Similar articles

Abstract: Aluminum (Al) is the most abundant metal element in the earth’s crust. On acid soils, at pH 5.5 or lower, part of insoluble Al-containing minerals become solubilized into soil solution, with resultant highly toxic effects on plant growth and development. Nevertheless, some plants have developed Al-tolerance mechanisms that enable them to counteract this Al toxicity. One such well-documented mechanism is the Al-induced secretion of organic acid anions, including citrate, malate, and oxalate, from plant roots. Once secreted, these anions chelate external Al ions, thus protecting the secreting plant from Al toxicity. Genes encoding the citrate and malate transporters responsible for secretion have been identified and characterized, and accumulating evidence indicates that regulation of the expression of these transporter genes is critical for plant Al tolerance. In this review, we outline the recent history of research into plant Al-tolerance mechanisms, with special emphasis on the physiology of Al-induced secretion of organic acid anions from plant roots. In particular, we summarize the identification of genes encoding organic acid transporters and review current understanding of genes regulating organic acid secretion. We also discuss the possible signaling pathways regulating the expression of organic acid transporter genes.

铝诱导植物根系分泌有机酸阴离子的机理及其调控

[1]Aguilera JG, Minozzo JAD, Barichello D, et al., 2016. Alleles of organic acid transporter genes are highly correlated with wheat resistance to acidic soil in field conditions. Theor Appl Genet, 129(7):1317-1331.

[2]Barceló J, Poschenrieder C, 2002. Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: a review. Environ Exp Bot, 48(1):75-92.

[3]Che J, Tsutsui T, Yokosho K, et al., 2018. Functional characterization of an aluminum (Al)-inducible transcription factor, ART2, revealed a different pathway for Al tolerance in rice. New Phytol, 220(1):209-218.

[4]Chen PY, Sjogren CA, Larsen PB, et al., 2019. A multi-level response to DNA damage induced by aluminium. Plant J, in press.

[5]Chen Q, Wu KH, Wang P, et al., 2013. Overexpression of MsALMT1, from the aluminum-sensitive Medicago sativa, enhances malate exudation and aluminum resistance in tobacco. Plant Mol Biol Rep, 31(3):769-774.

[6]Chen WW, Fan W, Lou HQ, et al., 2017. Regulating cytoplasmic oxalate homeostasis by Acyl activating enzyme3 is critical for plant Al tolerance. Plant Signal Behav, 12(1):e1276688.

[7]Chen ZC, Yokosho K, Kashino M, et al., 2013. Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus. Plant J, 76(1):10-23.

[8]Collins NC, Shirley NJ, Saeed M, et al., 2008. An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics, 179(1):669-682.

[9]Daspute AA, Kobayashi Y, Panda SK, et al., 2018. Characterization of CcSTOP1; a C2H2-type transcription factor regulates Al tolerance gene in pigeonpea. Planta, 247(1):201-214.

[10]Delhaize E, Craig S, Beaton CD, et al., 1993a. Aluminum tolerance in wheat (Triticum aestivum L.):I. uptake and distribution of aluminum in root apices. Plant Physiol, 103(3):685-693.

[11]Delhaize E, Ryan PR, Randall PJ, 1993b. Aluminum tolerance in wheat (Triticum aestivum L.):II. aluminum-stimulated excretion of malic acid from root apices. Plant Physiol, 103(3):695-702.

[12]Delhaize E, Ryan PR, Hebb DM, et al., 2004. Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Natl Acad Sci USA, 101(42):15249-15254.

[13]Ding ZJ, Yan JY, Xu XY, et al., 2013. WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J, 76(5):825-835.

[14]Durrett TP, Gassmann W, Rogers EE, 2007. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol, 144(1):197-205.

[15]Famoso AN, Zhao KY, Clark RT, et al., 2011. Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet, 7(8):e1002221.

[16]Fan W, Lou HQ, Gong YL, et al., 2015. Characterization of an inducible C2H2-type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol, 208(2):456-468.

[17]Fan W, Xu JM, Lou HQ, et al., 2016. Physiological and molecular analysis of aluminium-induced organic acid anion secretion from grain amaranth (Amaranthus hypochondriacus L.) roots. Int J Mol Sci, 17(5):608.

[18]Fan W, Xu JM, Wu P, et al., 2019. Alleviation by abscisic acid of Al toxicity in rice bean is not associated with citrate efflux but depends on ABI5-mediated signal transduction pathways. J Integr Plant Biol, 61(2):140-154.

[19]Fujii M, Yokosho K, Yamaji N, et al., 2012. Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun, 3:713.

[20]Furukawa J, Yamaji N, Wang H, et al., 2007. An aluminum-activated citrate transporter in barley. Plant Cell Physiol, 48(8):1081-1091.

[21]Garcia-Oliveira AL, Benito C, Prieto P, et al., 2013. Molecular characterization of TaSTOP1 homoeologues and their response to aluminium and proton (H⁺) toxicity in bread wheat (Triticum aestivum L.). BMC Plant Biol, 13:134.

[22]Hartwell BL, Pember FR, 1918. The presence of aluminum as a reason for the difference in the effects of so-called acid soil on barley and rye. Soil Sci, 6(4):259-280.

[23]Hoekenga OA, Maron LG, Piñeros MA, et al., 2006. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA, 103(25):9738-9743.

[24]Horst WJ, Wang YX, Eticha D, 2010. The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann Bot, 106(1):185-197.

[25]Huang CF, Yamaji N, Mitani N, et al., 2009. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell, 21(2):655-667.

[26]Huang CF, Yamaji N, Chen ZC, et al., 2012. A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J, 69(5):857-867.

[27]Huang S, Gao J, You JF, et al., 2018. Identification of STOP1-like proteins associated with aluminum tolerance in sweet sorghum (Sorghum bicolor L.). Front Plant Sci, 9:258.

[28]Iuchi S, Koyama H, Iuchi A, et al., 2007. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA, 104(23):9900-9905.

[29]Kashino-Fujii M, Yokosho K, Yamaji N, et al., 2018. Retrotransposon insertion and DNA methylation regulate aluminum tolerance in European barley accessions. Plant Physiol, 178(2):716-727.

[30]Kitagawa T, 1986. Genotypic variations in Al resistance in wheat and organic acid secretion. Jpn J Soil Sci Plant Nutr, 57:352-358.

[31]Kobayashi Y, Hoekenga OA, Itoh H, et al., 2007. Characterization of AtALMT1 expression in aluminum-inducible malate release and its role for rhizotoxic stress tolerance in Arabidopsis. Plant Physiol, 145(3):843-852.

[32]Kobayashi Y, Ohyama Y, Kobayashi Y, et al., 2014. STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol Plant, 7(2):311-322.

[33]Kochian LV, 1995. Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Plant Mol Biol, 46:237-260.

[34]Kochian LV, Hoekenga OA, Piñeros MA, 2004. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol, 55:459-493.

[35]Kochian LV, Piñeros MA, Liu JP, et al., 2015. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol, 66:571-598.

[36]Kollmeier M, Dietrich P, Bauer CS, et al., 2001. Aluminum activates a citrate-permeable anion channel in the aluminum-sensitive zone of the maize root apex. A comparison between an aluminum-sensitive and an aluminum-resistant cultivar. Plant Physiol, 126(1):397-410.

[37]Kundu A, Das S, Basu S, et al., 2019. GhSTOP1, a C2H2 type zinc finger transcription factor is essential for Aluminum and proton stress tolerance and lateral root initiation in cotton. Plant Biol, 21(1):35-44.

[38]Larsen PB, Geisler MJB, Jones CA, et al., 2005. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J, 41(3):353-363.

[39]Li GZ, Wang ZQ, Yokosho K, et al., 2018. Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol, 219(1):149-162.

[40]Li XF, Ma JF, Matsumoto H, 2000. Pattern of aluminum-induced secretion of organic acids differs between rye and wheat. Plant Physiol, 123(4):1537-1544.

[41]Li YY, Zhang YJ, Zhou Y, et al., 2009. Protecting cell walls from binding aluminum by organic acids contributes to aluminum resistance. J Integr Plant Biol, 51(6):574-580.

[42]Liang CY, Piñeros MA, Tian J, et al., 2013. Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiol, 161(3):1347-1361.

[43]Ligaba A, Katsuhara M, Ryan PR, et al., 2006. The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells. Plant Physiol, 142(3):1294-1303.

[44]Ligaba A, Kochian L, Piñeros M, 2009. Phosphorylation at S384 regulates the activity of the TaALMT1 malate transporter that underlies aluminum resistance in wheat. Plant J, 60(3):411-423.

[45]Ligaba-Osena A, Fei ZJ, Liu JP, et al., 2017. Loss-of-function mutation of the calcium sensor CBL1 increases aluminum sensitivity in Arabidopsis. New Phytol, 214(2):830-841.

[46]Liu JP, Magalhaes JV, Shaff J, et al., 2009. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J, 57(3):389-399.

[47]Liu MY, Chen WW, Xu JM, et al., 2013. The role of VuMATE1 expression in aluminium-inducible citrate secretion in rice bean (Vigna umbellata) roots. J Exp Bot, 64(7):1795-1804.

[48]Liu MY, Lou HQ, Chen WW, et al., 2018. Two citrate transporters coordinately regulate citrate secretion from rice bean root tip under aluminum stress. Plant Cell Environ, 41(4):809-822.

[49]Lou HQ, Gong YL, Fan W, et al., 2016a. A formate dehydrogenase confers tolerance to aluminum and low pH. Plant Physiol, 171(1):294-305.

[50]Lou HQ, Fan W, Xu JM, et al., 2016b. An oxalyl-CoA synthetase is involved in oxalate degradation and aluminum tolerance. Plant Physiol, 172(3):1679-1690.

[51]Ma JF, 2000. Role of organic acids in detoxification of aluminum in higher plants. Plant Cell Physiol, 41(4):383-390.

[52]Ma JF, 2007. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol, 264: 225-252.

[53]Ma JF, Zheng SJ, Matsumoto H, 1997. Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant Cell Physiol, 38(9):1019-1025.

[54]Ma Z, Miyasaka SC, 1998. Oxalate exudation by taro in response to Al. Plant Physiol, 118(3):861-865.

[55]Magalhaes JV, Liu JP, Guimarães CT, et al., 2007. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet, 39(9):1156-1161.

[56]Maron LG, Piñeros MA, Guimarães CT, et al., 2010. 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. Plant J, 61(5):728-740.

[57]Maron LG, Guimarães CT, Kirst M, et al., 2013. Aluminum tolerance in maize is associated with higher MATE1 gene copy number. Proc Natl Acad Sci USA, 110(13):5241-5246.

[58]Matsumoto H, 2000. Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol, 200:1-46.

[59]Matzenbacher RG, 1988. Advances made in developing wheats with better aluminum toxicity tolerance in Brazil. In: Klatt AR (Ed.), Wheat Production Constraints in Tropical Environments. CIMMYT, Mexico, p.285-304.

[60]Melo JO, Lana UGP, Piñeros MA, et al., 2013. Incomplete transfer of accessory loci influencing SbMATE expression underlies genetic background effects for aluminum tolerance in sorghum. Plant J, 73(2):276-288.

[61]Melo JO, Martins LGC, Barros BA, et al., 2019. Repeat variants for the SbMATE transporter protect sorghum roots from aluminum toxicity by transcriptional interplay in cis and trans. Proc Natl Acad Sci USA, 116(1):313-318.

[62]Miyasaka SC, Buta JG, Howell RK, et al., 1991. Mechanism of aluminum tolerance in snapbeans: root exudation of citric acid. Plant Physiol, 96(3):737-743.

[63]Morita A, Yanagisawa O, Maeda S, et al., 2011. Tea plant (Camellia sinensis L.) roots secrete oxalic acid and caffeine into medium containing aluminum. Soil Sci Plant Nutr, 57(6):796-802.

[64]Nezames CD, Sjogren CA, Barajas JF, et al., 2012. The Arabidopsis cell cycle checkpoint regulators TANMEI/ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell, 24(2):608-621.

[65]Ohyama Y, Ito H, Kobayashi Y, et al., 2013. Characterization of AtSTOP1 orthologous genes in tobacco and other plant species. Plant Physiol, 162(4):1937-1946.

[66]Osawa H, Matsumoto H, 2001. Possible involvement of protein phosphorylation in aluminum-responsive malate efflux from wheat root apex. Plant Physiol, 126(1):411-420.

[67]Pellet DM, Grunes DL, Kochian LV, 1995. Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta, 196(4):788-795.

[68]Pereira JF, Ryan PR, 2019. The role of transposable elements in the evolution of aluminium resistance in plants. J Exp Bot, 70(1):41-54.

[69]Pereira JF, Barichello D, Ferreira JR, et al., 2015. TaALMT1 and TaMATE1B allelic variability in a collection of Brazilian wheat and its association with root growth on acidic soil. Mol Breeding, 35(8):169.

[70]Piñeros MA, Kochian LV, 2001. A patch-clamp study on the physiology of aluminum toxicity and aluminum tolerance in maize. Identification and characterization of Al³⁺-induced anion channels. Plant Physiol, 125(1):292-305.

[71]Ramesh SA, Tyerman SD, Xu B, et al., 2015. GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun, 6:7879.

[72]Rengel Z, 2004. Aluminium cycling in the soil-plant-animal-human continuum. Biometals, 17(6):669-689.

[73]Rounds MA, Larsen PB, 2008. Aluminum-dependent root-growth inhibition in Arabidopsis results from AtATR-regulated cell-cycle arrest. Curr Biol, 18(19):1495-1500.

[74]Ryan PR, Delhaize E, 2010. The convergent evolution of aluminium resistance in plants exploits a convenient currency. Funct Plant Biol, 37(4):275-284.

[75]Ryan PR, Delhaize E, Jones DL, 2001. Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Physiol Plant Mol Biol, 52:527-560.

[76]Ryan PR, Raman H, Gupta S, et al., 2009. A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol, 149(1):340-351.

[77]Ryan PR, Raman H, Gupta S, et al., 2010. The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. Plant J, 64(3):446-455.

[78]Sasaki T, Yamamoto Y, Ezaki B, et al., 2004. A wheat gene encoding an aluminum-activated malate transporter. Plant J, 37(5):645-653.

[79]Sasaki T, Ryan PR, Delhaize E, et al., 2006. Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol, 47(10):1343-1354.

[80]Sawaki Y, Iuchi S, Kobayashi Y, et al., 2009. STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol, 150(1):281-294.

[81]Sawaki Y, Kobayashia Y, Kihara-Doi T, et al., 2014. Identification of a STOP1-like protein in Eucalyptus that regulates transcription of Al tolerance genes. Plant Sci, 223: 8-15.

[82]Sharma T, Dreyer I, Kochian L, et al., 2016. The ALMT family of organic acid transporters in plants and their involvement in detoxification and nutrient security. Front Plant Sci, 7:1488.

[83]Singh S, Tripathi DK, Singh S, et al., 2017. Toxicity of aluminium on various levels of plant cells and organism: a review. Environ Exp Bot, 137:177-193.

[84]Sjogren CA, Larsen PB, 2017. SUV2, which encodes an ATR-related cell cycle checkpoint and putative plant ATRIP, is required for aluminium-dependent root growth inhibition in Arabidopsis. Plant Cell Environ, 40(9):1849-1860.

[85]Sjogren CA, Bolaris SC, Larsen PB, 2015. Aluminum-dependent terminal differentiation of the Arabidopsis root tip is mediated through an ATR-, ALT2-, and SOG1-regulated transcriptional response. Plant Cell, 27(9):2501-2515.

[86]Takanashi K, Shitan N, Yazaki K, 2014. The multidrug and toxic compound extrusion (MATE) family in plants. Plant Biotechnol, 31(5):417-430.

[87]Taylor GJ, 1991. Current views of the aluminum stress response; the physiological basis of tolerance. Curr Top Plant Biochem Physiol, 10:57-93.

[88]Tokizawa M, Kobayashi Y, Saito T, et al., 2015. SENSITIVE TO PROTON RHIZOTOXICITY1, CALMODULIN BINDING TRANSCRIPTION ACTIVATOR2, and other transcription factors are involved in ALUMINUM-ACTIVATED MALATE TRANSPORTER1 expression. Plant Physiol, 167(3):991-1003.

[89]Tovkach A, Ryan PR, Richardson AE, et al., 2013. Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol, 161(2):880-892.

[90]Tsutsui T, Yamaji N, Ma JF, 2011. Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. Plant Physiol, 156(2):925-931.

[91]von Uexküll HR, Mutert E, 1995. Global extent, development and economic impact of acid soils. Plant soil, 171(1):1-15.

[92]Wu WW, Lin Y, Chen QQ, et al., 2018. Functional conservation and divergence of soybean GmSTOP1 members in proton and aluminum tolerance. Front Plant Sci, 9:570.

[93]Xia JX, Yamaji N, Kasai T, et al., 2010. Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci USA, 107(43):18381-18385.

[94]Xia JX, Yamaji N, Ma JF, 2013. A plasma membrane-localized small peptide is involved in rice aluminum tolerance. Plant J, 76(2):345-355.

[95]Yang JL, Zheng SJ, He YF, et al., 2005. Aluminium resistance requires resistance to acid stress: a case study with spinach that exudes oxalate rapidly when exposed to Al stress. J Exp Bot, 56(414):1197-1203.

[96]Yang JL, Zhang L, Li YY, et al., 2006a. Citrate transporters play a critical role in aluminium-stimulated citrate efflux in rice bean (Vigna umbellata) roots. Ann Bot, 97(4):579-584.

[97]Yang JL, Zheng SJ, He YF, et al., 2006b. Comparative studies on the effect of a protein-synthesis inhibitor on aluminium-induced secretion of organic acids from Fagopyrum esculentum Moench and Cassia tora L. roots. Plant Cell Environ, 29(2):240-246.

[98]Yang JL, Zhang L, Zheng SJ, 2008. Aluminum-activated oxalate secretion does not associate with internal content among some oxalate accumulators. J Integr Plant Biol, 50(9):1103-1107.

[99]Yang JL, Zhu XF, Peng YX, et al., 2011. Aluminum regulates oxalate secretion and plasma membrane H⁺-ATPase activity independently in tomato roots. Planta, 234(2):281-291.

[100]Yang XY, Yang JL, Zhou Y, et al., 2011. A de novo synthesis citrate transporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al-activated citrate efflux in rice bean (Vigna umbellata) root apex. Plant Cell Environ, 34(12):2138-2148.

[101]Yang ZM, Nian H, Sivaguru M, et al., 2001. Characterization of aluminium-induced citrate secretion in aluminium-tolerant soybean (Glycine max) plants. Physiol Plantarum, 113(1):64-71.

[102]Yokosho K, Yamaji N, Ma JF, 2010. Isolation and characterisation of two MATE genes in rye. Funct Plant Biol, 37(4):296-303.

[103]Yokosho K, Yamaji N, Ma JF, 2011. An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J, 68(6):1061-1069.

[104]Yokosho K, Yamaji N, Fujii-Kashino M, et al., 2016. Retrotransposon-mediated aluminum tolerance through enhanced expression of the citrate transporter OsFRDL4. Plant Physiol, 172(4):2327-2336.

[105]You JF, He YF, Yang JL, et al., 2005. A comparison of aluminum resistance among Polygonum species originating on strongly acidic and neutral soils. Plant Soil, 276(1-2):143-151.

[106]Zhang L, Wu XX, Wang JF, et al., 2018. BoALMT1, an Al-induced malate transporter in cabbage, enhances aluminum tolerance in Arabidopsis thaliana. Front Plant Sci, 8:2156.

[107]Zhang Y, Guo JL, Chen M, et al., 2018. The cell cycle checkpoint regulator ATR is required for internal aluminum toxicity-mediated root growth inhibition in Arabidopsis. Front Plant Sci, 9:118.

[108]Zhang Y, Zhang J, Guo JL, et al., 2019. F-box protein RAE1 regulates the stability of the aluminum-resistance transcription factor STOP1 in Arabidopsis. Proc Natl Acad Sci USA, 116(1):319-327.

[109]Zhao H, Huang W, Zhang YG, et al., 2018. Natural variation of CsSTOP1 in tea plant (Camellia sinensis) related to aluminum tolerance. Plant Soil, 431(1-2):71-87.

[110]Zheng SJ, Yang JL, 2005. Target sites of aluminum phytotoxicity. Biol Plant, 49(3):321-331.

[111]Zheng SJ, Ma JF, Matsumoto H, 1998. High aluminum resistance in buckwheat. I. Al-induced specific secretion of oxalic acid from root tips. Plant Physiol, 117(3):745-751.