Acyl Chain Length of Phosphatidylserine Is Correlated with Plant Lifespan

Citation: Li Y, Zheng G, Jia Y, Yu X, Zhang X, et al. ( Acyl Chain Length of Phosphatidylserine Is Correlated with Plant Lifespan Yan Li 0 Guowei Zheng 0 Yanxia Jia 0 Xiaomei Yu 0 Xudong Zhang 0 Buzhu Yu 0 Dandan Wang 0 Yanling Zheng 0 Xuejun Tian 0 Weiqi Li 0 Carl Ng, University College Dublin, Ireland 0 1 Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming, Yunnan , China , 2 Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences , Kunming, Yunnan , China , 3 Department of Biology, Honghe University , Mengzi, Yunnan , China Plant lifespan is affected by factors with genetic and environmental bases. The laws governing these two factors and how they affect plant lifespan are unclear. Here we show that the acyl chain length (ACL) of phosphatidylserine (PS) is correlated with plant lifespan. Among the detected eight head-group classes of membrane lipids with lipidomics based on triple quadrupole tandem mass spectrometry, the ACL of PS showed high diversity, in contrast to the ACLs of the other seven classes, which were highly conserved over all stages of development in all plant species and organs and under all conditions that we studied. Further investigation found that acyl chains of PS lengthened during development, senescence, and under environmental stresses and that increasing length was accelerated by promoted- senescence. The acyl chains of PS were limited to a certain carbon number and ceased to increase in length when plants were close to death. These findings suggest that the ACL of PS can count plant lifespan and could be a molecular scale ruler for measuring plant development and senescence. - Funding: The research was supported by grants from NSFC (30670474 & 30870571), Fund of State Key Laboratory of Phytochemistry and Plant Resources in West China (0807B01211 and 097C1211Z1), Kunming Institute of Botany (KSCX2-EW-J-24), Germplasm Bank of Wild Species, and CAS Innovation Program of Kunming Institute (540806321211), and 100 Talents Program, CAS. Lipid analysis was performed at the Kansas Lipidomics Research Center. 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. Plant lifespan is a complex manifestation of genetic and environmental factors that encompass both development and senescence. It greatly influences crop productivity, biodiversity, and ecological equilibrium. Lifespan may be extended by enhancing resistance to internal or external stresses in yeast and animal, as described by the stress resistance theory of ageing [1,2]. Telomere lengths can determine lifespan in mammals [3,4], but this does not correlate with lifespan in plants [5,6]. In Arabidopsis, for example, there was no significant difference in telomere length among the leaves at different stages of development [7]. Growth rings are widely used to measure the age of woody plants but they cannot predict the end of plant life. So far little is known about the determination of plant lifespan [8]. No change in primary structures of bio-molecules, DNA, proteins, saccharides, or lipids has been associated with development or lifespan of plants. Glycerolipids are major constituents of cellular membranes. They comprise a glycerol backbone, two acyl groups, and a head group (Figure S1). The acyl groups contain two fatty acid chains at the sn-1 and sn-2 positions of the glycerol backbone. The two fatty acid chains of the glycerolipids in cellular membranes usually comprise fewer than 18 carbon atoms per chain or 36 carbon atoms in total. Fatty acids with more than 18 carbon atoms per chain are known as very long chains of fatty acids (VLCFAs). VLCFAs mainly distribute in cuticular waxes, aliphatic suberins, phospholipids, sphingolipids and seed oils [9]. PS is a head-group class of membrane glycerolipids which contains VLCFA [10,11]. The glycerolipids in cellular membranes consist of multiple types of lipid molecule, which vary with respect to the head group, the lengths of the fatty acid chains, and the degree of unsaturation of the fatty acids. The cellular membranes in plants contain a highly diverse range of lipids, but the reasons for this diversity are not fully understood [12]. Using a lipidomics approach based on electrospray ionization and triple quadrupole tandem mass spectrometry (ESI-MS/MS) [11,13,14], we identified and quantified 140 molecular species of eight classes of membrane glycerolipid in nine plant species from five families. The plant species were chosen randomly. They comprised Arabidopsis and eight wild species that were distributed from alpine regions to maritime land areas and covered annual, biennial, and perennial species (Figure S2). Each molecular species was identified in relation to its total number of acyl carbon atoms and double bonds (Figure S3) [11,13]. We calculated the molar percentage (mol%) of each molecular species on the basis of its content (nmol/mg) (Figure S3). Then, using the distribution of molecular species for each class, we calculated the average number of acyl carbon atoms for each class of head group (Figure S4). Materials and Methods Plant materials, growth conditions and treatments We grew Arabidopsis ecotype Columbia (Col) and Crucihimalaya in soil, hydroponically using Hoaglands medium [15], and/ or on plates in MS media, as indicated, at 22uC, under light of 120 mmol/m2/s, and a 12/12 h photoperiod. For phytohormoneinduced senescence, we placed leaves that had been detached from 6-week-old plants onto filter paper that contained water, ABA (50 mM), or ethephon (50 mM, to release ethylene), and incubated them for the indicated number of days [16,17]. To induce senescence via gamma radiation, hydroponically grown plants aged 20 days were irradiated in a commercial 6uCo facility (FJX648G) at the indicated dose, grown under normal conditions, and sampled at the indicated times. To induce stress from heat shock, we incubated plates with plants aged 10 days in water at 44uC for 2 h [17]. To induce stress from dehydration, we placed plategrown plants onto filter paper and exposed them to air for the indicated time [18]. All reagents described above were obtained from Sigma. Lipid analysis and data processing We analysed lipid samples by ESI-MS/MS [13]. We processed the data in the same way that we have described in previous papers [14,19]. We quantified the lipids in each class in comparison to two internal standards. The lipid content was described as nmol/mg dry weight of plants. We analysed five replicates of each plant species at each sampling time. Paired values were subjected to a t test to determine statistical significance. The average carbon number (C) of the acyl chains in a given lipid (...truncated)