Biochemical, physiological and genetic analysis of aluminum tolerance of different rye species

Alscher, 2002, Role of superoxide dismutases (SODs) in controlling oxidative stress in plants, J. Exp. Bot., 53, 1331, 10.1093/jexbot/53.372.1331 Aniol, 1984, Chromosome location of genes controlling aluminium tolerance in wheat, rye and triticale, Can. J. Genet. Cytol., 26, 701, 10.1139/g84-111 Bona, 1993, Screening wheat and other small grains for acid soil tolerance, Landsc. Urban Plan., 27, 175, 10.1016/0169-2046(93)90046-G Bowler, 1992, Superoxide dismutase and stress tolerance, Annu. Rev. Plant Biol., 34, 83, 10.1146/annurev.pp.43.060192.000503 Chen, 2013, Overexpression of MsALMT1, from the aluminum-sensitive Medicago sativa enhances malate exudation and aluminum resistance in tobacco, Plant Mol. Biol. Rep., 31, 769, 10.1007/s11105-012-0543-2 Chen, 2013, Adaptation to acidic soil is achieved by increased numbers of cis-acting elements regulating ALMT1 expression in Holcus lanatus, Plant J., 76, 10 Collins, 2008, An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 Locus of Rye (Secale cereale L.), Genetics, 179, 669, 10.1534/genetics.107.083451 Contreras, 2014, Brachypodium distachyon: a model species for aluminium tolerance in Poaceae, Funct. Plant Biol., 41, 1270, 10.1071/FP13362 Delhaize, 1995, Aluminum toxicity and tolerance in plants, Plant Physiol., 107, 315, 10.1104/pp.107.2.315 Delhaize, 1993, Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices), Plant Physiol., 103, 695, 10.1104/pp.103.3.695 Devi, 2003, An intracellular mechanism of aluminum tolerance associated with high antioxidant status in cultured tobacco cells, J. Inorg. Biochem., 97, 59, 10.1016/S0162-0134(03)00182-X Du, 2010, Effects of aluminum on superoxide dismutase and peroxidase activities, and lipid peroxidation in the roots and calluses of soybeans differing in aluminum tolerance, Acta Physiol. Plant., 32, 883, 10.1007/s11738-010-0476-z El-Moneim, 2014, On the consequences of aluminium stress in rye: repression of two mitochondrial malate dehydrogenase mRNAs, Plant Biol., 17, 123, 10.1111/plb.12219 El-Moneim, 2014, Pectin methylesterase gene and aluminum tolerance in Secale cereale, Environ. Exp. Bot., 107, 125, 10.1016/j.envexpbot.2014.06.006 FAO: Food Agriculture Organization, 2018 Fontecha, 2007, Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.), Theor. Appl. Genet., 114, 249, 10.1007/s00122-006-0427-7 Fujii, 2012, Acquisition of aluminium tolerance by modification of a single gene in barley, Nat. Commun., 3, 713, 10.1038/ncomms1726 Furukawa, 2007, An aluminum-activated citrate transporter in barley, Plant Cell Physiol., 48, 1081, 10.1093/pcp/pcm091 Garcia-Oliveira, 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, 10.1186/1471-2229-13-134 Gruber, 2010, HvALMT1 from barley is involved in the transport of organic anions, J. Exp. Bot., 61, 1455, 10.1093/jxb/erq023 Gutmann, 1974, L-malate: determination with malate dehydrogenase and NAD, 1585 Hoekenga, 2006, AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis, Proc. Natl. Acad. Sci., 103, 9738, 10.1073/pnas.0602868103 Inostroza-Blancheteau, 2012, Molecular and physiological strategies to increase aluminum resistance in plants, Mol. Biol. Rep., 39, 2069, 10.1007/s11033-011-0954-4 Ishikawa, 2000, Comparison of the amount of citric and malic acids in Al media of seven plant species and two cultivars each in five plant species, Soil Sci. Plant Nutr., 46, 751, 10.1080/00380768.2000.10409141 Iuchi, 2007, Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance, Proc. Natl. Acad. Sci., 104, 9900, 10.1073/pnas.0700117104 Kim, 2001, Aluminium tolerance in triticale, wheat and rye, Euphytica, 120, 329, 10.1023/A:1017598219054 Kobayashi, 2014, STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis, Mol. Plant, 7, 311, 10.1093/mp/sst116 Kochian, 2004, How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency, Annu. Rev. Plant Biol., 55, 459, 10.1146/annurev.arplant.55.031903.141655 Kochian, 2015, Plant adaptation to acid soils: the molecular basis for crop aluminum resistance, Annu. Rev. Plant Biol., 66, 571, 10.1146/annurev-arplant-043014-114822 Li, 2000, Pattern of aluminum-induced secretion of organic acids differs between rye and wheat, Plant Physiol., 123, 1537, 10.1104/pp.123.4.1537 Liang, 2013, Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils, Plant Physiol., 161, 1347, 10.1104/pp.112.208934 Ligaba, 2006, The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminum resistance of plant cells, Plant Physiol., 142, 1294, 10.1104/pp.106.085233 Ligaba, 2012, Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux, Plant Cell Environ., 35, 1185, 10.1111/j.1365-3040.2011.02479.x Liu, 2009, Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance, Plant J., 57, 389, 10.1111/j.1365-313X.2008.03696.x Ma, 2010, Foreword: understanding how plants cope with acid soils, Funct. Plant Biol., 37, 2008, 10.1071/FPv37n4_FO Ma, 2001, Aluminium tolerance in plants and the complexing role of organic acids, Trends Plant Sci., 6, 273, 10.1016/S1360-1385(01)01961-6 Ma, 2014, Molecular mechanisms of Al tolerance in gramineous plants, Plant Soil, 381, 1, 10.1007/s11104-014-2073-1 Magalhaes, 2007, A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum, Nat. Genet., 39, 1156, 10.1038/ng2074 Maron, 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, 728, 10.1111/j.1365-313X.2009.04103.x Matsumoto, 2012, Aluminum toxicity recovery processes in root apices. Possible association with oxidative stress, Plant Sci., 185–186, 1, 10.1016/j.plantsci.2011.07.019 Pinto-Carnide, 1999, Aluminium tolerance variability in rye and wheat Portuguese germplasm, Genet. Resour. Crop Evol., 46, 81, 10.1023/A:1008642526392 Richards, 1998, Aluminum induces oxidative stress genes in Arabidopsis thaliana, Plant Physiol., 116, 409, 10.1104/pp.116.1.409 Ryan, 2010, The convergent evolution of aluminium resistance in plants exploits a convenient currency, Funct. Plant Biol., 37, 275, 10.1071/FP09261 Ryan, 2012, Adaptations to aluminum toxicity, 171 Ryan, 1995, Malate efflux from root apices and tolerance aluminum are highly correlated in wheat, Aust. J. Plant Physiol., 22, 531 Ryan, 2009, A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots, Plant Physiol., 149, 340, 10.1104/pp.108.129155 Ryan, 2010, The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils, J. Exp. Bot., 62, 9, 10.1093/jxb/erq272 Sánchez-Parra, 2014, The role of two superoxide dismutase mRNAs in rye aluminium tolerance, Plant Biol., 17, 694, 10.1111/plb.12281 Santos, 2018, Characterization, genetic diversity, phylogenetic relationships, and expression of the aluminum tolerance MATE1 gene in Secale species, Biol. Plant., 62, 109, 10.1007/s10535-017-0749-0 Sasaki, 2004, A wheat gene encoding an aluminum-activated malate transporter, Plant J., 37, 645, 10.1111/j.1365-313X.2003.01991.x Sawaki, 2009, STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities, Plant Physiol., 150, 281, 10.1104/pp.108.134700 Schoen, 2001, The conservation of wild plant species in seed banks, Bioscience, 51, 960, 10.1641/0006-3568(2001)051[0960:TCOWPS]2.0.CO;2 Silva, 2013, Rye oxidative stress under long term Al exposure, J. Plant Physiol., 170, 879, 10.1016/j.jplph.2013.01.015 Silva-Navas, 2012, The ScAACT1 gene at the Qalt5 locus as a candidate for increased aluminum tolerance in rye (Secale cereale L.), Mol. Breed., 30, 845, 10.1007/s11032-011-9668-5 Sivaguru, 2013, Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance, Plant J., 76, 297 Tahara, 2008, Aluminium distribution and reactive oxygen species accumulation in root tips of two Melaleuca trees differing in aluminium resistance, Plant Soil, 307, 167, 10.1007/s11104-008-9593-5 Tesfaye, 2001, Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum, Plant Physiol., 127, 1836, 10.1104/pp.010376 Yamaji, 2009, A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice, Plant Cell, 21, 3339, 10.1105/tpc.109.070771 Yamamoto, 2001, Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots, Plant Physiol., 125, 199, 10.1104/pp.125.1.199 Yamamoto, 2002, Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells, Plant Physiol., 128, 63, 10.1104/pp.010417 Yin, 2010, The involvement of lipid peroxide-derived aldehydes in aluminum toxicity of tobacco roots, Plant Physiol., 152, 1406, 10.1104/pp.109.151449 Yokosho, 2010, Isolation and characterisation of two MATE genes in rye, Funct. Plant Biol., 37, 296, 10.1071/FP09265 Yokosho, 2011, An Al-inducible MATE gene is involved in external detoxification of Al in rice, Plant J., 68, 1061, 10.1111/j.1365-313X.2011.04757.x Yokosho, 2016, Functional analysis of a MATE gene OsFRDL2 revealed its involvement in Al-induced secretion of citrate, but a lower contribution to Al tolerance in rice, Plant Cell Physiol., 57, 976, 10.1093/pcp/pcw026