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.
References
[1]
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408: 239–247. doi: 10.1038/35041687
[2]
Lane MA, Mattison J, Ingram DK, Roth GS (2002) Caloric restriction and aging in primates: Relevance to humans and possible CR mimetics. Microsc Res Tech 59: 335–338. doi: 10.1002/jemt.10214
[3]
Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, et al. (1990) Telomere reduction in human colorectal carcinoma and with ageing. Nature 346: 866–868. doi: 10.1038/346866a0
[4]
Allsopp RC, Vaziri H, Patterson C, Goldstein S, Younglai EV, et al. (1992) Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci U S A 89: 10114–10118. doi: 10.1073/pnas.89.21.10114
[5]
Broun P, Ganal MW, Tanksley SD (1992) Telomeric arrays display high levels of heritable polymorphism among closely related plant varieties. Proc Natl Acad Sci U S A 89: 1354–1357. doi: 10.1073/pnas.89.4.1354
[6]
Kilian A, Stiff C, Kleinhofs A (1995) Barley telomeres shorten during differentiation but grow in callus culture. Proc Natl Acad Sci U S A 92: 9555–9559. doi: 10.1073/pnas.92.21.9555
[7]
Zentgraf U, Hinderhofer K, Kolb D (2000) Specific association of a small protein with the telomeric DNA-protein complex during the onset of leaf senescence in Arabidopsis thaliana. Plant Mol Biol 42: 429–438.
[8]
Marba N, Duarte CM, Agusti S (2007) Allometric scaling of plant life history. Proc Natl Acad Sci U S A 104: 15777–15780. doi: 10.1073/pnas.0703476104
[9]
Kim J, Jung JH, Lee SB, Go YS, Kim HJ, et al. (2013) Arabidopsis 3-ketoacyl-coenzyme A synthase9 is involved in the synthesis of tetracosanoic acids as precursors of cuticular waxes, suberins, sphingolipids, and phospholipids. Plant Physiology 162: 567–580. doi: 10.1104/pp.112.210450
[10]
Millar AA, Smith MA, Kunst L (2000) All fatty acids are not equal: discrimination in plant membrane lipids. Trends Plant Sci 5: 95–101. doi: 10.1016/s1360-1385(00)01566-1
[11]
Devaiah SP, Roth MR, Baughman E, Li M, Tamura P, et al. (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochemistry 67: 1907–1924. doi: 10.1016/j.phytochem.2006.06.005
[12]
Buchanan B, Gruissem W, Jones R (2002) Biochemistry & Molecular Biology of Plants, pp. 499. John Wiley & Sons.
[13]
Welti R, Li W, Li M, Sang Y, Biesiada H, et al. (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277: 31994–32002. doi: 10.1074/jbc.m205375200
[14]
Zheng G, Tian B, Zhang F, Tao F, Li W (2011) Plant adaptation to frequent alterations between high and low temperatures: remodelling of membrane lipids and maintenance of unsaturation levels. Plant Cell Environ 34: 1431–1442. doi: 10.1111/j.1365-3040.2011.02341.x
[15]
Tocquin P, Corbesier L, Havelange A, Pieltain A, Kurtem E, et al. (2003) A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biol 3: 2. doi: 10.1186/1471-2229-3-2
[16]
Fan L, Zheng S, Wang X (1997) Antisense suppression of phospholipase D alpha retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9: 2183–2196. doi: 10.1105/tpc.9.12.2183
[17]
Choe HT, Whang M (1986) Effects of ethephon on aging and photosynthetic activity in isolated chloroplasts. Plant Physiol 80: 305–309. doi: 10.1104/pp.80.2.305
[18]
Katagiri T, Takahashi S, Shinozaki K (2001) Involvement of a novel Arabidopsis phospholipase D, AtPLDdelta, in dehydration-inducible accumulation of phosphatidic acid in stress signalling. Plant J 26: 595–605. doi: 10.1046/j.1365-313x.2001.01060.x
[19]
Welti R, Wang X (2004) Lipid species profiling: a high-throughput approach to identify lipid compositional changes and determine the function of genes involved in lipid metabolism and signaling. Curr Opin Plant Biol 7: 337–344. doi: 10.1016/j.pbi.2004.03.011
[20]
Collado M, Blasco MA, Serrano M (2007) Cellular senescence in cancer and aging. Cell 130: 223–233. doi: 10.1016/j.cell.2007.07.003
[21]
Boubriak, II, Grodzinsky DM, Polischuk VP, Naumenko VD, Gushcha NP, et al. (2008) Adaptation and impairment of DNA repair function in pollen of Betula verrucosa and seeds of Oenothera biennis from differently radionuclide-contaminated sites of Chernobyl. Ann Bot 101: 267–276. doi: 10.1093/aob/mcm276
[22]
Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci U S A 97: 4392–4397. doi: 10.1073/pnas.97.8.4392
[23]
Li W, Wang R, Li M, Li L, Wang C, et al. (2008) Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thaliana. J Biol Chem 283: 461–468. doi: 10.1074/jbc.m706692200
[24]
Zhang X, Wang R, Zhang F, Tan F, LI W (2013) Lipid profiling and tolerance to low-temperature stress in Thellungiella salsuginea in comparison with Arabidopsis thaliana. Biologia Plantarum 57: 149–153. doi: 10.1007/s10535-012-0137-8
[25]
Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, et al. (1992) Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148: 2207–2216.
[26]
Yamaoka Y, Yu Y, Mizoi J, Fujiki Y, Saito K, et al. (2011) PHOSPHATIDYLSERINE SYNTHASE1 is required for microspore development in Arabidopsis thaliana. Plant J 67: 648–661. doi: 10.1111/j.1365-313x.2011.04624.x
[27]
Schneiter R, Kohlwein SD (1997) Organelle structure, function, and inheritance in yeast: a role for fatty acid synthesis? Cell 88: 431–434. doi: 10.1016/s0092-8674(00)81882-6
[28]
Murphy DJ (2005) Plant lipids: biology, utilisation, and manipulation. Blackwell Pub: CRC Press, Oxford Boca Raton, FL. pp81.
[29]
Tang F, Watkins JW, Bermudez M, Gray R, Gaban A, et al. (2008) A life-span extending form of autophagy employs the vacuole-vacuole fusion machinery. Autophagy 4: 874–886. doi: 10.4161/auto.6556
[30]
Bouter A, Gounou C, Berat R, Tan S, Gallois B, et al. (2011) Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat Commun 2: 270. doi: 10.1038/ncomms1270