Abiotic factors influence plant storage lipid accumulation and composition

Plant Science

Volumn 243, Issue , 2016, Pages 1-9

  Singer, Stacy D ^a   Zou, Jitao ^b   Weselake, Randall J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

Enhancing seed oil content; Environmental stress; Improving seed oil quality; Oleaginous crops; Seed oil; Triacylglycerol biosynthesis

Indexed keywords

LIPID; PLANT PROTEIN;

BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT; PLANT SEED;

GENE EXPRESSION REGULATION, PLANT; LIPIDS; PLANT PROTEINS; PLANTS; SEEDS;

EID: 84947791559     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2015.11.003     Document Type: Review

References (124)

1. Dyer J.M., Stymne S., Green A.G., Carlsson A.S. High-value oils from plants. Plant J. 2008, 54:640-655.
2. Durrett T.P., Benning C., Ohlrogge J. Plant triacylglycerols as feedstocks for the production of biofuels. Plant J. 2008, 54:593-607.
3. Ohlrogge J.B., Browse J. Lipid biosynthesis. Plant Cell 1995, 7:957-970.
4. Sales-Campos H., Souza P.R., Peghini B.C., da Silva J.S., Cardoso C.R. An overview of the modulatory effects of oleic acid in health and disease. Mini Rev. Med. Chem. 2013, 13:201-210.
5. Farvid M.S., et al. Dietary linoleic acid and risk of coronary heart disease: a systematic review and meta-analysis of prospective cohort studies. Circulation 2014, 130:1568-1578.
6. Scarth R.T., Tang J.H. Modification of oil using conventional and transgenic approaches. Crop Sci. 2006, 46:1225-1236.
7. Harris H., McWilliam J.R., Mason W.K. Influence of temperature on oil content and composition of sunflower seed. Aust. J. Agric. Res. 1978, 29:1203-1212.
8. Rawsthorne S. Carbon flux and fatty acid synthesis in plants. Prog. Lipid Res. 2002, 41:182-196.
9. Weselake R.J., et al. Increasing the flow of carbon into seed oil. Biotechnol. Adv. 2009, 27:866-878.
10. Baud S., Lepiniec L. Physiological and developmental regulation of seed oil production. Prog. Lipid Res. 2010, 49:235-249.
11. Chapman K.D., Ohlrogge J.B. Compartmentation of triacylglycerol accumulation in plants. J. Biol. Chem. 2012, 287:2288-2294.
12. Bates P.D., Stymne S., Ohlrogge J. Biochemical pathways in seed oil synthesis. Curr. Opin. Plant Biol. 2013, 16:358-364.
13. Singer S.D., Greer M.S., Mietkiewska E., Pan X., Weselake R. Genetic engineering of lipid biosynthesis in seeds. Biotechnology of Crucifers 2013, 111-149. Springer, New York. S.K. Gupta (Ed.).
14. Li N., et al. FAX1, a novel membrane protein mediating plastid fatty acid transport. PLoS Biol. 2015, 13:e1002053.
15. Jain R.K., Coffey M., Lai K., Kumar A., MacKenzie S.L. Enhancement of seed oil content by expression of glycerol-3-phosphate acyltransferase genes. Biochem. Soc. Trans. 2000, 28:958-961.
16. Kim M.J., et al. Gene silencing of Sugar-dependent1 (JcSDP1), encoding a patatin-domain triacylglycerol lipase, enchances seed oil accumulation in Jatropha curcas. Biotechnol. Biofuels 2014, 7:36.
17. Qu J., et al. Development of marker-free transgenic Jatropha plants with increased levels of seed oleic acid. Biotechnol. Biofuels 2012, 5:10.
18. Pritchard F.M., Eagles H.A., Norton R.M., Salisbury P.A., Nicolas M. Environmental effects on seed composition of Victorian canola. Aust. J. Exp. Agric. 2000, 40:679-685.
19. Djanaguiraman M., Prasad P.V.V., Boyle D.L., Schapaugh W.T. Soybean pollen anatomy, viability and pod set under high temperature stress. J. Agron. Crop Sci. 2013, 199:171-177.
20. Carrera C., Martínez M.J., Dardanelli J., Balzarini M. Water deficit effect on the relationship between temperature during seed fill period and soybean seed oil and protein concentrations. Crop Sci. 2009, 49:990-998.
21. Canvin D.T. The effect of temperature on the oil content and fatty acid composition of oils from several oil seed crops. Can. J. Bot. 1965, 43:63-69.
22. Dornbos D.L., Mullen R.E. Soybean seed protein and oil contents and fatty acid composition adjustments by drought and temperature. J. Am. Oil Chem. Soc. 1992, 69:228-231.
23. Piper E.L., Boote K.J. Temperature and cultivar effects on soybean seed oil and protein concentrations. J. Am. Oil Chem. Soc. 1999, 76:1233-1241.
24. Pleines S., Friedt W. Genetic control of linolenic acid concentration in seed oil of rapeseed (Brassica napus L.). Theor. Appl. Genet. 1989, 78:793-797.
25. Wolf R.B., Cavins J.F., Kleiman R., Black L.T. Effect of temperature on soybean seed constituents: oil, protein, moisture, fatty acids, amino acids and sugars. J. Am. Oil Chem. Soc. 1982, 59:230-232.
26. Schulte L.R., et al. Increased growing temperature reduces content of polyunsaturated fatty acids in four oilseed crops. Ind. Crops Prod. 2013, 51:212-219.
27. Byfield G.E., Upchurch R.G. Effect of temperature on -9 stearoyl-ACP and ω-6 desaturase gene expression and fatty acid content in developing soybean seeds. Crop Sci. 2007, 47:1698-1704.
28. Kargiotidou A., Deli D., Galanopoulou D., Tsaftaris A., Farmaki T. Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum). J. Exp. Bot. 2008, 59:2043-2056.
29. Teixeira M.C., et al. Molecular cloning and expression analysis of three omega-6 desaturase genes from purslane (Portulaca oleracea L.). Biotechnol. Lett. 2009, 31:1089-1101.
30. Martínez-Rivas J.M., Sánchez-García A., Sicardo M.D., García-Díaz M.T., Mancha M. Oxygen-independent temperature regulation of the microsomal oleate desaturase (FAD2) activity in developing sunflower (Helianthus annuus) seeds. Physiol. Plant. 2003, 117:179-185.
31. Sánchez-García A., Mancha M., Heinz E., Martínez-Rivas J.M. Differential temperature regulation of three sunflower microsomal oleate desaturase (FAD2) isoforms overexpressed in Saccharomyces cerevisiae. Eur. J. Lipid Sci. Technol. 2004, 106:583-590.
32. Tang G.-Q., Novitzky W.P., Griffin H.C., Huber S.C., Dewey R.E. Oleate desaturase enzymes of soybean: evidence of regulation through differential stability and phosphorylation. Plant J. 2005, 44:433-446.
33. Harris P., James A.T. The effect of low temperatures on fatty acid biosynthesis in plants. Biochem. J. 1969, 112:325-330.
34. Rolletschek H., et al. Temperature-dependent endogenous oxygen concentration regulates microsomal oleate desaturase in developing sunflower seeds. J. Exp. Bot. 2007, 58:3171-3181.
35. Esteban A.B., Sicardo M.D., Mancha M., Martinez-Rivas J.M. Growth temperature control of the linoleic acid content in safflower (Carthamus tinctorius) seed oil. J. Agric. Food Chem. 2004, 52:332-336.
36. Guan L.L., et al. Developmental and growth temperature regulation of omega-3 fatty acid desaturase genes in safflower (Carthamus tinctorius L.). Genet. Mol. Res. 2014, 13:6623-6637.
37. Mendes A., et al. bZIP67 regulates the omega-3 fatty acid content of Arabidopsis seed oil by activating fatty acid desaturase3. Plant Cell 2013, 25:3104-3116.
38. Zhu Y., et al. Analysis of gene expression profiles of two near-isogenic lines differing at a QTL region affecting oil content at high temperatures during seed maturation in oilseed rape (Brassica napus L.). Theor. Appl. Genet. 2012, 124:515-531.
39. Talha M., Osman F. Effect of soil water stress on water economy and oil composition in sunflower (Helianthus annuus). J. Agric. Sci. 1974, 84:49-56.
40. Rotundo J.L., Westgate M.E. Meta-analysis of environmental stress on soybean seed composition. Field Crops Res. 2009, 110:147-156.
41. Rebey I.B., et al. Effect of drought on the biochemical composition and antioxidant activities of cumin (Cuminum cyminum L.) seeds. Ind. Crops Prod. 2012, 36:238-245.
42. Rotundo J.L., Westgate M.E. Rate and duration of seed component accumulation in water-stressed soybean. Crop Sci. 2010, 50:676-684.
43. Snyder R.L., Carlson R.E., Shaw R.H. Yield of indeterminate soybeans in response to multiple periods of soil-water stress during reproduction. Agron. J. 1982, 74:855-859.
44. Andriani J.M., Andrade F.H., Suero E.E., Dardanelli J.L. Water deficits during reproductive growth of soybeans: 1. Their effects on dry-matter accumulation, seed yield and its components. Agronomie 1991, 11:737-746.
45. DeSouza P.I., Egli D.B., Bruening W.P. Water stress during seed filling and leaf senescence in soybean. Agron. J. 1997, 89:807-812.
46. Brevedan R.E., Egli D.B. Short periods of water stress during seed filling, leaf senescence, and yield of soybean. Crop Sci. 2003, 43:2083-2088.
47. Anwar F., Zafar S.N., Rashid U. Characterization of Moringa oleifera seed oil from drought and irrigated regions of Punjab, Pakistan. Grasas Y Aceites 2006, 57:160-168.
48. Meckel L., Egli D.B., Philips R.E., Radcliffe D., Leggett J.E. Effect of moisture stress on seed growth in soybeans. Agron. J. 1984, 76:647-650.
49. Westgate M.E., Schussler J.R., Reicosky D.C., Brenner M.L. Effect of water deficits on seed development in soybean: II: conservation of seed growth rate. Plant Physiol. 1989, 91:980-985.
50. Desclaux D., Roumet P. Impact of drought stress on the phenology of two soybean (Glycine max L. Merr.) cultivars. Field Crops Res. 1996, 46:61-70.
51. Baldini M., Giovanardi R., Tahmasebi-Enferadi S., Vannozzi G.P. Effects of water regime on fatty acid accumulation and final fatty acid composition in the oil of standard and high oleic sunflower hybrids. Ital. J. Agron. 2002, 6:119-126.
52. Yang H.M., Zhang X.Y., Wang G.X. Relationships between stomatal character, photosynthetic character and seed chemical composition in grass pea at different water availabilities. J. Agric. Sci. 2004, 142:675-681.
53. Schussler J.R., Westgate M.E. Maize kernel set at low water potential. 1. Sensitivity to reduced assimilates during early kernel growth. Crop Sci. 1991, 31:1189-1195.
54. Shinozaki K., Yamaguchi-Shozaki K. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 2007, 58:221-227.
55. Radetzky R., Langheinrich U. Induction of accumulation and degradation of the 18.4-kDa oleosin in a triacylglycerol-storing cell culture of anise (Pimpinella anisum L.). Planta 1994, 194:1-8.
56. Weselake R.J., et al. Triacylglycerol biosynthesis and gene expression in microspore-derived cell suspension cultures of oilseed rape. J. Exp. Bot. 1998, 49:33-39.
57. Gao Y., Chen G., Weselake R.J. A rapid Nile red fluorescence-based method for triacylglycerol content in microspore-derived cell suspension cultures of Brassica napus. Lipids 2014, 49:1161-1168.
58. Davoren J.D., Nykiforuk C.L., Laroche A., Weselake R.J. Sucrose-induced changes in the transcriptome of cell suspension cultures of oilseed rape reveal genes associated with lipid biosynthesis. Plant Physiol. Biochem. 2002, 40:719-725.
59. Nykiforuk C.L., et al. Characterization of cDNAs encoding diacyglycerol acyltransferase from cultures of Brassica napus and sucrose-mediated induction of enzyme biosynthesis. Biochim. Biophys. Acta 2002, 1580:95-109.
60. Martin T., Oswald O., Graham I.A. Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon:nitrogen availability. Plant Physiol. 2002, 128:472-481.
61. Gong X., et al. Arabidopsis AtSUC2 and AtSUC4, encoding sucrose transporters, are required for abiotic stress tolerance in an ABA-dependent pathway. Physiol. Plant. 2015, 153:119-136.
62. Jako C., et al. Seed-specific over-expression of an Arabidopsis cDNA encoding a diacylglycerol acyltransferase enhances seed oil content and seed weight. Plant Physiol. 2001, 126:861-874.
63. Weselake R.J., et al. Metabolic control analysis is helpful for informed genetic manipulation of oilseed rape (Brassica napus) to increase seed oil content. J. Exp. Bot. 2008, 59:3543-3549.
64. Taylor D.C., et al. Molecular modification of triacylglycerol accumulation by over-expression of DGAT1 to produce canola with increased seed oil content under field conditions. Botany 2009, 87:533-543.
65. Lock Y.-Y., et al. Antisense suppression of type 1 diacylglycerol acyltransferase adversely affects plant development in Brassica napus. Physiol. Plant. 2009, 137:61-71.
66. Lu C., Hills J. Arabidopsis mutants deficient in diacylglycerol acyltransferase display increased sensitivity to abscisic acid, sugars, and osmotic stress during germination and seedling development. Plant Physiol. 2002, 12:1352-1358.
67. Flagella Z., Guilani M.M., Rotunno T., Di Caterina R., De Caro A. Effect of saline water on oil yield and quality of a high oleic sunflower (Helianthus annuus L.) hybrid. Eur. J. Agron. 2004, 21:267-272.
68. Yeilaghi H., et al. Effect of salinity on seed oil content and fatty acid composition of safflower (Carthamus tinctorius L.) genotypes. Food Chem. 2012, 130:618-625.
69. Francois L.E., Kleiman R. Salinity effects on vegetative growth, seed yield, and fatty acid composition of crambe. Agron. J. 1990, 82:1110-1114.
70. Smaoui A., Chérif A. Changes in molecular species of triacylglycerols in developing cotton seeds under salt stress. Biochem. Soc. Trans. 2000, 28:902-905.
71. Smirnoff N. The role of active oxygen in the response of plants to water deficit and dessication. New Phytol. 1993, 125:27-58.
72. Zhang H.-X., Hodson J.N., Williams J.P., Blumwald E. Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc. Nat. Acad. Sci. U. S. A. 2001, 98:12832-12836.
73. Ruuska S.A., Schwender J., Ohlrogge J.B. The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol. 2004, 136:2700-2709.
74. Rolletschek H., Borisjuk L., Koschorreck M., Wobus U., Weber H. Legume embryos develop in a hypoxic environment. J. Exp. Bot. 2002, 53:1099-1107.
75. Eastmond P.J., Kolacna L., Rawsthorne S. Photosynthesis by developing embryos of oilseed rape (Brassica napus L.). J. Exp. Bot. 1996, 47:1763-1769.
76. 2 refixation characteristics of developing canola seeds and silique wall. Aust. J. Plant Phys. 1998, 25:377-386.
77. Andrade F., Ferreiro M. Reproductive growth of maize, sunflower and soybean at different source levels during grain filling. Field Crops Res. 1996, 48:155-165.
78. de la Vega A.J., Chapman S.C., Hall A.J. Genotype by environment interaction and indirect selection for yield in sunflower. I. Two-mode pattern analysis of oil and biomass yield across environments in Argentina. Field Crops Res. 2001, 72:17-38.
79. de la Vega A.J., Hall A.J. Effects of planting date, genotype and their interaction on sunflower yield. II. Components of oil yield. Crop Sci. 2002, 42:1202-1210.
80. Goffman F.D., Alonso A.P., Schwender J., Shachar-Hill Y., Ohlrogge J.B. Light enables a very high efficiency of carbon storage in developing embryos of rapeseed. Plant Physiol. 2005, 138:2269-2279.
81. Li Y., Beisson F., Pollard M., Ohlrogge J. Oil content of Arabidopsis seeds: the influence of seed anatomy, light and plant-to-plant variation. Phytochemistry 2006, 67:904-915.
82. Seiler G.J. Analysis of the relationships of environmental factors with seed oil and fatty acid concentrations of wild annual sunflower. Field Crops Res. 1986, 15:57-72.
83. Echarte M.M., et al. Night temperature and intercepted solar radiation additively contribute to oleic acid percentage in sunflower oil. Field Crops Res. 2010, 119:27-35.
84. Izquierdo N.G., et al. Intercepted solar radiation affects oil fatty acid composition in crop species. Field Crops Res. 2009, 114:66-74.
85. Li R.J., Wang H.Z., Mao H., Lu Y.T., Hua W. Identification of differentially expressed genes in seeds of two near-isogenic Brassica napus lines with different oil content. Planta 2006, 224:952-962.
86. Collados R., Andreu V., Picorel R., Alfonso M. A light-sensitive mechanism differently regulates transcription and transcript stability of ω3 fatty-acid desaturases (FAD3FAD7 and FAD8) in soybean photosynthetic cell suspensions. FEBS Lett. 2006, 580:4934-4940.
87. Vigeolas H., van Dongen J.T., Waldeck P., Hühn D., Geigenberger P. Lipid storage metabolism is limited by the prevailing low oxygen concentrations within developing seeds of oilseed rape. Plant Physiol. 2003, 133:2048-2060.
88. Geigenberger P., Fernie A.R., Gibon Y., Christ M., Stitt M. Metabolic activity decreases as an adaptive response to low internal oxygen in growing potato tubers. Biol. Chem. 2000, 381:723-740.
89. Geigenberger P. Response of plant metabolism to too little oxygen. Curr. Opin. Plant Biol. 2003, 6:247-256.
90. Simontacchi M., Caro A., Puntarulo S. Oxygen-dependent increase of antioxidants in soybean embryonic axes. Int. J. Biochem. Cell Biol. 1995, 27:1211-1229.
91. Schwender J., Goffman F., Ohlrogge J.B., Shachar-Hill Y. Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 2004, 432:779-782.
92. Vigeolas H., Hühn D., Geigenberger P. Nonsymbiotic hemoglobin-2 leads to an elevated energy state and to a combined increase in polyunsaturated fatty acids and total oil content when overexpressed in developing seeds of transgenic Arabidopsis plants. Plant Physiol. 2011, 155:1435-1444.
93. Liu J., et al. The BnGRF2 gene (GRF2-like from Brassica napus) enhances seed oil production through regulating cell number and plant photosynthesis. J. Exp. Bot. 2012, 63:3727-3740.
94. Wilson D.O., et al. Changes in soybean seed oil and protein as influenced by manganese nutrition. Crop Sci. 1982, 22:948-952.
95. D'Hooghe P., et al. Evidence for proteomic and metabolic adaptations associated with alterations of seed yield and quality in sulfur-limited Brassica napus L. Mol. Cell. Proteom. 2014, 13:1165-1183.
96. Rathke G.-W., Christen O., Diepenbrock W. Effects of nitrogen source and rate on productivity and quality of winter oilseed rape (Brassica napus L.) grown in different crop rotations. Field Crops Res. 2005, 94:103-113.
97. Asare E., Scarisbrick D.H. Rate of nitrogen and sulphur fertilizers on yield, yield components and seed quality of oilseed rape (Brassica napus L.). Field Crops Res. 1995, 44:41-46.
98. Ozer H. Sowing date and nitrogen rate effects on growth, yield and yield components of two summer rapeseed cultivars. Eur. J. Agron. 2003, 19:453-463.
99. Barlóg P., Grzebisz W. Effect of timing and nitrogen fertilizer application on winter oilseed rape (Brassica napus L.). I. Growth dynamics and seed yield. J. Agron. Crop Sci. 2004, 190:305-313.
100. Hocking P.J., Randall P.J., Demarco D., Bamforth I. Assessment of the nitrogen status of field grown canola (Brassica napus L.) by plant analysis. Aust. J. Exp. Agric. 1997, 37:83-92.
101. Cheema M.A., Malik M.A., Hussain A., Shah S.H., Basra S.M.A. Effects of time and rate of nitrogen and phosphorus application on the growth and the seed and oil yields of canola (Brassica napus L.). J. Agron. Crop Sci. 2001, 186:103-110.
102. Öztürk Ö. Effects of source and rate of nitrogen fertilizer on yield, yield components and quality of winter rapeseed. Chil. J. Agric. Res. 2010, 70:132-141.
103. Rathke G.-W., Behrens T., Diepenbrock W. Integrated nitrogen management strategies to improve seed yield, oil content and nitrogen efficiency of winter oilseed rape (Brassica napus L.): a review. Agric. Ecosyst. Environ. 2006, 117:80-108.
104. Hu Q., et al. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 2008, 54:621-639.
105. Li Y., Han D., Sommerfeld M., Hu Q. Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresour. Technol. 2011, 102:123-129.
106. Yang Y., Yu X., Song L., An C. ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiol. 2011, 156:873-883.
107. Boyle N.R., et al. Three acyltransferases and nitrogen-responsive regulator are implicated in nitrogen starvation-induced triacylglycerol accumulation in Chlamydomonas. J. Biol. Chem. 2012, 287:15811-15825.
108. Msanne J., et al. Metabolic and gene expression changes triggered by nitrogen deprivation in the photoautotrophically grown microalgae Chlamydomonas reinhardtii and Coccomyxa sp. C-169. Phytochemistry 2012, 75:50-59.
109. Lin W., Oliver D.J. Role of triacylglycerols in leaves. Plant Sci. 2008, 175:233-237.
110. Martin B.A., Wilson R.F. Subcellular localization of triacylglycerol synthesis in spinach leaves. Lipids 1984, 19:117-121.
111. Xue L., et al. Characterization of the glycerolipid composition and biosynthetic capacity of pea root plastids. Plant Physiol. 1997, 113:549-557.
112. Kaup M.T., Froese C.D., Thompson J.E. A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol. 2002, 129:1616-1626.
113. Lippold F., et al. Fatty acid phytyl exter synthesis in chloroplasts of Arabidopsis. Plant Cell 2012, 24:2001-2014.
114. Chapman K.D., Dyer J.M., Mullen R.T. Commentary: why don't plant leaves get fat?. Plant Sci. 2013, 207:128-134.
115. Vanhercke T., Petrie J.R., Singh S.P. Energy densification of vegetative biomass through metabolic engineering. Biocatal. Agric. Biotechnol. 2014, 3:75-80.
116. Reynolds K.B., et al. Metabolic engineering of medium-chain fatty acid biosynthesis in Nicotiana benthamiana plant leaf lipids. Front. Plant Sci. 2015, 6. Article 164.
117. Ohlrogge J., Chapman K. Expanding the contribution of plant oils as biofuels. The seeds of green energy. Biochemist 2011, 33:34-38.
118. Zale J., et al. Metabolic engineering of sugarcane to accumulate energy-dense triacylglycerols in vegetative biomass. Plant Biotechnol. J. 2015, 10.1111/pbi.12411.
119. Troncoso-Ponce M.A., Cao X., Yang Z., Ohlrogge J.B. Lipid turnover during senescence. Plant Sci. 2013, 205-206:13-19.
120. Sakaki T., Saito K., Kawaguchi A., Kondo N., Yamada M. Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol. 1990, 94:766-772.
121. Sakaki T., Kondo N., Yamada M. Pathway for the synthesis of triacylglycerols from monogalactosyldiacylglycerols in ozone-fumigated spinach leaves. Plant Physiol. 1990, 94:773-780.
122. Higashi Y., Okazaki Y., Myouga F., Shinozaki K., Saito K. Landscape of the lipidome and transcriptome under heat stress in Arabidopsis thaliana. Sci. Rep. 2015, 5:10533.
123. Mueller S.P., Krause D.M., Mueller M.J., Fekete A. Accumulation of extra-chloroplastic triacylglycerols in Arabidopsis seedlings during heat acclimation. J. Exp. Bot. 2015, 66:4517-4526.
124. Moellering E.R., Muthan B., Benning C. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 2010, 330:226-228.