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Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize

Lei Gao,  Haifang Jiang,  Minze Li,  Danfeng Wang,  Hongtao Xiang,  Rong Zeng,  Limei Chen,  Xiaoyan Zhang,  Jianru Zuo,  Shuhua Yang,  Yiting Shi

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文章导航 > Journal of Genetics and Genomics  > 2023 > 优先出版
Lei Gao, Haifang Jiang, Minze Li, Danfeng Wang, Hongtao Xiang, Rong Zeng, Limei Chen, Xiaoyan Zhang, Jianru Zuo, Shuhua Yang, Yiting Shi. Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize[J]. 遗传学报. doi: 10.1016/j.jgg.2023.07.004
引用本文: Lei Gao, Haifang Jiang, Minze Li, Danfeng Wang, Hongtao Xiang, Rong Zeng, Limei Chen, Xiaoyan Zhang, Jianru Zuo, Shuhua Yang, Yiting Shi. Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize[J]. 遗传学报. doi: 10.1016/j.jgg.2023.07.004
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Lei Gao, Haifang Jiang, Minze Li, Danfeng Wang, Hongtao Xiang, Rong Zeng, Limei Chen, Xiaoyan Zhang, Jianru Zuo, Shuhua Yang, Yiting Shi. Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2023.07.004
Citation: Lei Gao, Haifang Jiang, Minze Li, Danfeng Wang, Hongtao Xiang, Rong Zeng, Limei Chen, Xiaoyan Zhang, Jianru Zuo, Shuhua Yang, Yiting Shi. Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2023.07.004
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Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize

doi: 10.1016/j.jgg.2023.07.004

  • a State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, Frontiers Science Center for Molecular Design Breeding, Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing 100193, China;

  • b State Key Laboratory of Wheat & Maize Crop Science, College of Life Sciences, Henan Agricultural University, Zhengzhou, Henan 450002, China;

  • c State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China. University of Chinese Academy of Sciences, Beijing 100101, China;

  • d Suihua Branch of Heilongjiang Academy of Agricultural Machinery Sciences, Suihua, Heilongjiang 152052, China

基金项目: 

The transgenic seeds of maize were created by Center for Crop Functional Genomics and Molecular Breeding of China Agricultural University. This work was supported by grants from the National Natural Science Foundation of China (32022008, 32272025, and 31921001), the Fundamental Research Funds for the Central Universities (2022TC137), and the Chinese Universities Scientific Fund (2023TC019).

详细信息
    通讯作者:

    Yiting Shi,Email:shiyiting@cau.edu.cn

Genetic and lipidomic analyses reveal the key role of lipid metabolism for cold tolerance in maize

  • a State Key Laboratory of Plant Environmental Resilience, College of Biological Sciences, Frontiers Science Center for Molecular Design Breeding, Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing 100193, China;

  • b State Key Laboratory of Wheat & Maize Crop Science, College of Life Sciences, Henan Agricultural University, Zhengzhou, Henan 450002, China;

  • c State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China. University of Chinese Academy of Sciences, Beijing 100101, China;

  • d Suihua Branch of Heilongjiang Academy of Agricultural Machinery Sciences, Suihua, Heilongjiang 152052, China

Funds: 

The transgenic seeds of maize were created by Center for Crop Functional Genomics and Molecular Breeding of China Agricultural University. This work was supported by grants from the National Natural Science Foundation of China (32022008, 32272025, and 31921001), the Fundamental Research Funds for the Central Universities (2022TC137), and the Chinese Universities Scientific Fund (2023TC019).

    摘要
  • 摘要: Lipid remodeling is crucial for cold tolerance in plants. However, the precise alternations of lipidomics during cold responses remains elusive, especially in maize (Zea mays L.). In addition, the key genes responsible for cold tolerance in maize lipid metabolism have not been identified. Here, we integrate lipidomic, transcriptomic, and genetic analysis to determine the profile of lipid remodeling caused by cold stress. We find that the homeostasis of cellular lipid metabolism is essential for maintaining cold tolerance of maize. Also, we detect 213 lipid species belonging to 14 major classes, covering phospholipids, glycerides, glycolipids, and free fatty acids. Various lipid metabolites undergo specific and selective alterations in response to cold stress, especially mono/di-unsaturated lysophosphatidic acid, lysophosphatidylcholine, phosphatidylcholine, and phosphatidylinositol, as well as polyunsaturated phosphatidic acid, monogalactosyldiacylglycerol, diacylglycerol, and triacylglycerol. In addition, we identify a subset of key enzymes, including ketoacyl-ACP synthase II, acyl-carrier protein 2, glycerol-3-phosphate acyltransferase, and stearoyl-ACP desaturase 2 involved in glycerolipid biosynthetic pathways are positive regulators of maize cold tolerance. These results reveal a comprehensive lipidomic profile during the cold response of maize and provide genetic resources for enhancing cold tolerance in crops.
    Abstract: Lipid remodeling is crucial for cold tolerance in plants. However, the precise alternations of lipidomics during cold responses remains elusive, especially in maize (Zea mays L.). In addition, the key genes responsible for cold tolerance in maize lipid metabolism have not been identified. Here, we integrate lipidomic, transcriptomic, and genetic analysis to determine the profile of lipid remodeling caused by cold stress. We find that the homeostasis of cellular lipid metabolism is essential for maintaining cold tolerance of maize. Also, we detect 213 lipid species belonging to 14 major classes, covering phospholipids, glycerides, glycolipids, and free fatty acids. Various lipid metabolites undergo specific and selective alterations in response to cold stress, especially mono/di-unsaturated lysophosphatidic acid, lysophosphatidylcholine, phosphatidylcholine, and phosphatidylinositol, as well as polyunsaturated phosphatidic acid, monogalactosyldiacylglycerol, diacylglycerol, and triacylglycerol. In addition, we identify a subset of key enzymes, including ketoacyl-ACP synthase II, acyl-carrier protein 2, glycerol-3-phosphate acyltransferase, and stearoyl-ACP desaturase 2 involved in glycerolipid biosynthetic pathways are positive regulators of maize cold tolerance. These results reveal a comprehensive lipidomic profile during the cold response of maize and provide genetic resources for enhancing cold tolerance in crops.
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    • 参考文献(64)
  • Allen, D.J., Ort, D.R., 2001. Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci. 6, 36-42.
    Arisz, S.A., Testerink, C., Munnik, T., 2009. Plant PA signaling via diacylglycerol kinase. Biochim.
    Biophys. Acta. 1791, 869-875.
    Chapman, K.D., Dyer, J.M., Mullen, R.T., 2012. Biogenesis and functions of lipid droplets in plants:Thematic Review Series:Lipid droplet synthesis and metabolism:from yeast to man. J. Lipid Res. 53, 215-226.
    Chen, M.J., Thelen, J.J., 2013. ACYL-LIPID DESATURASE 2 is required for chilling and freezing tolerance in Arabidopsis. Plant Cell 25, 1430-1444.
    Chen, Q.F., Xiao, S., Chye, M.L., 2008. Overexpression of the Arabidopsis 10-kilodalton acyl-coenzyme A-binding protein ACBP6 enhances freezing tolerance. Plant Physiol. 148, 304-315.
    Chinnusamy, V., Zhu, J., Zhu, J.K., 2007. Cold stress regulation of gene expression in plants. Trends Plant Sci. 12, 444-451.
    Ding, Y., Shi, Y., Yang, S., 2019. Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol. 222, 1690-1704.
    Ding, Y., Yang, H., Wu, S., Fu, D., Li, M., Gong, Z., Yang, S., 2022. CPK28-NLP7 module integrates cold-induced Ca2+ signal and transcriptional reprogramming in Arabidopsis. Sci. Adv. 8, eabn7901.
    Gao, F., McDaniel, J., Chen, E.Y., Rockwell, H., Lynes, M.D., Tseng, Y.H., Sarangarajan, R., Narain, N.R., Kiebish, M.A., 2016. Monoacylglycerol analysis using MS/MS(ALL) quadruple time of flight mass spectrometry. Metabolites 6, 25.
    Gu, Y., He, L., Zhao, C., Wang, F., Yan, B., Gao, Y., Li, Z., Yang, K., Xu, J., 2017. Biochemical and transcriptional regulation of membrane lipid metabolism in maize leaves under Low temperature. Front Plant Sci. 8, 2053.
    Guy, C., Kaplan, F., Kopka, J., Selbig, J., Hincha, D.K., 2008. Metabolomics of temperature stress. Physiol. Plant 132, 220-235.
    Iba, K., 2002. Acclimative response to temperature stress in higher plants:approaches of gene engineering for temperature tolerance. Annu. Rev. Plant Biol. 53, 225-245.
    Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., Thomashow, M.F., 1998. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104-106.
    Jiang, H., Shi, Y., Liu, J., Li, Z., Fu, D., Wu, S., Li, M., Yang, Z., Shi, Y., Lai, J., et al., 2022. Natural polymorphism of ZmICE1 contributes to amino acid metabolism that impacts cold tolerance in maize. Nat. Plants 8, 1176-1190.
    Kaplan, F., Kopka, J., Sung, D.Y., Zhao, W., Popp, M., Porat, R., Guy, C.L., 2007. Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J. 50, 967-981.
    Kue Foka, I.C., Ketehouli, T., Zhou, Y., Li, X.-W., Wang, F.-W., Li, H., 2020. The emerging roles of diacylglycerol kinase (DGK) in plant stress tolerance, growth, and development. Agronomy 10, 1375.
    Lam, S.M., Shui, G.H., 2013. Lipidomics as a principal tool for advancing biomedical research. J. Genet. Genomics 40, 375-390.
    Lam, S.M., Tian, H., Shui, G., 2017. Lipidomics, an route to accurate quantitation. Biochim. Biophys. Acta. Mol. Cell Biol. Lipids 1862, 752-761.
    Lam, S.M., Tong, L., Duan, X., Petznick, A., Wenk, M.R., Shui, G., 2014. Extensive characterization of human tear fluid collected using different techniques unravels the presence of novel lipid amphiphiles. J. Lipid Res. 55, 289-298.
    Lee, H., Zhang, Z.J., 2014. Agrobacterium-mediated transformation of maize (Zea mays) immature embryos. Methods Mol. Biol. 1099, 273-280.
    Li-Beisson, Y., Shorrosh, B., Beisson, F., Andersson, M.X., Arondel, V., Bates, P.D., Baud, S., Bird, D., Debono, A., Durrett, T.P., et al., 2013. Acyl-lipid metabolism. Arabidopsis Book 11, e0161.
    Li, Q., Shen, W., Zheng, Q., Fowler, D.B., Zou, J., 2016. Adjustments of lipid pathways in plant adaptation to temperature stress. Plant Signal Behav. 11, e1058461.
    Li, Y.P., Shi, Y.T., Li, M.Z., Fu, D.Y., Wu, S.F., Li, J.G., Gong, Z.Z., Liu, H.T., Yang, S.H., 2021. The CRY2-COP1-HY5-BBX7/8 module regulates blue light-dependent cold acclimation in Arabidopsis. Plant Cell 33, 3555-3573.
    Li, Z.Y., Fu, D.Y., Wang, X., Zeng, R., Zhang, X., Tian, J.G., Zhang, S.S., Yang, X.H., Tian, F., Lai, J.S., et al., 2022. The transcription factor bZIP68 negatively regulates cold tolerance in maize. Plant Cell 34, 2833-2851.
    Liao, P., Chen, Q.F., Chye, M.L., 2014. Transgenic Arabidopsis flowers overexpressing acyl-CoA-binding protein ACBP6 are freezing tolerant. Plant Cell Physiol. 55, 1055-1071.
    Liu, N.J., Wang, N., Bao, J.J., Zhu, H.X., Wang, L.J., Chen, X.Y., 2020. Lipidomic analysis reveals the importance of GIPCs in Arabidopsis leaf extracellular vesicles. Mol. Plant 13, 1523-1532.
    Liu, X., Zhai, S., Zhao, Y., Sun, B., Liu, C., Yang, A., Zhang, J., 2013. Overexpression of the phosphatidylinositol synthase gene (ZmPIS) conferring drought stress tolerance by altering membrane lipid composition and increasing ABA synthesis in maize. Plant Cell Environ. 36, 1037-1055.
    Liu, Y., Su, Y., Wang, X.M., 2013. Phosphatidic acid-mediated signaling. Adv. Exp. Med. Biol. 991, 159-176.
    Lu, J.L., Lam, S.M., Wan, Q., Shi, L.X., Huo, Y.N., Chen, L.L., Tang, X.L., Li, B.W., Wu, X.Y., Peng, K., et al., 2019. High-coverage targeted lipidomics reveals novel serum lipid predictors and lipid pathway dysregulation antecedent to type 2 diabetes onset in normoglycemic chinese adults. Diabetes Care 42, 2117-2126.
    Ma, Y., Dai, X., Xu, Y., Luo, W., Zheng, X., Zeng, D., Pan, Y., Lin, X., Liu, H., Zhang, D., et al., 2015. COLD1 confers chilling tolerance in rice. Cell 160, 1209-1221.
    Meng, X., Liang, Z., Dai, X., Zhang, Y., Mahboub, S., Ngu, D.W., Roston, R.L., Schnable, J.C., 2021. Predicting transcriptional responses to cold stress across plant species. Proc. Natl. Acad. Sci. USA 118, e2026330118.
    Miquel, M., James, D., Jr., Dooner, H., Browse, J., 1993. Arabidopsis requires polyunsaturated lipids for low-temperature survival. Proc. Natl. Acad. Sci. U. S. A. 90, 6208-6212.
    Moellering, E.R., Muthan, B., Benning, C., 2010. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228.
    Mongrand, S., Bessoule, J.J., Cabantous, F., Cassagne, C., 1998. The C16:3/C18:3 fatty acid balance in photosynthetic tissues from 468 plant species. Phytochemistry 49, 1049-1064.
    Nishida, I., Murata, N., 1996. CHILLING SENSITIVITY IN PLANTS AND CYANOBACTERIA:The crucial contribution of membrane lipids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 541-568.
    Ohlrogge, J., Browse, J., 1995. Lipid Biosynthesis. Plant Cell 7, 957-970.
    Okuley, J., Lightner, J., Feldmann, K., Yadav, N., Lark, E., Browse, J., 1994. Arabidopsis FAD2 gene encodes the enzyme that is essential for polyunsaturated lipid-synthesis. Plant Cell 6, 147-158.
    Olate, E., Jimenez-Gomez, J.M., Holuigue, L., Salinas, J., 2018. NPR1 mediates a novel regulatory pathway in cold acclimation by interacting with HSFA1 factors. Nat. Plants 4, 811-823.
    Orvar, B.L., Sangwan, V., Omann, F., Dhindsa, R.S., 2000. Early steps in cold sensing by plant cells:the role of actin cytoskeleton and membrane fluidity. Plant J. 23, 785-794.
    Pearce, R.S., 2001. Plant freezing and damage. Ann. Bot. 87, 417-424.
    Peppino Margutti, M., Gaveglio, V.L., Reyna, M., Pasquare, S.J., Racagni, G.E., Villasuso, A.L., 2018. Differential phosphatidic acid metabolism in barley leaves and roots induced by chilling temperature. Plant Physiol. Biochem. 132, 174-182.
    Pranneshraj, V., Sangha, M.K., Djalovic, I., Miladinovic, J., Djanaguiraman, M., 2022. Lipidomics-Assisted GWAS (lGWAS) approach for improving high-temperature stress tolerance of crops. Int. J. Mol. Sci. 23, 9389.
    Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V., 2009. Cold signalling and cold acclimation in plants. Adv. Bot. Res. 49, 35-150.
    Shi, Y., Ding, Y., Yang, S., 2018. Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci. 23, 623-637.
    Shui, G.H., Guan, X.L., Low, C.P., Chua, G.H., Goh, J.S.Y., Yang, H.Y., Wenk, M.R., 2010. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry:application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol. Biosyst. 6, 1008-1017.
    Suzuki, S., Awai, K., Ishihara, A., Yamauchi, K., 2016. Cold temperature blocks thyroid hormone-induced changes in lipid and energy metabolism in the liver of Lithobates catesbeianus tadpoles. Cell Biosci. 6, 19.
    Tan, W.J., Yang, Y.C., Zhou, Y., Huang, L.P., Xu, L., Chen, Q.F., Yu, L.J., Xiao, S., 2018. DIACYLGLYCEROL ACYLTRANSFERASE and DIACYLGLYCEROL KINASE modulate triacylglycerol and phosphatidic acid production in the plant response to freezing stress. Plant Physiol. 177, 1303-1318.
    Testerink, C., Munnik, T., 2005. Phosphatidic acid:a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10, 368-375.
    Thomashow, M.F., 1999. Plant cold acclimation:Freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599.
    Uemura, M., Joseph, R.A., Steponkus, P.L., 1995. Cold acclimation of Arabidopsis thaliana (Effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol. 109, 15-30.
    Wang, P.P., Shen, L.K., Guo, J.H., Jing, W., Qu, Y., Li, W.Y., Bi, R.R., Xuan, W., Zhang, Q., Zhang, W.H., 2019. Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED2 auxin efflux transporter in response to salt stress. Plant Cell 31, 250-271.
    Wang, X., 2001. Plant phospholipases. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 211-231.
    Wang, X., Chapman, K.D., 2013. Lipid signaling in plants. Front. Plant Sci. 4, 216.
    Welti, R., Li, W., Li, M., Sang, Y., Biesiada, H., Zhou, H.E., Rajashekar, C.B., Williams, T.D., Wang, X., 2002. Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem. 277, 31994-32002.
    Xie, K., Wu, S., Li, Z., Zhou, Y., Zhang, D., Dong, Z., An, X., Zhu, T., Zhang, S., Liu, S., et al., 2018. Map-based cloning and characterization of Zea mays male sterility33 (ZmMs33) gene, encoding a glycerol-3-phosphate acyltransferase. Theor. Appl. Genet. 131, 1363-1378.
    Xing, H.L., Dong, L., Wang, Z.P., Zhang, H.Y., Han, C.Y., Liu, B., Wang, X.C., Chen, Q.J., 2014. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 14, 327.
    Zeng, R., Li, Z., Shi, Y., Fu, D., Yin, P., Cheng, J., Jiang, C., Yang, S., 2021. Natural variation in a type-A response regulator confers maize chilling tolerance. Nat Commun. 12, 4713.
    Zhang, H., Dong, J., Zhao, X., Zhang, Y., Ren, J., Xing, L., Jiang, C., Wang, X., Wang, J., Zhao, S., et al., 2019. Research progress in membrane lipid metabolism and molecular mechanism in peanut cold tolerance. Front Plant Sci. 10, 838.
    Zhang, H., Jiang, C., Ren, J., Dong, J., Shi, X., Zhao, X., Wang, X., Wang, J., Zhong, C., Zhao, S., et al., 2020. An advanced lipid metabolism system revealed by transcriptomic and lipidomic analyses plays a central role in peanut cold tolerance. Front Plant Sci. 11, 1110.
    Zhao, H., Ma, B., Duan, K.X., Li, X.K., Lu, X., Yin, C.C., Tao, J.J., Wei, W., Zhang, W.K., Xin, P.Y., et al., 2020. The GDSL lipase MHZ11 modulates ethylene signaling in rice roots. Plant Cell 32, 1626-1643.
    Zhao, X., Wei, Y., Zhang, J., Yang, L., Liu, X., Zhang, H., Shao, W., He, L., Li, Z., Zhang, Y., et al., 2021. Membrane lipids' metabolism and transcriptional regulation in maize roots under cold stress. Front Plant Sci. 12, 639132.
    Zheng, G., Li, L., Li, W., 2016. Glycerolipidome responses to freezing- and chilling-induced injuries:examples in Arabidopsis and rice. BMC Plant Biol. 16, 70.
    Zheng, G., Tian, B., Zhang, F., Tao, F., Li, W., 2011. Plant adaptation to frequent alterations between high and low temperatures:remodelling of membrane lipids and maintenance of unsaturation levels. Plant Cell Environ. 34, 1431-1442.
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  • 收稿日期:  2023-07-11
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