植物应答铝毒的分子机制研究进展

doi:10.13560/j.cnki.biotech.bull.2020-0901

摘要/Abstract

摘要：

酸性土壤中的铝毒是限制农业生产和作物产量的主要因子之一,不同植物对铝毒响应不同。外部排斥机制和内部耐受机制是植物抗铝毒的最主要的两种生理机制。综述了铝毒对植物的危害;外源添加调节因子在植物缓解铝毒中的作用;耐铝基因的功能和转录调控;以及微生物群落在铝离子胁迫下对植物的影响;展望了未来的研究方向,并希望为之后相关研究提供依据。

关键词: 铝毒, 耐铝机制, 耐铝基因, 耐铝细菌

Abstract:

Aluminum toxicity in acid soils is one of the main factors limiting agricultural production and yields. Plants respond differently to aluminum toxicity. External exclusion and internal detoxification are the mains mechanisms for plants to resist aluminum toxicity. This review is including aluminum toxicity to plants,the role of exogenously added regulatory factors in plants to alleviate aluminum toxicity,the function and transcriptional regulation of aluminum-tolerant genes,and the impact of microbial communities on plants under aluminum ion stress. As well as the future research direction is prospected,aiming that this paper will provide a basis for related research in the future.

Key words: aluminum toxicity, aluminum-tolerant mechanism, aluminum-tolerant gene, aluminum-tolerant bacteria

黄凯, 张红宇, 张菡倩, 李元, 祖艳群, 陈建军. 植物应答铝毒的分子机制研究进展[J]. 生物技术通报, 2021, 37(3): 125-135.

HUANG Kai, ZHANG Hong-yu, ZHANG Han-qian, LI Yuan, ZU Yan-qun, CHEN Jian-jun. Research Progress on the Molecular Mechanism of Plants Response to Aluminum Toxicity[J]. Biotechnology Bulletin, 2021, 37(3): 125-135.

图/表 1

参考文献 90

[1]	梅文君, 许义兰, 杨永莲, 等. 酸铝胁迫对楚雄南苜蓿种子萌发及幼苗生长的影响[J]. 云南农业大学学报:自然科学, 2019,34(6):1012-1017.
	Mei WJ, Xu YL, Yang YL, et al. Effects of acid aluminum stress on the seed germination and seeding growth of Medicago hispida cv. Chuxiong[J]. Journal of Yunnan Agricultural University:Natural Science, 2019,34(6):1012-1017.
[2]	von Uexküll HR, Mutert E. Global extent, development and economic impact of acid soils[J]. Plant and Soil, 1995,171(1):1-15. doi: 10.1007/BF00009558 URL
[3]	Kochian LV, Hoekenga OA, Pineros MA. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency[J]. Annual Review of Plant Biology, 2004,55:459-493. doi: 10.1146/annurev.arplant.55.031903.141655 URL pmid: 15377228
[4]	吴文杰, 钱莲文. 常绿杨根伸长区铝毒指标性超微结构的研究[J]. 中南林业科技大学学报, 2015,35(11):5-9.
	Wu WJ, Qian LW. Indicative effects of acid and aluminum stress on cell ultrastructure in root elongation zone of evergreen poplar clone[J]. Journal of Central South University of Forestry & Technology, 2015,35(11):5-9.
[5]	Kochian LV, Piñeros MA, Liu P, et al. Plant adaptation to acid soils:the molecular basis for crop aluminum resistance[J]. Annual Review of Plant Biology, 2015,66:571-598. doi: 10.1146/annurev-arplant-043014-114822 pmid: 25621514
[6]	Ryan PR, Ditomaso JM, Kochian LV. Aluminum toxicity in roots:An investigation of spatial sensitivity and the role of the root cap[J]. Journal of Experimental Botany, 1993,44(2):437-446. doi: 10.1093/jxb/44.2.437 URL
[7]	杨亚军, 郭立泉, 杨春武. 植物耐铝的生理机制[J]. 植物生理学通讯, 2006(2):319-325.
	Yang YJ, Guo LQ, Yang CW, et al. Physiologic mechanism of aluminum tolerance in plants[J]. Plant Physiology Communications, 2006(2):319-325.
[8]	黄玉婷, 吴亚, 刘大林, 等. 铝胁迫对草本植物生理的影响机制[J]. 草业科学, 2018,35(6):1517-1527.
	Huang YT, Wu Y, Liu DL, et al, Advances in the understanding of mechanisms underlying the effects of aluminum stress on herbaceous plant physiology[J]. Pratacultural Sience, 2018,35(6):1517-1527.
[9]	Yamamoto Y. Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells[J]. Plant Physilology, 2002,128(1):63-72.
[10]	何虎翼, 何龙飞, 顾明华. 铝诱导植物程序性细胞死亡信号转导的研究进展[J]. 植物生理学报, 2011,47(4):321-330.
	He HY, He LF, Gu MH. The progress of signal transduction of aluminum-induced programmed cell death in plants[J]. Plant Physiology Journal, 2011,47(4):321-330.
[11]	He H, He L, Gu M. Interactions between nitric oxide and plant hormones in aluminum tolerance[J]. Plant Signal and Behavior, 2012,7(4):469-471. doi: 10.4161/psb.19312 URL
[10]	He H, Li Y, He LF. Role of nitric oxide and hydrogen sulfide in plant aluminum tolerance[J]. Biometals, 2019,32(1):1-9.
[13]	Tian QY, Sun DH, Zhao MG, et al. Inhibition of nitric oxide synthase(NOS)underlies aluminum induced inhibition of root elongation in Hibiscus moscheutos[J]. New Phytologist, 2007,174(2):322-331. doi: 10.1111/nph.2007.174.issue-2 URL
[14]	Sun C, Lu L, Liu L, et al. Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat(Triticum aestivum L.)[J]. New Phytologist, 2014,201(4):1240-1250. doi: 10.1111/nph.12597 URL
[15]	Sun C, Liu L, Yu Y, et al. Nitric oxide alleviates aluminum-induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat[J]. Journal of Integrative Plant Biology, 2015,57(6):550-561. doi: 10.1111/jipb.12298 URL
[16]	张茂林. 玉米根系响应铝胁迫的差异性生长反应和耐铝突变体的鉴定及功能分析[D]. 济南:山东大学, 2017.
	Zhang ML. Differential growth response of maize root system to aluminum stress and functional analysis of aluminum resistant mutant[D]. Ji’nan:Shandong University, 2017.
[17]	Wang P, Yu W, Zhang J, et al. Auxin enhances aluminum-induced citrate exudation through upregulation of GmMATE and activation of the plasma membrane H⁺-ATPase in soybean roots[J]. Annals of Botany, 2016,118(5):933-940. doi: 10.1093/aob/mcw133 URL pmid: 27474509
[18]	Yang Y, Wang QL, Geng MJ, et al. Effect of indole-3-acetic acid on aluminum-induced efflux of malic acid from wheat(Triticum aestivum L.). Plant and Soil, 2011,346(1-2):215-230.
[19]	Hou N, You J, Pang J, et al. The accumulation and transport of abscisic acid in soybean(Glycine max L.)under aluminum stress[J]. Plant and Soil, 2010,330(1-2):127-137. doi: 10.1007/s11104-009-0184-x URL
[20]	吴道铭, 曹华苹, 沈宏. 生长素及其运输蛋白对植物铝胁迫的响应[J]. 植物生理学报, 2014,50(8):1135-1143.
	Wu DM, Cao HP, Shen H. Response of auxin and its transporter to aluminum stress in plants[J]. Plant Physiology Journal, 2014,50(8):1135-1143.
[21]	Tian Q, Zhang X, Ramesh S, et al. Ethylene negatively regulates aluminum-induced malate efflux from wheat roots and tobacco cells transformed with TaALMT1[J]. Journal of Experimental Botany, 2014,65(9):2415-2426. doi: 10.1093/jxb/eru123 URL
[22]	Sun P, Tian QY, Chen J, et al. Aluminum-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin[J]. Journal of Experimental Botany, 2010,61(2):347-356. doi: 10.1093/jxb/erp306 URL pmid: 19858117
[23]	李交昆, 唐璐璐. 植物抗铝分子机制研究进展[J]. 生命科学, 2013,25(6):588-594.
	Li JK, Tang LL. Research advances on the molecular mechanisms of aluminum tolerance in plants[J]. Chinese Bulletin Life Science, 2013,25(6):588-594.
[24]	刘玉民. 酸铝环境马尾松根系分泌物特性及其缓解铝毒的根际效应[D]. 重庆:西南大学, 2018.
	Liu YM. The characteristics and rhizosphere effects in alleviating Al-toxicity of Pinus massoniana root exudation in acid-aluminum environment[D]. Chongqing:Xinan University, 2018.
[25]	Zhang X, Long Y, Huang J. Molecular mechanisms for coping with Al toxicity in plants[J]. International Journal of Molecular Sciences, 2019,20(7):1551. doi: 10.3390/ijms20071551 URL
[26]	范伟, 娄和强, 龚育龙, 等. 调控铝诱导根尖有机酸分泌的分子机制[J]. 植物生理学报, 2014,50(10):1469-1478.
	Fan W, Lou HQ, Gong YL, et al. Molecular mechanisms regulating aluminum-induced secretion of organic acids in root apex[J]. Plant Physiology Journal, 2014,50(10):1469-1478.
[27]	Sharma T, Dreyer I, Kochian L, et al. The ALMT family of organic acid transporters in plants and their involvement in detoxification and nutrient security[J]. Frontiers in Plant Science, 2016,7:1488. URL pmid: 27757118
[28]	Omote H, Hiasa M, Matsumoto T, et al. The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations[J]. Trends in Pharmacological Sciences, 2006,27(11):587-593. doi: 10.1016/j.tips.2006.09.001 URL pmid: 16996621
[29]	Sawaki Y, Iuchi S, Kobayashi Y, et al. STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities[J]. Plant Physiology, 2009,150(1):281-294. URL pmid: 19321711
[30]	Liang C, Piñeros MA, Tian J, et al. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils[J]. Plant Physiology, 2013,161(3):1347-1361. doi: 10.1104/pp.112.208934 URL
[31]	Maron LG, Piñeros MA, Guimarães CT, et al. Two functionally distinct members of the MATE(multi-drug and toxic compound extrusion)family of transporters potentially underlie two major aluminum tolerance QTLs in maize[J]. The Plant Journal, 2010,61(5):728-740. URL pmid: 20003133
[32]	Magalhaes JV, Liu J, Guimarães CT, et al. A gene in the multidrug and toxic compound extrusion(MATE)family confers aluminum tolerance in sorghum[J]. Nature Genetics, 2007,39(9):1156-1161. doi: 10.1038/ng2074 URL pmid: 17721535
[33]	Ma JF, Zheng SJ, Matsumoto H, et al. Detoxifying aluminum with buckwheat[J]. Nature, 1997,390(6660):569-570. doi: 10.1038/37514 URL pmid: 9403684
[34]	Ma Z, Miyasaka SC. Oxalate exudation by taro in response to Al[J]. Plant Physiology, 1998,118(3):861-865. pmid: 9808730
[35]	沈仁芳. 铝在土壤-植物中的行为及植物的适应机制[M]. 北京: 科学出版社, 2008.
	Shen RF. The behavior of aluminum in soil-plants and the adaptive mechanism of plants[M]. Beijing: Science Press, 2008.
[36]	Kidd PS, Llugany M, Poschenrieder C, et al. The role of root exudates in aluminum resistance and silicon-induced amelioration of aluminum toxicity in three varieties of maize(Zea mays)[J]. Journal of Experimental Botany, 2001,2(359):1339-1352.
[37]	Degenhardt J, Larsen PB, Kochian LV . Aluminum resistance in the Arabidopsis mutant alr-104 is caused by an aluminum-induced increase in rhizosphere pH[J]. Plant Physiology, 1998,117(1):19-27. doi: 10.1104/pp.117.1.19 URL pmid: 9576770
[38]	张冉, 韩博, 任健, 等. 铝对植物毒害及草本植物耐铝毒机制研究进展[J]. 云南农业大学学报:自然科学, 2020,35(2):353-360.
	Zhang R, Han B, Ren J, et al. Research progress on aluminum toxicity to plants and mechanisms of aluminum tolerance in herbaceous[J]. Journal of Yunnan Agricultural University:Natural Science, 2020,35(2):353-360.
[39]	Sasidharan R, Voesenek L, Pierik R. Cell wall modifying proteins mediate plant acclimatization to biotic and abiotic stresses[J]. Critical Reviews in Plant Sciences, 2011,30(6):548-562. doi: 10.1080/07352689.2011.615706 URL
[40]	Nagayama T, Nakamura A, Yamaji N, et al. Changes in the distribution of pectin in root border cells under aluminum stress[J]. Frontiers in Plant Science, 2019,10:1216. doi: 10.3389/fpls.2019.01216 pmid: 31632431
[41]	Yang JL, Li YY, Zhang YJ, et al. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex[J]. Plant Physiology, 2008,146(2):602-611. doi: 10.1104/pp.107.111989 URL pmid: 18083797
[42]	Huang CF, Yamaji N, Mitani N, et al. A bacterial-type ABC transporter is involved in aluminum tolerance in rice[J]. Plant Cell, 2009,21(2):655-667. doi: 10.1105/tpc.108.064543 URL pmid: 19244140
[43]	Zhu XF, Wan JX, Sun Y, et al. Xyloglucan endotransglucosylase-hydrolase17 interacts with xyloglucan endotransglucosylase-hydrolase31 to confer xyloglucan endotransglucosylase action and affect aluminum sensitivity in Arabidopsis[J]. Plant Physiology, 2014,165(4):1566-1574. URL pmid: 24948835
[44]	Xia J, Yamaji N, Kasai T, et al. Plasma membrane-localized transporter for aluminum in rice[J]. Proceedings of The National Academy of Sciences of The United States of America, 2010,107(43):18381-18385. URL pmid: 20937890
[45]	Chen ZC, Yamaji N, Horie T, et al. A magnesium transporter OsMGT1 plays a critical role in salt tolerance in rice[J]. Plant Physiol, 2017,174(3):1837-1849. doi: 10.1104/pp.17.00532 URL pmid: 28487477
[46]	Chen ZC, Yamaji N, Motoyama R, et al. Up-regulation of a magnesium transporter gene OsMGT1 is required for conferring aluminum tolerance in rice[J]. Plant Physiology, 2012,159(4):1624-1633. URL pmid: 22732245
[47]	王晓珠, 孙万梅, 马义峰, 等. 拟南芥ABC转运蛋白研究进展[J]. 植物生理学报, 2017,53(2):133-144.
	Wang XZ, Sun WM, Ma YF, et al. Research progress of ABC transporters in Arabidopsis thaliana[J]. Plant Physiology Journal, 2017,53(2):133-144.
[48]	Larsen PB, Geisler MJ, Jones CA. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis[J]. Plant Journal, 2005,1(3):353-363.
[49]	Negishi T, Oshima K, Hattori M, et al. Tonoplast- and plasma membrane-localized aquaporin-family transporters in blue hydrangea sepals of aluminum hyperaccumulating plant[J]. PLoS One, 2012,7(8):e43189. URL pmid: 22952644
[50]	Wang Y, Li R, Li D, et al. NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis[J]. Proceedings of The National Academy of Sciences of The United States of America, 2017,14(19):5047-5052.
[51]	Liu J, Magalhaes JV, Shaff J, et al. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance[J]. Plant Journal, 2009,57(3):389-399. doi: 10.1111/tpj.2009.57.issue-3 URL
[52]	Kobayashi Y, Ohyama Y, Kobayashi Y, et al. STOP2 activates transcription of several genes for Al and low pH tolerance that are regulated by STOP1 in Arabidopsis[J]. Molecular Plant, 2014,7(2):311-322. doi: 10.1093/mp/sst116 URL pmid: 23935008
[53]	Yamaji N, Huang CF, Nagao S, et al. A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice[J]. Plant Cell, 2009,21(10):3339-3349. doi: 10.1105/tpc.109.070771 pmid: 19880795
[54]	Ohyama Y, Ito H, Kobayashi Y, et al. Characterization of AtSTOP1 orthologous genes in tobacco and other plant species[J]. Plant Physiology, 2013,162(4):1937-1946. doi: 10.1104/pp.113.218958 URL
[55]	Ding ZJ, Yan JY, Xu XY, et al. WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis[J]. Plant Journal, 2013,76(5):825-835. doi: 10.1111/tpj.12337 URL
[56]	Arenhart RA, Bai Y, de Oliveira LFV, et al. New insights into aluminum tolerance in rice:the ASR5 protein binds the STAR1 promoter and other aluminum-responsive genes[J]. Molecular Plant, 2014,7(4):709-721. doi: 10.1093/mp/sst160 pmid: 24253199
[57]	Arenhart RA, De Lima JC, Pedron M, et al. Involvement of ASR genes in aluminum tolerance mechanisms in rice[J]. Plant Cell and Environment, 2013,36(1):52-67. doi: 10.1111/pce.2013.36.issue-1 URL
[58]	Daspute AA, Sadhukhan A, Tokizawa M, et al. Transcriptional regulation of aluminum-tolerance genes in higher plants:Clarifying the underlying molecular mechanisms[J]. Frontiers in Plant Science, 2017,8:1358. doi: 10.3389/fpls.2017.01358 URL pmid: 28848571
[59]	Collins NC, Shirley NJ, Saeed M, et al. An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye(Secale cereale L.)[J]. Genetics, 2008,179(1):669-682. URL pmid: 18493079
[60]	Maron LG, Guimarães CT, Kirst M, et al. Aluminum tolerance in maize is associated with higher MATE1 gene copy number[J]. Proceedings of The National Academy of Sciences of The United States of America, 2013,110(13):5241-5246. URL pmid: 23479633
[61]	Ferreira JR, Faria BF, Comar JM, et al. Is a non-synonymous SNP in the HvAACT1 coding region associated with acidic soil tolerance in barley?[J]. Genetics and Molecular Biology, 2017,40(2):480-490. doi: 10.1590/1678-4685-GMB-2016-0225 URL pmid: 28486573
[62]	Garcia Oliveira AL, Martins LP, Tolrá R, et al. Molecular characterization of the citrate transporter gene TaMATE1 and expression analysis of upstream genes involved in organic acid transport under Al stress in bread wheat(Triticum aestivum L.)[J]. Physiologia Plantarum, 2014,152(3):441-452. doi: 10.1111/ppl.12179 URL
[63]	Carvalho G, Schaffert RE, Malosetti M, et al. Back to acid soil fields:the citrate transporter SbMATE is a major asset for sustainable grain yield for sorghum cultivated on acid soils[J]. Genes Genomes Genetic, 2016,6(2):475-484.
[64]	Delhaize E, Ma JF, Ryan PR. Transcriptional regulation of aluminum tolerance genes[J]. Trends in Plant Science, 2012,17(6):341-348. doi: 10.1016/j.tplants.2012.02.008 URL
[65]	Ryan PR, Raman H, Gupta S, et al. The multiple origins of aluminum resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1[J]. Plant Journal, 2010,64(3):446-455. doi: 10.1111/tpj.2010.64.issue-3 URL
[66]	Chen ZC, Yokosho K, Kashino M, et al. Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus[J]. Plant Journal, 2013,76(1):10-23.
[67]	Che J, Tsutsui T, Yokosho K, Functional characterization of an aluminum(Al)-inducible transcription factor, ART2, revealed a different pathway for Al tolerance in rice[J]. New Phytologist, 2018,220(1):209-218. doi: 10.1111/nph.15252 URL
[68]	Xia J, Yamaji N, Ma JF. A plasma membrane-localized small peptide is involved in rice aluminum tolerance[J]. Plant Journal, 2013,76(2):345-355.
[69]	Li GZ, Wang ZQ, Yokosho K, et al. Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice(Oryza sativa)[J]. New Phytologist, 2018,219(1):149-162. doi: 10.1111/nph.2018.219.issue-1 URL
[70]	Melo JO, Martins LGC, Barros BA, et al. Repeat variants for the SbMATE transporter protect sorghum roots from aluminum toxicity by transcriptional interplay in cis and trans[J]. Proceedings of the National Academy of Sciences of the United States of America, 2019,116(1):313-318. doi: 10.1073/pnas.1808400115 URL pmid: 30545913
[71]	Huang S, Gao J, You J, et al. Identification of STOP1-Like proteins associated with aluminum tolerance in sweet sorghum(Sorghum bicolor L.)[J]. Frontiers in Plant Science, 2018,9:258. URL pmid: 29541086
[72]	Wu W, Lin Y, Chen Q, et al. Functional conservation and divergence of soybean GmSTOP1 members in proton and aluminum tolerance[J]. Frontiers in Plant Science, 2018,9:570. URL pmid: 29755502
[73]	Ligaba A, Katsuhara M, Ryan PR, The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells[J]. Plant Physiology, 2006,142(3):1294-1303. doi: 10.1104/pp.106.085233 URL pmid: 17028155
[74]	艾超, 孙静文, 王秀斌, 等. 植物根际沉积与土壤微生物关系研究进展[J]. 植物营养与肥料学报, 2015,21(5):1343-1351. doi: 10.11674/zwyf.2015.0530 URL
	Ai C, Sun JW, Wang XB, et al. Advances in the study of the relationship between plant rhizodeposition and soil microorganism[J]. Journal of Plant Nutrition and Fertilizer, 2015,21(5):1343-1351.
[75]	Etesami H, Maheshwari DK. Use of plant growth promoting rhizobacteria(PGPRs)with multiple plant growth promoting traits in stress agriculture:Action mechanisms and future prospects[J]. Ecotoxicology and Environmental Safety, 2018,156:225-246. doi: S0147-6513(18)30192-1 pmid: 29554608
[76]	Guo HL, Liu SJ, Xu J. Effects of arbuscular mycorrhizal fungi on growth and root traits of dicotyledons plants:A meta-analysis[J]. Chinese Journal of Ecology, 2017,36(7):1855-1864.
[77]	Arriagada CA, Herrera MA, Borie F, et al. Contribution of arbuscular mycorrhizal and saprobe fungi to the aluminum resistance of Eucalyptus globulus[J] Water Air and Soil Pollution, 2007,182(1-4):383-394. doi: 10.1007/s11270-007-9349-5 URL
[78]	Seguel A, Castillo CG, Morales A, et al. Arbuscular mycorrhizal symbiosis in four Al-tolerant wheat genotypes grown in an acidic andisol[J]. Journal of Soil Science and Plant Nutrition, 2016,16(1):164-173.
[79]	Vandamme E, Renkens M, Pypers P, et al. Root hairs explain P uptake efficiency of soybean genotypes grown in a P-deficient Ferralsol[J]. Plant and Soil, 2013,369(1-2):269-282. doi: 10.1007/s11104-012-1571-2 URL
[80]	Seguel A, Cumming JR, Klugh SK, et al. The role of arbuscular mycorrhizas in decreasing aluminum phytotoxicity in acidic soils:a review[J]. Mycorrhiza, 2013,23(3):167-183. doi: 10.1007/s00572-013-0479-x pmid: 23328806
[81]	Klugh KR, Cumming JR. Variations in organic acid exudation and aluminum resistance among arbuscular mycorrhizal species colonizing Liriodendron tulipifera[J]. Tree Physiology, 2007,27(8):1103-1112. doi: 10.1093/treephys/27.8.1103 URL pmid: 17472937
[82]	Aguilera P, Borie F, Seguel A, et al. Fluorescence detection of aluminum in arbuscular mycorrhizal fungal structures and glomalin using confocal laser scanning microscopy[J]. Soil Biology and Biochemisty, 2011,43(12):2427-2431.
[83]	Joner EJ, Briones R, Leyval C. Metal-binding capacity of arbuscular mycorrhizal mycelium[J]. Plant and Soil, 2000,226(2):227-234. doi: 10.1023/A:1026565701391 URL
[84]	Zerrouk IZ, Benchabane M, Khelifi L, et al. A Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress[J]. Journal of Plant Physiology, 2016,191:111-119. doi: 10.1016/j.jplph.2015.12.009 URL pmid: 26759938
[85]	de la Luz Mora M, Demanet R, Acuña JJ, et al. Aluminum-tolerant bacteria improve the plant growth and phosphorus content in ryegrass grown in a volcanic soil amended with cattle dung manure[J]. Applied Soil Ecology, 2017,115:19-26. doi: 10.1016/j.apsoil.2017.03.013 URL
[86]	Wang T, Liu MQ, Li HX. Inoculation of phosphate-solubilizing bacteria Bacillus thuringiensis B1 increases available phosphorus and growth of peanut in acidic soil[J]. Acta Agricultural Scandinavica Section B-Soil and Plant Science, 2014,64(3):252-259.
[87]	Delfim J, Schoebitz M, Paulino L, et al. Phosphorus availability in wheat, in volcanic soils inoculated with phosphate-solubilizing Bacillus thuringiensis[J]. Sustainability, 2018,10(2):144. doi: 10.3390/su10010144 URL
[88]	Silambarasan S, Logeswari P, Valentine A, et al. Role of Curtobacterium herbarum strain CAH5 on aluminum bioaccumulation and enhancement of Lactuca sativa growth under aluminum and drought stresses[J]. Ecotoxicology and Environmental Safety, 2019,183:109573. URL pmid: 31442809
[89]	Silambarasan S, Logeswari P, Cornejo P, et al. Simultaneous mitigation of aluminum, salinity and drought stress in Lactuca sativa growth via formulated plant growth promoting Rhodotorula mucilaginosa CAM4[J]. Ecotoxicology and Environmental Safety, 2019,180:63-72. doi: S0147-6513(19)30535-4 pmid: 31075717
[90]	Silambarasan S, Logeswari P, Cornejo P, et al. Role of plant growth-promoting rhizobacterial consortium in improving the Vigna radiata growth and alleviation of aluminum and drought stresses[J]. Environmental Science and Pollution Research, 2019,26(27):27647-27659. doi: 10.1007/s11356-019-05939-9 URL pmid: 31338767

植物物种	基因	功能	参考文献
水稻（Oryza sativa）	OsSTAR1	转运UDP-葡萄糖至细胞壁	[42]
水稻（Oryza sativa）	OsSTAR2	转运UDP-葡萄糖至细胞壁	[42]
水稻（Oryza sativa）	OsMGT1	运输镁离子至水稻细胞质	[45]
水稻（Oryza sativa）	OsART1	调控铝离子的耐受基因	[53]
水稻（Oryza sativa）	OsART2	调控铝离子的耐受基因	[67]
水稻（Oryza sativa）	OsASR1	调控铝离子的耐受基因	[57]
水稻（Oryza sativa）	OsASR5	调控铝离子的耐受基因	[56]
水稻（Oryza sativa）	OsALS1	把铝离子隔离至液泡中	[44]
水稻（Oryza sativa）	OsCDT3	结合根系细胞中的铝离子	[68]
水稻（Oryza sativa）	OsFRDL4	调节柠檬酸的转运	[69]
水稻（Oryza sativa）	OsNrat1	把铝转运至细胞质	[43]
拟南芥（Arabidopsis thaliana）	AtALMT1	调节苹果酸的转运	[29]
拟南芥（Arabidopsis thaliana）	AtMATE	调节柠檬酸的转运	[29]
拟南芥（Arabidopsis thaliana）	AtSTOP1	调控铝的耐受基因	[51]
拟南芥（Arabidopsis thaliana）	AtXHT-31	调节细胞壁的延伸	[43]
拟南芥（Arabidopsis thaliana）	AtWRKY46	调节铝的耐受基因	[55]
拟南芥（Arabidopsis thaliana）	AtALS3	运输铝离子至液泡中	[48]
拟南芥（Arabidopsis thaliana）	AtNIP1;2	运输苹果酸铝	[50]
高粱（Sorghum bicolor L.）	SbMATE1	调节柠檬酸的转运	[63]
高粱（Sorghum bicolor L.）	SbWRKY1	调节铝的耐受基因	[70]
高粱（Sorghum bicolor L.）	SbZNF1	调节铝的耐受基因	[70]
高粱（Sorghum bicolor L.）	SbSTOP1	AtSTOP1的同源基因	[71]
小麦（Triticum aestivum L.）	TaALMT1	调节苹果酸的转运	[65]
小麦（Triticum aestivum L.）	TaMATE1	调节柠檬酸的转运	[62]
小麦（Triticum aestivum L.）	TaSTOP1	AtSTOP1的同源基因	[61]
大豆（Glycine max）	GmALMT1	调节苹果酸的转运	[30]
大豆（Glycine max）	GmSTOP1-1	AtSTOP1的同源基因	[72]
大豆（Glycine max）	GmSTOP1-3	AtSTOP1的同源基因	[72]
玉米（Zea mays）	ZmMATE1	调节柠檬酸的转运	[60]
油菜（Brassica napus）	BnALMT1	调节苹果酸的转运	[73]
油菜（Brassica napus）	BnALMT2	调节苹果酸的转运	[73]
黑麦（Secale cereale L.）	ScALMT1	调节苹果酸的转运	[59]
黑麦（Secale cereale L.）	ScFRDL2	调节柠檬酸的转运	[59]
大麦（Hordeum vulgare L.）	HvAACT1	调节柠檬酸的转运	[61]

植物物种	基因	功能	参考文献
水稻（Oryza sativa）	OsSTAR1	转运UDP-葡萄糖至细胞壁	[42]
水稻（Oryza sativa）	OsSTAR2	转运UDP-葡萄糖至细胞壁	[42]
水稻（Oryza sativa）	OsMGT1	运输镁离子至水稻细胞质	[45]
水稻（Oryza sativa）	OsART1	调控铝离子的耐受基因	[53]
水稻（Oryza sativa）	OsART2	调控铝离子的耐受基因	[67]
水稻（Oryza sativa）	OsASR1	调控铝离子的耐受基因	[57]
水稻（Oryza sativa）	OsASR5	调控铝离子的耐受基因	[56]
水稻（Oryza sativa）	OsALS1	把铝离子隔离至液泡中	[44]
水稻（Oryza sativa）	OsCDT3	结合根系细胞中的铝离子	[68]
水稻（Oryza sativa）	OsFRDL4	调节柠檬酸的转运	[69]
水稻（Oryza sativa）	OsNrat1	把铝转运至细胞质	[43]
拟南芥（Arabidopsis thaliana）	AtALMT1	调节苹果酸的转运	[29]
拟南芥（Arabidopsis thaliana）	AtMATE	调节柠檬酸的转运	[29]
拟南芥（Arabidopsis thaliana）	AtSTOP1	调控铝的耐受基因	[51]
拟南芥（Arabidopsis thaliana）	AtXHT-31	调节细胞壁的延伸	[43]
拟南芥（Arabidopsis thaliana）	AtWRKY46	调节铝的耐受基因	[55]
拟南芥（Arabidopsis thaliana）	AtALS3	运输铝离子至液泡中	[48]
拟南芥（Arabidopsis thaliana）	AtNIP1;2	运输苹果酸铝	[50]
高粱（Sorghum bicolor L.）	SbMATE1	调节柠檬酸的转运	[63]
高粱（Sorghum bicolor L.）	SbWRKY1	调节铝的耐受基因	[70]
高粱（Sorghum bicolor L.）	SbZNF1	调节铝的耐受基因	[70]
高粱（Sorghum bicolor L.）	SbSTOP1	AtSTOP1的同源基因	[71]
小麦（Triticum aestivum L.）	TaALMT1	调节苹果酸的转运	[65]
小麦（Triticum aestivum L.）	TaMATE1	调节柠檬酸的转运	[62]
小麦（Triticum aestivum L.）	TaSTOP1	AtSTOP1的同源基因	[61]
大豆（Glycine max）	GmALMT1	调节苹果酸的转运	[30]
大豆（Glycine max）	GmSTOP1-1	AtSTOP1的同源基因	[72]
大豆（Glycine max）	GmSTOP1-3	AtSTOP1的同源基因	[72]
玉米（Zea mays）	ZmMATE1	调节柠檬酸的转运	[60]
油菜（Brassica napus）	BnALMT1	调节苹果酸的转运	[73]
油菜（Brassica napus）	BnALMT2	调节苹果酸的转运	[73]
黑麦（Secale cereale L.）	ScALMT1	调节苹果酸的转运	[59]
黑麦（Secale cereale L.）	ScFRDL2	调节柠檬酸的转运	[59]
大麦（Hordeum vulgare L.）	HvAACT1	调节柠檬酸的转运	[61]