Plant Sec14-like Phosphatidylinositol Transfer Proteins: Diverse Structures and Multi-Functions
MAO Hua-Ying, SU Ya-Chun, QUE You-Xiong*
Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry University / Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, China
Abstract：Sec14p, one of the phosphatidylinositol transfer proteins (PITPs), is originally found in Saccharomyces cerevisiae that has the functions of transporting phosphatidylinositol (phosphatidylinositol, PI) and phosphatidylcholine (phosphatidylcholine, PC) and is widely present in eukaryotes. Plant Sec14-like phosphatidylinositol transfer protein has high sequence homology with yeast Sec14p. In recent years, with the development of molecular biology and lipid genomics, more and more plant phosphatidylinositol transfer proteins have been excavated. In plants, the structure of those proteins has evolved from the original Sec14p domain to integrate with the membrane-localized Nlj16 domain and the vesicle transport Golgi dynamics (GOLD) domain, resulting in multi-functions, such as osmotic regulation, cell polarity growth, nodule development, protein transport, plant immune regulation and virus interactions. This paper reviews the differences and associations of structures and functions among Sec14-only proteins, Sec14-nodulin proteins and Sec14-GOLD proteins in plants, and highlights their multiple biological functions.
毛花英, 苏亚春, 阙友雄. 植物Sec14-like磷脂酰肌醇转运蛋白：变化的结构和多样的功能[J]. 农业生物技术学报, 2019, 27(2): 348-360.
MAO Hua-Ying, SU Ya-Chun, QUE You-Xiong. Plant Sec14-like Phosphatidylinositol Transfer Proteins: Diverse Structures and Multi-Functions. 农业生物技术学报, 2019, 27(2): 348-360.
[1] 董静. 2009. 棉花磷脂酰肌醇转运蛋白同源基因的克隆与功能分析[D]. 硕士学位论文, 西南大学, 导师: 肖月华. pp. 1-49. (Dong J.2009. Cloning and functional analysis of phosphatidylinositol transfer protein (PITP) homologous genes in cotton (Gossypium hirsutum L.)[D]. Thesis for M.S., Southwest University, Supervisor: Xiao Y H. pp. 1-49.) [2] 毛花英, 刘峰, 苏炜华, 等. 2018. 甘蔗磷脂酰肌醇转运蛋白基因ScSEC14响应干旱和盐胁迫[J]. 作物学报, 44(6): 824-835. (Mao H Y, Liu F, Su W H, et al.2018. A sugarcane phosphatidylinositol transfer protein gene ScSEC14 responds to drought and salt stresses[J]. Acta Agronomica Sinica, 44(6): 824-835.) [3] 莫萍丽. 2006. 拟南芥两个在花中特异表达的Sec14-like磷脂酰肌醇转移蛋白的分子生物学研究[D]. 博士学位论文, 厦门大学, 导师: 严重玲. pp. 1-90. (Mo P L.2006. Molecular biology of two Sec14-like phosphatidylinositol transfer proteins specifically expressed in Arabidopsis flowers[D]. Thesis for Ph.D., Xiamen University, Supervisor: Yan C L. pp. 1-90.) [4] 苏世超, 唐益苗, 徐磊, 等. 2016. 普通小麦TaSEC14p-5基因的克隆及表达分析[J]. 农业生物技术学报, 24(8): 1129-37. (Su S C, Tang Y M, Xu L, et al.2016. Cloning and expression analysis of TaSEC14p-5 gene from wheat (Triticum aestivum)[J]. Journal of Agricultural Biotechnology, 24(8): 1129-1137.) [5] Aitken J F, Van G H, Temkin M, et al.1990. The gene encoding the phosphatidylinositol transfer protein is essential for cell growth[J]. Journal of Biological Chemistry, 265(8): 4711-4717. [6] Anantharaman V, Aravind L.2002. The GOLD domain, a novel protein module involved in Golgi function and secretion[J]. Genome Biology, 3(5): 1-7. [7] Balla T.2013. Phosphoinositides: Tiny lipids with giant impact on cell regulation[J]. Physiological Reviews, 93(3): 1019-1137. [8] Berridge M J.1993. Inositol trisphosphate and calcium signalling[J]. Nature, 361(6410): 315-325. [9] Boevink P, Oparka K J.2005. Virus-host interactions during movement processes[J]. Plant Physiology, 138(4): 1815-1821. [10] Böhme K, Li Y, Charlot F, et al.2004. The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth[J]. Plant Journal, 40(5): 686-698. [11] Cowan A K.2006. Phospholipids as plant growth regulators[J]. Plant Growth Regulation, 48(2): 97-109. [12] Dangl J L, Jones J D.2001. Plant pathogens and integrated defence responses to infection[J]. Nature, 411(6839): 826-833. [13] de Mezer M, Turska-Taraska A, Kaczmarek Z, et al.2014. Differential physiological and molecular response of barley genotypes to water deficit[J]. Plant Physiology and Biochemistry, 80: 234-248. [14] Deng Z, Zhang X, Tang W, et al.2007. A proteomics study of brassinosteroid response in Arabidopsis[J]. Molecular & Cellular Proteomics Mcp, 6(12): 2058-2071. [15] Dove S K, Cooke F T, Douglas M R, et al.1997. Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis[J]. Nature, 390(6656): 187-192. [16] Gao X Q, Zhang X S.2012. Metabolism and roles of phosphatidylinositol 3-phosphate in pollen development and pollen tube growth in Arabidopsis[J]. Plant Signaling & Behavior, 7(2): 165-169. [17] Ghosh R, Bankaitis V A.2011. Phosphatidylinositol transfer proteins: Negotiating the regulatory interface between lipid metabolism and lipid signaling in diverse cellular processes[J]. Biofactors, 37(4): 290-308. [18] Ghosh R, de Campos M K, Huang J, et al.2015. Sec14-nodulin proteins and the patterning of phosphoinositide landmarks for developmental control of membrane morphogenesis[J]. Molecular Biology of the Cell, 26(9): 1764-1781. [19] Holt M R, Koffer A.2001. Cell motility: Proline-rich proteins promote protrusions[J]. Trends in Cell Biology, 11(1): 38-46. [20] Hou Q, Ufer G, Bartels D.2015. Lipid signalling in plant responses to abiotic stress[J]. Plant Cell & Environment, 39(5): 1029-1048. [21] Huang J, Ghosh R, Tripathi A, et al.2016. Two-ligand priming mechanism for potentiated phosphoinositide synthesis is an evolutionarily conserved feature of Sec14-like phosphatidylinositol and phosphatidylcholine exchange proteins[J]. Molecular Biology of the Cell, 27(14): 2317-2330. [22] Huang J, Kim C M, Xuan Y H, et al.2013. OsSNDP1, a Sec14-nodulin domain-containing protein, plays a critical role in root hair elongation in rice[J]. Plant Molecular Biology, 82(1-2): 39-50. [23] Janmey P A.1994. Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly[J]. Annual Review of Physiology, 56(1): 169-191. [24] Jones J D, Dangl J L.2006. The plant immune system[J]. Nature, 444(7117): 323-329. [25] Joyard J, Maréchal E, Miège C, et al.1998. Structure, distribution and biosynthesis of glycerolipids from higher plant chloroplasts. lipids in photosynthesis: Structure, function and genetics[M]. Springer, Netherlands, pp. 21-52. [26] Kammen A V.1984. Suggested nomenclature for plant genes involved in nodulation and symbiosis[J]. Plant Molecular Biology Reporter, 2(2): 43-45. [27] Kapranov P, Routt S M, Bankaitis V A, et al.2001. Nodule-specific regulation of phosphatidylinositol transfer protein expression in Lotus japonicus[J]. Plant Cell, 13(6): 1369-1382. [28] Kapranov P, de Bruijn F J, Szczyglowski K.1997. Novel, highly expressed late nodulin gene (LjNOD16) from Lotus japonicus[J]. Plant Physiology, 113(4): 1081-1090. [29] Kearns M A, Monks D E, Fang M, et al.1998. Novel developmentally regulated phosphoinositide binding proteins from soybean whose expression bypasses the requirement for an essential phosphatidylinositol transfer protein in yeast[J]. Embo Journal, 17(14): 4004-4017. [30] Kiba A, Nakano M, Vincent-Pope P, et al.2012. A novel Sec14 phospholipid transfer protein from Nicotiana benthamiana is up-regulated in response to Ralstonia solanacearum infection, pathogen associated molecular patterns and effector molecules and involved in plant immunity[J]. Journal of Plant Physiology, 169(10): 1017-1022. [31] Kiba A, Galis I, Hojo Y, et al.2014. SEC14 phospholipid transfer protein is involved in lipid signaling-mediated plant immune responses in Nicotiana benthamiana[J]. PLoS One, 9(5): e98150. [32] Kiełbowiczmatuk A, Banachowicz E, Turska-Tarska A, et al.2016. Expression and characterization of a barley phosphatidylinositol transfer protein structurally homologous to the yeast Sec14p protein[J]. Plant Science, 246: 98-111. [33] König S, Ischebeck T, Lerche J, et al.2008. Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants[J]. Biochemical Journal, 415(3): 387-399. [34] Kouchi, Hiroshi.1995. Symbiotic Nitrogen Fixation[J]. Plant Cell, 7(7): 869-885. [35] Lee Y, Kim Y, Jeon B, et al.2007. Phosphatidylinositol 4,5-bisphosphate is important for stomatal opening[J]. Plant Journal for Cell & Molecular Biology, 52(5): 803-816. [36] Mcreynolds L J, Luna E J.2004. Patellin1, a novel Sec14-like protein, localizes to the cell plate and binds phosphoinositides[J]. Plant Physiology, 136(2): 3080-3094. [37] Meijer H J, Berrie C P, Iurisci C, et al.2001. Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress[J]. Biochemical Journal, 360(2): 491-498. [38] Michell R H.2008. Inositol derivatives: Evolution and functions[J]. Nature Reviews Molecular Cell Biology, 9(2): 151-161. [39] Michell R H, Heath V L, Lemmon M A, et al.2006. Phosphatidylinositol 3,5-bisphosphate: Metabolism and cellular functions[J]. Trends in Biochemical Sciences, 31(1): 52-63. [40] Mo P, Zhu Y, Liu X, et al.2007. Identification of two phosphatidylinositol/phosphatidylcholine transfer protein genes that are predominately transcribed in the flowers of Arabidopsis thaliana[J]. Journal of Plant Physiology, 164(4): 478-486. [41] Monks D E, Aghoram K, Courtney P D, et al.2001. Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinases SPK1 and SPK2[J]. Plant Cell, 13(5): 1205-1219. [42] Mousley C J, Tyeryar K R, Vincentpope P, et al.2007. The Sec14-superfamily and the regulatory interface between phospholipid metabolism and membrane trafficking[J]. BBA-Molecular and Cell Biology of Lipids, 1771(6): 727-736. [43] Munnik T, Irvine R F, Musgrave A.1998. Phospholipid signalling in plants[J]. Biochim Biophysica Acta, 1389(3): 222-272. [44] Munnik T, Vermeer J E.2010. Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants[J]. Plant Cell & Environment, 33(4): 655-669. [45] Munnik T, Testerink C.2009. Plant phospholipid signaling: “in a nutshell”[J]. Journal of Lipid Research, 50 Suppl(Supplement): S260. [46] Nakamura Y.2017. Plant phospholipid diversity: Emerging functions in metabolism and protein-lipid interactions[J]. Trends in Plant Science, 22(12): 1027-1040. [47] Oldroyd G E.2013. Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants[J]. Nature Reviews Microbiology, 11(4): 252-263. [48] Peiro A, Izquierdogarcia A C, Sancheznavarro J A, et al.2014. Patellins 3 and 6, two members of the Plant Patellin family, interact with the movement protein of Alfalfa mosaic virus and interfere with viral movement[J]. Molecular Plant Pathology, 15(9): 881-891. [49] Peterman T K, Sequeira A S, Samia J A, et al.2006. Molecular cloning and characterization of patellin1, a novel sec14-related protein, from zucchini (Cucurbita pepo)[J]. Journal of Plant Physiology, 163(11): 1150-1158. [50] Phillips S E, Vincent P, Rizzieri K E, et al.2006. The diverse biological functions of phosphatidylinositol transfer proteins in eukaryotes[J]. Critical Reviews in Biochemistry and Molecular Biology, 41(1): 21-49. [51] Pieterse M J, Leon-Reyes A, Ent S V D, et al.2009. Networking by small-molecule hormones in plant immunity[J]. Nature Chemical Biology, 5(5): 308-316. [52] Saito K, Tautz L, Mustelin T.2007. The lipid-binding SEC 14 domain[J]. BBA-Molecular and Cell Biology of Lipids, 1771(6): 719-726. [53] Sha A, Qi Y, Shan Z, et al.2016. Identifying patellin-like genes in Glycine max and elucidating their response to phosphorus starvation[J]. Acta Physiologiae Plantarum, 38(6): 138. [54] Sha B, Phillips S E, Bankaitis V A, et al.1998. Crystal structure of the Saccharomyces cerevisiae phosphatidylinositol-transfer protein[J]. Nature, 391(6666): 506-510. [55] Szumlanski A L, Nielsen E.2010. Phosphatidylinositol 4-phosphate is required for tip growth in Arabidopsis thaliana[M]. Springer, Berlin, Heidelberg. pp. 65-77. [56] Takamasa S, Chiyuki M, Shingo N, et al.2016. Identification of phosphoinositide-binding protein PATELLIN2 as a substrate of Arabidopsis MPK4 MAP kinase during septum formation in cytokinesis[J]. Plant & Cell Physiology, 57(8): 1744-1755. [57] Van Paridon P A, Visser A J, Wirtz K W.1987. Binding of phospholipids to the phosphatidylinositol transfer protein from bovine brain as studied by steady-state and time-resolved fluorescence spectroscopy[J]. Biochimica et Biophysica Acta, 898(2): 172-180. [58] Vermeer J E M, Leeuwen W V, Tobeña-Santamaria R, et al.2006. Visualization of PtdIns3P dynamics in living plant cells[J]. Plant Journal, 47(5): 687-700. [59] Vincent P, Chua M, Nogue F, et al.2005. A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs[J]. Journal of Cell Biology, 168(5): 801-812. [60] Wang X, Shan X, Xue C, et al.2016. Isolation and functional characterization of a cold responsive phosphatidylinositol transfer-associated protein, ZmSEC14p, from maize (Zea may L.)[J]. Plant Cell Reports, 35(8): 1671-1686. [61] Welti R, Li W, Li M, et al.2002. Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis[J]. Journal of Biological Chemistry, 277(35): 31994-32002. [62] Wimalasekera R, Pejchar P, Holk A, et al.2010. Plant phosphatidylcholine-hydrolyzing phospholipases C NPC3 and NPC4 with roles in root development and brassinolide signaling in Arabidopsis thaliana[J]. Molecular Plant, 03(3): 610-625. [63] Winter D, Vinegar B, Nahal H, et al.2007. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets[J]. Plos One, 2(8): e718. [64] Wu C, Tan L, Van H M, et al.2017. Arabidopsis EXO70A1 recruits Patellin3 to the cell membrane independent of its role as an exocyst subunit[J]. Journal of Integrative Plant Biology, 59(12): 851-865. [65] Zipfel C.2008. Pattern-recognition receptors in plant innate immunity[J]. Current Opinion in Immunology, 20(1): 10-16.
