[an error occurred while processing this directive] [an error occurred while processing this directive]
[an error occurred while processing this directive]植物类囊体主要膜脂及其生物合成
†共同第一作者
收稿日期: 2023-03-02
录用日期: 2023-08-09
网络出版日期: 2023-09-25
基金资助
陕西省自然科学基础研究计划(2023-JC-QN-0245);西安市科技计划(22FWQY14)
The Major Membrane Lipids in Plant Thylakoids and Their Biosynthesis
†These authors contributed equally to this paper
Received date: 2023-03-02
Accepted date: 2023-08-09
Online published: 2023-09-25
叶绿体是绿色植物进行光合作用的主要场所, 类囊体是叶绿体中膜结构的主要成分。植物类囊体膜上分布着多种色素蛋白复合物和脂质。其中脂质成分约一半是糖脂质, 主要包括单半乳糖甘油二酯、双半乳糖甘油二酯和硫代异鼠李糖甘油二酯。磷脂在类囊体膜中的占比很小, 主要成分为磷脂酰甘油。光合作用相关的大多数色素蛋白复合物都镶嵌在排列规则的极性脂上, 这些膜脂对植物光合作用和生长发育至关重要。深入了解原核/真核生物类囊体膜中主要脂质的结构、功能及其生物合成, 有助于阐明光合作用光能及物质转化的调控机理, 为植物类囊体膜脂研究提供理论依据。
关键词: 生物合成; 双半乳糖甘油二酯; 单半乳糖甘油二酯; 磷脂酰甘油; 硫代异鼠李糖甘油二酯
刘潇潇 , 巩迪 , 高天鹏 , 殷俐娜 , 王仕稳 . 植物类囊体主要膜脂及其生物合成[J]. 植物学报, 2024 , 59(1) : 144 -155 . DOI: 10.11983/CBB23028
Chloroplast is the main place for photosynthesis of green plants, and thylakoid is the key component of the membrane structure in the chloroplast. Various protein complexes and lipids are distributed on the plant thylakoid membrane. About half of the lipid components are glycolipids, mainly including monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and sulfoquinovosyldiacylglycerol. The proportion of phospholipid in the membrane is very low, and the main phospholipid component is phosphatidylglycerol. Most protein complexes of photosynthesis are embedded in regularly arrranged polar lipids. These membrane lipids are essential for plant photosynthesis and growth. A comprehensive knowledge on the structure and function of the major lipids in thylakoid membranes in prokaryotes or eukaryotes and their biosynthesis will help our further study in understanding of the mechanism of photosynthesis light energy and substance conversion, and provide theoretical basis for the study of membrane lipids in plant thylakoids.
[1] | 匡廷云, 张其德, 郝迺斌, 林世青, 娄世庆, 李桐柱, 左宝玉 (1979). 叶绿体膜的结构与功能——(I)、叶绿体膜的结构、组成与光系统II功能的关系. 植物生理学报 5, 99-107. |
[2] | 李秋信, 迟伟, 季代丽 (2021). CURT1调控类囊体膜弯曲的研究进展. 植物学报 56, 462-469. |
[3] | 王俊斌, 许亦农 (2007). 单半乳糖甘油二酯缺失对茉莉酸生物合成的影响. 见: 2007中国植物生理学会全国学术会议论文摘要汇编. 石家庄: 中国植物生理学会. pp. 217. |
[4] | Andrews J, Mudd JB (1985). Phosphatidylglycerol synthesis in pea chloroplasts: pathway and localization. Plant Physiol 79, 259-265. |
[5] | Awai K, Maréchal E, Block MA, Brun D, Masuda T, Shimada H, Takamiya KI, Ohta H, Joyard J (2001). 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. Proc Natl Acad Sci USA 98, 10960-10965. |
[6] | 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. Plant J 33, 899-909. |
[7] | Benhassaine-Kesri G, Aid F, Demandre C, Kader JC, Mazliak P (2002). Drought stress affects chloroplast lipid metabolism in rape (Brassica napus) leaves. Physiol Plantarum 115, 221-227. |
[8] | Benning C (1998). Biosynthesis and function of the sulfolipid sulfoquinovosyl diacylglycerol. Annu Rev Plant Physiol Plant Mol Biol 49, 53-75. |
[9] | Benning C (2009). Mechanisms of lipid transport involved in organelle biogenesis in plant cells. Annu Rev Cell Dev Biol 25, 71-91. |
[10] | Benning C, Ohta H (2005). Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280, 2397-2400. |
[11] | Benson AA, Daniel H, Wiser R (1959). A sulfolipid in plants. Proc Natl Acad Sci USA 45, 1582-1587. |
[12] | Block MA, Dorne AJ, Joyard J, Douce R (1983). Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. II. Biochemical characterization. J Biol Chem 258, 13281-13286. |
[13] | Botté CY, Deligny M, Roccia A, Bonneau AL, Sa?dani N, Hardré H, Aci S, Yamaryo-Botté Y, Jouhet J, Dubots E, Loizeau K, Bastien O, Bréhélin L, Joyard J, Cintrat JC, Falconet D, Block MA, Rousseau B, Lopez R, Maréchal E (2011). Chemical inhibitors of monogalactosyldiacylglycerol synthases in Arabidopsis thaliana. Nat Chem Biol 7, 834-842. |
[14] | Carter HE, Mccluer RH, Slifer ED (1956). Lipids of wheat flour. I. Characterization of galactosylglycerol components. J Am Chem Soc 78, 3735-3738. |
[15] | Cook R, Lupette J, Benning C (2021). The role of chloroplast membrane lipid metabolism in plant environmental responses. Cells 10, 706. |
[16] | D?rmann P, Balbo I, Benning C (1999). Arabidopsis galactolipid biosynthesis and lipid trafficking mediated by DGD1. Science 284, 2181-2184. |
[17] | D?rmann P, Hoffmann-Benning S, Balbo I, Benning C (1995). Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyldiacylglycerol. Plant Cell 7, 1801-1810. |
[18] | Dorne AJ, Joyard J, Douce R (1990). Do thylakoids really contain phosphatidylcholine? Proc Natl Acad Sci USA 87, 71-74. |
[19] | Douce R (1974). Site of biosynthesis of galactolipids in spinach chloroplasts. Science 183, 852-853. |
[20] | 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. Photosynth Res 46, 287-293. |
[21] | Frentzen M (2004). Phosphatidylglycerol and sulfoquinovosyldiacylglycerol: anionic membrane lipids and phosphate regulation. Curr Opin Plant Biol 7, 270-276. |
[22] | Froehlich JE, Benning C, D?rmann P (2001). The digalactosyldiacylglycerol (DGDG) synthase DGD1 is inserted into the outer envelope membrane of chloroplasts in a manner independent of the general import pathway and does not depend on direct interaction with monogalactosyldiacylglycerol synthase for DGDG biosynthesis. J Biol Chem 276, 31806-31812. |
[23] | Gabruk M, Mysliwa-Kurdziel B, Kruk J (2017). MGDG, PG and SQDG regulate the activity of light-dependent protochlorophyllide oxidoreductase. Biochem J 474, 1307-1320. |
[24] | Gage DA, Huang ZH, Benning C (1992). Comparison of sulfoquinovosyl diacylglycerol from spinach and the purple bacterium Rhodobacter sphaeroides by fast atom bombardment tandem mass spectrometry. Lipids 27, 632-636. |
[25] | Guo JK, Zhang ZZ, Bi YR, Yang W, Xu YN, Zhang LX (2005). Decreased stability of photosystem I in dgd1 mutant of Arabidopsis thaliana. FEBS Lett 579, 3619-3624. |
[26] | Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009). Cyanobacterial photosystem II at 2.9-? resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16, 334-342. |
[27] | Hagio M, Sakurai I, Sato S, Kato T, Tabata S, Wada H (2002). Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. Plant Cell Physiol 43, 1456-1464. |
[28] | H?rtel H, D?rmann P, Benning C (2000). DGD1-independent biosynthesis of extraplastidic galactolipids after phosphate deprivation in Arabidopsis. Proc Natl Acad Sci USA 97, 10649-10654. |
[29] | H?rtel H, Lokstein H, D?rmann P, Grimm B, Benning C (1997). Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiol 115, 1175-1184. |
[30] | Heemskerk JW, Storz T, Schmidt RR, Heinz E (1990). Biosynthesis of digalactosyldiacylglycerol in plastids from 16:3 and 18:3 plants. Plant Physiol 93, 1286-1294. |
[31] | H?lzl G, Witt S, Kelly AA, Z?hringer U, Warnecke D, D?rmann P, Heinz E (2006). Functional differences between galactolipids and glucolipids revealed in photosynthesis of higher plants. Proc Natl Acad Sci USA 103, 7512-7517. |
[32] | Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008). Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54, 621-639. |
[33] | Jarvis P, D?rmann P, Peto CA, Lutes J, Benning C, Chory J (2000). Galactolipid deficiency and abnormal chloroplast development in the Arabidopsis MGD synthase 1 mutant. Proc Natl Acad Sci USA 97, 8175-8179. |
[34] | Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krau? N (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 ? resolution. Nature 411, 909-917. |
[35] | Kelly AA, D?rmann P (2002). DGD2, an Arabidopsis gene encoding a UDP-galactose-dependent digalactosyldiacylglycerol synthase is expressed during growth under phosphate-limiting conditions. J Biol Chem 277, 1166-1173. |
[36] | Kelly AA, Froehlich JE, D?rmann P (2003). Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15, 2694-2706. |
[37] | Kelly AA, Kalisch B, H?lzl G, Schulze S, Thiele J, Melzer M, Roston RL, Benning C, D?rmann P (2016). Synthesis and transfer of galactolipids in the chloroplast envelope membranes of Arabidopsis thaliana. Proc Natl Acad Sci USA 113, 10714-10719. |
[38] | Kobayashi K, Nakamura Y, Ohta H (2009). Type A and type B monogalactosyldiacylglycerol synthases are spatially and functionally separated in the plastids of higher plants. Plant Physiol Biochem 47, 518-525. |
[39] | Lee AG (2000). Membrane lipids: it’s only a phase. Curr Biol 10, R377-R380. |
[40] | Lim GH, Singhal R, Kachroo A, Kachroo P (2017). Fatty acid- and lipid-mediated signaling in plant defense. Annu Rev Phytopathol 55, 505-536. |
[41] | Lin YT, Chen LJ, Herrfurth C, Feussner I, Li HM (2016). Reduced biosynthesis of digalactosyldiacylglycerol, a major chloroplast membrane lipid, leads to oxylipin overproduction and phloem cap lignification in Arabidopsis. Plant Cell 28, 219-232. |
[42] | Liu ZF, Yan HC, Wang KB, Kuang TY, Zhang JP, Gui LL, An XM, Chang WR (2004). Crystal structure of spinach major light-harvesting complex at 2.72 ? resolution. Nature 428, 287-292. |
[43] | Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005). Towards complete cofactor arrangement in the 3.0 ? resolution structure of photosystem II. Nature 438, 1040-1044. |
[44] | Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2007). Lipids in photosystem II: interactions with protein and cofactors. Biochim Biophys Acta Bioener 1767, 509-519. |
[45] | Miège C, Maréchal E, Shimojima M, Awai K, Block MA, Ohta H, Takamiya KI, Douce R, Joyard J (1999). Biochemical and topological properties of type A MGDG synthase, a spinach chloroplast envelope enzyme catalyzing the synthesis of both prokaryotic and eukaryotic MGDG. Eur J Biochem 265, 990-1001. |
[46] | Minoda A, Sato N, Nozaki H, Okada K, Takahashi H, Sonoike K, Tsuzuki M (2002). Role of sulfoquinovosyl diacylglycerol for the maintenance of photosystem II in Chlamydomonas reinhardtii. Eur J Biochem 269, 2353-2358. |
[47] | Moellering ER, Benning C (2011). Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci 16, 98-107. |
[48] | Moellering ER, Muthan B, Benning C (2010). Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228. |
[49] | Moreau P, Bessoule JJ, Mongrand S, Testet E, Vincent P, Cassagne C (1998). Lipid trafficking in plant cells. Prog Lipid Res 37, 371-391. |
[50] | Müller F, Frentzen M (2001). Phosphatidylglycerophosphate synthases from Arabidopsis thaliana. FEBS Lett 509, 298-302. |
[51] | Murphy DJ (1982). The importance of non-planar bilayer regions in photosynthetic membranes and their stabilisation by galactolipids. FEBS Lett 150, 19-26. |
[52] | Riekhof WR, Sears BB, Benning C (2005). Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase BTA1Cr. Eukaryot Cell 4, 242-252. |
[53] | Rocha J, Sarkis J, Thomas A, Pitou L, Radzimanowski J, Audry M, Chazalet V, de Sanctis D, Palcic MM, Block MA, Girard-Egrot A, Maréchal E, Breton C (2016). Structural insights and membrane binding properties of MGD1, the major galactolipid synthase in plants. Plant J 85, 622-633. |
[54] | Sato N (2004). Roles of the acidic lipids sulfoquinovosyl diacylglycerol and phosphatidylglycerol in photosynthesis: their specificity and evolution. J Plant Res 117, 495-505. |
[55] | Sato N, Hagio M, Wada H, Tsuzuki M (2000). Requirement of phosphatidylglycerol for photosynthetic function in thylakoid membranes. Proc Natl Acad Sci USA 97, 10655-10660. |
[56] | Sato N, Sonoike K, Tsuzuki M, Kawaguchi A (1995a). Impaired photosystem II in a mutant of Chlamydomonas reinhardtii defective in sulfoquinovosyl diacylglycerol. Eur J Biochem 234, 16-23. |
[57] | Sato N, Tsuzuki M, Matsuda Y, Ehara T, Osafune T, Kawaguchi A (1995b). Isolation and characterization of mutants affected in lipid metabolism of Chlamydomonas reinhardtii. Eur J Biochem 230, 987-993. |
[58] | Schroda M (2020). Phosphoinositides regulate chloroplast processes. Proc Natl Acad Sci USA 117, 9154-9156. |
[59] | Shimojima M (2011). Biosynthesis and functions of the plant sulfolipid. Prog Lipid Res 50, 234-239. |
[60] | Shimojima M, Ohta H, Iwamatsu A, Masuda T, Shioi Y, Takamiya KI (1997). Cloning of the gene for monogalactosyldiacylglycerol synthase and its evolutionary origin. Proc Natl Acad Sci USA 94, 333-337. |
[61] | Standfuss J, Lamborghini M, Kühlbrandt W (2005). Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 ? resolution. EMBO J 24, 919-928. |
[62] | Steffen R, Kelly AA, Huyer J, D?rmann P, Renger G (2005). Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana wild type plants and mutants with genetically modified lipid content. Biochemistry 44, 3134-3142. |
[63] | Umena Y, Kawakami K, Shen JR, Kamiya N (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 ?. Nature 473, 55-60. |
[64] | Urzica EI, Vieler A, Hong-Hermesdorf A, Dudley Page M, Casero D, Gallaher SD, Kropat J, Pellegrini M, Benning C, Merchant SS (2013). Remodeling of membrane lipids in iron-starved Chlamydomonas. J Biol Chem 288, 30246-30258. |
[65] | Wada H, Murata N (2007). The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res 92, 205-215. |
[66] | Wang JB (2009). Monogalactosyldiacylglycerol deficiency affects jasmonic acid biosynthesis and defense responses to insect herbivores in Nicotiana tabacum. Plant Sci 176, 279-285. |
[67] | Wang SW, Uddin MI, Tanaka K, Yin LN, Shi ZH, Qi YH, Mano J, Matsui K, Shimomura N, Sakaki T, Deng XP, Zhang SQ (2014). Maintenance of chloroplast structure and function by overexpression of the rice MONOGALACTOSYLDIACYLGLYCEROL SYNTHASE gene leads to enhanced salt tolerance in tobacco. Plant Physiol 165, 1144-1155. |
[68] | Wang Z, Benning C (2012). Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochem Soc Trans 40, 457-463. |
[69] | Xu CC, Hartel H, Wada H, Hagio M, Yu B, Eakin C, Benning C (2002). The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129, 594-604. |
[70] | Xu CC, Yu B, Cornish AJ, Froehlich JE, Benning C (2006). Phosphatidylglycerol biosynthesis in chloroplasts of Arabidopsis mutants deficient in acyl-ACP glycerol-3- phosphate acyltransferase. Plant J 47, 296-309. |
[71] | Yu B, Benning C (2003). Anionic lipids are required for chloroplast structure and function in Arabidopsis. Plant J 36, 762-770. |
[72] | Yu B, Xu CC, Benning C (2002). Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99, 5732-5737. |
/
〈 | 〉 |