Abstract
Aims
Arbuscular mycorrhizal fungi (AMF) can enhance cadmium (Cd) tolerance and decrease Cd uptake of rice plant. However, in these processes, the essential role of reactive oxygen species (ROS)-antioxidants interactions is so far not investigated.
Methods
We inoculated AMF, Funneliformis mosseae (Fm) and Rhizophagus intraradices (Ri), to upland rice subjected to 0, 2 or 10 mg Cd kg−1 in soil. ROS, antioxidants, chlorophyll, mesophyll cell ultrastructure, Cd concentration and Cd transporters were measured.
Results
Results showed that the levels of ROS (i.e., superoxide, hydrogen peroxide and lipid peroxidation) were mitigated in +AMF + Cd treatments, especially in +Ri + Cd, compared with −AMF + Cd. For antioxidants, lower levels of catalase, peroxidase and superoxide dismutase, whereas higher levels of glutathione and glutathione peroxidase were observed in +AMF + Cd compared with −AMF + Cd. Chlorophyll content and mesophyll cell ultrastructure were improved by AMF. Cd concentrations in plants were significantly decreased in +AMF + Cd (10 mg Cd kg−1) treatments.
Conclusions
AMF not only decreased Cd accumulation in rice but also regulated the ROS scavenging activities. The variations of ROS and antioxidants were restrained to smaller ranges by AMF. AMF may assist in Cd restriction and thus helping the host to release glutathione for ROS scavenging.
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References
Aghababaei F, Raiesi F (2015) Mycorrhizal fungi and earthworms reduce antioxidant enzyme activities in maize and sunflower plants grown in cd-polluted soils. Soil Biol Biochem 86:87–97. https://doi.org/10.1016/j.soilbio.2015.03.009
Aloui A, Recorbet G, Gollotte A, Robert F, Valot B, Gianinazzi-Pearson V, Aschi-Smiti S, Dumas-Gaudot E (2009) On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 9:420–433. https://doi.org/10.1002/pmic.200800336
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701
Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42. https://doi.org/10.1007/s005720100097
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
Biermann B, Linderman RG (1981) Quantifying vesicular-arbuscular mycorrhizae: a proposed method towards standardization. New Phytol 87:63–67. https://doi.org/10.1111/j.1469-8137.1981.tb01690.x
Bonfante P, Anca I-A (2009) Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 63:363–383. https://doi.org/10.1146/annurev.micro.091208.073504
Cagno RD, Guidi L, Gara LD, Soldatini GF (2001) Combined cadmium and ozone treatments affect photosynthesis and ascorbate-dependent defences in sunflower. New Phytol 151:627–636. https://doi.org/10.1046/j.1469-8137.2001.00217.x
Chan WF, Li H, Wu FY, Wu SC, Wong MH (2013) Arsenic uptake in upland rice inoculated with a combination or single arbuscular mycorrhizal fungi. J Hazard Mater 262:1116–1122. https://doi.org/10.1016/j.jhazmat.2012.08.020
Chen X (2017) Effects of plant-microbes interaction on geotechnical properties of landfill topsoils. Ph.D. Thesis, The Hong Kong University of Science and Technology
Chen BD, Xiao XY, Zhu YG, Smith FA, Miao Xie Z, Smith SE (2007) The arbuscular mycorrhizal fungus Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by Medicago sativa Linn. Sci Total Environ 379:226–234. https://doi.org/10.1016/j.scitotenv.2006.07.038
Chen XW, Li H, Chan WF, Wu C, Wu F, Wu S, Wong MH (2012) Arsenite transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenite stress. Chemosphere 89:1248–1254. https://doi.org/10.1016/j.chemosphere.2012.07.054
Chen XW, Wu FY, Li H, Chan WF, Wu C, Wu SC, Wong MH (2013) Phosphate transporters expression in rice (Oryza sativa L.) associated with arbuscular mycorrhizal fungi (AMF) colonization under different levels of arsenate stress. Environ Exp Bot 87:92–99. https://doi.org/10.1016/j.envexpbot.2012.08.002
Chen H, Tang Z, Wang P, Zhao F-J (2018a) Geographical variations of cadmium and arsenic concentrations and arsenic speciation in Chinese rice. Environ Pollut 238:482–490. https://doi.org/10.1016/j.envpol.2018.03.048
Chen H, Yang X, Wang P, Wang Z, Li M, Zhao FJ (2018b) Dietary cadmium intake from rice and vegetables and potential health risk: a case study in Xiangtan, southern China. Sci Total Environ 639:271–277. https://doi.org/10.1016/j.scitotenv.2018.05.050
Chen XW, Kang Y, So PS, Ng CWW, Wong MH (2018c) Arbuscular mycorrhizal fungi increase the proportion of cellulose and hemicellulose in the root stele of vetiver grass. Plant Soil 425:309–319. https://doi.org/10.1007/s11104-018-3583-z
Chen XW, Wu L, Luo N, Mo CH, Wong MH, Li H (2019) Arbuscular mycorrhizal fungi and the associated bacterial community influence the uptake of cadmium in rice. Geoderma 337:749–757. https://doi.org/10.1016/j.geoderma.2018.10.029
Choppala G, Saifullah BN et al (2014) Cellular mechanisms in higher plants governing tolerance to cadmium toxicity. Crit Rev Plant Sci 33:374–391. https://doi.org/10.1080/07352689.2014.903747
de Andrade SAL, da Silveira APD, Jorge RA, de Abreu MF (2008) Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. Int J Phytorem 10:1–13. https://doi.org/10.1080/15226510701827002
Decros G, Baldet P, Beauvoit B, Stevens R, Flandin A, Colombié S, Gibon Y, Pétriacq P (2019) Get the balance right: ROS homeostasis and redox signalling in fruit. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.01091
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228. https://doi.org/10.1016/j.envexpbot.2014.06.021
Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987. https://doi.org/10.1111/j.1469-8137.2009.03031.x
Firmin S, Labidi S, Fontaine J, Laruelle F, Tisserant B, Nsanganwimana F, Pourrut B, Dalpé Y, Grandmougin A, Douay F, Shirali P, Verdin A, Lounès-Hadj Sahraoui A (2015) Arbuscular mycorrhizal fungal inoculation protects Miscanthus×giganteus against trace element toxicity in a highly metal-contaminated site. Sci Total Environ 527–528:91–99. https://doi.org/10.1016/j.scitotenv.2015.04.116
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100. https://doi.org/10.1104/pp.110.166181
Fryzova R, Pohanka M, Martinkova P et al (2018) Oxidative stress and heavy metals in plants. In: de Voogt P (ed) Reviews of environmental contamination and toxicology volume 245. Springer International Publishing, Cham, pp 129–156
Garg N, Aggarwal N (2012) Effect of mycorrhizal inoculations on heavy metal uptake and stress alleviation of Cajanus cajan (L.) Millsp. Genotypes grown in cadmium and lead contaminated soils. Plant Growth Regul 66:9–26. https://doi.org/10.1007/s10725-011-9624-8
González-Chávez M del CA, Ortega-Larrocea M del P, Carrillo-González R et al (2011) Arsenate induces the expression of fungal genes involved in as transport in arbuscular mycorrhiza. Fungal Biol 115:1197–1209. https://doi.org/10.1016/j.funbio.2011.08.005
Guo L, Chen A, He N, Yang D, Liu M (2018) Exogenous silicon alleviates cadmium toxicity in rice seedlings in relation to cd distribution and ultrastructure changes. J Soils Sediments 18:1691–1700. https://doi.org/10.1007/s11368-017-1902-2
Gupta DK, Pena LB, Romero-Puertas MC, Hernández A, Inouhe M, Sandalio LM (2017) NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity. Plant Cell Environ 40:509–526. https://doi.org/10.1111/pce.12711
Gutjahr C, Sawers RJH, Marti G, Andrés-Hernández L, Yang SY, Casieri L, Angliker H, Oakeley EJ, Wolfender JL, Abreu-Goodger C, Paszkowski U (2015) Transcriptome diversity among rice root types during asymbiosis and interaction with arbuscular mycorrhizal fungi. Proc Natl Acad Sci U S A 112:6754–6759. https://doi.org/10.1073/pnas.1504142112
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hildebrandt U, Regvar M, Bothe H (2007) Arbuscular mycorrhiza and heavy metal tolerance. Phytochemistry 68:139–146. https://doi.org/10.1016/j.phytochem.2006.09.023
Hu Y, Cheng H, Tao S (2016) The challenges and solutions for cadmium-contaminated rice in China: a critical review. Environ Int 92:515–532. https://doi.org/10.1016/j.envint.2016.04.042
Hu W, Huang B, Borggaard OK, Ye M, Tian K, Zhang H, Holm PE (2018) Soil threshold values for cadmium based on paired soil-vegetable content analyses of greenhouse vegetable production systems in China: implications for safe food production. Environ Pollut 241:922–929. https://doi.org/10.1016/j.envpol.2018.06.034
Jia X, Zhao Y, He Y, Chang Y (2018) Glomalin-related soil protein in the rhizosphere of Robinia pseudoacacia L. seedlings under higher air temperature combined with cd-contaminated soil. Eur J Soil Sci 69:634–645. https://doi.org/10.1111/ejss.12671
Jiang Q-Y, Tan S-Y, Zhuo F, Yang DJ, Ye ZH, Jing YX (2016a) Effect of Funneliformis mosseae on the growth, cadmium accumulation and antioxidant activities of Solanum nigrum. Appl Soil Ecol 98:112–120. https://doi.org/10.1016/j.apsoil.2015.10.003
Jiang Q-Y, Zhuo F, Long S-H, Zhao HD, Yang DJ, Ye ZH, Li SS, Jing YX (2016b) Can arbuscular mycorrhizal fungi reduce cd uptake and alleviate cd toxicity of Lonicera japonica grown in cd-added soils? Sci Rep 6:1–9. https://doi.org/10.1038/srep21805
Khan AR, Ullah I, Waqas M, Park GS, Khan AL, Hong SJ, Ullah R, Jung BK, Park CE, Ur-Rehman S, Lee IJ, Shin JH (2017) Host plant growth promotion and cadmium detoxification in Solanum nigrum, mediated by endophytic fungi. Ecotoxicol Environ Saf 136:180–188. https://doi.org/10.1016/j.ecoenv.2016.03.014
Kumar P, Lucini L, Rouphael Y, Cardarelli M, Kalunke RM, Colla G (2015) Insight into the role of grafting and arbuscular mycorrhiza on cadmium stress tolerance in tomato. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.00477
Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330. https://doi.org/10.1104/pp.104.050435
Lenoir I, Fontaine J, Tisserant B, Laruelle F, Lounès-Hadj Sahraoui A (2017) Beneficial contribution of the arbuscular mycorrhizal fungus, Rhizophagus irregularis, in the protection of Medicago truncatula roots against benzo[a]pyrene toxicity. Mycorrhiza 27:465–476. https://doi.org/10.1007/s00572-017-0764-1
Li Y, Peng J, Shi P, Zhao B (2009) The effect of cd on mycorrhizal development and enzyme activity of Glomus mosseae and Glomus intraradices in Astragalus sinicus L. Chemosphere 75:894–899. https://doi.org/10.1016/j.chemosphere.2009.01.046
Li H, Wu C, Ye ZH, Wu SC, Wu FY, Wong MH (2011) Uptake kinetics of different arsenic species in lowland and upland rice colonized with Glomus intraradices. J Hazard Mater 194:414–421. https://doi.org/10.1016/j.jhazmat.2011.08.004
Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY, Wong MH, Mo CH (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Environ 571:1183–1190. https://doi.org/10.1016/j.scitotenv.2016.07.124
Lin A, Zhang X, Chen M, Cao Q (2007) Oxidative stress and DNA damages induced by cadmium accumulation. J Environ Sci 19:596–602. https://doi.org/10.1016/S1001-0742(07)60099-0
Liu L-Z, Gong Z-Q, Zhang Y-L, Li P-J (2011) Growth, cadmium accumulation and physiology of marigold (Tagetes erecta L.) as affected by arbuscular mycorrhizal fungi. Pedosphere 21:319–327. https://doi.org/10.1016/S1002-0160(11)60132-X
Liu Y, Liu K, Li Y, Yang W, Wu F, Zhu P, Zhang J, Chen L, Gao S, Zhang L (2016) Cadmium contamination of soil and crops is affected by intercropping and rotation systems in the lower reaches of the Minjiang River in South-Western China. Environ Geochem Health 38:811–820. https://doi.org/10.1007/s10653-015-9762-4
Luo N, Li X, Chen AY, Zhang LJ, Zhao HM, Xiang L, Cai QY, Mo CH, Wong MH, Li H (2017) Does arbuscular mycorrhizal fungus affect cadmium uptake and chemical forms in rice at different growth stages? Sci Total Environ 599–600:1564–1572. https://doi.org/10.1016/j.scitotenv.2017.05.047
Maldonado-Mendoza IE, Harrison MJ (2018) RiArsB and RiMT-11: two novel genes induced by arsenate in arbuscular mycorrhiza. Fungal Biol 122:121–130. https://doi.org/10.1016/j.funbio.2017.11.003
Meharg AA, Cairney JWG (1999) Co-evolution of Mycorrhizal Symbionts and their hosts to metal-contaminated environments. In: Fitter AH, Raffaelli DG (eds) Advances in Ecological Research. Academic Press, Cambridge, pp 69–112
Meier S, Borie F, Bolan N, Cornejo P (2012) Phytoremediation of metal-polluted soils by arbuscular mycorrhizal fungi. Crit Rev Environ Sci Technol 42:741–775. https://doi.org/10.1080/10643389.2010.528518
Ministry of Ecology and Environment of the People’s Republic of China, Ministry of Natural Resources of the People’s Republic of China (2014) The Report on the National General Survey of Soil Contamination
Miransari M (2017) Arbuscular Mycorrhizal Fungi and heavy metal tolerance in plants. In: Wu Q-S (ed) Arbuscular Mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 147–161
Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19. https://doi.org/10.1016/j.tplants.2016.08.002
Miyadate H, Adachi S, Hiraizumi A, Tezuka K, Nakazawa N, Kawamoto T, Katou K, Kodama I, Sakurai K, Takahashi H, Satoh-Nagasawa N, Watanabe A, Fujimura T, Akagi H (2011) OsHMA3, a P1B-type of ATPase affects root-to-shoot cadmium translocation in rice by mediating efflux into vacuoles. New Phytol 189:190–199. https://doi.org/10.1111/j.1469-8137.2010.03459.x
Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52:561–591. https://doi.org/10.1146/annurev.arplant.52.1.561
Nordberg M (2003) CADMIUM | toxicology. In: Caballero B (ed) Encyclopedia of food sciences and nutrition, 2nd edn. Academic Press, Oxford, pp 739–745
Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 99:13324–13329. https://doi.org/10.1073/pnas.202474599
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
Qiu Q, Wang Y, Yang Z, Yuan J (2011) Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L.) cultivars differing in cadmium accumulation. Food Chem Toxicol 49:2260–2267. https://doi.org/10.1016/j.fct.2011.06.024
Rafiq MT, Aziz R, Yang X, Xiao W, Rafiq MK, Ali B, Li T (2014) Cadmium phytoavailability to rice (Oryza sativa L.) grown in representative Chinese soils. A model to improve soil environmental quality guidelines for food safety. Ecotoxicol Environ Saf 103:101–107. https://doi.org/10.1016/j.ecoenv.2013.10.016
Rehman ZU, Khan S, Brusseau ML, Shah MT (2017) Lead and cadmium contamination and exposure risk assessment via consumption of vegetables grown in agricultural soils of five-selected regions of Pakistan. Chemosphere 168:1589–1596. https://doi.org/10.1016/j.chemosphere.2016.11.152
Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365. https://doi.org/10.1093/jexbot/53.372.1351
Shi T, Zhang Y, Gong Y, Ma J, Wei H, Wu X, Zhao L, Hou H (2019) Status of cadmium accumulation in agricultural soils across China (1975–2016): from temporal and spatial variations to risk assessment. Chemosphere 230:136–143. https://doi.org/10.1016/j.chemosphere.2019.04.208
Siciliano V, Genre A, Balestrini R, Cappellazzo G, deWit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–1466. https://doi.org/10.1104/pp.107.097980
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London
Song Y, Wang Y, Mao W, Sui H, Yong L, Yang D, Jiang D, Zhang L, Gong Y (2017) Dietary cadmium exposure assessment among the Chinese population. PLoS One 12:e0177978. https://doi.org/10.1371/journal.pone.0177978
Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JPW, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193:755–769. https://doi.org/10.1111/j.1469-8137.2011.03948.x
van Rossum MWPC, Alberda M, van der Plas LHW (1997) Role of oxidative damage in tulip bulb scale micropropagation. Plant Sci 130:207–216. https://doi.org/10.1016/S0168-9452(97)00215-X
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
Wang X, Liu Y, Zeng G, Chai L, Song X, Min Z, Xiao X (2008) Subcellular distribution and chemical forms of cadmium in Bechmeria nivea (L.) gaud. Environ Exp Bot 62:389–395. https://doi.org/10.1016/j.envexpbot.2007.10.014
Wang MY, Chen AK, Wong MH, Qiu RL, Cheng H, Ye ZH (2011) Cadmium accumulation in and tolerance of rice (Oryza sativa L.) varieties with different rates of radial oxygen loss. Environ Pollut 159:1730–1736. https://doi.org/10.1016/j.envpol.2011.02.025
Wang P, Chen H, Kopittke PM, Zhao F-J (2019) Cadmium contamination in agricultural soils of China and the impact on food safety. Environ Pollut 249:1038–1048. https://doi.org/10.1016/j.envpol.2019.03.063
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Wu Q-S, Zou Y-N, Fathi Abd-Allah E (2014) Chapter 15 - Mycorrhizal association and ROS in plants. In: Ahmad P (ed) Oxidative damage to plants. Academic Press, San Diego, pp 453–475
Wu S, Zhang X, Sun Y, Wu Z, Li T, Hu Y, Su D, Lv J, Li G, Zhang Z, Zheng L, Zhang J, Chen B (2015) Transformation and immobilization of chromium by arbuscular mycorrhizal fungi as revealed by SEM–EDS, TEM–EDS, and XAFS. Environ Sci Technol 49:14036–14047. https://doi.org/10.1021/acs.est.5b03659
Wu S, Zhang X, Sun Y, Wu Z, Li T, Hu Y, Lv J, Li G, Zhang Z, Zhang J, Zheng L, Zhen X, Chen B (2016) Chromium immobilization by extra- and intraradical fungal structures of arbuscular mycorrhizal symbioses. J Hazard Mater 316:34–42. https://doi.org/10.1016/j.jhazmat.2016.05.017
Wu S, Zhang X, Huang L, Chen B (2019) Arbuscular mycorrhiza and plant chromium tolerance. Soil Ecol Lett 1:94–104. https://doi.org/10.1007/s42832-019-0015-9
Xiao Y, Tholen D, Zhu X-G (2016) The influence of leaf anatomy on the internal light environment and photosynthetic electron transport rate: exploration with a new leaf ray tracing model. J Exp Bot 67:6021–6035. https://doi.org/10.1093/jxb/erw359
Xue D, Jiang H, Deng X, Zhang X, Wang H, Xu X, Hu J, Zeng D, Guo L, Qian Q (2014) Comparative proteomic analysis provides new insights into cadmium accumulation in rice grain under cadmium stress. J Hazard Mater 280:269–278. https://doi.org/10.1016/j.jhazmat.2014.08.010
Yang Y, Liang Y, Ghosh A, Song Y, Chen H, Tang M (2015) Assessment of arbuscular mycorrhizal fungi status and heavy metal accumulation characteristics of tree species in a lead–zinc mine area: potential applications for phytoremediation. Environ Sci Pollut Res 22:13179–13193. https://doi.org/10.1007/s11356-015-4521-8
Ye W, Hu S, Wu L, Ge C, Cui Y, Chen P, Xu J, Dong G, Guo L, Qian Q (2017) Fine mapping a major QTL qFCC7L for chlorophyll content in rice (Oryza sativa L.) cv. PA64s. Plant Growth Regul 81:81–90. https://doi.org/10.1007/s10725-016-0188-5
Zhang XH, Zhu YG, Chen BD et al (2005) Arbuscular mycorrhizal fungi contribute to resistance of upland rice to combined metal contamination of soil. J Plant Nutr 28:2065–2077. https://doi.org/10.1080/01904160500320871
Zhang W, Lin K, Zhou J, Zhang W, Liu L, Zhang Q (2014) Cadmium accumulation, sub-cellular distribution and chemical forms in rice seedling in the presence of sulfur. Environ Toxicol Pharmacol 37:348–353. https://doi.org/10.1016/j.etap.2013.12.006
Zhao X-M, Yao L-A, Ma Q-L, Zhou GJ, Wang L, Fang QL, Xu ZC (2018) Distribution and ecological risk assessment of cadmium in water and sediment in Longjiang River, China: implication on water quality management after pollution accident. Chemosphere 194:107–116. https://doi.org/10.1016/j.chemosphere.2017.11.127
Acknowledgements
The present project was supported by National Natural Science Foundation of China (41877350), Guangzhou Municipal Science and Technology Project (201904010084), National Key R&D Program of China (2018YFD0800701), NSFC-Guangdong Joint Fund (U1501233), and Research Team Project of the Natural Science Foundation of Guangdong Province (2016A030312009). This work was also supported by Guangdong Provincial Key Laboratory of Soil and Groundwater Pollution Control (No. 2017B030301012) and State Environmental Protection Key Laboratory of Integrated Surface Water-Groundwater Pollution Control.
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Li, H., Chen, X.W., Wu, L. et al. Effects of arbuscular mycorrhizal fungi on redox homeostasis of rice under Cd stress. Plant Soil 455, 121–138 (2020). https://doi.org/10.1007/s11104-020-04678-y
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DOI: https://doi.org/10.1007/s11104-020-04678-y