Physiological and Molecular Mechanism of Plants Response to Copper Stress: A Review

doi:10.11924/j.issn.1000-6850.casb2022-0555

Abstract

Abstract:

Copper (Cu) is an essential metal for human body, animals and plants, and participates in various morphological, physiological and biochemical processes. Copper is a cofactor of many enzymes and plays an important role in photosynthesis, respiration and electron transport chain. It is also a structural component of defense genes. In order to provide more systematic theoretical reference for the future study of copper stress on plants, based on the adverse effects of excessive copper on physiological processes such as plant germination, growth, photosynthesis and anti-oxidation summarized in previous studies, this paper reviews the biological functions of copper, the toxicity of excessive copper to plant growth and development, the role of copper transporters and chaperone proteins, and the tolerance mechanism of plants to copper stress. The future research direction is prospected, which provides a basis for formulating effective strategies to maintain copper homeostasis.

Key words: copper toxicity, copper homeostasis, absorption, transport, tolerance mechanism

LI Jia, DU Ruiying, WANG Xu, CHEN Guang. Physiological and Molecular Mechanism of Plants Response to Copper Stress: A Review[J]. Chinese Agricultural Science Bulletin, 2023, 39(11): 18-28.

Figures/Tables 2

References 116

[1]	NAZIR F, HUSSAIN A, FARDUDDIN Q. Hydrogen peroxide modulate photosynthesis and antioxidant systems in tomato (Solanum lycopersicum L.) plants under copper stress[J]. Chemosphere, 2019, 230(9):544-558. doi: 10.1016/j.chemosphere.2019.05.001 URL
[2]	LENG X, MU Q, WANG X, et al. Transporters, chaperones, and P-type ATPases controlling grapevine copper homeostasis[J]. Funct. Integr. Genom., 2015, 15(6):673-684. doi: 10.1007/s10142-015-0444-1 URL
[3]	ZHANG D, LIU X, MA J, et al. Genotypic differences and glutathione metabolism response in wheat exposed to copper[J]. Environ. Exp. Bot., 2019, 157:250-259. doi: 10.1016/j.envexpbot.2018.06.032 URL
[4]	GONG Q, LI ZH, WANG L, et al. Gibberellic acid application on biomass, oxidative stress response, and photosynthesis in spinach (Spinacia oleracea L.) seedlings under copper stress[J]. Environ. Sci. Pollut. Res. Int., 2021, 28(38):53594-53604. doi: 10.1007/s11356-021-13745-5
[5]	王子诚, 陈梦霞, 杨毓贤, 等. 铜胁迫对植物生长发育影响与植物耐铜机制的研究进展[J]. 植物营养与肥料学报, 2021, 27(10):1849-1863.
[6]	袁猛. Xa13基因在水稻—白叶枯病菌互作和水稻生长发育中的功能研究[D]. 武汉: 华中农业大学, 2010.
[7]	HUANG X Y, DENG F, YAMAJI N, et al. A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain[J]. Nat. Commun., 2016, 7(1):12138. doi: 10.1038/ncomms12138
[8]	ADREES M, ALI S, RIZWAN M, et al. The effect of excess copper on growth and physiology of important food crops: A review[J]. Environ. Sci. Pollut. Res. Int., 2015, 22(11):8148-8162. doi: 10.1007/s11356-015-4496-5 URL
[9]	AZEEZ M O, ADESANWO O O, ADEPETU J A. Effect of Copper (Cu) application on soil available nutrients and uptake[J]. Acad. J., 2015, 10(5):359-364.
[10]	YRUELA I. Copper in plants: Acquisition, transport and interactions[J]. Funct. Plant Biol., 2009, 36(5):409-430. doi: 10.1071/FP08288 pmid: 32688656
[11]	MARQUES D M, DA SILVA A B, MANTOVANI J R, et al. Root morphology and leaf gas exchange in Peltophorum dubium (Spreng.) Taub. (Caesalpinioideae) exposed to copper-induced toxicity[J]. S. Afr. J. Bot., 2019, 121:186-192. doi: 10.1016/j.sajb.2018.11.007 URL
[12]	PARK S, BACK K. Melatonin promotes seminal root elongation and root growth in transgenic rice after germination[J]. J. Pineal Res., 2012, 53(4):385-389. doi: 10.1111/j.1600-079X.2012.01008.x pmid: 22640001
[13]	CUI Y, WANG M, YIN X, et al. OsMSR3, a small heat shock protein, confers enhanced tolerance to copper stress in Arabidopsis thaliana[J]. Int. j. mol. sci., 2019, 20(23):6096. doi: 10.3390/ijms20236096 URL
[14]	BATOOL R, HAMEED M, ASHRAF M, et al. Physio-Anatomical Responses of Plants to Heavy Metals[M]. Springer: Dordrecht, The Netherlands, 2015:79-96.
[15]	BALDI E, MIOTTO A, CERETTA CA, et al. Soil application of P can mitigate the copper toxicity in grapevine: physiological implications[J]. Sci. hortic., 2018, 238:400-407. doi: 10.1016/j.scienta.2018.04.070 URL
[16]	HIPPLER FWR, MATTOS DJ, BOARETTO RM, et al. Copper excess reduces nitrate uptake by Arabidopsis roots with specific effects on gene expression[J]. J. plant physiol., 2018, 228:158-165. doi: 10.1016/j.jplph.2018.06.005 URL
[17]	HIPPLER FWR, CIPRIANO DO, BOARETTO RM, et al. Citrus rootstocks regulate the nutritional status and antioxidant system of trees under copper stress[J]. Environ. exp. bot., 2016, 130:42-52. doi: 10.1016/j.envexpbot.2016.05.007 URL
[18]	HONG J, RICO CM, ZHAO L, et al. Toxic effects of copper-based nanoparticles or compounds to lettuce (Lactuca sativa) and alfalfa (Medicago sativa)[J]. Environ. sci. process. impacts, 2015, 17(1):177-185. doi: 10.1039/c4em00551a pmid: 25474419
[19]	ROY SK, CHO SW, KWON SJ, et al. Proteome characterization of copper stress responses in the roots of sorghum[J]. Biometals int. j. role met. ions biol. biochem. med., 2017, 30(5):765-785.
[20]	VASSILEV A, LIDON F, RAMALHO JC, et al. Effects of excess Cu on growth and photosynthesis of barley plants. Implication with a screening test for Cu tolerance[J]. J. cent. eur. agric., 2003, 4(3):225-236.
[21]	GONZALEZ-MENDOZA D, GIL FE, ESCOBOZA-GARCIA F, et al. Copper stress on photosynthesis of black mangle (Avicennia germinans)[J]. An. acad. bras. de cienc., 2013, 85(2):665-670. doi: 10.1590/S0001-37652013000200013 URL
[22]	HOSSAIN MS, ABDELRAHMAN M, TRAN CD, et al. Insights into acetate-mediated copper homeostasis and antioxidant defense in lentil under excessive copper stress[J]. Environ. pollut., 2020, 258:113544. doi: 10.1016/j.envpol.2019.113544 URL
[23]	PANOU-FILOTHEOU H, BOSABALIDIS AM, KARATAGLIS S. Effects of copper toxicity on leaves of oregano (Origanum vulgare subsp. hirtum)[J]. Ann. bot., 2001, 88(2):207-214. doi: 10.1006/anbo.2001.1441 URL
[24]	CAMBROLLE J, GARCIA J L, FIGUEROA M E, et al. Evaluating wild grapevine tolerance to copper toxicity[J]. Chemosphere, 2015, 120(120):171-178. doi: 10.1016/j.chemosphere.2014.06.044 URL
[25]	XU Q, QIU H, CHU W, et al. Copper ultrastructural localization, subcellular distribution, and phytotoxicity in Hydrilla verticillata (L.f.) Royle[J]. Environ. sci. pollut. res. int., 2013, 20(12):8672-8679. doi: 10.1007/s11356-013-1828-1 URL
[26]	YAMAJI N, MA JF. The node, a hub for mineral nutrient distribution in graminaceous plants[J]. Trends plant sci., 2014, 19(9):556-563. doi: 10.1016/j.tplants.2014.05.007 pmid: 24953837
[27]	SASAKI A, YAMAJI N, MA JF. Transporters involved in mineral nutrient uptake in rice[J]. J. exp. bot., 2016, 67(12):3645-3653. doi: 10.1093/jxb/erw060 pmid: 26931170
[28]	COLANGELO EP, GUERINOT ML. Put the metal to the petal: metal uptake and transport throughout plants[J]. Curr. opin. plant biol., 2006, 9(3):322-330. pmid: 16616607
[29]	GHAZARYAN K, MOVSESYAN H, GHAZARYAN N, et al. Copper phytoremediation potential of wild plant species growing in the mine polluted areas of Armenia[J]. Environ. pollut. 2019, 249:491-501. doi: S0269-7491(18)32979-8 pmid: 30928521
[30]	SANZ A, PIKE S, KHAN M A, et al. Copper uptake mechanism of Arabidopsis thaliana high-affinity COPT transporters[J]. Protoplasma 2018, 256:161-170. doi: 10.1007/s00709-018-1286-1
[31]	SENOVILLA M, ABREU I, ABREU I, et al. Medicago truncatula copper transporter 1 (MtCOPT1) delivers copper for symbiotic nitrogen fixation[J]. New phytol., 2018, 218(2):696-709. doi: 10.1111/nph.14992 pmid: 29349810
[32]	GARCIA-MOLINA A, ANDRES-COLAS N, PEREA-GARCIA A, et al. The Arabidopsis COPT6 transport protein functions in copper distribution under copper-deficient conditions[J]. Plant cell physiol., 2013, 54(8):1378-1390. doi: 10.1093/pcp/pct088 URL
[33]	BOUTIGNY S, SAUTRON E, FINAZZI G, et al. HMA1 and PAA1, two chloroplast-envelope PIB-ATPases, play distinct roles in chloroplast copper homeostasis[J]. J. exp. bot., 2014, 65(6):1529-1540. doi: 10.1093/jxb/eru020 pmid: 24510941
[34]	ANDRES-COLAS N, SANCENON V, RODRIGUEZ-NAVARRO S, et al. The Arabidopsis heavy metal P-type ATPase HMA5 interacts with metallochaperones and functions in copper detoxification of roots[J]. Plant j., 2006, 45(2):225-236. doi: 10.1111/tpj.2006.45.issue-2 URL
[35]	CATTY P, BOUTIGNY S, MIRAS R, et al. Biochemical characterization of AtHMA6/PAA1, a chloroplast envelope Cu(I)-ATPase[J]. J. biol. chem. 2011, 286(42):36188-36197. doi: 10.1074/jbc.M111.241034 pmid: 21878617
[36]	HIMELBLAU E, AMASINO RM. Nutrients mobilized from leaves of Arabidopsis thaliana during leaf senescence[J]. J. plant physiol., 2001, 158(10):1317-1323. doi: 10.1078/0176-1617-00608 URL
[37]	GAYOMBA S R, JUNG H I, YAN J, et al. The CTR/COPT-dependent copper uptake and SPL7-dependent copper deficiency responses are required for basal cadmium tolerance in A. thaliana[J]. Metallomics, 2013, 5(9):1262-1275. doi: 10.1039/c3mt00111c URL
[38]	WATERS B M, CHU H H, DIDONATO R J, et al. Mutations in arabidopsis yellow stripe-like1 and yellow stripe-like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds[J]. Plant physiol., 2006, 141(4):1446-1458. doi: 10.1104/pp.106.082586 pmid: 16815956
[39]	DIDONATO R J, ROBERTS L A, SANDERSON T, et al. Arabidopsis yellow stripe-like2 (YSL2): a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes[J]. Plant j. 2004, 39(3):403-414. doi: 10.1111/j.1365-313X.2004.02128.x pmid: 15255869
[40]	GUERINOT M L. The ZIP family of metal transporters[J]. Biochim. biophys. acta (bba)-biomembr. 2000, 1465(1-2):190-198. doi: 10.1016/S0005-2736(00)00138-3 URL
[41]	CARRIO-SEGUI À, ROMERO P, CURIE C, et al. Copper transporter COPT5 participates in the crosstalk between vacuolar copper and iron pools mobilisation[J]. Sci. rep. 2019, 9:4648. doi: 10.1038/s41598-018-38005-4
[42]	PEREA-GARCIA A, GARCIA-MOLINA A, ANDRES-COLAS N, et al. Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling[J]. Plant physiol., 2013, 162(1):180-194. doi: 10.1104/pp.112.212407 URL
[43]	LEE S, KIM YY, LEE Y, et al. Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein[J]. Plant physiol., 2007, 145(3):831-842. doi: 10.1104/pp.107.102236 pmid: 17827266
[44]	ZHENG L, YAMAJI N, YOKOSHO K, et al. YSL16 Is a phloem-localized transporter of the copper-nicotianamine Complex that is responsible for copper distribution in rice[J]. Plant cell, 2012, 24(9):3767-3782. doi: 10.1105/tpc.112.103820 URL
[45]	MARTINS V, BASSIL E, HANANA M, et al. Copper homeostasis in grapevine: functional characterization of the Vitis vinifera copper transporter 1[J]. Planta, 2014, 240(1):91-101. doi: 10.1007/s00425-014-2067-5 pmid: 24691572
[46]	MARTINS V, HANANA M, BLUMWALD E, et al. Copper transport and compartmentation in grape cells[J]. Plant cell physiol., 2012, 53:1866-1880. doi: 10.1093/pcp/pcs125 pmid: 22952251
[47]	LI H, FAN R, LI L, et al. Identification and characterization of a novel copper transporter gene family TaCT1 in common wheat[J]. Plant cell environ., 2014, 37(7):1561-1573. doi: 10.1111/pce.2014.37.issue-7 URL
[48]	BILLARD V, OURRY A, MAILLARD A, et al. Copperdeficiency in brassica napus induces copper remobilization, molybdenum accumulation and modification of the expression of chloroplastic proteins[J]. Plos one, 2017, 9(10):109889.
[49]	BERNAL M, TESTILLANO P S, ALFONSO M, et al. Identification and subcellular localization of the soybean copper P1B-ATPase GmHMA8 transporter[J]. J. struct. biol., 2007, 158(1):46-58. pmid: 17169574
[50]	MIKKELSEN M D, PEDAS P, SCHILLER M, et al. Barley HvHMA1 is a heavy metal pump involved in mobilizing organellar Zn and Cu and plays a role in metal loading into grains[J]. Plos one, 2012, 7(11):e49027. doi: 10.1371/journal.pone.0049027 URL
[51]	ARAKI R, MURATA J, MURATA Y. A novel barley yellow stripe 1-like transporter (HvYSL2) localized to the root endodermis transports metal-phytosiderophore complexes[J]. Plant cell physiol., 2011, 52(11):1931-1940. doi: 10.1093/pcp/pcr126 pmid: 21937676
[52]	DAI J, WANG N, XIONG H, et al. The yellow stripe-like (YSL) gene functions in internal copper transport in peanut[J]. Genes 2018, 9(12):635. doi: 10.3390/genes9120635 URL
[53]	PALMGREN M G, NISSEN P. P-type ATPases[J]. Annu. rev. biophys., 40(1):243-266. doi: 10.1146/biophys.2011.40.issue-1 URL
[54]	OMASITS U, AHRENS C H, MULLER S, et al. Protter: Interactive protein feature visualization and integration with experimental proteomic data[J]. Bioinformatics, 2014, 30(6):884-886. doi: 10.1093/bioinformatics/btt607 pmid: 24162465
[55]	MOLLER JV, OLESEN C, WINTHER A M L, et al. What can be learned about the function of a single protein from its various X-ray structures: the example of the sarcoplasmic calcium pump[J]. Methods mol. biol., 2010, 654:119-140. doi: 10.1007/978-1-60761-762-4_7 pmid: 20665264
[56]	BLABY-HAAS C E, PADILLA-BENAVIDES T, STUBE R, et al. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis[J]. Proc. natl. acad. sci., USA 2014, 111(50):5480-5487. doi: 10.1073/pnas.1400668111 URL
[57]	HUSSAIN D, HAYDON MJ, WANG Y, et al. P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis[J]. Plant cell, 2004, 16(5):1327-1339. doi: 10.1105/tpc.020487 pmid: 15100400
[58]	SEIGNEURIN-BERNY D, GRAVOT A, AUROY P, et al. HMA1, a new Cu-ATPase of the chloroplast envelope, is essential for growth under adverse light conditions[J]. J. biol. chem., 2006, 281(5):2882-2892. doi: 10.1074/jbc.M508333200 URL
[59]	MORENO I, NORAMBUENA L, MATURANA D, et al. AtHMA1 is a thapsigargin-sensitive Ca²⁺/Heavy metal pump[J]. J. biol. chem., 2008, 283(15):9633-9641. doi: 10.1074/jbc.M800736200 pmid: 18252706
[60]	LI J, LIANG H, YAN M, et al. Arbuscular mycorrhiza fungi facilitate rapid adaptation of Elsholtzia splendens to copper[J]. Sci. total environ., 2017, 599:1462-1468.
[61]	DEL POZO T, CAMBIAZO V, GONZALEZ M. Gene expression profiling analysis of copper homeostasis in Arabidopsis thaliana [J]. Biochem. biophys. res. commun., 2010, 393(2):248-252. doi: 10.1016/j.bbrc.2010.01.111 URL
[62]	WOESTE KE, KIEBER JJ. Strong loss-of-function mutation in RAN1 results in constitutive activation of the ethylene response pathway as well as a rosette-lethal phenotype[J]. Plant cell, 2000, 12(3):443-455. doi: 10.1105/tpc.12.3.443 URL
[63]	MIGOCKA M, POSYNIAK E, MACIASZCZYK-DZIUBINSKA E, et al. Functional and biochemical characterization of cucumber genes encoding two copper ATPases CsHMA5.1 and CsHMA5.2[J]. J. biol. chem., 2015, 290(25):15717-15729. doi: 10.1074/jbc.M114.618355 pmid: 25963145
[64]	JUNG H I, GAYOMBA S R, RUTZKE M A, et al. 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]. J. biol. chem., 2012, 287(40):33252-33267. doi: 10.1074/jbc.M112.397810 URL
[65]	SANCENON V, PUIG S, MIRA H, et al. Identification of a copper transporter family in Arabidopsis thaliana[J]. Plant mol. biol., 2003, 51(4):577-587. doi: 10.1023/A:1022345507112 URL
[66]	ANA R M, NURIA AC, CHARLOTTE P, et al. Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production[J]. Plant cell environ., 2013, 36(4):844-855. doi: 10.1111/pce.2013.36.issue-4 URL
[67]	GARCIA L, WELCHEN E, GONZALEZ D H. Mitochondria and copper homeostasis in plants[J]. Mitochondrion, 2014, 19:269-274. doi: 10.1016/j.mito.2014.02.011 URL
[68]	BOCK K W, HONYS D, WARD J M, et al. Integrating membrane transport with male gametophyte development and function through transcriptomics[J]. Plant physiol., 2006, 140(4):1151-1168. doi: 10.1104/pp.105.074708 pmid: 16607029
[69]	ANDRES-COLAS N, CARRIO-SEGUI A, ABDEL-GHANY S E, et al. Expression of the intracellular COPT3-mediated Cu transport is temporally regulated by the TCP16 transcription factor[J]. Front. plant sci., 2018, 9:910. doi: 10.3389/fpls.2018.00910 URL
[70]	KLAUMANN S, NICKOLAUS S D, FURST S H, et al. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana[J]. New phytol., 2011, 192(2):393-404. doi: 10.1111/j.1469-8137.2011.03798.x pmid: 21692805
[71]	GARCIA-MOLINA A, ANDRES-COLAS N, PEREA-GARCIA A, et al. The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency[J]. Plant j., 2011, 65(6):848-860. doi: 10.1111/tpj.2011.65.issue-6 URL
[72]	CARRIO-SEGUI A, GARCIA-MOLINA A, SANZ A, et al. Defective copper transport in the copt5 mutant affects cadmium tolerance[J]. Plant cell physiol., 2015, 56(3):442-454. doi: 10.1093/pcp/pcu180 URL
[73]	MILNER M J, SEAMON J, CRAFT E, et al. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis[J]. J. exp. bot., 2013(1):369-381. doi: 10.1093/jxb/ers315 pmid: 23264639
[74]	LIU X S, FENG S J, ZHANG B Q, et al. OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice[J]. BMC plant biol., 2019, 19(1):283. doi: 10.1186/s12870-019-1899-3 pmid: 31248369
[75]	CHEN C C, CHEN Y Y, TANG I C, et al. Arabidopsis SUMO E3 ligase SIZ1 is involved in excess copper tolerance[J]. Plant physiol., 2011, 156(4):2225-2234. doi: 10.1104/pp.111.178996 URL
[76]	ZHANG C, LU W, YANG Y, et al. OsYSL16 is required for preferential Cu distribution to floral rrgans in rice[J]. Plant cell physiol., 2018, 59(10):2039-2051. doi: 10.1093/pcp/pcy124 URL
[77]	GUO J, GREEN B R, MALDONADO M T. Sequence analysis and gene expression of potential components of copper transport and homeostasis in thalassiosira pseudonana[J]. Protist, 2015, 166(1):58-77. doi: 10.1016/j.protis.2014.11.006 pmid: 25562463
[78]	李一涵, 于浪柳, 李春燕, 等. 大麦NRAMP全基因组鉴定及重金属胁迫下基因表达分析[J]. 生物技术通报, 2022, 38(6):103-111. doi: 10.13560/j.cnki.biotech.bull.1985.2021-1006
[79]	CHOU M, SUN Y, YANG J, et al. Comprehensive analysis of phenotype, microstructure and global transcriptional profiling to unravel the effect of excess copper on the symbiosis between nitrogen-fixing bacteria and Medicago lupulina[J]. Sci. total environ., 2019, 656:1346-1357. doi: 10.1016/j.scitotenv.2018.12.005 URL
[80]	PALUMAA P. Copper chaperones. The concept of conformational control in the metabolism of copper[J]. FEBS lett., 2013, 587(13):1902-1910. doi: 10.1016/j.febslet.2013.05.019 pmid: 23684646
[81]	O"HALLORAN T V, CULOTTA V C. Metallochaperones, an intracellular shuttle service for metal ions[J]. J. biol. chem., 2000, 275(33):25057-25060. doi: 10.1074/jbc.R000006200 pmid: 10816601
[82]	MIRA H, MARTINEZ-GARCIA F, PENARRUBIA L. Evidence for the plant-specific intercellular transport of the Arabidopsis copper chaperone CCH[J]. Plant j., 2001, 25(5):521-528. pmid: 11309142
[83]	CHU C C, LEE W C, GUO W Y, et al. A copper chaperone for superoxide dismutase that confers three types of copper/zinc superoxide dismutase activity in Arabidopsis[J]. Plant physiol., 2005, 139(1):425-436. doi: 10.1104/pp.105.065284 URL
[84]	PUIG S, MIRA H, DORCEY E, et al. Higher plants possess two different types of ATX1-like copper chaperones[J]. Biochem. biophys. res. commun., 2007, 354(2):385-390. doi: 10.1016/j.bbrc.2006.12.215 URL
[85]	SHIN L J, LO J C, YEH K C. Copper chaperone antioxidant protein1 is essential for copper homeostasis[J]. Plant physiol., 2012, 159(3):1099-1110. doi: 10.1104/pp.112.195974 URL
[86]	SHIN L J, YEH K C. Overexpression of Arabidopsis ATX1 retards plant growth under severe copper deficiency[J]. Plant signal. behav., 2012, 7(9):1082-1083. doi: 10.4161/psb.21147 URL
[87]	ATTALLAH C V, WELCHEN E, GONZALEZ D H. The promoters of Arabidopsis thaliana genes AtCOX17and encoding a copper chaperone involved in cytochrome c oxidase biogenesis, are preferentially active in roots and anthers and induced by biotic and abiotic stress[J]. Physiol. plant., 2007, 129(1):123-134. doi: 10.1111/ppl.2007.129.issue-1 URL
[88]	PENARRUBIA L, ROMERO P, CARRIO-SEGUI A, et al. Temporal aspects of copper homeostasis and its crosstalk with hormones[J]. Front. plant sci., 2015, 6:255. doi: 10.3389/fpls.2015.00255 pmid: 25941529
[89]	KAPOOR D, SINGH S, KUMAR V, et al. Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS)[J]. Plant gene, 2019, 19:100182. doi: 10.1016/j.plgene.2019.100182 URL
[90]	ZHANG N, XUE C, WANG K, et al. Efficient oxidative degradation of fluconazole by a heterogeneous Fenton process with Cu-V bimetallic catalysts[J]. Chem. eng. j., 2020, 380:122516. doi: 10.1016/j.cej.2019.122516 URL
[91]	刘军, 温学森, 郎爱东. 植物根系分泌物成分及其作用的研究进展[J]. 食品与药品, 2007(3):63-65.
[92]	LYUBENOVA L, KUHN AJ, HOLTKEMEIER A, et al. Root exudation pattern of Typha latifolia L. plants after copper exposure[J]. Plant soil, 2013, 370:187-195. doi: 10.1007/s11104-013-1634-z URL
[93]	晋海军, 王海霞. 植物对重金属镉的吸收与耐受机制研究进展[J]. 中国农学通报, 2019, 35(24):52-57. doi: 10.11924/j.issn.1000-6850.casb19030015
[94]	YADAV P, KAUR R, KANWAR M K, et al. Castasterone confers copper stress tolerance by regulating antioxidant enzyme responses, antioxidants, and amino acid balance in B. juncea seedlings[J]. Ecotoxicol. environ. saf., 2018, 147:725-734. doi: 10.1016/j.ecoenv.2017.09.035 URL
[95]	朱奎正. β-氨基丁酸增强烟草抵御重金属铜、镉胁迫的初步研究[D]. 北京: 中国科学技术大学, 2014.
[96]	MIGOCKA M, MALAS K. Plant responses to copper:Molecular and regulatory mechanisms of copper uptake, distribution and accumulation in plants. In Plant Micronutrient Use Efficiency[M]. Academic Press: Cambridge, MA, USA, 2018:71-86.
[97]	PRINTZ B, LUTTS S, HAUSMAN J F, et al. Copper trafficking in plants and its implication on cell wall dynamics[J]. Front. plant sci., 2016, 7:601. doi: 10.3389/fpls.2016.00601 pmid: 27200069
[98]	GONG Q, WANG L, DAI T, et al. Effects of copper on the growth, antioxidant enzymes and photosynthesis of spinach seedlings[J]. Ecotoxicol. environ. saf., 2019, 171:771-780. doi: 10.1016/j.ecoenv.2019.01.016 URL
[99]	SHAHID M, POURRUT B, DUMAT C, et al. Heavy-metal-induced reactive oxygen species: phytotoxicity and physicochemical changes in plants[J]. Rev environ contam toxicol., 2014, 232:1-44. doi: 10.1007/978-3-319-06746-9_1 pmid: 24984833
[100]	谭珺隽. EDDS缓解过量铜对水稻生理生化和表观遗传学的影响[D]. 武汉: 武汉大学, 2014.
[101]	OGUNKUNLE C O, JIMOH M A, ASOGWA N T, et al. Effects of manufactured nano-copper on copper uptake, bioaccumulation and enzyme activities in cowpea grown on soil substrate[J]. Ecotoxicol environ. saf., 2018, 155(7):86-93. doi: 10.1016/j.ecoenv.2018.02.070 URL
[102]	SALEEM M H, KAMRAN M, ZHOU Y. et al. Appraising growth, oxidative stress and copper phytoextraction potential of flax (Linum usitatissimum L. ) grown in soil differentially spiked with copper[J]. J. environ. manag., 2020, 257(3):109994. doi: 10.1016/j.jenvman.2019.109994 URL
[103]	YOUNIS M E, TOURKY S M N, ELSHARKAWY S E A. Symptomatic parameters of oxidative stress and antioxidant defense system in Phaseolus vulgaris L. in response to copper or cadmium stress[J]. S. afr. j. bot. 2018, 117:207-214. doi: 10.1016/j.sajb.2018.05.019 URL
[104]	NOCTOR G, MHAMDI A, CHAOUCH S, et al. Glutathione in plants: an integrated overview[J]. Plant cell environ. 2012, 35(2):454-484. doi: 10.1111/j.1365-3040.2011.02400.x URL
[105]	CONTE S S, CHU H H, CHAN-RODRIGUEZ D, et al. Arabidopsis thaliana yellow stripe1-like4 and yellow stripe1-like6 localize to internal cellular membranes and are involved in metal ion homeostasis[J]. Front. plant, 2013, 4(283):283.
[106]	MOSTOFA M G, SERAJ Z I, FUJITA M. Exogenous sodium nitroprusside and glutathione alleviate copper toxicity by reducing copper uptake and oxidative damage in rice (Oryza sativa L. ) seedlings[J]. Protoplasma, 2014, 251(6):1373-1386. doi: 10.1007/s00709-014-0639-7 URL
[107]	ZLOBIN I E, KARTASHOV A V, SHPAKOVSKI G V. Different roles of glutathione in copper and zinc chelation in Brassica napus roots[J]. Plant physiol. biochem., 2017, 118:333-341. doi: 10.1016/j.plaphy.2017.06.029 URL
[108]	THOUNAOJAM TC, PANDA P, MAZUMDAR P, et al. Excess copper induced oxidative stress and response of antioxidants in rice[J]. Plant physiol. biochem., 2012, 53:33-39. doi: 10.1016/j.plaphy.2012.01.006 URL
[109]	RAUSER W E. Structure and function of metal chelators produced by plants: the case for organic acids, amino acids, phytin, and metallothioneins[J]. Cell biochem. biophys., 1999, 31(1):19-48. doi: 10.1007/BF02738153 pmid: 10505666
[110]	CARRASCO-GIL S, ALVAREZ-FERNANDEZ A, SOBRINO-PLATA J, et al. Complexation of Hg with phytochelatins is important for plant Hg tolerance[J]. Plant cell environ., 2011, 34(5):778-791. doi: 10.1111/pce.2011.34.issue-5 URL
[111]	NAVARRETE A, GONZALEZ A, GOMEZ M, et al. Copper excess detoxification is mediated by a coordinated and complementary induction of glutathione, phytochelatins and metallothioneins in the green seaweed Ulva compress[J]. Plant physiol. biochem., 2019, 135:423-431. doi: 10.1016/j.plaphy.2018.11.019 URL
[112]	LIU J, SHI X, QIAN M, et al. Copper-induced hydrogen peroxide upregulation of a metallothionein gene, OsMT2c, from Oryza sativa L. confers copper tolerance in Arabidopsis thaliana[J]. J. hazard. mater., 2015, 294:99-108. doi: 10.1016/j.jhazmat.2015.03.060 URL
[113]	BENATTI M R, YOOKONGKAEW N, MEETAM M, et al. Metallothionein deficiency impacts copper accumulation and redistribution in leaves and seeds of Arabidopsis[J]. New phytol., 2014, 202(3):940-951. doi: 10.1111/nph.2014.202.issue-3 URL
[114]	PAREDES S D, KORKMAZ A, MANCHESTER L C, et al. Phytomelatonin: a review[J]. J. exp. bot. 2009, 60:57-69. doi: 10.1093/jxb/ern284 pmid: 19033551
[115]	CAO Y Y, QI C D, LI S, et al. Melatonin alleviates copper toxicity via improving copper sequestration and ROS scavenging in cucumber[J]. Plant cell physiol., 2019, 60(3):562-574. doi: 10.1093/pcp/pcy226 URL
[116]	ZHAO X, XIA H, XIE Y, et al. Oxidation resistance of exogenous melatonin on leaves of kiwifruit seedlings under copper stress. In 2017 2nd International conference on civil, transportation and environmental engineering (ICCTE 2017), Advances in engineering research[C]. Atlantis press: Amsterdam, the netherlands, 2017:216-219.

物种		基因		表达模式	亚细胞定位	参考文献
拟南芥 Arabidopisis thaliana		AtCOPT1		大多数组织、根、生殖组织	质膜	[30-31]
		AtCOPT2		大多数组织、根	质膜	[31-32]
		AtCOPT3		生殖组织	质膜	[30]
		AtCOPT5		大多数组织、根、生殖组织	液泡	[32]
		AtCOPT6		生殖组织、木质部和韧皮部维管组织	质膜	[32]
		AtHMA1		绿色组织	叶绿体包膜	[33]
		AtHMA5		根、花	质膜	[34]
		AtHMA6		根、芽	叶绿体	[35]
		AtHMA7		根、花	内质网	[36]
		AtHMA8		地上部分	类囊体膜	[37]
		AtYSL1		大多数组织、根	质膜	[38]
		AtYSL2		大多数组织、根、茎	质膜、导管	[39]
		AtYSL3		幼叶、根、茎	质膜	[39]
		AtZIP2		根	细胞膜	[40]
		AtZIP4		根	—	[40]
水稻 Oryza sativa		OsCOPT1		大多数组织、根、茎	质膜	[41]
		OsCOPT2		大多数组织、根	质膜	[42]
		OsHMA5		节点处维管束的木质部区域、花梗、叶柄	质膜	[34]
		OsHMA9		木质部和韧皮部维管组织	质膜	[43]
		OsYSL16		根、茎、叶片的韧皮部和维管组织	质膜	[44]
蒺藜苜蓿 Medicago truncatula		MtCOPT1		根	质膜	[31]
		MtCOPT3		根瘤	—	[31]
		MtCOPT4		根	—	[31]
		MtCOPT5		根	—	[31]
		MtCOPT8		根、木质部和韧皮部维管组织	—	[31]
葡萄 Vitis vinifera		VvCTr1		木质部和韧皮部维管组织、叶、根	液泡膜	[45]
		VvCTr2		——	—	[46]
		VvCTr8		——	—	[46]
小麦 Triticum aestivum	TaCT1		木质部和韧皮部维管组织、根、穗		高尔基体	[47]
油菜 Brassica napus	BnHMA1		叶		—	[48]
油菜 Brassica napus	BnCOPT2		根		—	[48]
大豆 Glycine max	GmHMA8		叶		类囊体膜	[49]
大麦 Hordeum vulgare	HvHMA1		叶、籽粒		叶绿体包膜	[50]
大麦 Hordeum vulgare	HvYSL2		茎、幼叶、根内胚层		—	[51]
花生 Arachis hypogaea	AhYSL3.1		根、茎、幼叶、老叶		质膜	[52]
花生 Arachis hypogaea	AhYSL3.2		根、茎、幼叶、老叶		—	[52]

物种		基因		表达模式	亚细胞定位	参考文献
拟南芥 Arabidopisis thaliana		AtCOPT1		大多数组织、根、生殖组织	质膜	[30-31]
		AtCOPT2		大多数组织、根	质膜	[31-32]
		AtCOPT3		生殖组织	质膜	[30]
		AtCOPT5		大多数组织、根、生殖组织	液泡	[32]
		AtCOPT6		生殖组织、木质部和韧皮部维管组织	质膜	[32]
		AtHMA1		绿色组织	叶绿体包膜	[33]
		AtHMA5		根、花	质膜	[34]
		AtHMA6		根、芽	叶绿体	[35]
		AtHMA7		根、花	内质网	[36]
		AtHMA8		地上部分	类囊体膜	[37]
		AtYSL1		大多数组织、根	质膜	[38]
		AtYSL2		大多数组织、根、茎	质膜、导管	[39]
		AtYSL3		幼叶、根、茎	质膜	[39]
		AtZIP2		根	细胞膜	[40]
		AtZIP4		根	—	[40]
水稻 Oryza sativa		OsCOPT1		大多数组织、根、茎	质膜	[41]
		OsCOPT2		大多数组织、根	质膜	[42]
		OsHMA5		节点处维管束的木质部区域、花梗、叶柄	质膜	[34]
		OsHMA9		木质部和韧皮部维管组织	质膜	[43]
		OsYSL16		根、茎、叶片的韧皮部和维管组织	质膜	[44]
蒺藜苜蓿 Medicago truncatula		MtCOPT1		根	质膜	[31]
		MtCOPT3		根瘤	—	[31]
		MtCOPT4		根	—	[31]
		MtCOPT5		根	—	[31]
		MtCOPT8		根、木质部和韧皮部维管组织	—	[31]
葡萄 Vitis vinifera		VvCTr1		木质部和韧皮部维管组织、叶、根	液泡膜	[45]
		VvCTr2		——	—	[46]
		VvCTr8		——	—	[46]
小麦 Triticum aestivum	TaCT1		木质部和韧皮部维管组织、根、穗		高尔基体	[47]
油菜 Brassica napus	BnHMA1		叶		—	[48]
油菜 Brassica napus	BnCOPT2		根		—	[48]
大豆 Glycine max	GmHMA8		叶		类囊体膜	[49]
大麦 Hordeum vulgare	HvHMA1		叶、籽粒		叶绿体包膜	[50]
大麦 Hordeum vulgare	HvYSL2		茎、幼叶、根内胚层		—	[51]
花生 Arachis hypogaea	AhYSL3.1		根、茎、幼叶、老叶		质膜	[52]
花生 Arachis hypogaea	AhYSL3.2		根、茎、幼叶、老叶		—	[52]