John Browse, Washington State University

The characterization of lipid mutants and the experimental modification of lipid composition by molecular-genetic means have now revealed some broad generalizations about the roles of membrane lipids in the cell biology and physiology of plants (see also Web Topic 26.3). However, the biochemical and physical bases for the phenotypes that are observed remain uncertain. Changes in fatty acid composition have been shown to alter chloroplast size and architecture. Mutations that eliminate polyunsaturated fatty acids block photosynthesis and prevent the plant from growing autotrophically (McConn and Browse 1998).

Surprisingly, such mutant plants can grow on sucrose, indicating that photosynthesis is the only plant function that absolutely requires a polyunsaturated membrane. As described in textbook Chapter 13, however, polyunsaturated fatty acids are also required as precursors of signaling compounds which are necessary for such diverse functions as pollen development and plant defense, such as jasmonic acid, (Howe et al. 1996; McConn and Browse 1998; Vijayan et al. 1998).

One of the most extensively studied issues in membrane biology is the relationship between lipid composition and the ability of organisms to adjust to temperature changes (Wolter et al. 1992). For example, chill-sensitive plants experience sharp reductions in growth rate and development at temperatures between 0 and 12°C. The physical and physiological changes in chill-sensitive plants that are induced by exposure to low temperature, together with the subsequent expression of stress symptoms, are termed chilling injury (see textbook Chapter 26).

Many economically important crops, such as cotton, soybean, maize, rice, and many tropical and subtropical fruits, are classified as chill sensitive. In contrast, most plants of temperate origin are able to grow and develop at chilling temperatures and are classified as chill-resistant plants.

In attempts to link the biochemical and physiological changes associated with chilling injury with a single "trigger" or site of damage, it has been suggested that the primary event of chilling injury is a transition from a liquid-crystalline phase to a gel phase in the cellular membranes. According to this proposal, the transition from liquid-crystalline phase to gel phase would result in alterations in the metabolism of chilled cells and lead to injury and death of the chill-sensitive plants. The degree of unsaturation of the fatty acids would determine the temperature at which such damage occurs. A similar hypothesis has been proposed for chloroplast membranes in which the levels of disaturated phosphatidylglycerol (molecules containing no cis double bonds in the fatty acid chains) would determine the chilling sensitivity of plant species (Murata et al. 1992).

However, the most recent research indicates that the relationship of membrane unsaturation to plant temperature responses is more subtle and complex than is suggested in these earlier hypotheses. On the one hand, studies of five different Arabidopsis mutants have demonstrated that reduced unsaturation can result in plants that grow well at 22°C but are less robust than wild-type plants when grown at 2 to 5°C. These results were observed even though the lipid changes in most of the mutants are insufficient to cause a lipid phase transition. In addition, the responses of these mutants to low temperature appear quite distinct from classic chilling sensitivity, suggesting that normal chilling injury may not be related to the level of unsaturation of membrane lipids (Hugly and Somerville 1992; Miquel et al. 1993).

In one particular mutant, fab1, saturated forms of phosphatidylglycerol account for 43% of the total leaf phosphatidylglycerol—a higher percentage than is found in many chill-sensitive plants. Nevertheless, the mutant was completely unaffected (when compared with wild-type controls) by a range of low-temperature treatments that quickly led to the death of cucumber and other chill-sensitive plants (Wu and Browse 1995).

A complementary series of experiments has been carried out in tobacco, which is a chill-sensitive plant. The transgenic expression of exogenous genes in tobacco has been used specifically to decrease the level of saturated phosphatidylglycerol or to bring about a general increase in membrane unsaturation (Murata et al. 1992; Kodama et al. 1994; Ishizaki-Nishizawa et al. 1996). In each case, damage caused by chilling was alleviated to some extent. These new findings make it clear that the extent of membrane unsaturation or the presence of particular lipids, such as disaturated phosphatidylglycerol, can affect the responses of plants to low temperature. However, membrane lipid composition is not the major determinant of chilling sensitivity in plants.