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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Characterisation of HvALMT1 function in transgenic barley plants

Benjamin D. Gruber A B , Emmanuel Delhaize A , Alan E. Richardson A , Ute Roessner C , Richard A. James A , Susan M. Howitt B and Peter R. Ryan A D
+ Author Affiliations
- Author Affiliations

A CSIRO Plant Industry, GPO Box 1600, Canberra, ACT 2601, Australia.

B School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia.

C Australian Centre for Plant Functional Genomics and Metabolomics Australia, University of Melbourne, Melbourne, Vic. 3010, Australia.

D Corresponding author. Email: peter.ryan@csiro.au

Functional Plant Biology 38(2) 163-175 https://doi.org/10.1071/FP10140
Submitted: 29 June 2010  Accepted: 9 December 2010   Published: 1 February 2011

Abstract

HvALMT1 from barley (Hordeum vulgare L.) encodes a protein capable of facilitating the transport of malate and other organic anions when expressed in Xenopus oocytes. The HvALMT1 gene is primarily expressed in guard cells of stomata, in regions behind the root apex and at lateral root junctions. We investigated the function of HvALMT1 in planta by overexpressing it in barley under the control of a constitutive promoter. Transgenic plants expressing HvALMT1 at levels four to 9-fold greater than controls showed reduced growth and plants showing the highest expression failed to set seed. Although measurements of conductance indicated that stomatal function was not totally impaired in the transgenic plants the time taken for the stomata to close in response to low light was significantly longer compared with controls. Elemental and metabolomic analyses of the transgenic barley shoots revealed that the concentration of calcium and levels of ascorbate, serine, threonine and pentanoate were consistently greater (2- to 14-fold) in plants that overexpressed HvALMT1, whereas whole-shoot tissue levels of fumarate were significantly lower (60–85% reduction). Transgenic plants also showed significantly greater efflux of malate and succinate from their roots than control plants. Efflux of these organic anions occurred independently of Al3+ and conferred greater Al3+ resistance in solution culture and in acidic soil. These results are consistent with HvALMT1 contributing to anion homeostasis in the cytosol and osmotic adjustment by transporting organic anions out of the cell or by sequestering them into cytosolic vesicles.

Additional keywords: aluminium-resistance, fumarate, malate, metabolomics, Hordeum vulgare, succinate, transporter.


References

Ashraf M, McNeilly T (2004) Salinity tolerance in Brassica oilseeds. Critical Reviews in Plant Sciences 23, 157–174.
Salinity tolerance in Brassica oilseeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktl2msb4%3D&md5=d8b3cfe2f6fecc90035f48e634a75f1bCAS |

Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signalling and stomatal movement. The Plant Cell 16, 1143–1162.
The ascorbic acid redox state controls guard cell signalling and stomatal movement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOqsLc%3D&md5=22901507f07e318cfc898ee40c54f4a5CAS | 15084716PubMed |

Chia DW, Yoder TJ, Reiter WD, Gibson SI (2000) Fumaric acid: an overlooked form of fixed carbon in Arabidopsis and other plants. Planta 211, 743–751.
Fumaric acid: an overlooked form of fixed carbon in Arabidopsis and other plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXntFSis7Y%3D&md5=6c3b6feab28417779682a7d81049fb5cCAS | 11089689PubMed |

Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP (2008) An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179, 669–682.
An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsl2qtLk%3D&md5=a6e7fa6039ca31b31b584dd290749121CAS | 18493079PubMed |

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7mvVagsQ%3D%3D&md5=c9ab40d4c4c5e8216321cb905f7c65b8CAS | 10069079PubMed |

Delhaize E, Ryan PR, Randall PJ (1993) Aluminum tolerance in wheat (Triticum aestivum L.) II. Aluminum-stimulated excretion of malic acid from root apices. Plant Physiology 103, 695–702.

Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proceedings of the National Academy of Sciences of the United States of America 101, 15 249–15 254.
Engineering high-level aluminum tolerance in barley with the ALMT1 gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpsVSgurc%3D&md5=898e4ac87e8c9c71f9478905698cc573CAS |

Delhaize E, Gruber BD, Pittman JK, White RG, Leung H, Miao YS, Jiang LW, Ryan PR, Richardson AE (2007a) A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. The Plant Journal 51, 198–210.
A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFCnsLs%3D&md5=e800ad814009cd4e053ef3a37d7f24cdCAS | 17559518PubMed |

Delhaize E, Gruber BD, Ryan PR (2007b) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters 581, 2255–2262.
The roles of organic anion permeases in aluminium resistance and mineral nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1aiu74%3D&md5=fc4952e8e1a5e96dd3c37a49d2476d0cCAS | 17418140PubMed |

Durrett TP, Gassmann W, Rogers EE (2007) The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiology 144, 197–205.
The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1Kjt7k%3D&md5=ea5959b4fc9c9cff4496bc9af607e772CAS | 17351051PubMed |

Fernie AD, Martinoia E (2009) Malate. Jack of all trades or master of a few? Phytochemistry 70, 828–832.
Malate. Jack of all trades or master of a few?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsFKltrs%3D&md5=dbaea0be5a9147e71070b31b89d29793CAS | 19473680PubMed |

Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant & Cell Physiology 48, 1081–1091.
An aluminum-activated citrate transporter in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVKlsrrK&md5=bf78adb9c113f55f345652dfbbfc077bCAS | 17634181PubMed |

Green LS, Rogers EE (2004) FRD3 controls iron localisation in Arabidopsis. Plant Physiology 136, 2523–2531.
FRD3 controls iron localisation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrurw%3D&md5=98773cc63768735b99310b825a10eefcCAS | 15310833PubMed |

Gruber BD, Ryan PR, Richardson AE, Tyerman SD, Ramesh S, Hebb DM, Howitt SM, Delhaize E (2010) HvALMT1 from barley is involved in the transport of organic anions. Journal of Experimental Botany 61, 1455–1467.
HvALMT1 from barley is involved in the transport of organic anions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1Kgurg%3D&md5=4f49fe222240b5792c530d99b8e013afCAS | 20176888PubMed |

Ho CL, Saito K (2001) Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana. Amino Acids 20, 243–259.
Molecular biology of the plastidic phosphorylated serine biosynthetic pathway in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXks1Gjsrs%3D&md5=f832e17ce953be4ac12b743ef0a051d4CAS | 11354602PubMed |

Hoekenga OA, Maron LG, Piñeros MA, Cancado GMA, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 9738–9743.
AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVOntrY%3D&md5=e1237f887eaa9ad4f3e59dc0026499ceCAS | 16740662PubMed |

Huang CY, Roessner U, Eickmeier I, Genc Y, Callahan DL, Shirley N, Langridge P, Bacic A (2008) Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.). Plant & Cell Physiology 49, 691–703.
Metabolite profiling reveals distinct changes in carbon and nitrogen metabolism in phosphate-deficient barley plants (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvFWns78%3D&md5=4b22144430eda2ef94d74cdeb5ea93f2CAS | 18344526PubMed |

Jacobs A, Lunde C, Bacic A, Tester M, Roessner U (2007) The impact of constitutive heterologous expression of a moss Na+ transporter on the metabolomes of rice and barley. Metabolomics 3, 307–317.
The impact of constitutive heterologous expression of a moss Na+ transporter on the metabolomes of rice and barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFOntbjL&md5=9a8a875c86fe047531cb1740a9d43bcbCAS |

Kovermann P, Meyer S, Hortensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. The Plant Journal 52, 1169–1180.
The Arabidopsis vacuolar malate channel is a member of the ALMT family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1Wrtg%3D%3D&md5=3cc7bc6f6b8e1e44152905985b4968aeCAS | 18005230PubMed |

Koo BJ, Chang AC, Crowley DE, Page AL (2006) Characterisation of organic acids recovered from rhizosphere of corn grown on biosolids-treated medium. Communications in Soil Science and Plant Analysis 37, 871–887.
Characterisation of organic acids recovered from rhizosphere of corn grown on biosolids-treated medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Oqs7c%3D&md5=5dc3cd996641c8205ef7bc45ecb6186cCAS |

Liao M, Hocking PJ, Dong B, Delhaize E, Richardson AE, Ryan PR (2008) Genotypic variation in phosphorus efficiency among wheat genotypes grown on two contrasting Australian soils. Australian Journal of Agricultural Research 59, 157–166.
Genotypic variation in phosphorus efficiency among wheat genotypes grown on two contrasting Australian soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVGhsbg%3D&md5=f3ff706d2ebd56eced9c30bcd11bca44CAS |

Ligaba A, Katsuhara M, Ryan PR, Shibasaka M, Matsumoto H (2006) The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminium resistance of plant cells. Plant Physiology 142, 1294–1303.
The BnALMT1 and BnALMT2 genes from rape encode aluminum-activated malate transporters that enhance the aluminium resistance of plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eju7%2FP&md5=3c06864c7657bcca565f2decbd942066CAS | 17028155PubMed |

Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6, 273–278.
Aluminium tolerance in plants and the complexing role of organic acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFyjsL0%3D&md5=c5dc589b8db0ecc8c2844334330d9b6eCAS | 11378470PubMed |

Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KAS, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. The Plant Journal 63, 1054–1062.
AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12it7%2FO&md5=29578953ff5e3d6db7d9283e78e24c47CAS | 20626656PubMed |

Nunes-Nesi A, Carrari F, Lytovchenko A, Smith AMO, Ehlers Loureiro M, Ratcliffe RG, Sweetlove LJ, Fernie AR (2005) Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiology 137, 611–622.
Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Kqsbs%3D&md5=bbe4b6314e9c18f7dd9e0702c31ede18CAS | 15665243PubMed |

Nunes-Nesi A, Carrari F, Gibon Y, Sulpice R, Lytovchenko A, Fisahn J, Graham J, Ratcliffe RG, Sweetlove LJ, Fernie AR (2007) Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. The Plant Journal 50, 1093–1106.
Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvVWnt7k%3D&md5=6eb8293f384fbd2cb05c81f3f734915fCAS | 17461782PubMed |

Pereira J, Zhou G, Delhaize E, Richardson TM, Ryan PR (2010) Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Annals of Botany 106, 205–214.
Engineering greater aluminium resistance in wheat by over-expressing TaALMT1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWjsLY%3D&md5=043cd29731c337cea018d0fa1f4d6099CAS | 20338951PubMed |

Piñeros MA, Cançado GMA, Kochian LV (2008a) Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in Xenopus oocytes: functional and structural implications. Plant Physiology 147, 2131–2146.
Novel properties of the wheat aluminum tolerance organic acid transporter (TaALMT1) revealed by electrophysiological characterization in Xenopus oocytes: functional and structural implications.Crossref | GoogleScholarGoogle Scholar | 18550686PubMed |

Piñeros MA, Cancado GMA, Maron LG, Lyi SM, Menossi M, Kochian LV (2008b) Not all ALMT1-type transporters mediate aluminium-activated organic acid responses: the case of ZmALMT1 – an anion-selective transporter. The Plant Journal 53, 352–367.
Not all ALMT1-type transporters mediate aluminium-activated organic acid responses: the case of ZmALMT1 – an anion-selective transporter.Crossref | GoogleScholarGoogle Scholar | 18069943PubMed |

Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant, Cell & Environment 23, 397–405.
Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFCktLg%3D&md5=6b2596767b8c064eaf3a5656eca61658CAS |

Roelfsema MRG, Hedrich R (2005) In the light of stomatal opening: new insights into ‘the watergate’. New Phytologist 167, 665–691.
In the light of stomatal opening: new insights into ‘the watergate’.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVGisbfI&md5=c3a3a72fb5411c978a70cda592aae5d6CAS | 16101906PubMed |

Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. The Plant Cell 13, 11–29.

Roessner U, Patterson JH, Forbes MG, Fincher GB, Langridge P, Bacic A (2006) An investigation of boron toxicity in barley using metabolomics. Plant Physiology 142, 1087–1101.
An investigation of boron toxicity in barley using metabolomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1ejurfL&md5=8101a6ef7176bb7db795ea7bb177eff4CAS | 16998089PubMed |

Ryan PR, Delhaize E (2010) The convergent evolution of aluminium resistance in wheat exploits a convenient currency. Functional Plant Biology 37, 275–284.
The convergent evolution of aluminium resistance in wheat exploits a convenient currency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvVGhurk%3D&md5=f0b18976530e83362a3745fa7539dcd3CAS |

Ryan PR, Delhaize E, Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103–110.
Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXkvVemsLg%3D&md5=73578ded882e7fc8aedd4efee1efda48CAS |

Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminium-activated malate transporter. The Plant Journal 37, 645–653.
A wheat gene encoding an aluminium-activated malate transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXislyltr4%3D&md5=57f1dc0388889d7f83f260e2916bb220CAS | 14871306PubMed |

Sasaki T, Mori IC, Furuichi T, Munemasa S, Toyooka K, Matsuoka K, Murata Y, Yamamoto Y (2010) Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant & Cell Physiology 51, 354–365.
Closing plant stomata requires a homolog of an aluminum-activated malate transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjt1GnsL4%3D&md5=d7d5451a8f05281af23d82375078d92cCAS | 20154005PubMed |

Schünmann PHD, Llewellyn DJ, Surin B, Boevink P, De Feyter RC, Waterhouse PM (2003) A suite of novel promoters and terminators for plant biotechnology. Functional Plant Biology 30, 443–452.
A suite of novel promoters and terminators for plant biotechnology.Crossref | GoogleScholarGoogle Scholar |

Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. Journal of Experimental Botany 57, 711–726.
The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVOqtrk%3D&md5=a3d85552a5dadaa48d1204658b702b72CAS | 16473893PubMed |

Smirnoff N (1996) The function and metabolism of ascorbic acid in plants. Annals of Botany 78, 661–669.
The function and metabolism of ascorbic acid in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjtFKrtg%3D%3D&md5=750e610051390fc67cd6ef33cb38e995CAS |

Tingay S, McElroy D, Kalla R, Fieg S, Wang M, Thornton S, Brettell R (1997) Agrobacterium tumefaciens-mediated barley transformation. The Plant Journal 11, 1369–1376.
Agrobacterium tumefaciens-mediated barley transformation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXkslajurw%3D&md5=7953e95c7f63db8d0237eb345060e3f9CAS |

Tramontano WA, Delillo AR, Yung SY, Natarajan C, Kearns CM (1991) Short-chain fatty acid-induced effects on the cell cycle in root meristems of Pisum sativum. Physiologia Plantarum 82, 79–84.
Short-chain fatty acid-induced effects on the cell cycle in root meristems of Pisum sativum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFGhtbs%3D&md5=1271e9ad85328153e4cae5af65b689e1CAS |

Vierstra RD (1996) Proteolysis in plants: mechanisms and functions. Plant Molecular Biology 32, 275–302.
Proteolysis in plants: mechanisms and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjslCl&md5=5d2e1ac1aada8601d709595e6b23d9b6CAS | 8980483PubMed |

Viskari EL, Surakka J, Pasanen P, Mirme A, Kossi S, Ruuskanen J, Holopainen JK (2000) Responses of spruce seedlings (Picea abies) to exhaust gas under laboratory conditions. I: Plant–insect interactions. Environmental Pollution 107, 89–98.
Responses of spruce seedlings (Picea abies) to exhaust gas under laboratory conditions. I: Plant–insect interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkt1KgsQ%3D%3D&md5=2b0bb021db5692b88b6064729836307cCAS | 15093012PubMed |

von Post R, von Post L, Dayteg C, Nilsson M, Forster BP, Tuvesson S (2003) A high-throughput DNA extraction method for barley seed. Euphytica 130, 255–260.
A high-throughput DNA extraction method for barley seed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1KisLw%3D&md5=e952179b1cd43baeb423c59846b9b23aCAS |

Wang M-B, Waterhouse PM (2000) High-efficiency silencing of a β-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation. Plant Molecular Biology 43, 67–82.
High-efficiency silencing of a β-glucuronidase gene in rice is correlated with repetitive transgene structure but is independent of DNA methylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlvVCjsL8%3D&md5=4a3a66f7994a1c83f96d2b92a7ee0da6CAS | 10949375PubMed |

Wang M-B, Li Z-Y, Matthews PR, Upadhyaya NM, Waterhouse PM (1998) Improved vectors for Agrobacterium tumefaciens-mediated transformation of monocot plants. Acta Horticulturae 461, 401–405.

Wang JP, Raman H, Zhou MX, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theoretical and Applied Genetics 115, 265–276.
High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvFamu7s%3D&md5=3cd2acd706fbd405cff90dddf11d65e0CAS | 17551710PubMed |

Zhang WH, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD (2008) Characterisation of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. Plant & Cell Physiology 49, 1316–1330.
Characterisation of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ygt73M&md5=2e1ebc3ca65491ebad7c686dcb94cdadCAS | 18676980PubMed |

Zhu YR, Tao HL, Lv XY, Wang SF, Wang NN, Wang Y (2004) High level of endogenous L-serine initiates senescence in Spirodela polyrrhiza. Plant Science 166, 1159–1166.
High level of endogenous L-serine initiates senescence in Spirodela polyrrhiza.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivVWmu7o%3D&md5=080118c441317f2b1345ac9582bc28f2CAS |