Biochemical and Transcriptional Regulation of Membrane Lipid Metabolism in Maize Leaves Under Low Temperature

Overview

Journal Front Plant Sci

Date 2017 Dec 19

PMID 29250095

Citations 25

Authors

Yingnan Gu

Lin He

Changjiang Zhao

Feng Wang

Bowei Yan

Yuqiao Gao

Zuotong Li

Kejun Yang

Jingyu Xu

Affiliations

Soon will be listed here.

Abstract

Membrane lipid modulation is one of the major strategies plants have developed for cold acclimation. In this study, a combined lipidomic and transcriptomic analysis was conducted, and the changes in glycerolipids contents and species, and transcriptional regulation of lipid metabolism in maize leaves under low temperature treatment (5°C) were investigated. The lipidomic analysis showed an increase in the phospholipid phosphatidic acid (PA) and a decrease in phosphatidylcholine (PC). And an increase in digalactosyldiacylglycerol and a decrease in monogalactosyldiacylglycerol of the galactolipid class. The results implied an enhanced turnover of PC to PA to serve as precursors for galactolipid synthesis under following low temperature treatment. The analysis of changes in abundance of various lipid molecular species suggested major alterations of different pathways of plastidic lipids synthesis in maize under cold treatment. The synchronous transcriptomic analysis revealed that genes involved in phospholipid and galactolipid synthesis pathways were significantly up-regulated, and a comprehensive gene-metabolite network was generated illustrating activated membrane lipids adjustment in maize leaves following cold treatment. This study will help to understand the regulation of glycerolipids metabolism at both biochemical and molecular biological levels in 18:3 plants and to decipher the roles played by lipid remodeling in cold response in major field crop maize.

Citing Articles

Rhythmic lipid and gene expression responses to chilling in panicoid grasses.

Kenchanmane Raju S, Zhang Y, Mahboub S, Ngu D, Qiu Y, Harmon F J Exp Bot. 2024; 75(18):5790-5804.

PMID: 38808657 PMC: 11427832. DOI: 10.1093/jxb/erae247.

Evaluation of Lipid Quality in Fruit: Utilizing Lipidomic Approaches for Assessing the Impact of Biotic Stress on Pecans ().

Zhou L, Zhang W, Li Q, Cui M, Shen D, Shu J Foods. 2024; 13(7).

PMID: 38611280 PMC: 11011906. DOI: 10.3390/foods13070974.

Abiotic Stress in Crop Production.

Kopecka R, Kameniarova M, Cerny M, Brzobohaty B, Novak J Int J Mol Sci. 2023; 24(7).

PMID: 37047573 PMC: 10095105. DOI: 10.3390/ijms24076603.

Physiological and Transcriptomic Analyses Revealed That Humic Acids Improve Low-Temperature Stress Tolerance in Zucchini ( L.) Seedlings.

Li H, Kong F, Tang T, Luo Y, Gao H, Xu J Plants (Basel). 2023; 12(3).

PMID: 36771631 PMC: 9921430. DOI: 10.3390/plants12030548.

Adaptive strategies of plants to conserve internal phosphorus under P deficient condition to improve P utilization efficiency.

Soumya P, Vengavasi K, Pandey R Physiol Mol Biol Plants. 2022; 28(11-12):1981-1993.

PMID: 36573147 PMC: 9789281. DOI: 10.1007/s12298-022-01255-8.

References

Li Q, Shen W, Zheng Q, Fowler D, Zou J . Adjustments of lipid pathways in plant adaptation to temperature stress. Plant Signal Behav. 2016; 11(1):e1058461. PMC: 4871642. DOI: 10.1080/15592324.2015.1058461. View

Harwood J . Strategies for coping with low environmental temperatures. Trends Biochem Sci. 1991; 16(4):126-7. DOI: 10.1016/0968-0004(91)90052-w. View

Craddock C, Adams N, Bryant F, Kurup S, Eastmond P . PHOSPHATIDIC ACID PHOSPHOHYDROLASE Regulates Phosphatidylcholine Biosynthesis in Arabidopsis by Phosphatidic Acid-Mediated Activation of CTP:PHOSPHOCHOLINE CYTIDYLYLTRANSFERASE Activity. Plant Cell. 2015; 27(4):1251-64. PMC: 4558698. DOI: 10.1105/tpc.15.00037. View

Brautigam A, Shrestha R, Whitten D, Wilkerson C, Carr K, Froehlich J . Low-coverage massively parallel pyrosequencing of cDNAs enables proteomics in non-model species: comparison of a species-specific database generated by pyrosequencing with databases from related species for proteome analysis of pea chloroplast.... J Biotechnol. 2008; 136(1-2):44-53. DOI: 10.1016/j.jbiotec.2008.02.007. View

Wang Z, Xu C, Benning C . TGD4 involved in endoplasmic reticulum-to-chloroplast lipid trafficking is a phosphatidic acid binding protein. Plant J. 2012; 70(4):614-23. DOI: 10.1111/j.1365-313X.2012.04900.x. View

Ohlrogge J, Browse J . Lipid biosynthesis. Plant Cell. 1995; 7(7):957-70. PMC: 160893. DOI: 10.1105/tpc.7.7.957. View

Troncoso-Ponce M, Cao X, Yang Z, Ohlrogge J . Lipid turnover during senescence. Plant Sci. 2013; 205-206:13-9. DOI: 10.1016/j.plantsci.2013.01.004. View

Nakamura Y, Koizumi R, Shui G, Shimojima M, Wenk M, Ito T . Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc Natl Acad Sci U S A. 2009; 106(49):20978-83. PMC: 2791602. DOI: 10.1073/pnas.0907173106. View

Moellering E, Benning C . Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci. 2010; 16(2):98-107. DOI: 10.1016/j.tplants.2010.11.004. View

10.

DeBolt S, Scheible W, Schrick K, Auer M, Beisson F, Bischoff V . Mutations in UDP-Glucose:sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol. 2009; 151(1):78-87. PMC: 2735980. DOI: 10.1104/pp.109.140582. View

11.

Cline K, Keegstra K . Galactosyltransferases involved in galactolipid biosynthesis are located in the outer membrane of pea chloroplast envelopes. Plant Physiol. 1983; 71(2):366-72. PMC: 1066039. DOI: 10.1104/pp.71.2.366. View

12.

Li Q, Zheng Q, Shen W, Cram D, Fowler D, Wei Y . Understanding the biochemical basis of temperature-induced lipid pathway adjustments in plants. Plant Cell. 2015; 27(1):86-103. PMC: 4330585. DOI: 10.1105/tpc.114.134338. View

13.

Eastmond P, Quettier A, Kroon J, Craddock C, Adams N, Slabas A . Phosphatidic acid phosphohydrolase 1 and 2 regulate phospholipid synthesis at the endoplasmic reticulum in Arabidopsis. Plant Cell. 2010; 22(8):2796-811. PMC: 2947160. DOI: 10.1105/tpc.109.071423. View

14.

Frentzen M, Heinz E, McKeon T, Stumpf P . Specificities and selectivities of glycerol-3-phosphate acyltransferase and monoacylglycerol-3-phosphate acyltransferase from pea and spinach chloroplasts. Eur J Biochem. 1983; 129(3):629-36. DOI: 10.1111/j.1432-1033.1983.tb07096.x. View

15.

Narayanan S, Prasad P, Welti R . Wheat leaf lipids during heat stress: II. Lipids experiencing coordinated metabolism are detected by analysis of lipid co-occurrence. Plant Cell Environ. 2015; 39(3):608-17. PMC: 5141584. DOI: 10.1111/pce.12648. View

16.

Zheng G, Li L, Li W . Glycerolipidome responses to freezing- and chilling-induced injuries: examples in Arabidopsis and rice. BMC Plant Biol. 2016; 16:70. PMC: 4802656. DOI: 10.1186/s12870-016-0758-8. View

17.

Pierrugues O, Brutesco C, Oshiro J, Gouy M, Deveaux Y, Carman G . Lipid phosphate phosphatases in Arabidopsis. Regulation of the AtLPP1 gene in response to stress. J Biol Chem. 2001; 276(23):20300-8. DOI: 10.1074/jbc.M009726200. View

18.

Murakami Y, Tsuyama M, Kobayashi Y, Kodama H, Iba K . Trienoic fatty acids and plant tolerance of high temperature. Science. 2000; 287(5452):476-9. DOI: 10.1126/science.287.5452.476. View

19.

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. PMC: 4444972. DOI: 10.1038/srep10533. View

20.

Lin Y, Chen L, Herrfurth C, Feussner I, Li H . Reduced Biosynthesis of Digalactosyldiacylglycerol, a Major Chloroplast Membrane Lipid, Leads to Oxylipin Overproduction and Phloem Cap Lignification in Arabidopsis. Plant Cell. 2016; 28(1):219-32. PMC: 4746690. DOI: 10.1105/tpc.15.01002. View