Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Very-long-chain fatty acids (VLCFAs) in plant response to stress

Anatoly V. Zhukov https://orcid.org/0000-0002-7658-7915 A and Maria Shumskaya https://orcid.org/0000-0001-7916-462X B C
+ Author Affiliations
- Author Affiliations

A KA Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Street 35, 127276 Moscow, Russia.

B Department of Biology, School of Natural Sciences, Kean University, 1000 Morris Avenue, Union, NJ 07083, USA.

C Corresponding author. Email: mshumska@kean.edu

Functional Plant Biology 47(8) 695-703 https://doi.org/10.1071/FP19100
Submitted: 16 April 2019  Accepted: 25 March 2020   Published: 9 June 2020

Abstract

Plant growth is affected by various stresses leading to changes in metabolism. Stress conditions include a variety of biotic and abiotic factors such as pathogens, drought, high and low temperatures and heavy metals. Among multiple physiological responses to stress, there is an adaptive modification in membrane lipid constituents. In particular, the composition of membrane very-long-chain fatty acids (VLCFAs) changes both qualitatively and quantitatively. Here, we evaluate the current data on the effects of stress on plant VLCFAs composition. In summary, some stress conditions lead to an increase of the total amount of saturated and, in certain cases, unsaturated VLCFAs. Currently, it is not completely clear how these molecules participate in the biology of plant cell membranes. Their possible functional roles are discussed.

Additional keywords: cell membranes, cold stress, cuticle, drought, heavy metals, salt, waxes.


References

Abbadi A, Domergue F, Bauer J, Napier JA, Welti R, Zähringer U, Cirpus P, Heinz E (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. The Plant Cell 16, 2734–2748.
Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation.Crossref | GoogleScholarGoogle Scholar | 15377762PubMed |

Ammar WB, Nouairi I, Zarrouk M, Jemal F (2008) The effect of cadmium on lipid and fatty acid biosynthesis in tomato leaves. Biologia 63, 86–93.
The effect of cadmium on lipid and fatty acid biosynthesis in tomato leaves.Crossref | GoogleScholarGoogle Scholar |

Andersen E, Küpper H (2013) Cadmium toxicity in plants. Metal Ions in Life Sciences 11, 395–413.
Cadmium toxicity in plants.Crossref | GoogleScholarGoogle Scholar |

Azachi M, Sadka A, Fishtr M, Goldshlag P, Gokhman I, Zamir A (2002) Salt induction of fatty acid elongase and membrane lipid modification in the extreme halotolerant alga Dunaliella salina. Plant Physiology 129, 1320–1329.
Salt induction of fatty acid elongase and membrane lipid modification in the extreme halotolerant alga Dunaliella salina.Crossref | GoogleScholarGoogle Scholar | 12114585PubMed |

Bach L, Faure JD (2010) Role of very-long-chain fatty acids in plant development, when chain length does matter. Comptes Rendus Biologies 333, 361–370.
Role of very-long-chain fatty acids in plant development, when chain length does matter.Crossref | GoogleScholarGoogle Scholar | 20371111PubMed |

Bach L, Michaelson LV, Haslam R, Bellec Y, Gissot L, Marion J, Da Costa M, Boutin J-P, Miquel M, Teller F, Domergue F, Markham JE, Beaudoin F, Napier JA, Faure JD (2008) The plant very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proceedings of the National Academy of Sciences of the United States of America 105, 14727–14731.
The plant very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development.Crossref | GoogleScholarGoogle Scholar | 18799749PubMed |

Cacas JL, Vailleau F, Davoine C, Ennar N, Agnel JP, Tronchet M, Ponchet M, Blein JP, Roby D (2005) The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response. Plant, Cell & Environment 28, 1367–1378.
The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response.Crossref | GoogleScholarGoogle Scholar |

Cassagne C, Lessire R, Bessoule JJ, Moreau P, Creach A, Schneider F, Sturbois B (1994) Biosynthesis of very long chain fatty acid in higher plants. Progress in Lipid Research 33, 55–69.
Biosynthesis of very long chain fatty acid in higher plants.Crossref | GoogleScholarGoogle Scholar | 8190743PubMed |

Chaffai R, Marzouk B, El Ferjani E (2005) Aluminum mediates compositional alterations of polar lipid classes in maize seedlings. Phytochemistry 66, 1903–1912.
Aluminum mediates compositional alterations of polar lipid classes in maize seedlings.Crossref | GoogleScholarGoogle Scholar | 16099483PubMed |

De Bigault Du Granrut A, Cacas JL (2016) How very-long-chain fatty acids could signal stressful conditions in plants? Frontiers in Plant Science 7, 1490
How very-long-chain fatty acids could signal stressful conditions in plants?Crossref | GoogleScholarGoogle Scholar | 27803703PubMed |

Elloumi N, Zouari M, Chaari L, Jomni C, Marzouk B, Abdallah FB (2014) Effects of cadmium on lipids of almond seedlings (Prunus dulcis). Botanical Studies 55, 61
Effects of cadmium on lipids of almond seedlings (Prunus dulcis).Crossref | GoogleScholarGoogle Scholar | 28510983PubMed |

Gajewska E, Bernat P, Długoński J, Skłodowska M (2012) Effect of nickel on membrane integrity, lipid peroxidation and fatty acid composition in wheat seedlings. Journal Agronomy & Crop Science 198, 286–294.
Effect of nickel on membrane integrity, lipid peroxidation and fatty acid composition in wheat seedlings.Crossref | GoogleScholarGoogle Scholar |

Haslam TM, Kunst L (2013) Extending the story of very-long-chain fatty acid elongation. Plant Science 210, 93–107.
Extending the story of very-long-chain fatty acid elongation.Crossref | GoogleScholarGoogle Scholar | 23849117PubMed |

Haslam TM, Haslam R, Thoraval D, Pascal S, Delude C, Domergue F, Fernández AM, Beaudoin F, Napier JA, Kunst L, Joubès J (2015) ECERIFERUM2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation. Plant Physiology 167, 682–692.
ECERIFERUM2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation.Crossref | GoogleScholarGoogle Scholar | 25596184PubMed |

Hegebarth D, Buschhaus C, Joubès J, Thoraval D, Bird D, Jetter R (2017) Arabidopsis ketoacyl‐CoA synthase 16 (KCS16) forms C36/C38 acyl precursors for leaf trichome and pavement surface wax. Plant, Cell & Environment 40, 1761–1776.
Arabidopsis ketoacyl‐CoA synthase 16 (KCS16) forms C36/C38 acyl precursors for leaf trichome and pavement surface wax.Crossref | GoogleScholarGoogle Scholar |

Ivanova TV, Myasoedov NA, Pchelkin VP, Tsydendambaev VD, Vereshchagin AG (2009) Increased content of very-long-chain fatty acids in the lipids of halophyte vegetative organs. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 56, 787–794.
Increased content of very-long-chain fatty acids in the lipids of halophyte vegetative organs.Crossref | GoogleScholarGoogle Scholar |

Ivanova TV, Maiorova OV, Orlova YV, Kuznetsova EI, Khalilova LA, Myasoedov NA, Balnokin YV, Tsydendambaev VD (2016) Cell ultrastructure and fatty acid composition of lipids in vegetative organs of Chenopodium album L. under salt stress conditions. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 63, 763–775.
Cell ultrastructure and fatty acid composition of lipids in vegetative organs of Chenopodium album L. under salt stress conditions.Crossref | GoogleScholarGoogle Scholar |

Kargiotidou A, Deli D, Galanopoulou D, Tsaftaris A, Farmaki T (2008) Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum). Journal of Experimental Botany 59, 2043–2056.
Low temperature and light regulate delta 12 fatty acid desaturases (FAD2) at a transcriptional level in cotton (Gossypium hirsutum).Crossref | GoogleScholarGoogle Scholar | 18453533PubMed |

Kolattukudy PE (2001) Polyesters in higher plants. Advances in Biochemical Engineering/Biotechnology 71, 1–49.
Polyesters in higher plants.Crossref | GoogleScholarGoogle Scholar | 11217409PubMed |

Kuiper PJC (1968) Lipids in grape roots in relation to chloride transport. Plant Physiology 43, 1367–1371.
Lipids in grape roots in relation to chloride transport.Crossref | GoogleScholarGoogle Scholar |

Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research 42, 51–80.
Biosynthesis and secretion of plant cuticular wax.Crossref | GoogleScholarGoogle Scholar | 12467640PubMed |

Lee SH, Ahn SJ, Im YJ, Cho K, Chung CC, Cho BH, Han O (2005) Differential impact of low temperature on fatty acid unsaturation and lipoxygenase activity in figleaf gourd and cucumber roots. Biochemical and Biophysical Research Communications 330, 1194–1198.
Differential impact of low temperature on fatty acid unsaturation and lipoxygenase activity in figleaf gourd and cucumber roots.Crossref | GoogleScholarGoogle Scholar | 15823569PubMed |

Liu W, Li W, He Q, Daud MK, Chen J, Zhu S (2015) Characterization of 19 genes encoding membrane-bound fatty acid desaturases and their expression profiles in Gossypium raimondii under low temperature. PLoS One
Characterization of 19 genes encoding membrane-bound fatty acid desaturases and their expression profiles in Gossypium raimondii under low temperature.Crossref | GoogleScholarGoogle Scholar | 26720755PubMed |

Lü S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA (2009) Arabidopsis CER8 encodes LONG-CHAIN-ACYL-COA SYNTHASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. The Plant Journal 59, 553–564.
Arabidopsis CER8 encodes LONG-CHAIN-ACYL-COA SYNTHASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis.Crossref | GoogleScholarGoogle Scholar | 19392700PubMed |

Lucini L, Bernardo J (2015) Comparison of proteome response to saline and zinc stress in lettuce. Frontiers in Plant Science 6, 240
Comparison of proteome response to saline and zinc stress in lettuce.Crossref | GoogleScholarGoogle Scholar | 25932029PubMed |

Mabuchi K, Maki Y, Tomotaka I, Suzuki T, Nomoto M, Sakaoka S, Morikami A, Higashiyama T, Tada Y, Busch W, Tsukagoshi H (2018) MYB30 links ROS signaling, root cell elongation, and plant immune responses. Proceedings of the National Academy of Sciences of the United States of America 115, E4710–E4719.
MYB30 links ROS signaling, root cell elongation, and plant immune responses.Crossref | GoogleScholarGoogle Scholar | 29712840PubMed |

Makarenko SP, Konenkina TA, Suvorova GG, Oskorbina MV (2014) Seasonal changes in the fatty acid composition of Pinus sylvestris needle lipids. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 61, 119–123.
Seasonal changes in the fatty acid composition of Pinus sylvestris needle lipids.Crossref | GoogleScholarGoogle Scholar |

Marichali A, Dallali S, Ouerghemmi S, Sebei H, Casabianca H, Hosni K (2016) Responses of Nigella sativa L. to zinc excess: focus on germination, growth, yield and yield components, lipid and terpene metabolism, and total phenolics and antioxidant activities. Journal of Agricultural and Food Chemistry 64, 1664–1675.
Responses of Nigella sativa L. to zinc excess: focus on germination, growth, yield and yield components, lipid and terpene metabolism, and total phenolics and antioxidant activities.Crossref | GoogleScholarGoogle Scholar | 26853463PubMed |

Millar AA, Wrischer M, Kunst L (1998) Accumulation of very-long-chain fatty acids in membrane glycerolipids is associated with dramatic alterations in plant morphology. The Plant Cell 10, 1889–1902.
Accumulation of very-long-chain fatty acids in membrane glycerolipids is associated with dramatic alterations in plant morphology.Crossref | GoogleScholarGoogle Scholar | 9811796PubMed |

Mironov KS, Shumskaya MA, Sidorov RA, Trofimova MS, Los DA (2018) Membrane physical state and stress regulation in Synechocystis: fluidizing alcohols repress fatty acid desaturation. The Plant Journal 96, 1007–1017.
Membrane physical state and stress regulation in Synechocystis: fluidizing alcohols repress fatty acid desaturation.Crossref | GoogleScholarGoogle Scholar | 30194781PubMed |

Mironov KS, Sinetova MA, Shumskaya M, Los DA (2019) Universal molecular triggers of stress responses in cyanobacterium Synechocystis. Life (Basel) 9, 67
Universal molecular triggers of stress responses in cyanobacterium Synechocystis.Crossref | GoogleScholarGoogle Scholar |

Nawrath C (2002) The biopolymers cutin and suberin. The Arabidopsis Book/American Society of Plant Biologists.
The biopolymers cutin and suberin.Crossref | GoogleScholarGoogle Scholar |

Neess D, Bek S, Engelsby H, Gallego SF, Faergeman NJ (2015) Long-chain acyl-CoA esters in metabolism and signaling: role of acyl-CoA binding proteins. Progress in Lipid Research 59, 1–25.
Long-chain acyl-CoA esters in metabolism and signaling: role of acyl-CoA binding proteins.Crossref | GoogleScholarGoogle Scholar | 25898985PubMed |

Nekrasov EV, Shelikhan VA, Svetashev VI (2019) Fatty acid composition of gametophytes of Matteuccia struthiopteris (L.) Tod. (Onocleaceae, Polypodiophyta). Botanica Pacifica 8, 63–66.
Fatty acid composition of gametophytes of Matteuccia struthiopteris (L.) Tod. (Onocleaceae, Polypodiophyta).Crossref | GoogleScholarGoogle Scholar |

Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the critical contribution of membrane lipids. Annual Review of Plant Physiology and Plant Molecular Biology 47, 541–568.
Chilling sensitivity in plants and cyanobacteria: the critical contribution of membrane lipids.Crossref | GoogleScholarGoogle Scholar | 15012300PubMed |

Nobusawa T, Okushima Y, Nagata N, Kojima M, Sakakibara H, Umeda M (2013) Synthesis of very-long-chain fatty acids in the epidermis controls plant organ growth by restricting cell proliferation. PLoS Biology 11,
Synthesis of very-long-chain fatty acids in the epidermis controls plant organ growth by restricting cell proliferation.Crossref | GoogleScholarGoogle Scholar | 23585732PubMed |

Pettitt TR, Jones AL, Harwood JL (1989) Lipids of the marine red algae, Chondreus crispus and Polysiphonia lanosa. Phytochemistry 28, 399–405.
Lipids of the marine red algae, Chondreus crispus and Polysiphonia lanosa.Crossref | GoogleScholarGoogle Scholar |

Popov VN, Antipina OV, Pchelkin VP, Tsydendambaev VD (2012) Changes in the content and composition of lipid fatty acids in tobacco leaves and roots at low-temperature hardening. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 59, 177–182.
Changes in the content and composition of lipid fatty acids in tobacco leaves and roots at low-temperature hardening.Crossref | GoogleScholarGoogle Scholar |

Post-Beittenmiller D (1996) Biochemistry and molecular biology of wax production in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 405–430.
Biochemistry and molecular biology of wax production in plants.Crossref | GoogleScholarGoogle Scholar | 15012295PubMed |

Raffaele S, Leger A, Roby D (2009) Very long chain fatty acid and lipid signaling in the response of plants to pathogens. Plant Signaling & Behavior 4, 94–99.
Very long chain fatty acid and lipid signaling in the response of plants to pathogens.Crossref | GoogleScholarGoogle Scholar |

Razeq FM, Kosma DK, Rowland O, Molina I (2014) Extracellular lipids of Camelina sativa: characterization of chloroform-extractable waxes from aerial and subterranean surfaces. Phytochemistry 106, 188–196.
Extracellular lipids of Camelina sativa: characterization of chloroform-extractable waxes from aerial and subterranean surfaces.Crossref | GoogleScholarGoogle Scholar | 25081105PubMed |

Román A, Hernández ML, Soria-García A, López-Gomollón S, Lagunas B, Picorel R, Martínez-Rivas JM, Alfonso M (2015) Non-redundant contribution of the plastidial FAD8 ω-3 desaturase to glycerolipid unsaturation at different temperatures in Arabidopsis. Molecular Plant 8, 1599–1611.
Non-redundant contribution of the plastidial FAD8 ω-3 desaturase to glycerolipid unsaturation at different temperatures in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26079601PubMed |

Rozentsvet OA, Bogdanova ES, Murzaeva SV (2011) Composition of lipids and fatty acids in the forming leaves of the fern Matteuccia sthruthiopteris in the presence of cadmium. Trudy Karelskogo nauchnogo zentra RAN 3, 97–104.

Sanina NM, Goncharova SN, Kostesky EY (2003) Seasonal changes in thermotropic behavior of phospho- and glycolipids from Laminaria japonica. In ‘Advanced research on plant lipids’. (Eds N Murata, M Yamada, I Nishida, H Okuyama, J Sekiya, W Hajime) p. 385–388. (Kluwer Academic Publishers: Dordrecht, Netherlands)

Scotti-Campos P, Pais IP, Partelli FL, Batista-Santos P, Ramalho JC (2014) Phospholipids profile in chloroplasts of Coffea spp. genotypes differing in cold acclimation ability. Journal of Plant Physiology 171, 243–249.
Phospholipids profile in chloroplasts of Coffea spp. genotypes differing in cold acclimation ability.Crossref | GoogleScholarGoogle Scholar | 23988560PubMed |

Sui N, Wang Y, Liu S, Yang Z, Wang F, Wan S (2018) Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut. Frontiers in Plant Science 9, 7
Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut.Crossref | GoogleScholarGoogle Scholar | 29403517PubMed |

Teixeira MC, Carvalho IS, Brodelius M (2010) ω-3 Fatty acid desaturase genes isolated from purslane (Portulaca oleracea, L.): expression in different tissues and response to cold and wound stress. Journal of Agricultural and Food Chemistry 58, 1870–1877.
ω-3 Fatty acid desaturase genes isolated from purslane (Portulaca oleracea, L.): expression in different tissues and response to cold and wound stress.Crossref | GoogleScholarGoogle Scholar | 20070085PubMed |

Trenkamp S, Martin W, Tietjen K (2004) Specific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides. Proceedings of the National Academy of Sciences of the United States of America 101, 11903–11908.
Specific and differential inhibition of very-long-chain fatty acid elongases from Arabidopsis thaliana by different herbicides.Crossref | GoogleScholarGoogle Scholar | 15277688PubMed |

Tshabuse F, Farrant JM, Humbert L, Moura D, Rainteau D, Espinasse C, Taghki AI, Merlier F, Acket S, Rafudeen M, Thomasset B, Ruelland E (2018) Glycerolipid analysis during desiccation and recovery of the resurrection plant Xerophyta humilis (Bak) Dur and Schinz. Plant, Cell & Environment 41, 533–547.
Glycerolipid analysis during desiccation and recovery of the resurrection plant Xerophyta humilis (Bak) Dur and Schinz.Crossref | GoogleScholarGoogle Scholar |

Tsydendambaev VD, Ivanova TV, Khalilova LA, Kurkova EB, Myasoedov NA, Balnokin YV (2013) Fatty acid composition of lipids in vegetative organs of the halophyte Suaeda altissima under different levels of salinity. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 60, 661–671.
Fatty acid composition of lipids in vegetative organs of the halophyte Suaeda altissima under different levels of salinity.Crossref | GoogleScholarGoogle Scholar |

Tuteja N, Sopory SK (2008) Chemical signaling under abiotic stress environment in plants. Plant Signaling & Behavior 3, 525–536.
Chemical signaling under abiotic stress environment in plants.Crossref | GoogleScholarGoogle Scholar |

Wallis JG, Browse J (2002) Mutants of Arabidopsis reveal many roles for membrane lipids. Progress in Lipid Research 41, 254–278.
Mutants of Arabidopsis reveal many roles for membrane lipids.Crossref | GoogleScholarGoogle Scholar | 11814526PubMed |

Wu J, Seliskar DM, Cfllaghtr JL (2005) The response of plasma membrane lipid composition in callus of the halophyte Spartina patens (Poaceae) to salinity stress. American Journal of Botany 92, 852–858.
The response of plasma membrane lipid composition in callus of the halophyte Spartina patens (Poaceae) to salinity stress.Crossref | GoogleScholarGoogle Scholar | 21652466PubMed |

Xie LJ, Yu LJ, Chen Q, Wang FZ, Huang L, Xia FN, Zhu TR, Wu JX, Yin J, Liao B, Yao N, Shu W, Xiao S (2015) Arabidopsis acyl-CoA-binding protein ACBP3 participates in plant response to hypoxia by modulating very-long-chain fatty acid metabolism. The Plant Journal 81, 53–67.
Arabidopsis acyl-CoA-binding protein ACBP3 participates in plant response to hypoxia by modulating very-long-chain fatty acid metabolism.Crossref | GoogleScholarGoogle Scholar | 25284079PubMed |

Yu C, Wang HS, Yang S, Tang XF, Duan M, Meng QW (2009) Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. Plant Physiology and Biochemistry 47, 1102–1112.
Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato.Crossref | GoogleScholarGoogle Scholar | 19648018PubMed |

Zemanová V, Pavlík M, Kyjaková P, Pavlíková D (2015) Fatty acid profiles of ecotypes of hyperaccumulator Noccaea caerulescens growing under cadmium stress. Journal of Plant Physiology 180, 27–34.
Fatty acid profiles of ecotypes of hyperaccumulator Noccaea caerulescens growing under cadmium stress.Crossref | GoogleScholarGoogle Scholar | 25886397PubMed |

Zhang J, Liu H, Sun J, Li B, Zhu Q, Chen S, Zhang H (2012) Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PLoS One
Arabidopsis fatty acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth.Crossref | GoogleScholarGoogle Scholar | 23300923PubMed |

Zhang Y-L, Zhang C-L, Wang G-L, Qi C-H, Zhao Q, You C-X, Li Y-Y, Hao Y-J (2019) The R2R3 MYB transcription factor MdMYB30 modulates plant resistance against pathogens by regulating cuticular wax biosynthesis. BMC Plant Biology 19, 362
The R2R3 MYB transcription factor MdMYB30 modulates plant resistance against pathogens by regulating cuticular wax biosynthesis.Crossref | GoogleScholarGoogle Scholar | 31426743PubMed |

Zheng H, Rowland O, Kunst L (2005) Disruptions of the Arabidopsis enoil-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. The Plant Cell 17, 1467–1481.
Disruptions of the Arabidopsis enoil-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis.Crossref | GoogleScholarGoogle Scholar | 15829606PubMed |

Zhigacheva IV, Burlakova EB, Misharina TA, Terenina MB, Krikunova NI, Generosova IP, Shugaev AG, Fattakhov SG (2013) Fatty acid composition of membrane lipids and energy metabolism in mitochondria of pea seedlings under water deficit. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 60, 212–220.
Fatty acid composition of membrane lipids and energy metabolism in mitochondria of pea seedlings under water deficit.Crossref | GoogleScholarGoogle Scholar |

Zhu X, Xiong L (2013) Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice. Proceedings of the National Academy of Sciences of the United States of America 110, 17790–17795.
Putative megaenzyme DWA1 plays essential roles in drought resistance by regulating stress-induced wax deposition in rice.Crossref | GoogleScholarGoogle Scholar | 24127586PubMed |

Zhukov AV (2015) Palmitic acid and its role in the structure and functions of plant cell membranes. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 62, 706–713.
Palmitic acid and its role in the structure and functions of plant cell membranes.Crossref | GoogleScholarGoogle Scholar |

Zhukov AV, Lebedeva NI, Vereshchagin AG (2001) The effect of helminthosporic root rot on the composition of acyl lipids of wheat seedlings. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 48, 181–189.
The effect of helminthosporic root rot on the composition of acyl lipids of wheat seedlings.Crossref | GoogleScholarGoogle Scholar |