Maintenance or Collapse: Responses of Extraplastidic Membrane Lipid Composition to Desiccation in the Resurrection Plant Paraisometrum mileense

Li W (2014) Maintenance or Collapse: Responses of Extraplastidic Membrane Lipid Composition to Desiccation in the Resurrection Plant Paraisometrum mileense. PLoS ONE 9(7): e103430. doi:10.1371/journal.pone.0103430 Maintenance or Collapse: Responses of Extraplastidic Membrane Lipid Composition to Desiccation in the Resurrection Plant Paraisometrum mileense Aihua Li 0 Dandan Wang 0 Buzhu Yu 0 Xiaomei Yu 0 Weiqi Li 0 Jin-Song Zhang, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, China 0 1 Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Science , Kunming , China , 2 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming , China , 3 University of Chinese Academy of Sciences , Beijing , China Resurrection plants usually grow in specific or extreme habitats and have the capacity to survive almost complete water loss. We characterized the physiological and biochemical responses of Paraisometrum mileense to extreme desiccation and found that it is a resurrection plant. We profiled the changes in lipid molecular species during dehydration and rehydration in P. mileense, and compared these with corresponding changes in the desiccation-sensitive plant Arabidopsis thaliana. One day of desiccation was lethal for A. thaliana but not for P. mileense. After desiccation and subsequent rewatering, A. thaliana showed dramatic lipid degradation accompanied by large increases in levels of phosphatidic acid (PA) and diacylglycerol (DAG). In contrast, desiccation and rewatering of P. mileense significantly decreased the level of monogalactosyldiacylglycerol and increased the unsaturation of membrane lipids, without changing the level of extraplastidic lipids. Lethal desiccation in P. mileense caused massive lipid degradation, whereas the PA content remained at a low level similar to that of fresh leaves. Neither damage nor repair processes, nor increases in PA, occurred during non-lethal desiccation in P. mileense. The activity of phospholipase D, the main source of PA, was much lower in P. mileense than in A. thaliana under control conditions, or after either dehydration or rehydration. It was demonstrated that low rates of phospholipase Dmediated PA formation in P. mileense might limit its ability to degrade lipids to PA, thereby maintaining membrane integrity following desiccation. - Funding: This research was supported by grants from the National Natural Science Foundation of China (31070262), Kunming Institute of Botany (KSCX2-EW-J24), the Germplasm Bank of Wild Species, the CAS Innovation Program of Kunming Institute (540806321211), as well as the 100-Talents Program of CAS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. . These authors contributed equally to this work. Drought is a major factor that limits plant growth and yield. In most parts of the world, drought continuously affects crop production and is of growing concern given the increasing demand for food production by the expanding global population [1,2]. Most crops are sensitive to drought, and except their seeds and pollen grains, their tissues cannot withstand water stress below 20% relative water content (RWC) [3]. However, a small group of so-called resurrection plants can tolerate extreme loss of water (desiccation) to 10% RWC or less [3]. Upon rewatering, the vegetative tissues of resurrection plants can quickly revive from the quiescent state that they enter upon loss of almost all of their free water [4]. Resurrection plants are excellent models to explore the physiological, biochemical, and molecular basis of desiccation tolerance [5]. A better understanding of the unique features of resurrection plants might benefit efforts to improve crop yields under conditions of water deficit. Resurrection plants exhibit a series of distinct morphological, physiological, biochemical, and genetic protective mechanisms to resist or respond to extreme desiccation. The folding and reexpansion of leaves are the most obvious morphological changes that occur during desiccation and subsequent rewatering; folding might prevent the production of reactive oxygen species (ROS) induced by light during drying and rehydration [4,69]. Inward shrinking of the cell wall and dehydration-induced membrane shrinking are typical responses of resurrection plants to desiccation [5,6,10]. In these plants, photosynthetic activity is retained during mild drought, is lost during severe desiccation, and returns upon subsequent rehydration [7,1114]. Resurrection plants do not necessarily share the same physiological strategies, and sometimes even employ completely opposite strategies to deal with extreme desiccation. For example, the osmoprotectant proline is widely used to resist cellular dehydration in plants. However, whereas some resurrection plants accumulate proline following desiccation, others do not [1517]. In addition, some resurrection plants (poikilochlorophyllous species) lose their chlorophyll and degrade their thylakoid membranes to prevent the production of photosynthetically generated ROS during dehydration [9,18]. Other resurrection plants (homoiochlorophyllous species), such as Craterostigma plantagineum and Haberlea rhodopensis, retain their chlorophyll and thylakoid structures [19,20]. The ability of resurrection plants to maintain antioxidant activity even after severe cellular dehydration is thought to account in large part for their distinctive capacity to resist desiccation [9,21]. Osmoregulatory substances, such as sucrose, alleviate cellular dehydration and oxidative stress in resurrection plants [2225]. Many genes that function in drought tolerance have been cloned from resurrection plants and characterized [2629]. Transformation of certain plants with some of these genes improves drought resistance significantly [30]. The powerful approaches of transcriptomics [31,32], proteomics [3336], and metabolomics [1] have enabled extensive investigation of the mechanisms that resurrection plants use to resist severe dehydration at the levels of global changes in gene expression and the abundances of proteins and metabolites. Lipid metabolism during and following desiccation was recently reported in Craterostigma plantagineum [37]. However, especially given that the tolerance strategies used by resurrection plants are often species-specific, little is known about how molecular species of membrane lipids respond to severe dehydration and subsequent rehydration, and how the changes in lipid profiles contribute to ability to survive extreme desiccation. Maintenance of membrane integrity and fluidity is of critical importance to ensure that resurrection plants can survive cellular dehydration [5,38]. Several membran (...truncated)