A Role for Membrane Lipid Polyunsaturation in Chloroplast Biogenesis at Low Temperature

Abstract

Two different mutants of Arabidopsis thaliana deficient in chloroplast membrane lipid polyunsaturation were indistinguishable in appearance from the wild-type when grown at 22 degrees C. By contrast, leaf tissues of the mutants that developed during growth at 5 degrees C were chlorotic, whereas the wild type was not. This is the first direct evidence that chloroplast lipid polyunsaturation contributes to low-temperature fitness. Chloroplasts from mutant lines grown at 5 degrees C were much smaller than those of the wild-type, and the thylakoid membrane content was reduced by up to 70%. However, there was no discernible effect of low temperature on chloroplasts that developed prior to exposure to low temperatures. These and related observations suggest that the high degree of chloroplast membrane lipid polyunsaturation is required for some aspect of chloroplast biogenesis.

A Suppressor of fab1 Challenges Hypotheses on the Role of Thylakoid Unsaturation in Photosynthetic Function

“…This hypothesis is consistent with the other evidence discussed above (Murata et al, 1982;Murata and Yamaya, 1984;Roughan, 1985;Murata et al, 1992;Ishizaki-Nishizawa et al, 1996). It is therefore unexpected that a further increase in chloroplast 16:0 should provide a suppressor phenotype, especially when fad5 mutant plants are themselves compromised in growth and chloroplast biogenesis at low temperature (Hugly and Somerville, 1992).…”

“…Mutants with smaller decreases in thylakoid unsaturation are substantially indistinguishable from wild type when grown at 22°C, but exhibit defects in biogenesis and maintenance of chloroplasts at temperatures below 5°C. These mutants include fad5, fad6, the double mutant fad7 fad8, and the triple mutant fad3 fad7 fad8 (Hugly and Somerville, 1992;Murakami et al, 2000;Routaboul et al, 2000). A role for thylakoid unsaturation in maintaining photosynthetic function at low temperatures is also supported by experiments in which transgenic expression of fatty acid desaturases in chillingsensitive plant species resulted in increased survival of plants at low temperatures (Kodama et al, 1994;Ishizaki-Nishizawa et al, 1996;Murakami et al, 2000).…”

“…The Arabidopsis desaturation mutants fad5, fad6, fad7 fad8, and fad3 fad7 fad8 all show chlorosis and reduced growth rates when grown at 4°C, but the plants are nevertheless able to complete their life cycle (Hugly and Somerville, 1992;Murakami et al, 2000;Routaboul et al, 2000). Another Arabidopsis mutant, fatty acid biosynthesis 1 (fab1), exhibits a distinct lowtemperature phenotype.…”

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

“…The fad5 (Hugly and Somerville, 1992) and act1 (Kunst et al, 1988) mutants, each possessing a mutation that primarily effects the prokaryotic pathway, were indistinguishable from wild-type plants when raised under standard growth temperature, but they were more thermal tolerant and display higher growth rate at high temperature (Kunst et al, 1988;Falcone et al, 2004;Routaboul et al, 2012). In this study, fad5 and act1 were subjected to low-temperature treatment.…”

“…Significant reduction of 16:3 in leaves (Supplemental Table 3) confirmed the repression of the prokaryotic pathway in these mutants. The fad5 mutant was previously shown to develop chlorosis in leaves at 5°C (Hugly and Somerville, 1992) and therefore was included in our experiments as a control for cold treatment. As shown in Figure 6, similar to the fad5 mutant, gly1 developed chlorotic leaves after 3 weeks at 5°C.…”