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Plant function and evolutionary biology
RESEARCH ARTICLE

Lipid remodelling plays an important role in wheat (Triticum aestivum) hypoxia stress

Le Xu A B , Rui Pan A , Meixue Zhou A C , Yanhao Xu A and Wenying Zhang https://orcid.org/0000-0001-6241-7563 A D
+ Author Affiliations
- Author Affiliations

A Hubei Collaborative Innovation Centre for Grain Industry/ Engineering Research Centre of Ecology and Agricultural Use of Wetland, Ministry of Education, Yangtze University, Jingzhou 434025, China.

B Guangdong Provincial Key Laboratory of Biotechnology for Plant Development, School of Life Sciences, South China Normal University, Guangzhou 510631, China.

C Tasmanian Institute of Agriculture, University of Tasmania, Private Bag 1375, Prospect, Tas. 7250, Australia.

D Corresponding author. Email: wyzhang@yangtzeu.edu.cn

Functional Plant Biology 47(1) 58-66 https://doi.org/10.1071/FP19150
Submitted: 28 May 2019  Accepted: 3 September 2019   Published: 10 December 2019

Abstract

Membrane lipid remodelling is one of the strategies that plants have developed to combat abiotic stress. In this study, physiological, lipidomic and proteome analyses were conducted to investigate the changes in glycerolipid and phospholipid concentrations in the wheat (Triticum aestivum L.) cultivars CIGM90.863 and Seri M82 under hypoxia treatment. The growth of CIGM90.863 remained unaffected, whereas Seri M82 was significantly stunted after 8 days of hypoxia treatment. The concentrations of all lipids except lysophosphatidylglycerol were significantly higher in the leaves of Seri M82 than in CIGM90.863 under normal growth conditions. The lipid profile changed significantly under hypoxia stress and varied between genotypes for some of the lipids. Phosphatidic acids remained unchanged in Seri M82 but they were gradually induced in CIGM90.863 in response to hypoxia stress because of the higher phospholipase D expression and lower expression of diglycerol kinase and phosphatidate phosphatases. In contrast, digalactosyldiacylglycerol content was highly stable in CIGM90.863 following hypoxia treatment, although it decreased significantly in Seri M82. Phosphatidylglycerol and lipoxygenase showed a stronger and faster response in CIGM90.863 than in Seri M82 under hypoxia stress. Different membrane lipid adjustments in wheat under oxygen deficiency conditions could be partly responsible for the differing tolerance of Seri M82 and CIGM90.863. This study will help us to better understand how wheat tolerates hypoxia stress by regulating lipid remodelling.

Additional keywords: Cell membrane integrity, oxygen deficiency, proteome analysis.


References

Arisz SA, Van WR, Roels W, Zhu JK, Haring MA, Munnik T (2013) Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase. Frontiers in Plant Science 4, 1
Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase.Crossref | GoogleScholarGoogle Scholar | 23346092PubMed |

Armstrong W (1980) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
Aeration in higher plants.Crossref | GoogleScholarGoogle Scholar |

Aronsson H, Schottler MA, Kelly AA, Sundqvist C, Dormann P, Karim S, Jarvis P (2008) Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiology 148, 580–592.
Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves.Crossref | GoogleScholarGoogle Scholar | 18641085PubMed |

Aubourg SP (1993) Review: interaction of malondialdehyde with biological molecules – new trends about reactivity and significance. International Journal of Food Science & Technology 28, 323–335.
Review: interaction of malondialdehyde with biological molecules – new trends about reactivity and significance.Crossref | GoogleScholarGoogle Scholar |

Babiychuk E, Müller F, Eubel H, Braun HP, Frentzen M, Kushnir S (2003) Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation but is dispensable for mitochondrial function. The Plant Journal 33, 899–909.
Arabidopsis phosphatidylglycerophosphate synthase 1 is essential for chloroplast differentiation but is dispensable for mitochondrial function.Crossref | GoogleScholarGoogle Scholar | 12609031PubMed |

Bahl J, Francke B, Monégr R (1976) Lipid composition of envelopes prolamellar bodies and other plastid membranes in etiolated green and greening wheat leaves. Planta 129, 193–201.
Lipid composition of envelopes prolamellar bodies and other plastid membranes in etiolated green and greening wheat leaves.Crossref | GoogleScholarGoogle Scholar | 24430956PubMed |

Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annual Review of Plant Biology 59, 313–339.
Flooding stress: acclimations and genetic diversity.Crossref | GoogleScholarGoogle Scholar | 18444902PubMed |

Chen J, Burke JJ, Xin Z, Xu C, Velten J (2006) Characterization of the Arabidopsis thermosensitive mutant atts02 reveals an important role for galactolipids in thermotolerance. Plant, Cell & Environment 29, 1437–1448.
Characterization of the Arabidopsis thermosensitive mutant atts02 reveals an important role for galactolipids in thermotolerance.Crossref | GoogleScholarGoogle Scholar |

Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment 26, 17–36.
Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots.Crossref | GoogleScholarGoogle Scholar |

Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar | 20847100PubMed |

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
Flooding tolerance: suites of plant traits in variable environments.Crossref | GoogleScholarGoogle Scholar |

Davey MW, Stals E, Panis B, Keulemans J, Swennen RL (2005) High-throughput determination of malondialdehyde in plant tissues. Analytical Biochemistry 347, 201–207.
High-throughput determination of malondialdehyde in plant tissues.Crossref | GoogleScholarGoogle Scholar | 16289006PubMed |

de Vries AH, Mark AEM, Marrink SJ (2004) The binary mixing behavior of phospholipids in a bilayer: a molecular dynamics study. The Journal of Physical Chemistry B 108, 2454–2463.
The binary mixing behavior of phospholipids in a bilayer: a molecular dynamics study.Crossref | GoogleScholarGoogle Scholar |

Dore MHI (2005) Climate change and changes in global precipitation patterns: what do we know? Environment International 31, 1167–1181.
Climate change and changes in global precipitation patterns: what do we know?Crossref | GoogleScholarGoogle Scholar |

Droppa M, Horváth G, Hideg É, Farkas T (1995) The role of phospholipids in regulating photosynthetic electron transport activities: treatment of thylakoids with phospholipase C. Photosynthesis Research 46, 287–293.
The role of phospholipids in regulating photosynthetic electron transport activities: treatment of thylakoids with phospholipase C.Crossref | GoogleScholarGoogle Scholar | 24301594PubMed |

Eastman PAK, Rashid A, Camm EL (1997) Changes of the photosystem 2 activity and thylakoid proteins in spruce seedlings during water stress. Photosynthetica 34, 201–210.
Changes of the photosystem 2 activity and thylakoid proteins in spruce seedlings during water stress.Crossref | GoogleScholarGoogle Scholar |

Erdmann B, Wiedenroth EM (1986) Changes in the root system of wheat seedlings following root anaerobiosis II. Morphology and anatomy of evolution forms. Annals of Botany 58, 607–616.
Changes in the root system of wheat seedlings following root anaerobiosis II. Morphology and anatomy of evolution forms.Crossref | GoogleScholarGoogle Scholar |

Eugene WE (1998) Membrane lipids: what membrane physical properties are conserve during physiochemically-induced membrane restructuring? Integrative and Comparative Biology 38, 280–290.
Membrane lipids: what membrane physical properties are conserve during physiochemically-induced membrane restructuring?Crossref | GoogleScholarGoogle Scholar |

Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Current Opinion in Plant Biology 14, 296–302.
Salt stress signals shape the plant root.Crossref | GoogleScholarGoogle Scholar | 21511515PubMed |

Greenway H, Gibbs J (2003) Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and for energy consuming processes. Functional Plant Biology 30, 999–1036.
Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and for energy consuming processes.Crossref | GoogleScholarGoogle Scholar |

Hamrouni I, Salah HB, Marzouk B (2001) Effects of water-deficit on lipids of safflower aerial parts. Phytochemistry 58, 277–280.
Effects of water-deficit on lipids of safflower aerial parts.Crossref | GoogleScholarGoogle Scholar | 11551551PubMed |

Hansbro PM, Byard SJ, Bushby RJ, Turnbull PJH, Boden N, Saunders MR, Novelli R, Reid DG (1992) The conformational behaviour of phosphatidylinositol in model membranes: 2H-NMR studies. Biochimica et Biophysica Acta (BBA) – Biomembranes 1112, 187–196.
The conformational behaviour of phosphatidylinositol in model membranes: 2H-NMR studies. Crossref | GoogleScholarGoogle Scholar |

Härtel H, Lokstein H, Dörmann P, Grimm B, Benning C (1997) Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiology 115, 1175–1184.
Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 9390443PubMed |

Herzog M, Striker GG, Colmer TD, Pedersen O (2016) Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology. Plant, Cell & Environment 39, 1068–1086.
Mechanisms of waterlogging tolerance in wheat – a review of root and shoot physiology.Crossref | GoogleScholarGoogle Scholar |

Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611.
Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.Crossref | GoogleScholarGoogle Scholar |

Hölzl G, Witt S, Gaude N, Melzer M, Schottler MA, Dormann P (2009) The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiology 150, 1147–1159.
The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19403724PubMed |

Hossain MA, Uddin SN (2011) Mechanisms of waterlogging tolerance in wheat: morphological and metabolic adaptations under hypoxia or anoxia. Australian Journal of Crop Science 5, 1094–1101.

Larkindale J, Huang B (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide and ethylene. Journal of Plant Physiology 161, 405–413.
Thermotolerance and antioxidant systems in Agrostis stolonifera: involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide and ethylene.Crossref | GoogleScholarGoogle Scholar | 15128028PubMed |

Liu Z, Yan H, Wang K, Kuang T, Zhang J, Gui L, An X, Chang W (2004) Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution. Nature 428, 287–292.
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution.Crossref | GoogleScholarGoogle Scholar | 15029188PubMed |

Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040–1044.
Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II.Crossref | GoogleScholarGoogle Scholar | 16355230PubMed |

McLoughlin F, Testerink C (2013) Phosphatidic acid, a versatile water-stress signal in roots. Frontiers in Plant Science 4, 525
Phosphatidic acid, a versatile water-stress signal in roots.Crossref | GoogleScholarGoogle Scholar | 24391659PubMed |

Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends in Plant Science 16, 98–107.
Galactoglycerolipid metabolism under stress: a time for remodeling.Crossref | GoogleScholarGoogle Scholar | 21145779PubMed |

Muramatsu K, Masumizu T, Maitani Y, Hwang SH, Kohno M, Takayama K, Nagai T (2000) Electron spin resonance studies of dipalmitoylphosphatidylcholine liposomes containing soybean-derived sterylglucoside. Chemical & Pharmaceutical Bulletin 48, 610–613.
Electron spin resonance studies of dipalmitoylphosphatidylcholine liposomes containing soybean-derived sterylglucoside.Crossref | GoogleScholarGoogle Scholar |

Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8: a ubiquitin-like protein required for autophagosome formation mediates membrane tethering and hemifusion. Cell 130, 165–178.
Atg8: a ubiquitin-like protein required for autophagosome formation mediates membrane tethering and hemifusion.Crossref | GoogleScholarGoogle Scholar | 17632063PubMed |

Nguyen TN, Tuan PA, Mukherjee S, Ayele BT (2018) Hormonal regulation in adventitious roots and during their emergence under waterlogged conditions in wheat (Triticum aestivum L.). Journal of Experimental Botany 69, 4065–4082.
Hormonal regulation in adventitious roots and during their emergence under waterlogged conditions in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 29788353PubMed |

Pan R, He D, Xu L, Zhou M, Li C, Wu C, Xu YH, Zhang WY (2019) Proteomic analysis reveals response of differential wheat (Triticum aestivum L.) genotypes to oxygen deficiency stress. BMC Genomics 20, 60
Proteomic analysis reveals response of differential wheat (Triticum aestivum L.) genotypes to oxygen deficiency stress.Crossref | GoogleScholarGoogle Scholar | 30658567PubMed |

Ponnamperuma FN (1972) The chemistry of submerged soils. Advances in Agronomy 24, 29–96.
The chemistry of submerged soils.Crossref | GoogleScholarGoogle Scholar |

Quartacci MF, Pinzino C, Sgherri C, Navari-Izzo F (1995) Lipid composition and protein dynamics in thylakoids of two wheat cultivars differently sensitive to drought. Plant Physiology 108, 191–197.
Lipid composition and protein dynamics in thylakoids of two wheat cultivars differently sensitive to drought.Crossref | GoogleScholarGoogle Scholar | 12228463PubMed |

Repellin A, Pham TAT, Tashakorie A, Sahsah Y, Daniel C, Zuilyfodil Y (1997) Leaf membrane lipids and drought tolerance in young coconut palms (Cocos nucifera L.). European Journal of Agronomy 6, 25–33.
Leaf membrane lipids and drought tolerance in young coconut palms (Cocos nucifera L.).Crossref | GoogleScholarGoogle Scholar |

Sakurai I, Hagio M, Gombos Z, Tyystjarvi T, Pakkarinen V, Aro E, Wada H (2003) Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. Plant Physiology 133, 1376–1384.
Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery.Crossref | GoogleScholarGoogle Scholar | 14551333PubMed |

Sakurai I, Mizusawa N, Ohashi S, Kobayashi M, Wada H (2007) Effects of the lack of phosphatidylglycerol on the donor side of Photosystem II. Plant Physiology 144, 1336–1346.
Effects of the lack of phosphatidylglycerol on the donor side of Photosystem II.Crossref | GoogleScholarGoogle Scholar | 17513482PubMed |

Shipley GG, Green JP, Nichols BW (1973) The phase behavior of monogalactosyl digalactosyl and sulphoquinovosyl diglycerides. Biochimica et Biophysica Acta 311, 531–544.
The phase behavior of monogalactosyl digalactosyl and sulphoquinovosyl diglycerides.Crossref | GoogleScholarGoogle Scholar | 4738152PubMed |

Sundgren TK, Uhlen AK, Lillemo M, Briese C, Wojciechowski T (2018) Rapid seedling establishment and a narrow root stele promotes waterlogging tolerance in spring wheat. Journal of Plant Physiology 227, 45–55.
Rapid seedling establishment and a narrow root stele promotes waterlogging tolerance in spring wheat.Crossref | GoogleScholarGoogle Scholar | 29735176PubMed |

Süss KH (1986) Biosynthetic cause of in vivo acquired thermotolerance of photosynthetic light reactions and metabolic responses of chloroplasts to heat stress. Plant Physiology 81, 192–199.
Biosynthetic cause of in vivo acquired thermotolerance of photosynthetic light reactions and metabolic responses of chloroplasts to heat stress.Crossref | GoogleScholarGoogle Scholar | 16664773PubMed |

Tyanova S, Temu T, Cox J (2016) The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nature Protocols 11, 2301–2319.
The MaxQuant computational platform for mass spectrometry-based shotgun proteomics.Crossref | GoogleScholarGoogle Scholar | 27809316PubMed |

Vikström S, Li L, Karlsson OP, Wieslander A (1999) Key role of the diglucosyldiacylglycerol synthase for the nonbilayer–bilayer lipid balance of Acholeplasma laidlawii membranes. Biochemistry 38, 5511–5520.
Key role of the diglucosyldiacylglycerol synthase for the nonbilayer–bilayer lipid balance of Acholeplasma laidlawii membranes.Crossref | GoogleScholarGoogle Scholar | 10220338PubMed |

Villareal RL, Sayre K, Banuelos O, Mujeebkazi A (2001) Registration of four synthetic hexaploid wheat Triticum turgidum/Aegilops tauschii germplasm lines tolerant to waterlogging. Crop Science 41, 274
Registration of four synthetic hexaploid wheat Triticum turgidum/Aegilops tauschii germplasm lines tolerant to waterlogging.Crossref | GoogleScholarGoogle Scholar |

Vu HS, Pamela T, Galeva NA, Ratnesh C, Roth MR, Williams TD, Wang X, Shah J, Welti R (2011) Direct infusion mass spectrometry of oxylipin-containing Arabidopsis membrane lipids reveals varied patterns in different stress responses. Plant Physiology 158, 324–339.
Direct infusion mass spectrometry of oxylipin-containing Arabidopsis membrane lipids reveals varied patterns in different stress responses.Crossref | GoogleScholarGoogle Scholar | 22086419PubMed |

Vu HS, Shiva S, Roth MR, Tamura P, Zheng L, Li M, Sarowar S, Honey S, McEllhiney D, Hinkes P, Seib L, Williams TD, Gadbury G, Wang X, Shah J, Welti R (2014) Lipid changes after leaf wounding in Arabidopsis thaliana: expanded lipidomic data form the basis for lipid co-occurrence analysis. The Plant Journal 80, 728–743.
Lipid changes after leaf wounding in Arabidopsis thaliana: expanded lipidomic data form the basis for lipid co-occurrence analysis.Crossref | GoogleScholarGoogle Scholar | 25200898PubMed |

Wada H, Murata N (1998) Membrane lipids in cyanobacteria. In ‘Lipids in photosynthesis: structure function and genetics’. (Eds P-A Siegenthaler, N Murata) pp. 65–81. (Kluwer Academic Publishers: Dordrecht, The Netherlands).

Wang X, Wang C, Sang Y, Qin C, Welti R (2002) Networking of phospholipases in plant signal transduction. Physiologia Plantarum 115, 331–335.
Networking of phospholipases in plant signal transduction.Crossref | GoogleScholarGoogle Scholar | 12081524PubMed |

Wang M, Shen Y, Tao F, Yang S, Li W (2016) Submergence induced changes of molecular species in membrane lipids in Arabidopsis thaliana. Plant Diversity 38, 156–162.
Submergence induced changes of molecular species in membrane lipids in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 30159460PubMed |

Webb MS, Green BR (1991) Biochemical and biophysical properties of thylakoid acyl lipids. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1060, 133–158.
Biochemical and biophysical properties of thylakoid acyl lipids. Crossref | GoogleScholarGoogle Scholar |

Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. The Journal of Biological Chemistry 277, 31994–32002.
Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12077151PubMed |

Welti R, Shah J, Li W, Li M, Chen J, Burke JJ, Fauconnier M-L, Chapman K, Chye M-L, Wang X (2007) Plant lipidomics: discerning biological function by profiling plant complex lipids using mass spectrometry. Frontiers in Bioscience 12, 2494–2506.
Plant lipidomics: discerning biological function by profiling plant complex lipids using mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 17127258PubMed |

Xiao S, Gao W, Chen Q, Chan SW, Zheng S-X, Ma J, Wang M, Welti R, Chye M-L (2010) Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence. The Plant Cell 22, 1463–1482.
Overexpression of Arabidopsis acyl-CoA binding protein ACBP3 promotes starvation-induced and age-dependent leaf senescence.Crossref | GoogleScholarGoogle Scholar | 20442372PubMed |

Xie LJ, Yu L, Chen QF, Wang FZ, Huang L, Xia FN, Zhu T-R, Wu J-X, 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 |

Yang P, Li X, Wang X, Chen H, Chen F, Shen S (2007) Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 7, 3358–3368.
Proteomic analysis of rice (Oryza sativa) seeds during germination.Crossref | GoogleScholarGoogle Scholar | 17849412PubMed |

Yao HY, Xue HW (2018) Phosphatidic acid (PA) plays key roles regulating plant development and stress responses. Journal of Integrative Plant Biology 60, 851–863.
Phosphatidic acid (PA) plays key roles regulating plant development and stress responses.Crossref | GoogleScholarGoogle Scholar | 29660254PubMed |

Yuan LB, Dai YS, Xie LJ, Yu LJ, Zhou Y, Lai YX, Yang YC, Xu L, Chen QF, Xiao S (2017) Jasmonate regulates plant responses to reoxygenation through activation of antioxidant synthesis. Plant Physiology 173, 1864–1880.
Jasmonate regulates plant responses to reoxygenation through activation of antioxidant synthesis.Crossref | GoogleScholarGoogle Scholar | 28082717PubMed |

Zeng F, Konnerup D, Shabala L, Zhou M, Colmer TD, Zhang G, Shabala S (2014) Linking oxygen availability with membrane potential maintenance and K+ retention of barley roots: implications for waterlogging stress tolerance. Plant, Cell & Environment 37, 2325–2338.
Linking oxygen availability with membrane potential maintenance and K+ retention of barley roots: implications for waterlogging stress tolerance.Crossref | GoogleScholarGoogle Scholar |

Zheng G, Tian B, Zhang F, Tao F, Li W (2011) Plant adaptation to frequent alterations between high and low temperatures: remodeling of membrane lipids and maintenance of unsaturation levels. Plant, Cell & Environment 34, 1431–1442.
Plant adaptation to frequent alterations between high and low temperatures: remodeling of membrane lipids and maintenance of unsaturation levels.Crossref | GoogleScholarGoogle Scholar |