Skip to main content
SpringerLink
Log in

TaALMT1 and TaMATE1B allelic variability in a collection of Brazilian wheat and its association with root growth on acidic soil

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Repeated blocks in the TaALMT1 promoter as well as a transposon insertion in the TaMATE1B upstream region have been correlated with the level of gene expression, organic acid efflux, and ultimately aluminum (Al3+) resistance in wheat (Triticum aestivum L.). In this study, we investigated the allelic polymorphism related to the TaALMT1 and TaMATE1B promoter regions in 300 Brazilian wheat genotypes and the correlation of that variation with root growth on acid soil. In addition, SSR markers were used to determine the genetic variability of the genotypes. Seven TaALMT1 promoter alleles (Types I–VII) were detected based on size of PCR products. The most common alleles were Type V and Type VI (71.3 and 11.9 %, respectively), and these are generally associated with higher levels of TaALMT1 expression and Al3+ resistance. The promoter alleles Type I and Type II, which are usually associated with Al3+ sensitivity, were detected in 12.2 % of the genotypes. The insertion in the TaMATE1B promoter, associated with greater Al3+ resistance, was identified in 80 genotypes. Combination among the alleles allowed the separation in 12 haplotypes were 68 genotypes presented the TaALMT1 promoters Type V and Type VI along with the transposon insertion in the TaMATE1B promoter. However, the most represented haplotype was Type V without the insertion (176 genotypes). Short-term soil experiment, performed in 33 genotypes representing the 12 haplotypes, revealed that the higher relative root length was observed in some genotypes presenting TaALMT1 promoters Type V or Type VI and the transposon insertion in the TaMATE1B promoter. Moreover, when comparing genotypes inside the same haplotype, the transposon insertion was significantly advantageous for a few materials. However, the majority the genotypes presenting the insertion in the TaMATE1B promoter did not outperform the genotypes without the insertion but showing the same TaALMT1 promoter. Analysis using SSR markers, with an average PIC of 0.60, showed high genetic diversity among the genotypes belonging to different haplotypes. The alleles and the genetically diverse genotypes reported here should be considered for wheat-breeding programs aiming increments in wheat Al3+ resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson JA, Churchill GA, Autrique JE, Tanksley SD, Sorrells ME (1993) Optimizing parental selection for genetic linkage maps. Genome 36:181–186

    Article  CAS  PubMed  Google Scholar 

  • Baier AC, Somers DJ, Gusiafson JP (1995) Aluminium tolerance in wheat: correlating hydroponic evaluations with field soil performances. Plant Breeding 114:291–296

    Article  CAS  Google Scholar 

  • Bertan I, Carvalho FIF, Oliveira AC, Silva JAG, Benin G, Vieira EA, Silva GO, Hartwig I, Valério IP, Finatto T (2006) Dissimilaridade genética entre genótipos de trigo avaliados em cultivo hidropônico sob estresse por alumínio. Bragantia 65:55–63

    Article  CAS  Google Scholar 

  • Cai S, Bai GH, Zhang D (2008) Quantitative trait loci for aluminum resistance in Chinese wheat landrace FSW. Theor Appl Genet 117:49–56

    Article  CAS  PubMed  Google Scholar 

  • Camargo CEO, Oliveira OF (1981) Tolerância de cultivares de trigo a diferentes níveis de alumínio em solução nutritiva e no solo. Bragantia 40:21–31

    Article  Google Scholar 

  • Camargo CEO, Felicio JC, Rocha Junior LS (1987) Trigo: tolerância ao alumínio em solução nutritiva. Bragantia 46:183–190

    CAS  Google Scholar 

  • Camargo CEO, Ferreira-Filho AWP, Ramos LCS, Pettinelli-Junior A, Castro JL, Felicio JC, Salomon MV, Mistro JC (2003) Comportamento de linhagens diaplóides de trigo em dois locais do Estado de São Paulo. Bragantia 62:217–226

    Article  Google Scholar 

  • Camargo CEO, Felicio JC, Ferreira Filho AWP, Lobato MTV (2006) Tolerância de genótipos de trigo comum, trigo duro e triticale à toxicidade de alumínio em soluções nutritivas. Bragantia 65:43–53

    CAS  Google Scholar 

  • Coelho MAO, Condé ABT, Yamanaka CH, Corte HR (2010) Avaliação da produtividade de trigo (Triticum aestivum L.) de sequeiro em Minas Gerais. Biosci J 26:717–723

    Google Scholar 

  • de Sousa CNA (1998) Classification of Brazilian wheat cultivars for aluminium toxicity in acid soils. Plant Breed 117:217–221

    Article  Google Scholar 

  • de Sousa CAN, Caierão E (2014) Cultivares de trigo indicadas para cultivo no Brasil e instituições criadoras—1922 a 2014, 2nd edn. Embrapa, Brasília

    Google Scholar 

  • 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 Physiol 103:695–702

    PubMed Central  CAS  PubMed  Google Scholar 

  • Delhaize E, Ryan PR, Hebb DM, Yamamoto Y, Sasaki T, Matsumoto H (2004) Engineering high-level aluminum tolerance in barley with the ALMT1 gene. Proc Acad Sci USA 101:15249–15254

    Article  CAS  Google Scholar 

  • Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Lett 581:2255–2262

    Article  CAS  PubMed  Google Scholar 

  • Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR, Richardson AE (2009) Transgenic barley (Hordeum vulgare L.) expressing the wheat aluminium resistance gene (TaALMT1) shows enhanced phosphorus nutrition and grain production when grown on an acid soil. Plant Biotech J 7:391–400

    Article  CAS  Google Scholar 

  • Delhaize E, James RA, Ryan PR (2012a) Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil. New Phytol 195:609–619

    Article  CAS  PubMed  Google Scholar 

  • Delhaize E, Ma JF, Ryan PR (2012b) Transcriptional regulation of aluminium tolerance genes. Trends Plant Sci 17:341–348

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf material. Phytochem Bull 19:11–15

    Google Scholar 

  • Eagles HA, Cane K, Trevaskis B, Vallance N, Eastwood RF, Gororo NN, Kuchel H, Martin PJ (2014) Ppd1, Vrn1, ALMT1 and Rht genes and their effects on grain yield in lower rainfall environments in southern Australia. Crop Pasture Sci 65:159–170

    Article  CAS  Google Scholar 

  • Echart CL, Cavalli-Molina S (2001) Fitotoxicidade do alumínio: efeitos, mecanismo de tolerância e seu controle genético. Ciência Rural 31:531–541

    Article  Google Scholar 

  • FAO (2000) Land resource potential and constraints at regional and country levels. Land and Water Development Division, Rome

    Google Scholar 

  • Garcia-Oliveira AL, Martins-Lopes P, Tolrá R, Poschenrieder C, Tarquis M, Guedes-Pinto H, Benito C (2014) 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). Physiol Plant 152:441–452

    Article  CAS  PubMed  Google Scholar 

  • Garvin DF, Carver BF (2003) Role of the genotype in tolerance to acidity and aluminum toxicity. In: Rengel Z (ed) Handbook of soil acidity. Marcel Dekker Inc., New York, pp 387–406

    Google Scholar 

  • Guo P, Bai G, Carver B, Li R, Bernardo A, Baum M (2007) Transcriptional analysis between two wheat near-isogenic lines contrasting in aluminum tolerance under aluminum stress. Mol Genet Genomics 277:1–12

    Article  CAS  PubMed  Google Scholar 

  • Houde M, Diallo AO (2008) Identification of genes and pathways associated with aluminum stress and tolerance using transcriptome profiling of wheat near-isogenic lines. BMC Genom 9:400

    Article  Google Scholar 

  • Hu SW, Bai GH, Carver BF, Zhang DD (2008) Diverse origins of aluminum-resistance sources in wheat. Theor Appl Genet 118:29–41

    Article  CAS  PubMed  Google Scholar 

  • Huang XQ, Börner AB, Röder MS, Ganal MW (2002) Assessing genetic diversity of wheat (Triticum aestivum L.) germplasm using microsatellite markers. Theor Appl Genet 105:699–707

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Piñeros MA, Liu J, Magalhaes JV (2015) Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol 66:23.1–23.28

    Article  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Piñeros MA, Kochian LV (2014) The role of aluminum sensing and signaling in plant aluminum resistance. J Integr Plant Biol 56:221–230

    Article  CAS  PubMed  Google Scholar 

  • Ma HX, Bai GH, Lu WZ (2006) Quantitative trait loci for aluminum resistance in wheat cultivar Chinese spring. Plant Soil 283:239–249

    Article  CAS  Google Scholar 

  • Magalhães JV, Liu J, Guimarães CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE, Hoekenga OA, Piñeros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161

    Article  PubMed  Google Scholar 

  • Pereira JF, Zhou G, Delhaize E, Richardson T, Zhou M, Ryan PR (2010) Engineering greater aluminium resistance in wheat by over-expressing TaALMT1. Ann Bot 106:205–214

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raman H, Zhang K, Cakir M, Appels R, Garvin DF et al (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48:781–791

    Article  CAS  PubMed  Google Scholar 

  • Raman H, Ryan PR, Raman R, Stodart BJ, Zhang K, Martin P, Wood R, Sasaki T, Yamamoto Y, Mackay M, Hebb DM, Delhaize E (2008) Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.). Theor Appl Genet 116:343–354

    Article  CAS  PubMed  Google Scholar 

  • Raman H, Stodart B, Ryan PR, Delhaize E, Emebiri L, Raman R, Coombes N, Milgate A (2010) Genome-wide association analyses of common wheat (Triticum aestivum L.) germplasm identifies multiple loci for aluminium resistance. Genome 53:957–966

    Article  CAS  PubMed  Google Scholar 

  • Röder MS, Korzum V, Wendehake K, Plashke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed Central  PubMed  Google Scholar 

  • Ryan PR, Raman H, Gupta S, Horst WJ, Delhaize E (2009) A second mechanism for aluminum resistance in wheat relies on the constitutive efflux of citrate from roots. Plant Physiol 149:340–351

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ryan PR, Raman H, Gupta S, Sasaki T, Yamamoto Y, Delhaize E (2010) The multiple origins of aluminium resistance in hexaploid wheat include Aegilops tauschii and more recent cis mutations to TaALMT1. Plant J 64:446–455

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Tyerman SD, Sasaki T, Furuichi T, Yamamoto Y, Zhang WH, Delhaize E (2011) The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. J Exp Bot 62:9–20

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, James RA, Weligama C, Delhaize E, Rattey A, Lewis DC, Bovill WD, McDonald G, Rathjen TM, Wang E, Fettell NA, Richardson AE (2014) Can citrate efflux from roots improve phosphorus uptake by plants? Testing the hypothesis with near-isogenic lines of wheat. Physiol Plant 151:230–242

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Ryan PR, Delhaize E, Hebb DM, Ogihara Y, Kawaura K, Noda K, Kojima T, Toyoda A, Matsumoto H, Yamamoto Y (2006) Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol 47:1343–1354

    Article  CAS  PubMed  Google Scholar 

  • Scheeren PL, Caierão E, Silva MS, Nascimento AJ, Caetano VR, Bassoi MC, Brunetta D, Albrecht JC, Quadros WJ, Sousa PG, Trindade MG, Sobrinho JS, Wiethölter S, Cunha GR (2008) Challenges to wheat production in Brazil. In: Reynolds MP, Pietragalla J, Braun HJ (eds) International symposium on wheat yield potential. CIMMYT, pp 167–170

  • Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  • Schuster I, Vieira ESN, Silva GJ, Franco FA, Marchioro VS (2009) Genetic variability in Brazilian wheat cultivars assessed by microsatellite markers. Genet Mol Biol 32:557–563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5:233–241

    Article  CAS  PubMed  Google Scholar 

  • Stodart BJ, Raman H, Coombes N, Mackay M (2007) Evaluating landraces of bread wheat Triticum aestivum L. for tolerance to aluminium under low pH conditions. Genet Resour Crop Evol 54:759–766

    Article  Google Scholar 

  • Tang C, Nuruzzaman M, Rengel Z (2003) Screening wheat genotypes for tolerance of soil acidity. Aust J Agr Res 54:445–452

    Article  Google Scholar 

  • Tovkach A, Ryan PR, Richardson AE, Lewis DC, Rathjen TM, Ramesh S, Tyerman SD, Delhaize E (2013) Transposon-mediated alteration of TaMATE1B expression in wheat confers constitutive citrate efflux from root apices. Plant Physiol 161:880–892

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. Plant Soil 171:1–15

    Article  Google Scholar 

  • Warburton ML, Crossa J, Franco J, Kazi M, Trethowan R, Rajaram S, Pfeiffer W, Zhang P, Dreisigacker S, van Ginkel M (2006) Bringing wild relatives back into the family: recovering genetic diversity in CIMMYT improved wheat germplasm. Euphytica 149:289–301

    Article  CAS  Google Scholar 

  • Yamada T (2005) The Cerrado of Brazil: a success story of production on acid soils. Soil Sci Plant Nutr 51:317–620

    Google Scholar 

  • Zhang WH, Ryan PR, Sasaki T, Yamamoto Y, Sullivan W, Tyerman SD (2008) Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana Tabacum L.) cells. Plant Cell Physiol 49:1316–1330

    Article  CAS  PubMed  Google Scholar 

  • Zheng SJ, Ma JF, Matsumoto H (1998) Continuous secretion of organic acids is related to aluminum resistance during relatively long-term exposure to aluminium stress. Physiol Plant 103:209–214

    Article  CAS  Google Scholar 

  • Zhou LL, Bai GH, Carver B, Zhang DD (2007) Identification of new sources of aluminum resistance in wheat. Plant Soil 297:105–118

    Article  CAS  Google Scholar 

  • Zhou G, Delhaize E, Zhou M, Ryan PR (2013) The barley MATE gene, HvAACT1, increases citrate efflux and Al3+ tolerance when expressed in wheat and barley. Ann Bot 112:603–612

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhou G, Pereira JF, Delhaize E, Zhou M, Magalhaes JV, Ryan PR (2014) Enhancing the aluminium tolerance of barley by expressing the citrate transporter genes SbMATE and FRD3. J Exp Bot 65:2381–2390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are thankful to Embrapa (Empresa Brasileira de Pesquisa Agropecuária) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for financial support (project Embrapa 02.11.08.001.00.00 and PNPD 560516/2010-0 fellowship to Jorge González Aguilera). We thank Dr Sirio Wietholter and his team for the soil analysis, and Dr. Douglas Lau for supplying reagents. We are grateful to Dr. Emmanuel Delhaize and Dr. Peter R. Ryan (CSIRO Agriculture) and to Dr. Caroline Turchetto for valuable discussions.

Author information

Author notes

  1. Diliane Barichello

    Present address: Instituto Agronômico do Paraná, Rodovia Celso Garcia Cid, km 375, Londrina, PR, CEP 86047-902, Brazil

Authors and Affiliations

  1. Embrapa Trigo, Rodovia BR 285 km 294, Passo Fundo, RS, CEP 99001-970, Brazil

    Jorge Fernando Pereira, Jorge González Aguilera, Luciano Consoli & José Pereira da Silva Júnior

  2. Universidade de Passo Fundo, Rodovia BR 285, Passo Fundo, RS, CEP 99052-900, Brazil

    Diliane Barichello & Jéssica Rosset Ferreira

  3. Embrapa Clima Temperado, Rodovia BR 392 km 78, Pelotas, RS, CEP 96001-970, Brazil

    Sandro Bonow

  4. Embrapa Uva e Vinho, Rua Livramento 515, Bento Gonçalves, RS, CEP 95700-000, Brazil

    Adeliano Cargnin

Authors
  1. Jorge Fernando Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Diliane Barichello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jéssica Rosset Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jorge González Aguilera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Luciano Consoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. José Pereira da Silva Júnior
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sandro Bonow
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adeliano Cargnin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jorge Fernando Pereira.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pereira, J.F., Barichello, D., Ferreira, J.R. et al. TaALMT1 and TaMATE1B allelic variability in a collection of Brazilian wheat and its association with root growth on acidic soil. Mol Breeding 35, 169 (2015). https://doi.org/10.1007/s11032-015-0363-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-015-0363-9

Keywords

Search

Navigation