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Advances in Studies on the COPT Proteins in Arabidopsis thaliana

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  • 1 Tianjin Key Laboratory of Animal and Plant Resistance, College of Life Sciences, Tianjin Normal University, Tianjin 300387, China
    2 Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

Received date: 2019-03-13

  Accepted date: 2019-06-18

  Online published: 2019-06-26

Abstract

Copper (Cu) is an essential trace element in plants and is involved in many physiological and biochemical reactions as a cofactor of various enzymes. Cu deficiency and excess can affect the normal growth and development, so plants have developed sophisticated regulatory networks to strictly control Cu content. The copper transporter COPT, having high affinity with Cu can regulate the absorption and transport of Cu, and plays an important role in maintaining Cu homeostasis. COPT proteins are involved in different processes of Cu transport, such as uptake of Cu from the external environment, export of Cu from organelles, transport of Cu over long distances, and mobilization and redistribution of Cu between different organs. In addition, COPT proteins play an important role in maintaining homeostasis of other ions, regulating the circadian clock, involving in synthesis of plant hormones and perception of hormone signals. Here we summarize the recent advances in the expression and localization, regulatory mechanisms, and biological functions of COPT proteins in the model plant Arabidopsis thaliana.

Cite this article

Hui Wang,Jinjin Li,Jinyu Xu,Peng Liu,Haiyan Zhang . Advances in Studies on the COPT Proteins in Arabidopsis thaliana[J]. Chinese Bulletin of Botany, 2019 , 54(6) : 786 -796 . DOI: 10.11983/CBB19045

References

[1] 房茜, 李鹏, 靳思, 印莉萍 ( 2007). 酵母和植物中铜的转运系统及其调控. 植物学通报 24, 807-815.
[2] 侯金丽 ( 2015). 铜离子的生物学特性及其吸收转运调控机制研究进展. 现代农业科技 652, 158.
[3] 门中华, 李生秀 ( 2009). 植物生物节律性研究进展. 生物学杂志 26, 55-57.
[4] 王超旻, 程楠, 韩咏竹, 胡文彬 ( 2013). 细胞内铜转运系统的研究进展. 安徽卫生职业技术学院学报 12, 82-83.
[5] 王靖, 徐虹, 李珣, 郑锦乾, 王立红 ( 2008). 铜绿微囊藻生物钟蛋白KaiC的自激活活性和自身相互作用研究. 海洋环境科学 27, 67-70.
[6] 王夏芳 ( 2015). 铜离子对环境危害现状及对策研究. 国土与自然资源研究 1, 57-59.
[7] 姚浩群 ( 2012). 金属离子与金属颗粒生物学活性实验研究. 博士论文. 广州: 南方医科大学. pp. 63-68.
[8] 袁金红, 李靖锐, 张海燕 ( 2016). 植物铜转运蛋白的结构和功能. 植物学报 51, 849-858.
[9] 张红晓, 张芬琴 ( 2011). 铜在植物细胞中的运输和分布. 洛阳理工学院学报(自然科学版) 21, 1-5.
[10] 张美琪, 陈林, 王晶 ( 2018). 铜转运蛋白与癌症的研究进展. 中国科学: 化学 48, 1385-1393.
[11] 赵雪芹, 张海燕, 刘维仲 ( 2012). 植物铜转运相关蛋白研究进展. 广西植物 32, 280-284.
[12] 赵艳, 徐迎春, 柴翠翠, 周燕 ( 2010). 铜胁迫对狭叶香蒲生长及生理特性的影响. 广西植物 30, 367-372.
[13] Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T ( 2005). Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17, 1233-1251.
[14] Andrés-Colás N, Carrió-Seguí A, Abdel-Ghany SE, Pilon M, Pe?arrubia L ( 2018). Expression of the intracellular COPT3-mediated Cu transport is temporally regulated by the TCP16 transcription factor. Front Plant Sci 9, 910.
[15] Andrés-Colás N, Perea-García A, Puig S, Pe?arrubia L ( 2010). Deregulated copper transport affects Arabidopsis development especially in the absence of environmental cycles. Plant Physiol 153, 170-184.
[16] Balandin T, Castresana C ( 2002). AtCOX17, an Arabidop- sis homolog of the yeast copper chaperone COX17. Plant Physiol 129, 1852-1857.
[17] Bell-Pedersen D, Shinohara ML, Loros JJ, Dunlap JC ( 1996). Circadian clock-controlled genes isolated from Neurospora crassa are late night-to early morning specific. Proc Natl Acad Sci USA 93, 13096-13101.
[18] Bernal M, Casero D, Singh V, Wilson GT, Grande A, Yang HJ, Dodani SC, Pellegrini M, Huijser P, Connolly EL, Merchant SS, Kr?mer U ( 2012). Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24, 738-761.
[19] Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H ( 2006). Integrating mem- brane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140, 1151-1168.
[20] Borjigin J, Payne AS, Deng J, Li XD, Wang MM, Ovodenko B, Gitlin JD, Snyder SH ( 1999). A novel pineal night- specific ATPase encoded by the Wilson disease gene. J Neurosci 19, 1018-1026.
[21] Burkhead JL, Reynolds KAG, Abdel-Ghany SE, Cohu CM, Pilon M ( 2009). Copper homeostasis. New Phytol 182, 799-816.
[22] Cardon G, H?hmann S, Klein J, Nettesheim K, Saedler H, Huijser P ( 1999). Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237, 91-104.
[23] Carrió-Seguí A, Garcia-Molina A, Sanz A, Pe?arrubia L ( 2015). Defective copper transport in the copt5 mutant affects cadmium tolerance. Plant Cell Physiol 56, 442-454.
[24] Carrió-Seguí à, Romero P, Sanz A, Pe?arrubia L ( 2016). Interaction between ABA signaling and copper homeostasis in Arabidopsis thaliana. Plant Cell Physiol 57, 1568-1582.
[25] Coego A, Brizuela E, Castillejo P, Ruíz S, Koncz C, del Pozo JC, Pi?eiro M, Jarillo JA, Paz-Ares J, León J, The TRANSPLANTA Consortium ( 2014). The TRANSPLANTA collection of Arabidopsis lines: a resource for functional analysis of transcription factors based on their conditional overexpression. Plant J 77, 944-953.
[26] Garcia L, Welchen E, Gonzalez DH ( 2014). Mitochondria and copper homeostasis in plants. Mitochondrion 19, 269-274.
[27] Garcia-Molina A, Andrés-Colás N, Perea-García A, Del Valle-Tascón S, Pe?arrubia L, Puig S ( 2011). The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency. Plant J 65, 848-860.
[28] Garcia-Molina A, Andrés-Colás N, Perea-García A, Neumann U, Dodani SC, Huijser P, Pe?arrubia L, Puig S ( 2013). The Arabidopsis COPT6 transport protein functions in copper distribution under copper-deficient conditions. Plant Cell Physiol 54, 1378-1390.
[29] Gavnholt B, Larsen K ( 2002). Molecular biology of plant laccases in relation to lignin formation. Physiol Plant 116, 273-280.
[30] Gayomba SR, Jung HI, Yan JP, Danku J, Rutzke MA, Bernal M, Kr?mer U, Kochian LV, Salt DE, Vatamaniuk OK ( 2013). The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana. Metallomics 5, 1262-1275.
[31] Gorecka K, Cvikrová M, Kowalska U, Eder J, Szafrańska K, Górecki R, Janas KM ( 2007). The impact of Cu treatment on phenolic and polyamine levels in plant material regenerated from embryos obtained in anther culture of carrot. Plant Physiol Biochem 45, 54-61.
[32] Grat?o PL, Polle A, Lea PJ, Azevedo RA ( 2005). Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32, 481-494.
[33] H?nsch R, Mendel RR ( 2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12, 259-266.
[34] Jung HI, Gayomba SR, Rutzke MA, Craft E, Kochian LV, Vatamaniuk OK ( 2012). COPT6 is a plasma membrane transporter that functions in copper homeostasis in Arabidopsis and is a novel target of SQUAMOSA promoter- binding protein-like 7. J Biol Chem 287, 33252-33267.
[35] Kampfenkel K, Kushnir S, Babiychuk E, Inzé D, Van Montagu M ( 1995). Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J Biol Chem 270, 28479-28486.
[36] Klaumann S, Nickolaus SD, Fürst SH, Starck S, Schneider S, Ekkehard Neuhaus H, Trentmann O ( 2011). The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol 192, 393-404.
[37] Komori H, Higuchi Y ( 2010). Structure and molecular evolution of multicopper blue proteins. Biomol Concepts 1, 31-40.
[38] Kuper J, Llamas A, Hecht HJ, Mendel RR, Schwarz G ( 2004). Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430, 803-806.
[39] Li HX, Fan RC, Li LB, Wei B, Li GL, Gu LQ, Wang XP, Zhang XQ ( 2014). Identification and characterization of a novel copper transporter gene family TaCT1 in common wheat. Plant Cell Environ 37, 1561-1573.
[40] Lv QD, Zhong YJ, Wang YG, Wang ZY, Zhang L, Shi J, Wu ZC, Liu Y, Mao CZ, Yi KK, Wu P ( 2014). SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell 26, 1586-1597.
[41] Martín-Trillo M, Cubas P ( 2010). TCP genes: a family snapshot ten years later. Trends Plant Sci 15, 31-39.
[42] Mishra P, Panigrahi KC ( 2015). GIGANTEA—an emerging story. Front Plant Sci 6, 8.
[43] Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, Givan SA, McEntee C, Kay SA, Chory J ( 2007). The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb Symp Quant Biol 72, 353-363.
[44] Nagae M, Nakata M, Takahashi Y ( 2008). Identification of negative cis-acting elements in response to copper in the chloroplastic iron superoxide dismutase gene of the moss Barbula unguiculata. Plant Physiol 146, 1687-1696.
[45] Page MD, Janette K, Hamel PP, Merchant SS ( 2009). Two Chlamydomonas CTR copper transporters with a novel cys-met motif are localized to the plasma membrane and function in copper assimilation. Plant Cell 21, 928-943.
[46] Pe?arrubia L, Andrés-Colás N, Moreno J, Puig S ( 2010). Regulation of copper transport in Arabidopsis thaliana: a biochemical oscillator? J Biol Inorg Chem 15, 29-36.
[47] Pe?arrubia L, Romero P, Carrió-Seguí A, Andrés-Bordería A, Moreno J, Sanz A ( 2015). Temporal aspects of copper homeostasis and its crosstalk with hormones. Front Plant Sci 6, 255.
[48] Perea-García A, Andrés-Bordería A, Mayo de Andrés S, Sanz A, Davis AM, Davis SJ, Huijser P, Pe?arrubia L ( 2016a). Modulation of copper deficiency responses by diurnal and circadian rhythms in Arabidopsis thaliana. J Exp Bot 67, 391-403.
[49] Perea-García A, Garcia-Molina A, Andrés-Colás N, Vera-Sirera F, Pérez-Amador MA, Puig S, Pe?arrubia L ( 2013). Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling. Plant Physiol 162, 180-194.
[50] Perea-García A, Sanz A, Moreno J, Andrés-Bordería A, De Andrés SM, Davis AM, Huijser P, Davis SJ, Pe?arrubia L ( 2016b). Daily rhythmicity of high affinity copper transport. Plant Signal Behav 11, e1140291.
[51] Puga MI, Mateos I, Charukesi R, Wang ZY, Franco-orrilla JM, De Lorenzo L, Irigoyen ML, Masiero S, Bustos R, Rodríguez J, Leyva A, Rubio V, Sommer H, Paz-Ares J ( 2014). Spx1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc Natl Acad Sci USA 111, 14947-14952.
[52] Raven JA, Evans MCW, Korb RE ( 1999). The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60, 111-150.
[53] Rodríguez FI, Esch JJ, Hall AE, Binder BM, Schaller GE, Bleecker AB ( 1999). A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283, 996-998.
[54] Sancenón V, Puig S, Mateu-Andrés I, Dorcey E, Thiele DJ, Pe?arrubia L ( 2004). The Arabidopsis copper transporter COPT1 functions in root elongation and pollen development. J Biol Chem 279, 15348-15355.
[55] Sancenón V, Puig S, Mira H, Thiele DJ, Pe?arrubia L ( 2003). Identi?cation of a copper transporter family in Arabidopsis thaliana. Plant Mol Biol 51, 577-587.
[56] Seo PJ, Mas P ( 2015). STRESSing the role of the plant circadian clock. Trends Plant Sci 20, 230-237.
[57] Sommer F, Kropat J, Malasarn D, Grossoehme NE, Chen X, Giedroc DP, Merchant SS ( 2010). The CRR1 nutritIonal copper sensor in Chlamydomonas contains two distinct metal-responsive domains. Plant Cell 22, 4098-4113.
[58] Tiwari M, Venkatachalam P, Penarrubia L, Sahi SV ( 2017). COPT2, a plasma membrane located copper transporter, is involved in the uptake of Au in Arabidopsis. Sci Rep 7, 11430.
[59] Wang HL, Du HM, Li HY, Huang Y, Ding JZ, Liu C, Wang N, Lan H, Zhang SZ ( 2018). Identification and functional characterization of the ZmCOPT copper transporter family in maize. PLoS One 13, e0199081.
[60] Wang XH, Li HY, Du XB, Harris J, Guo ZJ, Sun HZ ( 2012). Activation of carboplatin and nedaplatin by the N-terminus of human copper transporter 1 (hCTR1). Chem Sci 3, 3206-3215.
[61] Waters BM, McInturf SA, Stein RJ ( 2012). Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J Exp Bot 63, 5903-5918.
[62] Wintz H, Fox T, Wu YY, Feng V, Chen WQ, Chang HS, Zhu T, Vulpe C ( 2003). Expression profiles of Arabidopsis thaliana in mineral deficiencies reveal novel transporters involved in metal homeostasis. J Biol Chem 278, 47644-47653.
[63] Wu XB, Sinani D, Kim H, Lee J ( 2009). Copper transport activity of yeast Ctr1 is down-regulated via its C terminus in response to excess copper. J Biol Chem 284, 4112-4122.
[64] Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C ( 2012). The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1, 639-647.
[65] Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T ( 2009). SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21, 347-361.
[66] Yan SP, Dong XN ( 2014). Perception of the plant immune signal salicylic acid. Curr Opin Plant Biol 20, 64-68.
[67] Yruela I ( 2009). Copper in plants: acquisition, transport and interactions. Funct Plant Biol 36, 409-430.
[68] Yu PL, Yuan JH, Deng X, Ma M, Zhang HY ( 2014). Subcellular targeting of bacterial CusF enhances Cu accumulation and alters root to shoot Cu translocation in Arabidopsis. Plant Cell Physiol 55, 1568-1581.
[69] Yu PL, Yuan JH, Zhang H, Deng X, Ma M, Zhang HY ( 2016). Engineering metal-binding sites of bacterial CusF to enhance Zn/Cd accumulation and resistance by subcellular targeting. J Hazard Mater 302, 275-285.
[70] Yu ZL, Zhang JG, Wang XC, Chen J ( 2008). Excessive copper induces the production of reactive oxygen species, which is mediated by phospholipase D, nicotinamide adenine dinucleotide phosphate oxidase and antioxidant systems. J Integr Plant Biol 50, 157-167.
[71] Yuan M, Chu ZH, Li XH, Xu CG, Wang SP ( 2010). The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell 22, 3164-3076.
[72] Yuan M, Li XH, Xiao JH, Wang SP ( 2011). Molecular and functional analyses of COPT/Ctr-type copper transporter-like gene family in rice. BMC Plant Biol 11, 69.
[73] Zhang HY, Zhao X, Li JG, Cai HQ, Deng XW, Li L ( 2014). MicroRNA408 is critical for the HY5-SPL7 gene network that mediates the coordinated response to light and copper. Plant Cell 26, 4933-4953.
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