From sensing to acclimation: The role of membrane lipid remodeling in plant responses to low temperatures

Shomo, Zachery D.; Li, Fangyi; Smith, Cailin N.; Edmonds, Sydney R.; Roston, Rebecca L.

doi:10.1093/plphys/kiae382

Title: From sensing to acclimation: The role of membrane lipid remodeling in plant responses to low temperatures

Journal Article · 19 July 2024 · Plant Physiology (Bethesda)

DOI: https://doi.org/10.1093/plphys/kiae382 · OSTI ID:2475886

; Li, Fangyi;

; Edmonds, Sydney R.;

Abstract Low temperatures pose a dramatic challenge to plant viability. Chilling and freezing disrupt cellular processes, forcing metabolic adaptations reflected in alterations to membrane compositions. Understanding the mechanisms of plant cold tolerance is increasingly important due to anticipated increases in the frequency, severity, and duration of cold events. This review synthesizes current knowledge on the adaptive changes of membrane glycerolipids, sphingolipids, and phytosterols in response to cold stress. We delve into key mechanisms of low-temperature membrane remodeling, including acyl editing and headgroup exchange, lipase activity, and phytosterol abundance changes, focusing on their impact at the subcellular level. Furthermore, we tabulate and analyze current gycerolipidomic data from cold treatments of Arabidopsis, maize, and sorghum. This analysis highlights congruencies of lipid abundance changes in response to varying degrees of cold stress. Ultimately, this review aids in rationalizing observed lipid fluctuations and pinpoints key gaps in our current capacity to fully understand how plants orchestrate these membrane responses to cold stress.

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0021101

OSTI ID:: 2475886

Journal Information:: Plant Physiology (Bethesda), Journal Name: Plant Physiology (Bethesda) Journal Issue: 3 Vol. 196; ISSN 0032-0889

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (156)

Chilling sensitivity of Arabidopsis thaliana with genetically engineered membrane lipids. Wolter, F. P.; Schmidt, R.; Heinz, E. The EMBO Journal, Vol. 11, Issue 13 https://doi.org/10.1002/j.1460-2075.1992.tb05573.x	journal	December 1992
Direct Infusion Mass Spectrometry for Complex Lipid Analysis Gutbrod, Katharina; Peisker, Helga; Dörmann, Peter Methods in Molecular Biology https://doi.org/10.1007/978-1-0716-1362-7_7	book	May 2021
Plant Sphingolipid Metabolism and Function Luttgeharm, Kyle D.; Kimberlin, Athen N.; Cahoon, Edgar B. Lipids in Plant and Algae Development https://doi.org/10.1007/978-3-319-25979-6_11	book	March 2016
Formation of multiplex lamellae by equilibrium slow freezing of cortical parenchyma cells of mulberry and its possible relationship to freezing tolerance Fujikawa, S.; Takabe, K. Protoplasma, Vol. 190, Issue 3-4 https://doi.org/10.1007/BF01281318	journal	September 1996
Breeding approaches and genomics technologies to increase crop yield under low-temperature stress Jha, Uday Chand; Bohra, Abhishek; Jha, Rintu Plant Cell Reports, Vol. 36, Issue 1 https://doi.org/10.1007/s00299-016-2073-0	journal	November 2016
Low-temperature tolerance and genetic potential in wheat (Triticum aestivum L.): response to photoperiod, vernalization, and plant development Limin, Allen E.; Fowler, D. Brian Planta, Vol. 224, Issue 2 https://doi.org/10.1007/s00425-006-0219-y	journal	January 2006
Long- and short-term freezing induce different types of injury in Arabidopsis thaliana leaf cells Nagao, M.; Arakawa, K.; Takezawa, D. Planta, Vol. 227, Issue 2 https://doi.org/10.1007/s00425-007-0633-9	journal	October 2007
Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes Nagano, Minoru; Ishikawa, Toshiki; Ogawa, Yoshie Planta, Vol. 240, Issue 1 https://doi.org/10.1007/s00425-014-2065-7	journal	April 2014
The role of sterols in plant response to abiotic stress Rogowska, Agata; Szakiel, Anna Phytochemistry Reviews, Vol. 19, Issue 6 https://doi.org/10.1007/s11101-020-09708-2	journal	July 2020
Lipid transport required to make lipids of photosynthetic membranes LaBrant, Evan; Barnes, Allison C.; Roston, Rebecca L. Photosynthesis Research, Vol. 138, Issue 3 https://doi.org/10.1007/s11120-018-0545-5	journal	June 2018
Genome-wide identification and abiotic stress responses of DGK gene family in maize Gu, Yingnan; Zhao, Changjiang; He, Lin Journal of Plant Biochemistry and Biotechnology https://doi.org/10.1007/s13562-017-0424-8	journal	September 2017
A precise localization of cardiolipin in plant cells Bligny, Richard; Douce, Roland Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 617, Issue 2 https://doi.org/10.1016/0005-2760(80)90168-X	journal	February 1980
Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. Block, M. A.; Dorne, A. J.; Joyard, J. Journal of Biological Chemistry, Vol. 258, Issue 21 https://doi.org/10.1016/S0021-9258(17)44113-5	journal	November 1983
Arabidopsis mutants deficient in polyunsaturated fatty acid synthesis. Biochemical and genetic characterization of a plant oleoyl-phosphatidylcholine desaturase. Miquel, M.; Browse, J. Journal of Biological Chemistry, Vol. 267, Issue 3 https://doi.org/10.1016/S0021-9258(18)45974-1	journal	January 1992
The C16:3\C18:3 fatty acid balance in photosynthetic tissues from 468 plant species Mongrand, Sébastien; Bessoule, Jean-Jacques; Cabantous, Francis Phytochemistry, Vol. 49, Issue 4 https://doi.org/10.1016/S0031-9422(98)00243-X	journal	October 1998
Plant sterols and the membrane environment Hartmann, M. Trends in Plant Science, Vol. 3, Issue 5 https://doi.org/10.1016/S1360-1385(98)01233-3	journal	May 1998
Phospholipase D- and phosphatidic acid-mediated signaling in plants Li, Maoyin; Hong, Yueyun; Wang, Xuemin Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1791, Issue 9 https://doi.org/10.1016/j.bbalip.2009.02.017	journal	September 2009
Lysolipid incorporation in dipalmitoylphosphatidylcholine bilayer membranes enhances the ion permeability and drug release rates at the membrane phase transition Mills, Jeffrey K.; Needham, David Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1716, Issue 2 https://doi.org/10.1016/j.bbamem.2005.08.007	journal	October 2005
Permeability across lipid membranes Shinoda, Wataru Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 10 https://doi.org/10.1016/j.bbamem.2016.03.032	journal	October 2016
Role of phosphatidic acid in plant galactolipid synthesis Dubots, Emmanuelle; Botté, Cyrille; Boudière, Laurence Biochimie, Vol. 94, Issue 1 https://doi.org/10.1016/j.biochi.2011.03.012	journal	January 2012
1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana Alonso-Blanco, Carlos; Andrade, Jorge; Becker, Claude Cell, Vol. 166, Issue 2 https://doi.org/10.1016/j.cell.2016.05.063	journal	July 2016
Effects of ether vs. ester linkage on lipid bilayer structure and water permeability Guler, S. Deren; Ghosh, D. Dipon; Pan, Jianjun Chemistry and Physics of Lipids, Vol. 160, Issue 1 https://doi.org/10.1016/j.chemphyslip.2009.04.003	journal	July 2009
AtMic60 Is Involved in Plant Mitochondria Lipid Trafficking and Is Part of a Large Complex Michaud, Morgane; Gros, Valérie; Tardif, Marianne Current Biology, Vol. 26, Issue 5 https://doi.org/10.1016/j.cub.2016.01.011	journal	March 2016
Confocal cryomicroscopic analysis and cryodynamics of endoplasmic reticulum in herbaceous plant cells Kobayashi, Shion; Kutsuna, Natsumaro; Tanino, Karen K. Environmental and Experimental Botany, Vol. 106 https://doi.org/10.1016/j.envexpbot.2014.02.002	journal	October 2014
Recent insights into cell responses to cold stress in plants: Signaling, defence, and potential functions of phosphatidic acid Wu, Jiaxu; Nadeem, Muhmmad; Galagedara, Lakshman Environmental and Experimental Botany, Vol. 203 https://doi.org/10.1016/j.envexpbot.2022.105068	journal	November 2022
Identification of an Arabidopsis thaliana gene for cardiolipin synthase located in mitochondria Katayama, Kenta; Sakurai, Isamu; Wada, Hajime FEBS Letters, Vol. 577, Issue 1-2 https://doi.org/10.1016/j.febslet.2004.10.009	journal	October 2004
Phosphatidylcholine is transferred from chemically‐defined liposomes to chloroplasts through proteins of the chloroplast outer envelope membrane Yin, Congfei; Andersson, Mats X.; Zhang, Hongsheng FEBS Letters, Vol. 589, Issue 1 https://doi.org/10.1016/j.febslet.2014.11.044	journal	December 2014
Biophysical analysis of the plant-specific GIPC sphingolipids reveals multiple modes of membrane regulation Mamode Cassim, Adiilah; Navon, Yotam; Gao, Yu Journal of Biological Chemistry, Vol. 296 https://doi.org/10.1016/j.jbc.2021.100602	journal	January 2021
Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize Gao, Lei; Jiang, Haifang; Li, Minze Journal of Genetics and Genomics, Vol. 51, Issue 3 https://doi.org/10.1016/j.jgg.2023.07.004	journal	March 2024
Modeling of regulatory loops controlling galactolipid biosynthesis in the inner envelope membrane of chloroplasts Maréchal, Eric; Bastien, Olivier Journal of Theoretical Biology, Vol. 361 https://doi.org/10.1016/j.jtbi.2014.07.013	journal	November 2014
Emerging Roles of Sphingolipid Signaling in Plant Response to Biotic and Abiotic Stresses Ali, Usman; Li, Hehuan; Wang, Xuemin Molecular Plant, Vol. 11, Issue 11 https://doi.org/10.1016/j.molp.2018.10.001	journal	November 2018
Multifunctional annexins Laohavisit, Anuphon; Davies, Julia M. Plant Science, Vol. 177, Issue 6 https://doi.org/10.1016/j.plantsci.2009.09.008	journal	December 2009
Long-chain base kinase1 affects freezing tolerance in Arabidopsis thaliana Huang, Xiaozhen; Zhang, Yao; Zhang, Xiaoyan Plant Science, Vol. 259 https://doi.org/10.1016/j.plantsci.2017.03.009	journal	June 2017
Linum usitatissimum FAD2A and FAD3A enhance seed polyunsaturated fatty acid accumulation and seedling cold tolerance in Arabidopsis thaliana Wang, Jianjun; Liu, Zijin; Liu, Hua Plant Science, Vol. 311 https://doi.org/10.1016/j.plantsci.2021.111014	journal	October 2021
Long chain base changes triggered by a short exposure of Arabidopsis to low temperature are altered by AHb1 non-symbiotic haemoglobin overexpression Guillas, Isabelle; Guellim, Amira; Rezé, Nathalie Plant Physiology and Biochemistry, Vol. 63 https://doi.org/10.1016/j.plaphy.2012.11.020	journal	February 2013
Lipids of plant membrane rafts Cacas, Jean-Luc; Furt, Fabienne; Le Guédard, Marina Progress in Lipid Research, Vol. 51, Issue 3 https://doi.org/10.1016/j.plipres.2012.04.001	journal	July 2012
Plant lipids: Key players of plasma membrane organization and function Mamode Cassim, Adiilah; Gouguet, Paul; Gronnier, Julien Progress in Lipid Research, Vol. 73 https://doi.org/10.1016/j.plipres.2018.11.002	journal	January 2019
Structural and functional roles of non-bilayer lipid phases of chloroplast thylakoid membranes and mitochondrial inner membranes Garab, Győző; Yaguzhinsky, Lev S.; Dlouhý, Ondřej Progress in Lipid Research, Vol. 86 https://doi.org/10.1016/j.plipres.2022.101163	journal	April 2022
Sphingolipid metabolism, transport, and functions in plants: Recent progress and future perspectives Liu, Ning-Jing; Hou, Li-Pan; Bao, Jing-Jing Plant Communications, Vol. 2, Issue 5 https://doi.org/10.1016/j.xplc.2021.100214	journal	September 2021
Molecular Structure and Permeability at the Interface between Phase-Separated Membrane Domains Cordeiro, Rodrigo M. The Journal of Physical Chemistry B, Vol. 122, Issue 27 https://doi.org/10.1021/acs.jpcb.8b03406	journal	May 2018
Cardiolipin Effects on Membrane Structure and Dynamics Unsay, Joseph D.; Cosentino, Katia; Subburaj, Yamunadevi Langmuir, Vol. 29, Issue 51 https://doi.org/10.1021/la402669z	journal	September 2013
Genetically engineered alteration in the chilling sensitivity of plants Murata, N.; Ishizaki-Nishizawa, O.; Higashi, S. Nature, Vol. 356, Issue 6371 https://doi.org/10.1038/356710a0	journal	April 1992
The plasma membrane–bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana Li, Weiqi; Li, Maoyin; Zhang, Wenhua Nature Biotechnology, Vol. 22, Issue 4 https://doi.org/10.1038/nbt949	journal	March 2004
A new class of plant lipid is essential for protection against phosphorus depletion Okazaki, Yozo; Otsuki, Hitomi; Narisawa, Tomoko Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2512	journal	February 2013
Permeability of membranes in the liquid ordered and liquid disordered phases Ghysels, An; Krämer, Andreas; Venable, Richard M. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13432-7	journal	December 2019
Membrane thickness, lipid phase and sterol type are determining factors in the permeability of membranes to small solutes Frallicciardi, Jacopo; Melcr, Josef; Siginou, Pareskevi Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-29272-x	journal	March 2022
Ca2+-permeable mechanosensitive channels MCA1 and MCA2 mediate cold-induced cytosolic Ca2+ increase and cold tolerance in Arabidopsis Mori, Kendo; Renhu, Na; Naito, Maho Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-017-17483-y	journal	January 2018
Warm hole in Pacific Arctic sea ice cover forced mid-latitude Northern Hemisphere cooling during winter 2017–18 Tachibana, Yoshihiro; Komatsu, Kensuke K.; Alexeev, Vladimir A. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-41682-4	journal	April 2019
Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation, but is dispensable for mitochondrial function : Arabidopsis Babiychuk, Elena; Müller, Frank; Eubel, Holger The Plant Journal, Vol. 33, Issue 5 https://doi.org/10.1046/j.1365-313X.2003.01680.x	journal	February 2003
Anionic lipids are required for chloroplast structure and function in Arabidopsis Yu, Bin; Benning, Christoph The Plant Journal, Vol. 36, Issue 6 https://doi.org/10.1046/j.1365-313X.2003.01918.x	journal	December 2003
The Electric Properties of Plant Cell Membranes I. The Electric Capacitance of Suspensions of Mitochondria, Chloroplasts, and Chlorella Sp. Hope, Ab Australian Journal of Biological Sciences, Vol. 9, Issue 1 https://doi.org/10.1071/BI9560053	journal	January 1956
Yield stability for cereals in a changing climate Powell, Nicola; Ji, Xuemei; Ravash, Rudabe Functional Plant Biology, Vol. 39, Issue 7 https://doi.org/10.1071/FP12078	journal	January 2012
Two types of MGDG synthase genes, found widely in both 16:3 and 18:3 plants, differentially mediate galactolipid syntheses in photosynthetic and nonphotosynthetic tissues in Arabidopsis thaliana Awai, K.; Marechal, E.; Block, M. A. Proceedings of the National Academy of Sciences, Vol. 98, Issue 19 https://doi.org/10.1073/pnas.181331498	journal	September 2001
Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas García-Cerdán, José G.; Schmid, Eva M.; Takeuchi, Tomomi Proceedings of the National Academy of Sciences, Vol. 117, Issue 22 https://doi.org/10.1073/pnas.1916948117	journal	May 2020
Lamellar-to-hexagonalII phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration. Gordon-Kamm, W. J.; Steponkus, P. L. Proceedings of the National Academy of Sciences, Vol. 81, Issue 20 https://doi.org/10.1073/pnas.81.20.6373	journal	October 1984
Altered regulation of lipid biosynthesis in a mutant of Arabidopsis deficient in chloroplast glycerol-3-phosphate acyltransferase activity Kunst, L.; Browse, J.; Somerville, C. Proceedings of the National Academy of Sciences, Vol. 85, Issue 12, p. 4143-4147 https://doi.org/10.1073/pnas.85.12.4143	journal	June 1988
Transformation of the cryobehavior of rye protoplasts by modification of the plasma membrane lipid composition Steponkus, Peter L.; Uemura, Matsuo; Balsamo, Ronald A. Proceedings of the National Academy of Sciences, Vol. 85, Issue 23 https://doi.org/10.1073/pnas.85.23.9026	journal	December 1988
Arabidopsis requires polyunsaturated lipids for low-temperature survival. Miquel, M.; James, D.; Dooner, H. Proceedings of the National Academy of Sciences, Vol. 90, Issue 13 https://doi.org/10.1073/pnas.90.13.6208	journal	July 1993
Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance Artus, Nancy N.; Uemura, Matsuo; Steponkus, Peter L. Proceedings of the National Academy of Sciences, Vol. 93, Issue 23 https://doi.org/10.1073/pnas.93.23.13404	journal	November 1996
Consequences of ω-6-Oleate Desaturase Deficiency on Lipid Dynamics and Functional Properties of Mitochondrial Membranes ofArabidopsis thaliana Caiveau, Olivier; Fortune, Dominique; Cantrel, Catherine Journal of Biological Chemistry, Vol. 276, Issue 8 https://doi.org/10.1074/jbc.M006231200	journal	February 2001
The Phosphatidic Acid Binding Site of the Arabidopsis Trigalactosyldiacylglycerol 4 (TGD4) Protein Required for Lipid Import into Chloroplasts Wang, Zhen; Anderson, Nicholas Scott; Benning, Christoph Journal of Biological Chemistry, Vol. 288, Issue 7 https://doi.org/10.1074/jbc.M112.438986	journal	January 2013
Structural Determinants Allowing Transferase Activity in SENSITIVE TO FREEZING 2, Classified as a Family I Glycosyl Hydrolase Roston, Rebecca L.; Wang, Kun; Kuhn, Leslie A. Journal of Biological Chemistry, Vol. 289, Issue 38 https://doi.org/10.1074/jbc.M114.576694	journal	August 2014
Differential Effect of Plant Lipids on Membrane Organization Grosjean, Kevin; Mongrand, Sébastien; Beney, Laurent Journal of Biological Chemistry, Vol. 290, Issue 9 https://doi.org/10.1074/jbc.M114.598805	journal	February 2015
Membranes as Structural Antioxidants Schmid-Siegert, Emanuel; Stepushenko, Olga; Glauser, Gaetan Journal of Biological Chemistry, Vol. 291, Issue 25 https://doi.org/10.1074/jbc.M116.729921	journal	June 2016
Profiling Membrane Lipids in Plant Stress Responses: ROLE OF PHOSPHOLIPASE Dα IN FREEZING-INDUCED LIPID CHANGES IN Welti, Ruth; Li, Weiqi; Li, Maoyin Journal of Biological Chemistry, Vol. 277, Issue 35 https://doi.org/10.1074/jbc.M205375200	journal	June 2002
Differential Degradation of Extraplastidic and Plastidic Lipids during Freezing and Post-freezing Recovery in Arabidopsis thaliana Li, Weiqi; Wang, Ruiping; Li, Maoyin Journal of Biological Chemistry, Vol. 283, Issue 1 https://doi.org/10.1074/jbc.M706692200	journal	October 2007
Structural Determinants of Water Permeability through the Lipid Membrane Mathai, John C.; Tristram-Nagle, Stephanie; Nagle, John F. The Journal of General Physiology, Vol. 131, Issue 1 https://doi.org/10.1085/jgp.200709848	journal	December 2007
Theory of Passive Permeability through Lipid Bilayers Nagle, John F.; Mathai, John C.; Zeidel, Mark L. Journal of General Physiology, Vol. 131, Issue 1 https://doi.org/10.1085/jgp.200709849	journal	December 2007
North American cold events following sudden stratospheric warming in the presence of low Barents-Kara Sea sea ice Zhang, Pengfei; Wu, Yutian; Chen, Gang Environmental Research Letters, Vol. 15, Issue 12 https://doi.org/10.1088/1748-9326/abc215	journal	November 2020
YeastARV1Is Required for Efficient Delivery of an Early GPI Intermediate to the First Mannosyltransferase during GPI Assembly and Controls Lipid Flow from the Endoplasmic Reticulum Kajiwara, Kentaro; Watanabe, Reika; Pichler, Harald Molecular Biology of the Cell, Vol. 19, Issue 5 https://doi.org/10.1091/mbc.e07-08-0740	journal	May 2008
Variation in climatic tolerance, but not stomatal traits, partially explains Pooideae grass species distributions Das, Aayudh; Prakash, Anoob; Dedon, Natalie Annals of Botany, Vol. 128, Issue 1 https://doi.org/10.1093/aob/mcab046	journal	March 2021
Diversity in sphingolipid metabolism across land plants Haslam, Tegan M.; Feussner, Ivo Journal of Experimental Botany, Vol. 73, Issue 9 https://doi.org/10.1093/jxb/erab558	journal	February 2022
Oligogalactolipid production during cold challenge is conserved in early diverging lineages Barnes, Allison C.; Myers, Jennifer L.; Surber, Samantha M. Journal of Experimental Botany, Vol. 74, Issue 17 https://doi.org/10.1093/jxb/erad241	journal	June 2023
Molecular, cellular, and physiological responses to phosphatidic acid formation in plants Testerink, C.; Munnik, T. Journal of Experimental Botany, Vol. 62, Issue 7 https://doi.org/10.1093/jxb/err079	journal	March 2011
EARLY RESPONSE TO DEHYDRATION 7 Remodels Cell Membrane Lipid Composition during Cold Stress in Arabidopsis Barajas-Lopez, Juan de Dios; Tiwari, Arjun; Zarza, Xavier Plant and Cell Physiology, Vol. 62, Issue 1 https://doi.org/10.1093/pcp/pcaa139	journal	November 2020
Alternative Oxidase Involvement in Cold Stress Response of Arabidopsis thaliana fad2 and FAD3+ Cell Suspensions Altered in Membrane Lipid Composition Matos, Ana Rita; Hourton-Cabassa, Cécile; Ciçek, Dominique Plant and Cell Physiology, Vol. 48, Issue 6 https://doi.org/10.1093/pcp/pcm061	journal	June 2007
Cryobehavior of the Plasma Membrane in Protoplasts Isolated from Cold-Acclimated Arabidopsis Leaves is Related to Surface Area Regulation Yamazaki, Tomokazu; Kawamura, Yukio; Uemura, Matsuo Plant and Cell Physiology, Vol. 49, Issue 6 https://doi.org/10.1093/pcp/pcn068	journal	June 2008
Chloroplast Galactolipids: The Link Between Photosynthesis, Chloroplast Shape, Jasmonates, Phosphate Starvation and Freezing Tolerance Li, Hsou-min; Yu, Chun-Wei Plant and Cell Physiology, Vol. 59, Issue 6 https://doi.org/10.1093/pcp/pcy088	journal	May 2018
Chloroplast membrane lipid remodeling protects against dehydration by limiting membrane fusion and distortion Chng, Choon-Peng; Wang, Kun; Ma, Wei Plant Physiology, Vol. 188, Issue 1 https://doi.org/10.1093/plphys/kiab512	journal	November 2021
Defining the lipidome of Arabidopsis leaf mitochondria: Specific lipid complement and biosynthesis capacity Liu, Yi-Tse; Senkler, Jennifer; Herrfurth, Cornelia Plant Physiology, Vol. 191, Issue 4 https://doi.org/10.1093/plphys/kiad035	journal	January 2023
All members of the Arabidopsis DGAT and PDAT acyltransferase families operate during high and low temperatures Shomo, Zachery D.; Mahboub, Samira; Vanviratikul, Hathaichanok Plant Physiology, Vol. 195, Issue 1 https://doi.org/10.1093/plphys/kiae074	journal	February 2024
Activation of Phospholipases C and D Is an Early Response to a Cold Exposure in Arabidopsis Suspension Cells Ruelland, Eric; Cantrel, Catherine; Gawer, Myriam Plant Physiology, Vol. 130, Issue 2 https://doi.org/10.1104/pp.006080	journal	September 2002
A Comparison of Freezing Injury in Oat and Rye: Two Cereals at the Extremes of Freezing Tolerance Webb, M. S.; Uemura, M.; Steponkus, P. L. Plant Physiology, Vol. 104, Issue 2 https://doi.org/10.1104/pp.104.2.467	journal	February 1994
Cold Acclimation of Arabidopsis thaliana (Effect on Plasma Membrane Lipid Composition and Freeze-Induced Lesions) Uemura, M.; Joseph, R. A.; Steponkus, P. L. Plant Physiology, Vol. 109, Issue 1 https://doi.org/10.1104/pp.109.1.15	journal	September 1995
Analysis of Acyl Fluxes through Multiple Pathways of Triacylglycerol Synthesis in Developing Soybean Embryos Bates, Philip D.; Durrett, Timothy P.; Ohlrogge, John B. Plant Physiology, Vol. 150, Issue 1 https://doi.org/10.1104/pp.109.137737	journal	March 2009
Depletion of the Membrane-Associated Acyl-Coenzyme A-Binding Protein ACBP1 Enhances the Ability of Cold Acclimation in Arabidopsis Du, Zhi-Yan; Xiao, Shi; Chen, Qin-Fang Plant Physiology, Vol. 152, Issue 3 https://doi.org/10.1104/pp.109.147066	journal	January 2010
DONGLE and DEFECTIVE IN ANTHER DEHISCENCE1 Lipases Are Not Essential for Wound- and Pathogen-Induced Jasmonate Biosynthesis: Redundant Lipases Contribute to Jasmonate Formation Ellinger, Dorothea; Stingl, Nadja; Kubigsteltig, Ines Ingeborg Plant Physiology, Vol. 153, Issue 1 https://doi.org/10.1104/pp.110.155093	journal	March 2010
Involvement of Arabidopsis ACYL-COENZYME A DESATURASE-LIKE2 (At2g31360) in the Biosynthesis of the Very-Long-Chain Monounsaturated Fatty Acid Components of Membrane Lipids Smith, Mark A.; Dauk, Melanie; Ramadan, Hussein Plant Physiology, Vol. 161, Issue 1 https://doi.org/10.1104/pp.112.202325	journal	November 2012
Acyl Editing and Headgroup Exchange Are the Major Mechanisms That Direct Polyunsaturated Fatty Acid Flux into Triacylglycerols Bates, Philip D.; Fatihi, Abdelhak; Snapp, Anna R. Plant Physiology, Vol. 160, Issue 3 https://doi.org/10.1104/pp.112.204438	journal	August 2012
Effect of Cold Acclimation on the Lipid Composition of the Inner and Outer Membrane of the Chloroplast Envelope Isolated from Rye Leaves Uemura, M.; Steponkus, P. L. Plant Physiology, Vol. 114, Issue 4 https://doi.org/10.1104/pp.114.4.1493	journal	August 1997
DIACYLGLYCEROL ACYLTRANSFERASE and DIACYLGLYCEROL KINASE Modulate Triacylglycerol and Phosphatidic Acid Production in the Plant Response to Freezing Stress Tan, Wei-Juan; Yang, Yi-Cong; Zhou, Ying Plant Physiology, Vol. 177, Issue 3 https://doi.org/10.1104/pp.18.00402	journal	May 2018
DIACYLGLYCEROL ACYLTRANSFERASE1 Contributes to Freezing Tolerance Arisz, Steven A.; Heo, Jae-Yun; Koevoets, Iko T. Plant Physiology, Vol. 177, Issue 4 https://doi.org/10.1104/pp.18.00503	journal	June 2018
Phosphatidylglycerol Composition Is Central to Chilling Damage in the Arabidopsis fab1 Mutant Gao, Jinpeng; Lunn, Daniel; Wallis, James G. Plant Physiology, Vol. 184, Issue 4 https://doi.org/10.1104/pp.20.01219	journal	October 2020
Molecular biology of the plasma membrane of higher plants. Sussman, M. R.; Harper, J. F. The Plant Cell, Vol. 1, Issue 10 https://doi.org/10.1105/tpc.1.10.953	journal	October 1989
The Essential Nature of Sphingolipids in Plants as Revealed by the Functional Identification and Characterization of the Arabidopsis LCB1 Subunit of Serine Palmitoyltransferase Chen, Ming; Han, Gongshe; Dietrich, Charles R. The Plant Cell, Vol. 18, Issue 12 https://doi.org/10.1105/tpc.105.040774	journal	December 2006
Calcium-Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1 Yamazaki, Tomokazu; Kawamura, Yukio; Minami, Anzu The Plant Cell, Vol. 20, Issue 12 https://doi.org/10.1105/tpc.108.062679	journal	December 2008
ACYL-LIPID DESATURASE2 Is Required for Chilling and Freezing Tolerance in Arabidopsis Chen, Mingjie; Thelen, Jay J. The Plant Cell, Vol. 25, Issue 4 https://doi.org/10.1105/tpc.113.111179	journal	April 2013
The Importance of Cardiolipin Synthase for Mitochondrial Ultrastructure, Respiratory Function, Plant Development, and Stress Responses in Arabidopsis Pineau, Bernard; Bourge, Mickaël; Marion, Jessica The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.118018	journal	October 2013
Cardiolipin-Mediated Mitochondrial Dynamics and Stress Response in Arabidopsis Pan, Ronghui; Jones, A. Daniel; Hu, Jianping The Plant Cell, Vol. 26, Issue 1 https://doi.org/10.1105/tpc.113.121095	journal	January 2014
Understanding the Biochemical Basis of Temperature-Induced Lipid Pathway Adjustments in Plants Li, Qiang; Zheng, Qian; Shen, Wenyun The Plant Cell, Vol. 27, Issue 1 https://doi.org/10.1105/tpc.114.134338	journal	January 2015
Arabidopsis Mutants Reveal Multiple Roles for Sterols in Plant Development Clouse, Steven D. The Plant Cell, Vol. 14, Issue 9 https://doi.org/10.1105/tpc.140930	journal	September 2002
A Plastid Phosphatidylglycerol Lipase Contributes to the Export of Acyl Groups from Plastids for Seed Oil Biosynthesis Wang, Kun; Froehlich, John E.; Zienkiewicz, Agnieszka The Plant Cell, Vol. 29, Issue 7 https://doi.org/10.1105/tpc.17.00397	journal	July 2017
HEAT INDUCIBLE LIPASE1 Remodels Chloroplastic Monogalactosyldiacylglycerol by Liberating α-Linolenic Acid in Arabidopsis Leaves under Heat Stress Higashi, Yasuhiro; Okazaki, Yozo; Takano, Kouji The Plant Cell, Vol. 30, Issue 8 https://doi.org/10.1105/tpc.18.00347	journal	July 2018
Isolation and Characterization of an Arabidopsis Mutant Deficient in the Thylakoid Lipid Digalactosyl Diacylglycerol Dormann, P.; Hoffmann-Benning, S.; Balbo, I. The Plant Cell Online, Vol. 7, Issue 11, p. 1801-1810 https://doi.org/10.1105/tpc.7.11.1801	journal	November 1995
Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Knight, H.; Trewavas, A. J.; Knight, M. R. The Plant Cell, Vol. 8, Issue 3 https://doi.org/10.1105/tpc.8.3.489	journal	March 1996
Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content: Gene-metabolite linkages at low temperature Kaplan, Fatma; Kopka, Joachim; Sung, Dong Yul The Plant Journal, Vol. 50, Issue 6 https://doi.org/10.1111/j.1365-313X.2007.03100.x	journal	April 2007
FATTY ACID DESATURASE4 of Arabidopsis encodes a protein distinct from characterized fatty acid desaturases: FATTY ACID DESATURASE4 of Arabidopsis encodes a distinct protein Gao, Jinpeng; Ajjawi, Imad; Manoli, Arthur The Plant Journal, Vol. 60, Issue 5 https://doi.org/10.1111/j.1365-313X.2009.04001.x	journal	December 2009
Sphingolipid Δ8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis: Sphingolipid Δ8 unsaturation in Arabidopsis Chen, Ming; Markham, Jonathan E.; Cahoon, Edgar B. The Plant Journal, Vol. 69, Issue 5 https://doi.org/10.1111/j.1365-313X.2011.04829.x	journal	December 2011
Phytosphingosine-phosphate is a signal for AtMPK6 activation and Arabidopsis response to chilling Dutilleul, Christelle; Benhassaine-Kesri, Ghouziel; Demandre, Chantal New Phytologist, Vol. 194, Issue 1 https://doi.org/10.1111/j.1469-8137.2011.04017.x	journal	January 2012
Sphingolipids: towards an integrated view of metabolism during the plant stress response Huby, Eloïse; Napier, Johnathan A.; Baillieul, Fabienne New Phytologist, Vol. 225, Issue 2 https://doi.org/10.1111/nph.15997	journal	July 2019
Evidence for ACD5 ceramide kinase activity involvement in Arabidopsis response to cold stress Dutilleul, Christelle; Chavarria, Heidy; Rézé, Nathalie Plant, Cell & Environment, Vol. 38, Issue 12 https://doi.org/10.1111/pce.12578	journal	July 2015
Lipid signalling in plant responses to abiotic stress: Lipid signalling in plant responses to abiotic stress Hou, Quancan; Ufer, Guido; Bartels, Dorothea Plant, Cell & Environment, Vol. 39, Issue 5 https://doi.org/10.1111/pce.12666	journal	February 2016
Functions and interaction of plant lipid signalling under abiotic stresses Liang, Y.; Huang, Y.; Liu, C. Plant Biology, Vol. 25, Issue 3 https://doi.org/10.1111/plb.13507	journal	February 2023
Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana: Lipidomics of Arabidopsis cold acclimation Degenkolbe, Thomas; Giavalisco, Patrick; Zuther, Ellen The Plant Journal, Vol. 72, Issue 6 https://doi.org/10.1111/tpj.12007	journal	October 2012
Acylated monogalactosyl diacylglycerol: prevalence in the plant kingdom and identification of an enzyme catalyzing galactolipid head group acylation in Arabidopsis thaliana Nilsson, Anders K.; Johansson, Oskar N.; Fahlberg, Per The Plant Journal, Vol. 84, Issue 6 https://doi.org/10.1111/tpj.13072	journal	December 2015
Leveraging GWAS data to identify metabolic pathways and networks involved in maize lipid biosynthesis Li, Hui; Thrash, Adam; Tang, Juliet D. The Plant Journal, Vol. 98, Issue 5 https://doi.org/10.1111/tpj.14282	journal	March 2019
Membrane lipid polyunsaturation mediated by FATTY ACID DESATURASE 2 ( FAD 2 ) is involved in endoplasmic reticulum stress tolerance in Arabidopsis thaliana Nguyen, Van Cam; Nakamura, Yuki; Kanehara, Kazue The Plant Journal, Vol. 99, Issue 3 https://doi.org/10.1111/tpj.14338	journal	June 2019
AKR2A interacts with KCS1 to improve VLCFAs contents and chilling tolerance of Arabidopsis thaliana Chen, Lin; Hu, Wenjun; Mishra, Neelam The Plant Journal, Vol. 103, Issue 4 https://doi.org/10.1111/tpj.14848	journal	June 2020
Mechanisms and functions of membrane lipid remodeling in plants Yu, Linhui; Zhou, Chao; Fan, Jilian The Plant Journal, Vol. 107, Issue 1 https://doi.org/10.1111/tpj.15273	journal	May 2021
A chloroplast diacylglycerol lipase modulates glycerolipid pathway balance in Arabidopsis Yu, Linhui; Shen, Wenyun; Fan, Jilian The Plant Journal, Vol. 115, Issue 2 https://doi.org/10.1111/tpj.16228	journal	April 2023
Freezing Tolerance in Plants Requires Lipid Remodeling at the Outer Chloroplast Membrane Moellering, Eric R.; Muthan, Bagyalakshmi; Benning, Christoph Science, Vol. 330, Issue 6001 https://doi.org/10.1126/science.1191803	journal	August 2010
Plant Lipids: Metabolism, Mutants, and Membranes Somerville, C.; Browse, J. Science, Vol. 252, Issue 5002 https://doi.org/10.1126/science.252.5002.80	journal	April 1991
Chloroplast Lipids and Their Biosynthesis Hölzl, Georg; Dörmann, Peter Annual Review of Plant Biology, Vol. 70, Issue 1 https://doi.org/10.1146/annurev-arplant-050718-100202	journal	April 2019
Lipid Droplets: Packing Hydrophobic Molecules Within the Aqueous Cytoplasm Guzha, Athanas; Whitehead, Payton; Ischebeck, Till Annual Review of Plant Biology, Vol. 74, Issue 1 https://doi.org/10.1146/annurev-arplant-070122-021752	journal	November 2022
Critical Phenomena in Plasma Membrane Organization and Function Shaw, Thomas R.; Ghosh, Subhadip; Veatch, Sarah L. Annual Review of Physical Chemistry, Vol. 72, Issue 1 https://doi.org/10.1146/annurev-physchem-090419-115951	journal	April 2021
Seed Storage Oil Mobilization Graham, Ian A. Annual Review of Plant Biology, Vol. 59, Issue 1, p. 115-142 https://doi.org/10.1146/annurev.arplant.59.032607.092938	journal	June 2008
Membrane Trafficking in Plants Jürgens, Gerd Annual Review of Cell and Developmental Biology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.cellbio.20.082503.103057	journal	November 2004
Chilling Injury in Plants Lyons, James M. Annual Review of Plant Physiology, Vol. 24, Issue 1 https://doi.org/10.1146/annurev.pp.24.060173.002305	journal	June 1973
Glycerolipid Synthesis: Biochemistry and Regulation Browse, J.; Somerville, C. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 42, Issue 1 https://doi.org/10.1146/annurev.pp.42.060191.002343	journal	June 1991
Glycerolipidome responses to freezing- and chilling-induced injuries: examples in Arabidopsis and rice Zheng, Guowei; Li, Lixia; Li, Weiqi BMC Plant Biology, Vol. 16, Issue 1 https://doi.org/10.1186/s12870-016-0758-8	journal	March 2016
Acyl-Lipid Metabolism Li-Beisson, Yonghua; Shorrosh, Basil; Beisson, Fred The Arabidopsis Book, Vol. 11 https://doi.org/10.1199/tab.0161	journal	January 2013
The calcium transporter ANNEXIN1 mediates cold‐induced calcium signaling and freezing tolerance in plants Liu, Qiangbo; Ding, Yanglin; Shi, Yiting The EMBO Journal, Vol. 40, Issue 2 https://doi.org/10.15252/embj.2020104559	journal	December 2020
The ins and outs of endoplasmic reticulum‐controlled lipid biosynthesis Jacquemyn, Julie; Cascalho, Ana; Goodchild, Rose E. EMBO reports, Vol. 18, Issue 11 https://doi.org/10.15252/embr.201643426	journal	October 2017
Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase Arisz, Steven A.; van Wijk, Ringo; Roels, Wendy Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00001	journal	January 2013
Plant plasma membrane proteomics for improving cold tolerance Takahashi, Daisuke; Li, Bin; Nakayama, Takato Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00090	journal	January 2013
Lipid signaling in plants Wang, Xuemin; Chapman, Kent D. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00216	journal	January 2013
Importance of the hexagonal lipid phase in biological membrane organization Jouhet, Juliette Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00494	journal	January 2013
Biochemical and Transcriptional Regulation of Membrane Lipid Metabolism in Maize Leaves under Low Temperature Gu, Yingnan; He, Lin; Zhao, Changjiang Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02053	journal	November 2017
Lipid Trafficking at Membrane Contact Sites During Plant Development and Stress Response Michaud, Morgane; Jouhet, Juliette Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00002	journal	January 2019
Why Do Plants Convert Sitosterol to Stigmasterol? Aboobucker, Siddique I.; Suza, Walter P. Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00354	journal	March 2019
Phospholipid:Diacylglycerol Acyltransferase1 Overexpression Delays Senescence and Enhances Post-heat and Cold Exposure Fitness Demski, Kamil; Łosiewska, Anna; Jasieniecka-Gazarkiewicz, Katarzyna Frontiers in Plant Science, Vol. 11 https://doi.org/10.3389/fpls.2020.611897	journal	December 2020
Membrane Lipids’ Metabolism and Transcriptional Regulation in Maize Roots Under Cold Stress Zhao, Xunchao; Wei, Yulei; Zhang, Jinjie Frontiers in Plant Science, Vol. 12 https://doi.org/10.3389/fpls.2021.639132	journal	April 2021
Sphingolipid Long-Chain Base Phosphate Degradation Can Be a Rate-Limiting Step in Long-Chain Base Homeostasis Lambour, Benjamin; Glenz, René; Forner, Carmen Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.911073	journal	June 2022
Tackling functional redundancy of Arabidopsis fatty acid elongase complexes Batsale, Marguerite; Alonso, Marie; Pascal, Stéphanie Frontiers in Plant Science, Vol. 14 https://doi.org/10.3389/fpls.2023.1107333	journal	January 2023
Responses of sorghum to cold stress: A review focused on molecular breeding Vera Hernández, Pedro Fernando; Mendoza Onofre, Leopoldo Ernesto; Rosas Cárdenas, Flor de Fátima Frontiers in Plant Science, Vol. 14 https://doi.org/10.3389/fpls.2023.1124335	journal	February 2023
The Role of Chloroplast Membrane Lipid Metabolism in Plant Environmental Responses Cook, Ron; Lupette, Josselin; Benning, Christoph Cells, Vol. 10, Issue 3 https://doi.org/10.3390/cells10030706	journal	March 2021
GmFAD3A, A ω-3 Fatty Acid Desaturase Gene, Enhances Cold Tolerance and Seed Germination Rate under Low Temperature in Rice Wang, Xin; Yu, Chao; Liu, Yi International Journal of Molecular Sciences, Vol. 20, Issue 15 https://doi.org/10.3390/ijms20153796	journal	August 2019
Involvement of Salicylic Acid and Other Phenolic Compounds in Light-Dependent Cold Acclimation in Maize Pál, Magda; Janda, Tibor; Majláth, Imre International Journal of Molecular Sciences, Vol. 21, Issue 6 https://doi.org/10.3390/ijms21061942	journal	March 2020
Biosynthesis and the Roles of Plant Sterols in Development and Stress Responses Du, Yinglin; Fu, Xizhe; Chu, Yiyang International Journal of Molecular Sciences, Vol. 23, Issue 4 https://doi.org/10.3390/ijms23042332	journal	February 2022
Lipidomics-Assisted GWAS (lGWAS) Approach for Improving High-Temperature Stress Tolerance of Crops Pranneshraj, Velumani; Sangha, Manjeet Kaur; Djalovic, Ivica International Journal of Molecular Sciences, Vol. 23, Issue 16 https://doi.org/10.3390/ijms23169389	journal	August 2022
Specific Changes in Arabidopsis thaliana Rosette Lipids during Freezing Can Be Associated with Freezing Tolerance Vu, Hieu Sy; Shiva, Sunitha; Samarakoon, Thilani Metabolites, Vol. 12, Issue 5 https://doi.org/10.3390/metabo12050385	journal	April 2022
The Role of Triacylglycerol in Plant Stress Response Lu, Junhao; Xu, Yang; Wang, Juli Plants, Vol. 9, Issue 4 https://doi.org/10.3390/plants9040472	journal	April 2020
Comparative Transcriptome and Lipidome Analyses Reveal Molecular Chilling Responses in Chilling‐Tolerant Sorghums Marla, Sandeep R.; Shiva, Sunitha; Welti, Ruth The Plant Genome, Vol. 10, Issue 3 https://doi.org/10.3835/plantgenome2017.03.0025	journal	November 2017
A mechanistic model of COR15 protein function in plant freezing tolerance: integration of structural and functional characteristics Thalhammer, Anja; Hincha, Dirk K. Plant Signaling & Behavior, Vol. 9, Issue 12 https://doi.org/10.4161/15592324.2014.977722	journal	December 2014
The role of phytosterols in plant adaptation to temperature Dufourc, Erick J. Plant Signaling & Behavior, Vol. 3, Issue 2 https://doi.org/10.4161/psb.3.2.5051	journal	February 2008
Responses of Unsaturated Fatty Acid in Membrane Lipid and Antioxidant Enzymes to Chilling Stress in Sweet Sorghum (Sorghum bicolor (L.) Moench) Seedling Guo, Yuanyuan; Liu, Shanshan; Yang, Zhen Journal of Agricultural Science, Vol. 8, Issue 9 https://doi.org/10.5539/jas.v8n9p71	journal	August 2016

Similar Records

From sensing to acclimation: The role of membrane lipid remodeling in plant responses to low temperatures

Journal Article · 2024 · Plant Physiology (Bethesda) · OSTI ID:2578926

Shomo, Zachery; Li, Fangyi; Smith, Cailin; +2 more

Chloroplast lipid biosynthesis is fine-tuned to thylakoid membrane remodeling during light acclimation

Journal Article · 2020 · Plant Physiology (Bethesda) · OSTI ID:1831301

Yu, Linhui; Fan, Jilian; Zhou, Chao; +1 more

Mechanisms and functions of membrane lipid remodeling in plants

Journal Article · 2021 · The Plant Journal · OSTI ID:1777423

Yu, Linhui; Zhou, Chao; Fan, Jilian; +2 more

Title: From sensing to acclimation: The role of membrane lipid remodeling in plant responses to low temperatures

Citation Formats

References (156)

Similar Records

Related Subjects