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An efficient marker-assisted backcrossing strategy for enhancing barley (Hordeum vulgare L.) production under acidity and aluminium toxicity

Abstract

To feed the predicted extra two billion people by 2050, crop production must increase on existing cultivated land at a rate that challenges our current capability. Acid soils and aluminium (Al3+) toxicity restrict productivity worldwide but also offer the greatest opportunity for increases in global food production. Our understanding of the physiology, genetic control and the identification of genomic regions underlying Al resistance in important staple crops has increased greatly over the past 20 years, enabling the application of molecular breeding. In this study, we report the application of an efficient marker-assisted backcrossing (MAB) strategy for the introgression of the HvAACT1 gene which confers Al resistance in barley (Hordeum vulgare L.). We conducted foreground and background selection using microsatellite (SSR) markers linked to HvAACT1 and SSR-based linkage maps, along with embryo rescue and a cost-effective DNA preparation method shortening the breeding cycle to ~18 months. The MAB strategy enabled the development of homozygous (BC3F2) Al-resistant lines with the smallest introgressed region and 98.7 % of the recurrent parent genome. The Al-resistant line yielded significantly more seeds (121 %) than its isogenic line in soil-based assays containing 12 % of Al saturation. This MAB strategy could be extended to other staple crops with similar molecular toolboxes, expanding their cultivation onto acid soils, and contributing to greater yield stability and food security, particularly in developing countries.

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References

  • Baik BK, Ullrich SE (2008) Barley for food: characteristics, improvement, and renewed interest. J Cereal Sci 48:233–242

    Article  CAS  Google Scholar 

  • Bernardo R, Yu J (2007) Prospects for genomewide selection for quantitative traits in maize. Crop Sci 47:1082–1090

    Article  Google Scholar 

  • Bertrand C, Collar Y, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Phil Trans R Soc B 363:557–572

    Article  Google Scholar 

  • Blamey FPC, Robinson NJ, Asher CJ (1992) Interspecific differences in aluminium tolerance in relation to root cation-exchange capacity. Plant Soil 146:77–82

    Article  CAS  Google Scholar 

  • Ceretta CA (1988) Aluminium tolerance in maize cultivars. Documentos Centro Nacional de Pesquisa de Milho e Sorgo 6:492–498

    Google Scholar 

  • Chu Y, Wu CL, Holbrook CC, Tillman BL, Person G, Ozias-Akins P (2011) Marker-assisted selection to pyramid nematode resistance and the high oleic trait in peanut. Plant Genome 4:110–117

    Article  CAS  Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szucs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genom 10:582

    Article  Google Scholar 

  • Delhaize E, Ryan P, Randall P (1993) Aluminum tolerance in wheat (Triticum aestivum L.).II aluminium-stimulated excretion of malic acid from root apices. Plant Physiol 103:695–702

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • FAO (2011) The state of the world’s land and water resources for food and agriculture (SOLAW)—managing systems at risk. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • FAOSTAT (2009) Production of crops. Available at http://faostat.fao.org/site/567/default.aspx (verified 20 Dic 2011). FAO, Rome

  • Ferreira JJ, Campa A, Perez-Vega E, Rodriguez-Suarez C, Giraldez R (2012) Introgression and pyramiding into common bean market class fabada of genes conferring resistance to anthracnose and potyvirus. Theor Appl Genet 124:777–788

    PubMed  Article  Google Scholar 

  • Fontecha G, Silva-Navas J, Benito C, Mestres MA, Espino FJ, Hernandez-Riquer MV, Gallego FJ (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 114:249–260

    PubMed  Article  CAS  Google Scholar 

  • Frisch M (2005) Optimum design of marker-assisted backcross programs. In: Loerz H, Wenzel G (eds) Biotechnology in agriculture and forestry, vol 55. Springer, Berlin, pp 319–334

    Google Scholar 

  • Frisch M, Bohn M, Melchinger A (1999) Comparison of selection strategies for marker-assisted backcrossing of a gene. Crop Sci 39:1295–1301

    Article  Google Scholar 

  • Fujii M, Yokosho K, Yamaji N, Saisho D, Yamane M, Takahashi H, Sato K, Nakazono M, Ma JF (2012) Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun 3:713. doi:10.1038/ncomms1726

    PubMed  Article  Google Scholar 

  • 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 Physiol 48:1081–1091

    PubMed  Article  CAS  Google Scholar 

  • Gallardo F, Borie F, Alvear M, von Baer E (1999) Evaluation of aluminum tolerance of three barley cultivars by two short-term screening methods and field experiments. Soil Sci Plant Nutr 3:713–719

    Article  Google Scholar 

  • Gallego FJ, Benito C (1997) Genetic control of aluminium tolerance in rye (Secale cereale L.). Theor Appl Genet 95:393–399

    Article  CAS  Google Scholar 

  • Gupta PK, Langridge P, Mir RR (2010) Marker-assisted wheat breeding: present status and future possibilities. Mol Breed 26:145–161

    Article  Google Scholar 

  • Heffner EL, Sorrells ME, Jannink JL (2009) Genomic selection for crop improvement. Crop Sci 49:1–12

    Article  CAS  Google Scholar 

  • Hoekenga OA, Maron LG, Pineros MA, Cancado GMA, Shaff J, Yuriko K, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Hiroyuki K, Kochian LV (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 103:9738–9743

    PubMed  Article  CAS  Google Scholar 

  • Horsley RD, Schwarz PB, Hammond JJ (1995) Genetic diversity in malt quality of North American six-rowed spring barley germplasm. Crop Sci 35:113–118

    Article  Google Scholar 

  • Jefferies SP, King BJ, Barr R, Warner P, Logue SJ, Langridge P (2003) Marker-assisted backcross introgression of the Yd2 gene conferring resistance to barley yellow dwarf virus in barley. Plant Breed 122:52–56

    Article  CAS  Google Scholar 

  • Kosambi DD (1944) The estimation of the map distance from recombination values. Ann Eugen 12:172–175

    Google Scholar 

  • Li JZ, Sjakste TG, Röder MS, Ganal MW (2003) Development and genetic mapping of 127 new microsatellite markers in barley. Theor Appl Genet 107:1021–1027

    PubMed  Article  CAS  Google Scholar 

  • Ligaba A, Shen H, Shibata K, Yamamoto Y, Tanakamaru S, Matsumoto H (2004) The role of phosphorus in aluminum-induced citrate and malate exudation in rape (Brassica napus L.). Physiol Plant 120:575–584

    PubMed  Article  CAS  Google Scholar 

  • 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 aluminum resistance of plant cells. Plant Physiol 142:1294–1303

    PubMed  Article  CAS  Google Scholar 

  • Liu Z, Biyashev R, Saghai Marrof M (1996) Development of simple sequence repeat DNA markers and their integration into a barley linkage map. Theor Appl Genet 93:869–876

    Article  CAS  Google Scholar 

  • Liu J, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57:389–399

    PubMed  Article  CAS  Google Scholar 

  • Ma JF, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acids. Trends Plant Sci 6:273–278

    PubMed  Article  CAS  Google Scholar 

  • Ma JF, Nagao S, Sato K, Ito H, Furukawa J, Takeda K (2004) Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. J Exp Bot 55:1335–1341

    PubMed  Article  CAS  Google Scholar 

  • Magalhaes JV, Liu J, Guimaraes CT, Lana UGP, Alves VMC, Wang YH, Schaffert RE, Hoekenga OA, Pineros 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

    PubMed  Article  CAS  Google Scholar 

  • Michelmore R, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832

    PubMed  Article  CAS  Google Scholar 

  • Minella E, Sorrells ME (1992) Aluminum tolerance in barley: genetic relationships among genotypes of diverse origin. Crop Sci 32:593–598

    Article  CAS  Google Scholar 

  • Moose SP, Mumm RH (2008) Molecular plant breeding as the foundation for 21st century crop improvement. Plant Physiol 147:969–977

    PubMed  Article  CAS  Google Scholar 

  • Newton AC, Flavell AJ, George TS, Leat P, Mullholland B, Ramsay L, Revoredo-Giha C, Russell J, Steffenson BJ, Swanston JS, Thomas WTB, Waugh R, White PJ, Bingham IJ (2011) Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security. Food Sec 3:141–178

    Article  Google Scholar 

  • Nguyen VT, Burrow MD, Nguyen HT, Le BT, Le TD, Paterson AH (2001) Molecular mapping of genes conferring aluminium tolerance in rice (Oryza sativa L.). Theor Appl Genet 102:1002–1010

    Article  CAS  Google Scholar 

  • Pandey S, Ceballos H, Magnavaca R, Bahia Filho AFC, Duque-Vargas J, Vinasco LE (1994) Genetics of tolerance to soil acidity in tropical maize. Crop Sci 34:1511–1514

    Article  Google Scholar 

  • Peñaloza E, Martinez J, Montenegro A, Corcuera L (2004) Response of two lupin species to phytotoxic aluminum. Chil J Agric Res 64:127–138

    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

    PubMed  Article  CAS  Google Scholar 

  • Polle E, Konzak CF, Kittrick JA (1978) Visual detection of aluminum tolerance levels in wheat by hematoxylin staining of seedling roots. Crop Sci 18:823–827

    Article  CAS  Google Scholar 

  • Prigge V, Melchinger AE, Dhillon BS, Frisch M (2009) Efficiency gain of marker-assisted backcrossing by sequentially increasing marker densities over generations. Theor Appl Genet 119:23–32

    PubMed  Article  CAS  Google Scholar 

  • Raman H, Gustafson P (2011) Molecular breeding of cereals for aluminum resistance. In: Costa de Oliveira A, Varshney RK (eds) Roots genomics. Springer, Berlin, pp 251–287

    Chapter  Google Scholar 

  • Raman H, Moroni S, Sato K, Read J, Scott J (2002) Identification of AFLP and microsatellite markers linked with an aluminium tolerance gene in barley (Hordeum vulgare L.). Theor Appl Genet 105:458–464

    PubMed  Article  CAS  Google Scholar 

  • Raman H, Karakousis A, Moroni JS, Raman R, Read BJ, Garvin DF, Kochian LV, Sorrells ME (2003) Development and allele diversity of microsatellite markers linked to the aluminium tolerance gene Alp in barley. Aust J Agric Res 54:1315–1321

    Article  CAS  Google Scholar 

  • Raman H, Zhang K, Cakir M, Appels R, Garvin D, Maron L, Kochian L, Moroni J, Raman R, Imtiaz M, Drake-Brockman F, Waters I, Martin P, Sasaki T, Yamamoto Y, Matsumoto H, Hebb D, Delhaize E, Ryan P (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48:781–791

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Ramsay L, Macaulay M, Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards K, Tuvesson S, Morgante M, Massari A, Maestri E, Marmiroli N, Sjakste T, Ganal M, Powell W, Waugh R (2000) A simple sequence repeat-based linkage map of barley. Genetics 156:1997–2005

    PubMed  CAS  Google Scholar 

  • Reid DA, Jones GD, Armiger WH, Foy CD, Koch EJ, Starling TM (1969) Differential aluminum tolerance of winter barley varieties and selections in associated greenhouse and field experiments. Agron J 61:218–222

    Article  Google Scholar 

  • Salgotra RK, Gupta BB, Millwood RJ, Balasubramaniam M, Stewart CN Jr (2012) Introgression of bacterial leaf blight resistance and aroma genes using functional marker-assisted selection in rice (Oryza sativa L.). Euphytica 187:313–323

    Article  CAS  Google Scholar 

  • SAS Institute (2001) SAS/STAT users guide, ver. 8.02. SAS Institute, Cary

    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

    PubMed  Article  CAS  Google Scholar 

  • Schmalenbach I, March TJ, Bringezu T, Waugh R, Pillen K (2011) High-resolution genotyping of wild barley introgression lines and fine-mapping of the threshability locus thresh-1 using the Illumina GoldenGate assay. G3 (Bethesda) 1:187–196

  • Schmierer DA, Kandemir N, Kudrna DA, Jones BL, Ullrich SE, Kleinhofs A (2004) Molecular marker-assisted selection for enhanced yield in malting barley. Mol Breed 14:463–473

    Article  CAS  Google Scholar 

  • Servin B, Hospital F (2002) Optimal positioning of markers to control genetic background in marker assisted backcrossing. J Hered 93:214–217

    PubMed  Article  CAS  Google Scholar 

  • Silva JA, Carvalho FI, Coimbra JL, Benin G, Oliveira AC, Vieira EA, Finatto T, Bertan I, Silva GO, Garcia SM (2006) Tolerance to aluminium toxicity in oat (Avena sativa L.) in hydroponic cultivation, Revista Brasileira de Agrociencia. Faculdade de Agronomia Eliseu Maciel, Universidade Federal de Pelotas, Pelotas, Brazil 2:265–271

  • Silva-Navas J, Benito C, Téllez-Robledo B, Abd El-Moneim D, Gallego FJ (2012) The ScAACT1 gene at the Q alt5 locus as a candidate for increased aluminum tolerance in rye (Secale cereale L.). Mol Breed 30:845–856

    Article  CAS  Google Scholar 

  • Stam P (2003) Marker-assisted introgression: speed at any cost? Eucarpia leafy vegetables. (http://www.leafyvegetables.nl)

  • Tang Y, Sorrells M, Kochian L, Garvin D (2000) Identification of RFLP markers linked to the barley aluminum tolerance gene Alp. Crop Sci 40:778–782

    Article  CAS  Google Scholar 

  • Tanksley S (1998) Marker-assisted selection: new tools and strategies. Trend Plant Sci 3:236–239

    Article  Google Scholar 

  • Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822

    PubMed  Article  CAS  Google Scholar 

  • van Berloo R (2008) GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered 99:232–236

    PubMed  Article  Google Scholar 

  • van Berloo R, Stam P (1999) Comparison between marker-assisted selection and phenotypical selection in a set of Arabidopsis thaliana recombinant inbred lines. Theor Appl Genet 98:113–118

    Article  Google Scholar 

  • Van Ooijen JW (2006) JoinMap® 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • Varshney RK, Marcel TC, Ramsay L, Russell J, Röder MS, Stein N, Waugh R, Langridge P, Niks RE, Graner A (2007) A high density barley microsatellite consensus map with 775 SSR loci. Theor Appl Genet 114:1091–1103

    PubMed  Article  CAS  Google Scholar 

  • Wang H, Qi M, Cutler AJ (1993) A simple method of preparing plant samples for PCR. Nucleic Acids Res 21:4153–4154

    PubMed  Article  CAS  Google Scholar 

  • 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.). Theor Appl Genet 115:265–276

    PubMed  Article  CAS  Google Scholar 

  • Wood S, Sebastian K, Scherr SJ (2000) Pilot analysis of global ecosystems: agroecosystems. Rosen, Washington

    Google Scholar 

  • Zhao X, Tan G, Xing Y, Wie L, Chao Q, Zuo W, Lübberstedt T, Xu M (2012) Marker-assisted introgression of qHSR1 to improve maize resistance to head smut. Mol Breed. doi:10.1007/s11032-011-9694-3

    Google Scholar 

  • Zheng SJ (2010) Crop production on acidic soils: overcoming aluminium toxicity and phosphorus deficiency. Ann Bot 106:183–184

    PubMed  Article  Google Scholar 

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Acknowledgments

The authors acknowledge the financial support from CGNA and CONICYT Regional/GORE Araucanía/CGNA/R10C100, and INIA for providing infrastructure. The authors are grateful to Dr. Patrick M. Hayes and Rudy Rivas for supplying Dayton and Andes-171-96 seeds, respectively. Dr. Genyi Li is also gratefully acknowledged for his helpful suggestions in preparing this manuscript.

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Correspondence to Haroldo Salvo-Garrido.

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Soto-Cerda, B.J., Peñaloza, E.H., Montenegro, A.B. et al. An efficient marker-assisted backcrossing strategy for enhancing barley (Hordeum vulgare L.) production under acidity and aluminium toxicity. Mol Breeding 31, 855–866 (2013). https://doi.org/10.1007/s11032-013-9839-7

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Keywords

  • Marker-assisted backcrossing
  • Barley
  • Acid soil
  • Aluminium toxicity
  • Food security