Molecular and Microbial Mechanisms of Plant Response to Copper Stress
ZHANG Jing1, WANG Jian-Feng3, GONG Ji-Yi1,2, WANG Li1, CHEN Xian-Lei1, CHEN Lan-Lan1, LI Na1, LIU Jie1,2, YI Yin1,2,*
1 School of Life Sciences, Guizhou Normal University, Guiyang 550001, China; 2 Key Laboratory of National Forestry and Grassland Administration for Biodiversity Conservation of Southwest Karst Mountains, Guizhou Normal University, Guiyang 550001, China; 3 State Key Laboratory of Herbage Improvement and Grassland Agroecosystems/Center for Grassland Microbiome, Lanzhou University, Lanzhou 730000, China
Abstract:At present, soil heavy metal pollution has become a global major environmental issue. Copper (Cu) is an essential trace element for plants, but high concentrations of copper have toxic effects on plants. In order to adapt to copper stress environments, plants have developed various copper-tolerant molecular and microbiological mechanisms. This article introduces the role of hyperaccumulating plants in copper-contaminated soil, systematically outlining the morphological, physiological, molecular, and rhizospheric microbiological mechanisms of plant responses to copper stress, including the following: The physiological defense and absorption transport mechanisms of plants against copper; Plant growth promoting rhizobacteria (PGPR) enhancing plant tolerance to copper stress by promoting plant nutrient absorption and secreting growth-regulating substances; PGPR reducing copper damage to plants by inducing systemic resistance and adsorbing accumulated copper ions; The mechanisms of plant responses to copper stress mediated by rhizospheric microbial community structure and function; And the changes in rhizospheric microbial community structure in response to different copper stresses. This article provides scientific support for the future breeding of copper-tolerant plant germplasm and the management and restoration of copper-contaminated soil.
[1] 沈甜, 王琼瑶, 崔永亮,等. 2020.植物根际促生细菌对蒲儿根富集铜及土壤理化性质的影响[J].农业环境科学学报, 39(3): 572-580. (Shen T, Wang Q Y, Cui Y L, et al.2020. Effects of plant growth-promoting rhizobacteria on the copper enrichment ability of Sinosenecio oldhamianus and physicochemical properties of soil[J]. Journal of Agro-Environment Science, 39(3): 572-580.) [2] 张越, 满奕, 卜芋芬, 等. 2020. 细胞骨架参与调控细胞壁形成的研究进展[J]. 中国科学:生命科学, 50: 176-186. (Zhang Y, Man Y, Bu Y F, et al.2020. Role of cytoskeleton in plant cell wall formation (in Chinese)[J]. Scientia Sinica Vitae, 50: 176-186.) [3] Abdel-Ghany S E, Burkhead J L, Gogolin K A, et al.2005. At CCS is a functional homolog of the yeast copper chaperone Ccs1/Lys7[J]. FEBS Letters, 579(11): 2307-2312. [4] Adrees M, Ali S, Rizwan M, et al.2015. The effect of excess copper on growth and physiology of important food crops: A review[J]. Environmental Science and Pollution Research, 22: 8148-8162. [5] Ahemad M.2015. Phosphate-solubilizing bacteria-assisted phytoremediation of metalliferous soils: A review[J]. 3 Biotech, 5(2): 111-121. [6] Babu A G, Kim J D, Oh B T.2013. Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1[J]. Journal of Hazardous Materials, 250: 477-483. [7] Balzano S, Sardo A, Blasio M, et al.2020. Microalgal metalothioneins and phytochelatins and their potential use in bioremediation[J]. Frontiers in Microbiology, 11: 517. [8] Beckett H T, Davis R D, 1977. Upper critical levels of toxic elements in plants[J]. New Phytologist, 79(1): 95-106. [9] Bhattacharyya D, Duta S, Yu S M, et al.2018. Taxonomic and functional changes of bacterial communities in the rhizosphere of kimchi cabbage after seed bacterization with Proteus vulgaris JBLS202[J]. The Plant Pathology Journal, 34(4): 286. [10] Blaby-Haas C E, Padilla-Benavides T, Stübe R, et al.2014. Evolution of a plant-specific copper chaperone family for chloroplast copper homeostasis[J]. Proceedings of the National Academy of Sciences of the USA, 111(50): E5480-E5487. [11] Bossuyt B T, Janssen C R, 2004. Long-term acclimation of Pseudokirchneriella subcapitata (Korshikov) Hindak to different copper concentrations: Changes in tolerance and physiology[J]. Aquatic Toxicology, 68(1): 61-74. [12] Cao Y Y, Qi C D, Li S, et al.2019. Melatonin alleviates copper toxicity via improving copper sequestration and ROS scavenging in cucumber[J]. Plant and Cell Physiology, 60(3): 562-574. [13] Carlos M H J, Stefani P V Y, Janette A M, et al.2016. Assessing the effects of heavy metals in ACC deaminase and IAA production on plant growth-promoting bacteria[J]. Microbiological Research, 188: 53-61. [14] Carrió-Seguí À, Romero P, Curie C, et al.2019. Copper transporter COPT5 participates in the crosstalk between vacuolar copper and iron pools mobilisation[J]. Scientific Reports, 9(1): 4648. [15] Catty P, Boutigny S, Miras R, et al.2011. Biochemical characterization of AtHMA6/PAA1, a chloroplast envelope Cu (I)-ATPase[J]. Journal of Biological Chemistry, 286(42): 36188-36197. [16] Chen B, Luo S, Wu Y, et al.2017. The effects of the endophytic bacterium Pseudomonas fluorescens Sasm05 and IAA on the plant growth and cadmium uptake of Sedum alfredii Hance[J]. Frontiers in Microbiology, 8: 2538. [17] Chen C C, Chen Y Y, Tang I C, et al.2011. Arabidopsis SUMO E3 ligase SIZ1 is involved in excess copper tolerance[J]. Plant Physiology, 156(4): 2225-2234. [18] Chen G, Li J, Han H, et al.2022. Physiological and molecular mechanisms of plant responses to copper stress[J]. International Journal of Molecular Sciences, 23(21): 12950. [19] Chiou W Y, Hsu F C.2019. Copper toxicity and prediction models of copper content in leafy vegetables[J]. Sustainability, 11(22): 6215. [20] Cobbett C, Goldsbrough P.2002. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis[J]. Annual Review of Plant Biology, 53(1): 159-182. [21] Colangelo E P, Guerinot M L.2006. Put the metal to the petal: metal uptake and transport throughout plants[J]. Current Opinion in Plant Biology, 9(3): 322-330. [22] Colzi I, Arnetoli M, Gallo A, et al.2012. Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L.[J]. Environmental and Experimental Botany, 78: 91-98. [23] DiDonato Jr R J, Roberts L A, Sanderson T, et al.2004. Arabidopsis Yellow Stripe‐Like2 (YSL2): A metal‐regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes[J]. The Plant Journal, 39(3): 403-414. [24] Dimkpa C O, Merten D, Svatoš A, et al.2009. Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores[J]. Soil Biology and Biochemistry, 41(1): 154-162. [25] Edward E J, King W S, Teck S L C, et al.2013. Antagonistic activities of endophytic bacteria against Fusarium wilt of black pepper (Piper nigrum)[J]. International Journal of Agriculture & Biology, 15(2): 291-296. [26] Fardeau S, Mullie C, Dassonville-Klimpt A, et al.2011. Bacterial iron uptake: A promising solution against multidrug resistant bacteria[M]//, Toledo M V(eds.), Science Against Microbial Pathogens: Communicating Current Research and Technological Advances, pp. 695-705. [27] Feigl G, Kumar D, Lehotai N, et al.2013. Physiological and morphological responses of the root system of Indian mustard (Brassica juncea L. Czern.) and rapeseed (Brassica napus L.) to copper stress[J]. Ecotoxicology and Environmental Safety, 94: 179-189. [28] Garcia L, Welchen E, Gonzalez D H.2014. Mitochondria and copper homeostasis in plants[J]. Mitochondrion, 19: 269-274. [29] Gechev T S, Van Breusegem F, Stone J M, et al.2006. Reactive oxygen species as signals that modulate plant stress responses and programmed cell death[J]. Bioessays, 28(11): 1091-1101. [30] Ghazaryan K, Movsesyan H, Ghazaryan N.et al.2019. Copper phytoremediation potential of wild plant species growing in the mine polluted areas of Armenia[J]. Environmental Pollution, 249: 491-501. [31] Gomes M P, Nogueira M D O G, Castro E M D, et al.2011. Ecophysiological and anatomical changes due to uptake and accumulation of heavy metal in Brachiaria decumbens[J]. Scientia Agricola, 68: 566-573. [32] Gong Q, Li Z, Wang L, et al.2021. Gibberellic acid application on biomass, oxidative stress response, and photosynthesis in spinach (Spinacia oleracea L.) seedlings under copper stress[J]. Environmental Science and Pollution Research, 28(38): 53594-53604. [33] Górska M, Roszyk E, 2019. Wood structure of Scots pine (Pinus sylvestris L.) growing on flotation tailings[J]. Folia Forestalia Polonica, 61(2): 112-122. [34] Goswami D, Thakker J N, Dhandhukia P C.2016. Portraying mechanics of plant growth promoting rhizobacteria (PGPR): A review[J]. Cogent Food & Agriculture, 2(1): 1127500. [35] Gupta R, Khan F, Alqahtani F M, et al.2024. Plant growth-promoting rhizobacteria (PGPR) assisted bioremediation of heavy metal toxicity[J]. Applied Biochemistry and Biotechnology, 196(5): 2928-2956. [36] Hall J Á, 2002. Cellular mechanisms for heavy metal detoxification and tolerance[J]. Journal of Experimental Botany, 53(366): 1-11. [37] Hamidpour M, Karamooz M, Akhgar A, et al.2019. Adsorption of cadmium and zinc onto micaceous minerals: Effect of siderophore desferrioxamine B[J]. Pedosphere, 29(5): 590-597. [38] Hoque M N, Tahjib-Ul-Arif M, Hannan A, et al.2021. Melatonin modulates plant tolerance to heavy metal stress: Morphological responses to molecular mechanisms[J]. International Journal of Molecular Sciences, 22(21): 11445. [39] Huang X Y, Deng F, Yamaji N, et al.2016. A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain[J]. Nature Communications, 7(1): 12138. [40] Jiang C Y, Sheng X F, Qian M, et al.2008. Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil[J]. Chemosphere, 72(2): 157-164. [41] Ju W, Jin, X, Liu L, et al.2020. Rhizobacteria inoculation benefits nutrient availability for phytostabilization in copper contaminated soil: Drivers from bacterial community structures in rhizosphere[J]. Applied Soil Ecology, 150: 103450. [42] Jung H I, Gayomba S R, Rutzke M A, et al.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]. Journal of Biological Chemistry, 287(40): 33252-33267. [43] Karthik C, Arulselvi P I, 2017. Biotoxic effect of chromium (VI) on plant growth-promoting traits of novel Cellulosimicrobium funkei strain AR8 isolated from Phaseolus vulgaris rhizosphere[J]. Geomicrobiology Journal, 34(5): 434-442. [44] Keiblinger K M, Schneider M, Gorfer M, et al.2018. Assessment of Cu applications in two contrasting soils-effects on soil microbial activity and the fungal community structure[J]. Ecotoxicology, 27: 217-233. [45] Khalid S, Shahid M, Niazi N K, et al.2017. A comparison of technologies for remediation of heavy metal contaminated soils[J]. Journal of Geochemical Exploration, 182: 247-268. [46] Klaumann S, Nickolaus S D, Fürst S H, et al.2011. The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana[J]. New Phytologist, 192(2): 393-404. [47] Konno H, Nakato T, Nakashima S, et al.2005. Lygodium japonicum fern accumulates copper in the cell wall pectin[J]. Journal of Experimental Botany, 56(417): 1923-1931. [48] Kosakivska I V, Babenko L M, Romanenko K O, et al.2021. Molecular mechanisms of plant adaptive responses to heavy metals stress[J]. Cell Biology International, 45(2): 258-272. [49] Kunito T, Saeki K, Oyaizu H, et al.1999. Influences of copper forms on the toxicity to microorganisms in soils[J]. Ecotoxicology and Environmental Safety, 44(2): 174-181. [50] Li C, Wang X, Huang H, et al.2021. Effect of multiple heavy metals pollution to bacterial diversity and community structure in farmland soils[J]. Human and Ecological Risk Assessment: An International Journal, 27(3): 724-741. [51] Li J, Yu J, Du D, et al.2019. Analysis of anatomical changes and cadmium distribution in Aegiceras corniculatum (L.) Blanco roots under cadmium stress[J]. Marine Pollution Bulletin, 149: 110536. [52] Li S, Lu S, Wang J, et al.2023. Responses of physiological, morphological and anatomical traits to abiotic stress in woody plants[J]. Forests, 14(9): 1784. [53] Li Y H, Yu L L, Li C Y, et al.2022. Whole genome identification of barley NRAMP and gene expression analysis under heavy metal stress[J]. Biotechnology Bulletin, 38(6): 103. [54] Lidon F C, Henriques F S, 1998. Role of rice shoot vacuoles in copper toxicity regulation[J]. Environmental and Experimental Botany, 39(3): 197-202. [55] Liu X S, Feng S J, Zhang B Q, et al.2019. OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice[J]. BMC Plant Biology, 19: 1-16. [56] Ma Y, Oliveira R S, Freitas H, et al.2016a. Biochemical and molecular mechanisms of plant-microbe-metal interactions: Relevance for phytoremediation[J]. Frontiers in Plant Science, 7: 918. [57] Ma Y, Rajkumar M, Zhang C, et al.2016b. Beneficial role of bacterial endophytes in heavy metal phytoremediation[J]. Journal of Environmental Management, 174: 14-25. [58] Manoj S R, Karthik C, Kadirvelu K, et al.2020. Understanding the molecular mechanisms for the enhanced phytoremediation of heavy metals through plant growth promoting rhizobacteria: A review[J]. Journal of Environmental Management, 254: 109779. [59] Marques D M, Da Silva A B, Mantovani J R, et al.2019. Root morphology and leaf gas exchange in Peltophorum dubium (Spreng.) Taub. (Caesalpinioideae) exposed to copper-induced toxicity[J]. South African Journal of Botany, 121: 186-192. [60] Mohite B V, Koli S H, Patil S V, 2018. Heavy metal stress and its consequences on exopolysaccharide (EPS)-producing Pantoea agglomerans[J]. Applied Biochemistry and Biotechnology, 186: 199-216. [61] Naik M M, Dubey S K, 2013. Lead resistant bacteria: lead resistance mechanisms, their applications in lead bioremediation and biomonitoring[J]. Ecotoxicology and Environmental Safety, 98: 1-7. [62] Napoli M, Cecchi S, Grassi C, et al.2019. Phytoextraction of copper from a contaminated soil using arable and vegetable crops[J]. Chemosphere, 219: 122-129. [63] Navarrete A, González A, Gómez M, et al.2019. Copper excess detoxification is mediated by a coordinated and complementary induction of glutathione, phytochelatins and metallothioneins in the green seaweed Ulva compressa[J]. Plant Physiology and Biochemistry, 135: 423-431. [64] Omasits U, Ahrens C H, Müller S, et al.2014. Protter: Interactive protein feature visualization and integration with experimental proteomic data[J]. Bioinformatics, 30(6): 884-886. [65] Palanivel T M, Pracejus B, Victor R, 2020. Phytoremediation potential of castor (Ricinus communis L.) in the soils of the abandoned copper mine in Northern Oman: Implications for arid regions[J]. Environmental Science and Pollution Research, 27: 17359-17369. [66] Park S, Back K, 2012. Melatonin promotes seminal root elongation and root growth in transgenic rice after germination[J]. Journal of Pineal Research, 53(4): 385-389. [67] Perea-García A, Garcia-Molina A, Andrés-Colás N, et al.2013. Arabidopsis copper transport protein COPT2 participates in the cross talk between iron deficiency responses and low-phosphate signaling[J]. Plant Physiology, 162(1): 180-194. [68] Pires C, Franco A R, Pereira S I, et al.2017. Metal (loid)-contaminated soils as a source of culturable heterotrophic aerobic bacteria for remediation applications[J]. Geomicrobiology Journal, 34(9): 760-768. [69] Qin C, Quan L, Wang C, et al.2022. Differential physiological responses of copper-sensitive and copper-tolerant Elsholtzia species to copper toxicity: The character of cell walls and their subfractions[J]. Journal of Soil Science and Plant Nutrition, 22(4): 4168-4178. [70] Rauser W E, 1999. Structure and function of metal chelators produced by plants: The case for organic acids, amino acids, phytin, and metallothioneins[J]. Cell Biochemistry and Biophysics, 31: 19-48. [71] Robson A D, Loneragan J F, Gartrell J W, et al.1984. Diagnosis of copper deficiency in wheat by plant analysis[J]. Australian Journal of Agricultural Research, 35(3): 347-358. [72] Rono J K, Le Wang L, Wu X C, et al.2021. Identification of a new function of metallothionein-like gene OsMT1e for cadmium detoxification and potential phytoremediation[J]. Chemosphere, 265: 129136. [73] Schlüter U, Mascher M, Colmsee C, et al.2012. Maize source leaf adaptation to nitrogen deficiency affects not only nitrogen and carbon metabolism but also control of phosphate homeostasis[J]. Plant Physiology, 160(3): 1384-1406. [74] Sessitsch A, Kuffner M, Kidd P, et al.2013. The role of plant-associated bacteria in the mobilization and phytoextraction of trace elements in contaminated soils[J]. Soil Biology and Biochemistry, 60: 182-194. [75] Shahid M, Pourrut B, Dumat C, et al.2014. Heavy-metal-induced reactive oxygen species: Phytotoxicity and physicochemical changes in plants[J]. Reviews of Environmental Contamination and Toxicology, 232: 1-44. [76] Sharma S S, Dietz K J, Mimura T.2016. Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants[J]. Plant, Cell & Environment, 39(5): 1112-1126. [77] Shen R F, Zhao X Q.2015. Role of soil microbes in the acquisition of nutrients by plants[J]. Acta Ecologica Sinica, 35(20): 6584-6591. [78] Shi Y, Lou K, Li C, 2009. Promotion of plant growth by phytohormone-producing endophytic microbes of sugar beet[J]. Biology and Fertility of Soils, 45: 645-653. [79] Shin M N, Shim J, You Y, et al.2012. Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma[J]. Journal of Hazardous Materials, 199: 314-320. [80] Silambarasan S, Logeswari P, Valentine A, et al.2020. Pseudomonas citronellolis strain SLP6 enhances the phytoremediation efficiency of Helianthus annuus in copper contaminated soils under salinity stress[J]. Plant and Soil, 457: 241-253. [81] Singh R P, Jha P N, 2018. Priming with ACC-utilizing bacterium attenuated copper toxicity, improved oxidative stress tolerance, and increased phytoextraction capacity in wheat[J]. Environmental Science and Pollution Research, 25: 33755-33767. [82] Staňová A, Ďurišová E, Banásová V, et al.2012. Root system morphology and primary root anatomy in natural non-metallicolous and metallicolous populations of three Arabidopsis species differing in heavy metal tolerance[J]. Biologia, 67: 505-516. [83] Sugiyama A, Ueda Y, Zushi T, et al.2014. Changes in the bacterial community of soybean rhizospheres during growth in the field[J]. PLOS ONE, 9(6): e100709. [84] Tan J, He S, Yan S, et al.2014. Exogenous EDDS modifies copper-induced various toxic responses in rice[J]. Protoplasma, 251: 1213-1221. [85] Wang G L, Que F, Xu Z S, et al.2015. Exogenous gibberellin altered morphology, anatomic and transcriptional regulatory networks of hormones in carrot root and shoot[J]. BMC Plant Biology, 15: 1-12. [86] Wang H, Du H, Li H, et al.2018. Identification and functional characterization of the ZmCOPT copper transporter family in maize[J]. PLOS ONE, 13(7): e0199081. [87] Wang Y, Li Q, Shi J, et al.2008. Assessment of microbial activity and bacterial community composition in the rhizosphere of a copper accumulator and a non-accumulator[J]. Soil Biology and Biochemistry, 40(5): 1167-1177. [88] Wang Y, Shi J, Wang H, et al.2007. The influence of soil heavy metals pollution on soil microbial biomass, enzyme activity, and community composition near a copper smelter[J]. Ecotoxicology and Environmental Safety, 67(1): 75-81. [89] Wang Y P, Li Q, Qi L, et al.2010. Differences in the rhizosphere microbial activity and community composition of commelina communis along a copper contamination gradient[J]. Communications in Soil Science and Plant Analysis, 41(17): 2046-2056. [90] Xia Y, Farooq M A, Javed M T, et al.2020. Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance[J]. Plant Physiology and Biochemistry, 151: 640-649. [91] Xia Y, Qi Y, Yuan Y, et al.2012. Overexpression of Elsholtzia haichowensis metallothionein 1 (EhMT1) in tobacco plants enhances copper tolerance and accumulation in root cytoplasm and decreases hydrogen peroxide production[J]. Journal of Hazardous Materials, 233: 65-71. [92] Xu C, Chen X, Duan D, et al.2015. Effect of heavy-metal-resistant bacteria on enhanced metal uptake and translocation of the Cu-tolerant plant, Elsholtzia splendens[J]. Environmental Science and Pollution Research, 22: 5070-5081. [93] Xu W, Xiang P, Liu X, et al.2020. Closely-related species of hyperaccumulating plants and their ability in accumulation of As, Cd, Cu, Mn, Ni, Pb and Zn[J]. Chemosphere, 251: 126334. [94] Yusuf M, Khan T A, Fariduddin Q, 2016. Interaction of epibrassinolide and selenium ameliorates the excess copper in Brassica juncea through altered proline metabolism and antioxidants[J]. Ecotoxicology and Environmental Safety, 129: 25-34. [95] Zappala M N, Ellzey J T, Bader J, et al.2013. Prosopis pubescens (screw bean mesquite) seedlings are hyperaccumulators of copper[J]. Archives of Environmental Contamination and Toxicology, 65: 212-223. [96] Zeng Q, Ding X, Wang J, et al.2022. Insight into soil nitrogen and phosphorus availability and agricultural sustainability by plant growth-promoting rhizobacteria[J]. Environmental Science and Pollution Research, 29(30): 45089-45106. [97] Zhang C, Lu W, Yang Y, et al.2018a. OsYSL16 is required for preferential Cu distribution to floral organs in rice[J]. Plant and Cell Physiology, 59(10): 2039-2051. [98] Zhang D, Liu X, Ma J, et al.2019. Genotypic differences and glutathione metabolism response in wheat exposed to copper[J]. Environmental and Experimental Botany, 157: 250-259. [99] Zhang J, Martinoia E, Lee Y, 2018b. Vacuolar transporters for cadmium and arsenic in plants and their applications in phytoremediation and crop development[J]. Plant and Cell Physiology, 59(7): 1317-1325. [100] Zhang Y X, Chai T Y, Burkard G, 1999. Research advances on the mechanisms of heavy metal tolerance in plants[J]. Acta Botanica Sinica, 41(5): 453-457. [101] Zheng L, Yamaji N, Yokosho K, et al.2012. YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice[J]. The Plant Cell, 24(9): 3767-3782. [102] Zhu Y, Wang Y, He X, et al.2023. Plant growth-promoting rhizobacteria: A good companion for heavy metal phytoremediation[J]. Chemosphere, 338: 139475.