Review of advances in the study of plant ABCG transporters

doi:10.11686/cyxb2014415

Abstract

Abstract: The ATP-binding cassette (ABC) transporters are members of a protein superfamily that constitutes one of the largest protein families known in plants. The ABC subfamily G (ABCG) consists of a single ABC cassette in the amino terminal. ABCG includes both the half-size molecular transporter white-brown complex (WBC) and the full-size molecular transporter pleiotropic drug resistance (PDR). ABCG is made up of a wide variety of substances (including antibiotics, phytohormones, lignin monolignols, lipids and secondary metabolites) that are involved in many kinds of metabolic processes during the plant life cycle. This paper reviews recent advances in studies of the molecular structure and function of ABCG transporters. Research hotspots and future directions are also considered.

ZHANG Jing, CHEN Meng-Ci, MA Qing, WEI Li, WANG Suo-Min. Review of advances in the study of plant ABCG transporters[J]. Acta Prataculturae Sinica, 2015, 24(7): 180-188.

References

[1] Verrier P J, Bird D, Burla B, et al . Plant ABC proteins a unified nomenclature and updated inventory. Trends in Plant Science, 2008, 13: 151-159.
[2] Bairoch A. Prosite: a dictionary of sites and patterns in proteins. Nucleic Acids Research, 1992, 20: 2013-2018.
[3] Ewart G D, Cannell D, Cox G B, et al . Mutational analysis of the traffic ATPase (ABC) transporters involved in uptake of eye pigment precursors in Drosophila melanogaster , implications for structure-function relationships. Journal of Biological Chemistry, 1994, 269: 10370-10377.
[4] Tarr P T, Tarling E J, Bojanic D D, et al . Emerging new paradigms for ABCG transporters. Biochimica et Biophysica Acta-Molecular and Cell Biology of Lipids, 2009, 1791: 584-593.
[5] McFarlane H E, Shin J J, Bird D A, et al . Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. The Plant Cell, 2010, 22: 3066-3075.
[6] Jasinski M, Ducos E, Martinoia E, et al . The ATP-Binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis . Plant Physiology, 2003, 131: 1169-1177.
[7] Çaklr B, Klllçkaya O. Whole-Genome survey of the putative ATP-binding cassette transporter family genes in Vitis vinifera . PLOS One, 2013, 8: e78860.
[8] Sugiyama A, Shitan N, Sato S, et al . Genome-wide analysis of ATP-binding cassette (ABC) proteins in a model legume plant, Lotus japonicus : comparison with Arabidopsis ABC protein family. DNA Research, 2006, 13: 205-228.
[9] Jasinski M, Banasiak J, Radom M, et al . Full-size ABC transporters from the ABCG subfamily in Medicago truncatula . Molecular Plant Microbe Interaction, 2009, 22: 921-931.
[10] Neyfakh A A. Mystery of multidrug transporters: the answer can be simple. Molecular Microbiology, 2002, 44: 1123-1130.
[11] Mentewab A, Stewart C N. Overexpression of an Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nature Biotechnology, 2005, 23: 1177-1180.
[12] Kang B G, Ye X, Osburn L D, et al . Transgenic hybrid aspen overexpressing the AtWBC 19 gene encoding an ATP-binding cassette transporter confers resistance to four amino glycoside antibiotics. Plant Cell Reports, 2010, 29: 643-650.
[13] Chen W, Zhang M M, Song Y Y, et al . Impacts of heavy metals on the fluorescence characteristics and root morphology of 2 turfgrass species. Acta Prataculturae Sinica, 2014, 23(3): 333-342.
[14] Li X, Wu Y J, Sun L X. Growth and physiological responses of three warm-season turfgrasses to lead stress. Acta Prataculturae Sinica, 2014, 23(4): 171-180.
[15] Gao H N, Ma G T, Li C X, et al . Effects of a microorganism on grass seedling physiological and biochemical characteristics when grown in Cr(VI) polluted soil. Acta Prataculturae Sinica, 2014, 23(4): 189-194.
[16] Pourrut B, Shahid M, Dumat C, et al . Lead uptake, toxicity, and detoxification in plants. Reviews of Environmental Contamination and Toxicology, 2011, 213: 113-136.
[17] Lee M, Lee K, Lee J, et al . AtPDR12 contributes to lead resistance in Arabidopsis . Plant Physiology, 2005, 138: 827-836.
[18] Kim D Y, Bovet L, Maeshima M, et al . The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. The Plant Journal, 2007, 50: 207-218.
[19] Kim D Y, Jin J Y, Alejandrob S, et al . Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis . Physiologia Plantarum, 2010, 139: 170-180.
[20] Multani D S, Briggs S P, Chamberlin M A, et al . Loss of an MDR transporter in compact stalks of maize br 2 and sorghum dw 3 mutants. Science, 2003, 302: 81-84.
[21] Geisler M, Murphy A S. The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Letters, 2006, 580: 1094-1102.
[22] Ito H, Gray W M. A gain-of-function mutation in the Arabidopsis pleiotropic drug resistance transporter PDR9 confers resistance to auxinic herbicides. Plant Physiology, 2006, 142: 63-74.
[23] Strader L C, Monroe-Augustus M, Rogers K C, et al . Arabidopsis iba response 5 ( ibr 5) suppressors separate responses to various hormones. Genetics, 2008, 180: 2019-2031.
[24] Strader L C, Bartel B. The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-Butyric acid. The Plant Cell, 2009, 21: 1992-2007.
[25] R u ˙ žiĉka K, Strader L C, Bailly A, et al . Arabidopsis PIS 1 encodes the ABCG37 transporter of auxinic compounds including the auxin precursor indole-3-butyric acid. Proceedings of the National Academy of Sciences of USA, 2010, 107: 10749-10753.
[26] Ko D, Kang J, Kiba T, et al . Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proceedings of the National Academy of Sciences of USA, 2014, 111: 7150-7155.
[27] Zhang K W, Novak O, Wei Z Y, et al . Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nature Communacation, 2014, doi:10.1038/ncomms4274.
[28] Le Hir R, Sorin C, Chakraborti D, et al . ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis . Plant Journal, 2013, 76: 811-824.
[29] Kanno Y, Hanada A, Chiba Y, et al . Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of USA, 2012, 109: 9653-9658.
[30] Kang J, Hwang J U, Lee M, et al . PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proceedings of the National Academy of Sciences of USA, 2010, 107: 2355-2360.
[31] Kuromori T, Miyaji T, Hikaru Y, et al . ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proceedings of the National Academy of Sciences of USA, 2010, 107: 2361-2366.
[32] Umehara M, Hanada A, Yoshida S, et al . Inhibition of shoot branching by new terpenoid plant hormones. Nature, 2008, 455: 195-200.
[33] Gomez-Roldan V, Fermas S, Brewer P B, et al . Strigolactone inhibition of shoot branching. Nature, 2008, 455: 189-194.
[34] Yang H X, Liu R J, Guo S X. Effects of arbuscular mycorrhizal fungus Glomus mosseae on the growth characteristics of Festuca arundinacea under salt stress conditions. Acta Prataculturae Sinica, 2014, 23(4): 195-203.
[35] Wu Q S, Yuan F Y, Fei Y J, et al . Effects of arbuscular mycorrhizal fungi on root system architecture and sugar contents of white clover. Acta Prataculturae Sinica, 2014, 23(1): 199-204.
[36] Kretzschmar T, Kohlen W, Sasse J, et al . A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature, 2012, 483: 341-346.
[37] Sharda J N, Koide R T. Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi. New Phytologist, 2008, 180: 696-701.
[38] Brewer P B, Dun E A, Ferguson B J, et al . Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis . Plant Physiology, 2009, 150: 482-493.
[39] Crawford S, Shinohara N, Sieberer T, et al . Strigolactones enhance competition between shoot branches by dampening auxin transport. Development, 2010, 137: 2905-2913.
[40] Hart J J, Ditomaso J M, Linscott D L, et al . Transport interactions between paraquat and polyamines in roots of intact maize seedlings. Plant Physiology, 1992, 99: 1400-1405.
[41] Xi J, Xu P, Xiang C B. Loss of AtPDR11, a plasma membrane-localized ABC transporter, confers paraquat tolerance in Arabidopsis thaliana . The Plant Journal, 2012, 69: 782-791.
[42] Hart J J, DiTomaso J M, Kochian L V. Characterization of paraquat transport in protoplasts from maize ( Zea mays L.) suspension cells. Plant Physiology, 1993, 103: 963-969.
[43] Whetten R, Sederoff R. Lignin biosynthesis. Plant Cell, 1995, 7:1001-1013.
[44] Miao Y C, Liu C J. ATP-binding cassette-like transporters are involved in the transport of lignin precursors across plasma and vacuolar membranes. Proceedings of the National Academy of Sciences of USA, 2010, 107: 22728-22733.
[45] Alejandro S, Lee Y, Tohge T, et al . AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Current Biology, 2012, 22: 1207-1212.
[46] Neinhuis C, Barthlott W. Characterization and distribution of water-repellent, self-cleaning plant surfaces. Annals of Botany, 1997, 79: 667-677.
[47] Bernard A, Joubès J. Arabidopsis cuticular waxes: Advances in synthesis, export and regulation. Progress in Lipid Research, 2013, 52: 110-129.
[48] Li J J, Huang J H, Xie S C. Plant wax and its response to environmental conditions. Acta Ecologica Sinica, 2011, 31(2): 565-574.
[49] Kunst L, Samuels A L. Biosynthesis and secretion of plant cuticular wax. Progress in Lipid Research, 2003, 42: 51-80.
[50] Pighin J A, Zheng H, Balakshin L J, et al . Plant cuticular lipid export requires an ABC transporter. Science, 2004, 306: 702-704.
[51] Bird D, Beisson F, Brigham A, et al . Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. The Plant Journal, 2007, 52: 485-498.
[52] Panikashvilia D, Shi J X, Samuel B. The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Molecular Plant, 2010, 3: 563-575.
[53] Luo B, Xue X Y, Hu W L, et al . An ABC transporter gene of Arabidopsis thaliana , AtWBC 11, is involved in cuticle development and prevention of organ fusion. Plant & Cell Physiology, 2007, 48: 1790-1802.
[54] Panikashvili D, Sigal S G, Tali M, et al . The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiology, 2007, 145: 1345-1360.
[55] Chen G X, Komatsuda T, Ma J F, et al . An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proceedings of the National Academy of Sciences of USA, 2011, 108: 12354-12359.
[56] Bessire M, Borel S, Fabre G, et al . A member of the pleiotropic drug resistance family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis . The Plant Cell, 2011, 23: 1958-1970.
[57] Panikashvili D, Shi J X, Schreiber L, et al . The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytologist, 2011, 190: 113-124.
[58] Huang L C, Jin L, Zhang S Z, et al . Pollen release mechanisms of papilionaceous plants(Faboideae). Acta Prataculturae Sinica, 2013, 22(6): 305-314.
[59] Quilichini T D, Friedmann M C, Samuels A L, et al . ATP-Binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis . Plant Physiology, 2010, 154: 678-690.
[60] Choi H, Jin J Y, Choi S, et al . An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. The Plant Journal, 2011, 65: 181-193.
[61] Choi H, Ohyama K, Kim Y Y, et al . The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat. The Plant Cell, 2014, 26: 310-324.
[62] Qin P, Tu B, Wang Y, et al . ABCG 15 encodes an ABC transporter protein, and is essential for post-meiotic anther and pollen exine development in rice. Plant & Cell Physiology, 2013, 54: 138-154.
[63] Weston L A, Ryan P R, Watt M. Mechanisms for cellular transport and release of allelochemicals from plant root into the rhizosphere. Journal of Experimental Botany, 2012, 63: 3445-3454.
[64] Campbell E J, Schenk P M, Kazan K, et al . Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defense signaling pathways in Arabidopsis . Plant Physiology, 2003, 133: 1272-1284.
[65] Stukkens Y, Bultreys A, Grec S, et al . NpPDR1, a pleiotropic drug resistance-type ATP binding cassette transporter from Nicotiana plumbaginifolia , plays a major role in plant pathogen defense. Plant Physiology, 2005, 139: 341-352.
[66] Kobae Y, Sekino T, Yoshioka H, et al . Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana , causes hypersensitive cell death upon pathogen infection. Plant Cell Physiology, 2006, 47: 309-318.
[67] Stein M, Dittgen J, Sanchez-Rodriguez C, et al . Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to non-host resistance to inappropriate pathogens that enter by direct penetration. The Plant Cell, 2006, 18: 731-746.
[68] Sasabe M, Toyoda K, Shiraishi T, et al . cDNA cloning and characterization of tobacco ABC transporter: NtPDR1 is a novel elicitor-responsive gene. FEBS Letters, 2002, 518: 164-168.
[69] Crouzet J, Roland J, Peeters E, et al . NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum , is involved in diterpene transport. Plant Molecular Biology, 2013, 82: 181-192.
[70] Bultreys A, Trombik T, Drozak A, et al . Nicotiana plumbaginifolia plants silenced for the ATP-binding cassette transporter gene NpPDR 1 show increased susceptibility to a group of fungal and oomycete pathogens. Molecular Plant Pathology, 2009, 10: 651-663.
[71] Eichhorn H, Klinghammer M, Becht P, et al . Isolation of a novel ABC-transporter gene from soybean induced by salicylic acid. Journal of Experimental Botany, 2006, 57: 2193-2201.
[72] Moons A. Transcriptional profiling of the PDR gene family in rice roots in response to plant growth regulators, redox perturbations and weak organic acid stresses. Planta, 2008, 229: 53-71.
[73] Krattinger S G, Lagudah E S, Spielmeyer W, et al . A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 2009, 323: 1360-1363.
[74] Banasiak J, Biała W, Staszków A, et al . A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. Journal of Experimental Botany, 2013, 64: 1005-1015.
[75] Bienert M D, Gerlitz S E, Drozak A, et al . A pleiotropic drug resistance transporter in Nicotiana tabacum is involved in defense against the herbivore Manduca sexta . The Plant Journal, 2012, 72: 745-757.
[76] Sugiyama A, Shitan N, Yazaki K. Involvement of a soybean ATP binding cassette-type transporter in the secretion of genistein, a signal flavonoid in legume-rhizobium symbiosis. Plant Physiology, 2007, 144: 2000-2008.
[77] Sugiyama A, Shitan N, Yazaki K. Signaling from soybean roots to rhizobium, an ATP-binding casstte-type transporter mediates genistein secretion. Plant Signaling & Behavior, 2008, 3: 38-40.
[78] Zhang Q, Blaylock L A, Harrison M J. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. The Plant Cell, 2010, 22: 1483-1497.
[79] Gutjahr C, Radovanovic D, Geoffroy J, et al . The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. The Plant Journal, 2012, 69: 906-920.
[13] 陈伟, 张苗苗, 宋阳阳, 等. 重金属离子对2种草坪草荧光特性及根系形态的影响. 草业学报, 2014, 23(3): 333-342.
[14] 李西, 吴亚娇, 孙凌霞. 铅胁迫对三种暖季型草坪草生长和生理特性的影响. 草业学报, 2014, 23(4): 171-180.
[15] 高海宁, 马国泰, 李彩霞, 等. 菌剂对铬污染土壤中坪草幼苗生理生化的影响. 草业学报, 2014, 23(4): 189-194.
[34] 杨海霞, 刘润进, 郭绍霞. AM真菌摩西球囊霉对盐胁迫条件下高羊茅生长特性的影响. 草业学报, 2014, 23(4): 195-203.
[35] 吴强盛, 袁芳英, 费永俊, 等. 丛枝菌根真菌对白三叶根系构型和糖含量的影响. 草业学报, 2014, 23(1): 199-204.
[48] 李婧婧, 黄俊华, 谢树成. 植物蜡质及其与环境的关系. 生态学报, 2011, 31(2): 565-574.
[58] 黄利春, 金樑, 张树振, 等. 蝶形花亚科植物花粉释放机制. 草业学报, 2013, 22(6): 305-314.