followed a significant latitudinal cline, while the fatty acids in phospholipids did not respond to latitude as expected. The expected plastic response to temperature was observed for all the triacylglycerol fatty acids whereas only oleic acid showed the expected pattern in phospholipids. Considerable phenotypic variation of the fatty acids in both the lipid types was seen.ConclusionWe report the first evidence supporting adaptive evolution of seed triacylglycerols in Arabidopsis on a latitudinal cline as seen in other species and also their plastic adaptive response to growing temperature. We show that as expected there is no genetic correlations between the fatty acids in triacylglycerols and phospholipids, indicating selection can act on seed triacylglycerols without being constrained by the fatty acid requirements of the phospholipids. Phospholipid fatty acids do not respond to latitude and temperature as seen elsewhere and needs further investigation. Thus, the adaptive response of Arabidopsis and the genetic tools available for manipulating Arabidopsis, makes it an excellent system for studying seed oil evolution and also for breeding seed oil crops especially the Brassica species.

Highlights

Natural selection acts on multiple traits in an organism, and the final outcome of adaptive evolution may be constrained by the interaction of physiological and functional integration of those traits
Latitudinal variation in TAGs and PLs The relative proportion of total saturated fatty acid (FA) in TAGs decreased significantly with increasing latitude when plants were grown at low temperatures (q = 0.007, BHFDR = 0.024, r2 = 0.191, Figure 1A, Table 2)
The slope trended in the same direction but was non-significant when controlled for multiple tests, albeit marginally for one test (q = 0.056; BH-false discovery rate (FDR) = 0.192, Table 2)

Summary

Introduction

Natural selection acts on multiple traits in an organism, and the final outcome of adaptive evolution may be constrained by the interaction of physiological and functional integration of those traits. In plants the relative proportions of unsaturated fatty acids in phospholipids and seed triacylglycerols often increases adaptively in response to lower growing temperatures to increase fitness. Natural selection acts upon the whole organism rather than on isolated traits, and adaptive evolution may be constrained by the interaction between traits that are functionally or physiologically integrated. Most seed plants at the time of seed production have two major fatty acid (FA) sinks: the triacylglycerols (TAGs) and the phospholipids (PLs). In the ER, FAs may be elongated and more highly desaturated before they are incorporated into TAGs and PLs [16,17,18]. Both PLs and TAGs are synthesized by adding FAs to a glycerol backbone

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