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Genetic diversity for aluminum tolerance in sorghum

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Abstract

Genetic variation for aluminum (Al) tolerance in plants has allowed the development of cultivars that are high yielding on acidic, Al toxic soils. However, knowledge of intraspecific variation for Al tolerance control is needed in order to assess the potential for further Al tolerance improvement. Here we focused on the major sorghum Al tolerance gene, Alt SB , from the highly Al tolerant standard SC283 to investigate the range of genetic diversity for Al tolerance control in sorghum accessions from diverse origins. Two tightly linked STS markers flanking Alt SB were used to study the role of this locus in the segregation for Al tolerance in mapping populations derived from different sources of Al tolerance crossed with a common Al sensitive tester, BR012, as well as to isolate the allelic effects of Alt SB in near-isogenic lines. The results indicated the existence not only of multiple alleles at the Alt SB locus, which conditioned a wide range of tolerance levels, but also of novel sorghum Al tolerance genes. Transgressive segregation was observed in a highly Al tolerant breeding line, indicating that potential exists to exploit the additive or codominant effects of distinct Al tolerance loci. A global, SSR-based, genetic diversity analysis using a broader sorghum set revealed the presence of both multiple Alt SB alleles and different Al tolerance genes within highly related accessions. This suggests that efforts toward broadening the genetic basis for Al tolerance in sorghum may benefit from a detailed analysis of Al tolerance gene diversity within subgroups across a target population.

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References

  • Agrama HA, Tuinstra MR (2003) Phylogenetic diversity and relationships among sorghum accessions using SSRs and RAPDs. Afr J Biotechnol 10:334–340

    Google Scholar 

  • Aldrich PR, Doebley J (1992) Restriction fragment variation in the nuclear and chloroplast genomes of cultivated and wild Sorghum bicolor. Theor Appl Genet 85:293–302

    Google Scholar 

  • Aniol A (1990) Genetics of tolerance to aluminum in wheat (Triticum aestivum L. Thell). Plant Soil 123:223–227

    Article  CAS  Google Scholar 

  • Aniol A, Gustafson JP (1984) Chromosome location of genes controlling aluminum tolerance in wheat, rye and triticale. Can J Genet Cytol 26:701–705

    Google Scholar 

  • Berzonsky W (1992) The genomic inheritance of aluminum tolerance in ‘Atlas 66’ wheat. Genome 35:689–693

    Google Scholar 

  • Borgonovi RA, Schaffert RE, Pitta GVE, Magnavaca R, Alves VMC (1987) Aluminum tolerance in sorghum. In: Gabelman HW, Loughman BC (eds) Genetic aspects of plant mineral nutrition. Martinus Nijhoff Publishers, Dordrecht, pp 213–221

    Google Scholar 

  • Borrero JC, Pandey S, Ceballos H, Magnavaca R, Bahia Filho AFC (1995) Genetic variances for tolerance to soil acidity in a tropical maize population. Maydica 40:283–288

    Google Scholar 

  • Camargo CEO (1981) Melhoramento do trigo. I. Hereditariedade da tolerância à toxicidade do alumínio. Bragantia 40:33–45

    Google Scholar 

  • Cui YX, Xu GW, Magill CW, Schertz KF, Hart GE (1995) RFLP-based assay of Sorghum bicolor (L) Moench genetic diversity. Theor Appl Genet 90:787–796

    Article  CAS  Google Scholar 

  • Dean RE, Dahlberg JA, Hopkins MS, Mitchell SE, Kresovich S (1999) Genetic redundancy and diversity among ‘Orange’ accessions in the U.S. national sorghum collection as assessed with simple sequence repeat (SSR) markers. Crop Sci 39:1215–1221

    Article  Google Scholar 

  • Delhaize E, Craig S, Beaton CD, Bennet RJ, Jagadish VC, Randall PJ (1993a) Aluminum tolerance in wheat (Triticum aestivum L.) I. Uptake and distribution of aluminum in root apices. Plant Physiol 103:685–693

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Deu M, Gonzalez-de-Leon D, Glaszmann J-C, Degremont I, Chantereau J, Lanaud C, Hamon P (1994) RFLP diversity in cultivated sorghum in relation to racial differentiation. Theor Appl Genet 88:838–844

    Article  CAS  Google Scholar 

  • Deu M, Rattunde F, Chantereau J (2006) A global view of genetic diversity in cultivated sorghums using a core collection. Genome 49:168–180

    PubMed  CAS  Google Scholar 

  • Devos KM, Atkinson MD, Chinoy CN, Francis HA, Harcourt RL, Koebner RMD, Liu CJ, Masojć P, Xie DX, Gale MD (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85:673–680

    CAS  Google Scholar 

  • Dice LR (1945) Measures of the amount of ecologic association between species. Ecology 26:297–302

    Article  Google Scholar 

  • Foy CD, Duncan RR, Waskom RM, Miller DR (1993) Tolerance of sorghum genotypes to an acid, aluminum toxic tatum subsoil. J Plant Nutr 16:97–127

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gallego FJ, Calles B, Benito C (1998a) Molecular markers linked to the aluminum tolerance gene Alt1 in rye (Secale cereale L.). Theor Appl Genet 97:1104–1109

    Article  CAS  Google Scholar 

  • Gallego FJ, López-Solanilla E, Figueiras AM, Benito C (1998b) Chromosomal location of PCR fragments as a source of DNA markers linked to aluminum tolerance genes in rye. Theor Appl Genet 96:426–434

    Article  CAS  Google Scholar 

  • Garvin DF, BF Carver (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 

  • Gaut BS (2002) Evolutionary dynamics of grass genomes. New Phytol 154:15–28

    Article  CAS  Google Scholar 

  • Harlan JR, de Wet JMJ (1972) A simplified classification of cultivated sorghum. Crop Sci 12:172–176

    Article  Google Scholar 

  • Hoekenga OA, Vision TJ, Shaff JE, Monforte AJ, Lee GP, Howell SH, Kochian LV (2003) Identification and characterization of aluminum tolerance loci in Arabidopsis (Landsberg erecta × Columbia) by quantitative trait locus mapping. A physiologically simple but genetically complex trait. Plant Physiol 132:936–948

    Article  PubMed  CAS  Google Scholar 

  • Hoekenga OA, Maron LG, Piñeros MA, Cançado 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. Proc Natl Acad Sci USA 103:9738–9743

    Article  PubMed  CAS  Google Scholar 

  • Johnson JP, Carver BF, Baligar VC (1997) Expression of aluminum tolerance transferred from Atlas 66 to Hard Winter Wheat. Crop Sci 37:103–108

    Article  CAS  Google Scholar 

  • Kerridge PC, Kronstad WE (1968) Evidence of genetic resistance to aluminum toxicity in wheat (Triticum aestivum Vill., Host). Agron J 60:710–711

    Article  Google Scholar 

  • Khatiwada SP, Senadhira D, Carpena AL, Zeigler RS, Fernandez PG (1996) Variability and genetics of tolerance for aluminum toxicity in rice (Oryza sativa L). Theor Appl Genet 93:738–744

    Article  CAS  Google Scholar 

  • Kobayashi Y, Koyama H (2002) QTL analysis of Al tolerance in recombinant inbred lines of Arabidopsis thaliana. Plant Cell Physiol 43:1526–1533

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi Y, Furuta Y, Ohno T, Hara T, Koyama H (2005) Quantitative trait loci controlling aluminium tolerance in two accessions of Arabidopsis thaliana (Landsberg erecta and Cape Verde Islands). Plant Cell Environ 28:1516–1524

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Luo M-C, Dvorak J (1996) Molecular mapping of an aluminum tolerance locus on chromosome 4D of Chinese Spring wheat. Euphytica 91:31–35

    CAS  Google Scholar 

  • Ma H-X, Bai G-H, Carver BF, Zhou L-L (2005) Molecular mapping of a quantitative trait locus for aluminum tolerance in wheat cultivar Atlas 66. Theor Appl Genet 112:51–57

    Article  PubMed  CAS  Google Scholar 

  • Ma JF, Taketa S, Yang ZM (2000) Aluminum tolerance genes on the short arm of chromosome 3R are linked to organic acid release in Triticale. Plant Physiol 122:687–694

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Magalhaes JV (2006) Aluminum tolerance genes are conserved between monocots and dicots. Proc Natl Acad Sci USA 103:9749–9750

    Article  PubMed  CAS  Google Scholar 

  • Magalhaes JV, Garvin DF, Wang Y, Sorrells ME, Klein PE, Schaffert RE, Li L, Kochian LV (2004) Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the Poaceae. Genetics 167:1905–1914

    Article  PubMed  CAS  Google Scholar 

  • Magnavaca R, Gardner CO, Clark RB (1987) Inheritance of aluminum tolerance in maize. In: Gabelman HW, Loughman BC (eds) Genetic aspects of plant mineral nutrition. Martinus Nijhoff Publishers, Dordrecht, pp 201–121

    Google Scholar 

  • Mao C-z, Yang L, Zheng B-s, Wu Y-r, Liu F-y, Yi Ke-k, Wu P (2004) Comparative mapping of QTLs for Al tolerance in rice and identification of positional Al-induced genes. J Zhejiang Univ Sci 5:634–643

    Article  PubMed  Google Scholar 

  • Matos M, Camacho MV, Pérez-Flores V, Pernaute B, Pinto-Carnide O, Benito C (2005) A new aluminum tolerance gene located on rye chromosome arm 7RS. Theor Appl Genet 111:360–369

    Article  PubMed  CAS  Google Scholar 

  • Menz MA, Klein RR, Unruh NC, Rooney WL, Klein PE, Mullet JE (2004) Genetic diversity of public inbreds of sorghum determined by mapped AFLP and SSR markers. Crop Sci 44:1236–1244

    Article  CAS  Google Scholar 

  • Miftahudin, Chikmawati T, Ross K, Scoles GJ, Gustafson JP (2005) Targeting the aluminum tolerance gene Alt3 region in rye, using rice/rye micro-colinearity. Theor Appl Genet 110:906–913

    Article  PubMed  CAS  Google Scholar 

  • Miftahudin, Scoles GJ, Gustafson JP (2002) AFLP markers tightly linked to the aluminum-tolerance gene Alt3 in rye (Secale cereale L.). Theor Appl Genet 104:626–631

    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 

  • Nei M, Li WH (1979) Mathematical models for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    Article  PubMed  CAS  Google Scholar 

  • Nguyen BD, Brar DS, Bui BC, Nguyen TV, Pham LN, Nguyen HT (2003) Identification and mapping of the QTL for aluminum tolerance introgressed from new source, Oryza rufipogon Griff., into indica rice (Oryza sativa L.). Theor Appl Genet 106:583–593

    PubMed  CAS  Google Scholar 

  • Nguyen VT, Nguyen BD, Sarkarung S, Martinez C, Paterson AH, Nguyen HT (2002) Mapping of genes controlling aluminum tolerance in rice: comparison of different genetic backgrounds. Mol Genet Genomics 267:772–780

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ninamango-Cárdenas FE, Guimarães CT, Martins PR, Parentoni SN, Carneiro NP, Lopes MA, Moro JR, Paiva E (2003) Mapping QTLs for aluminum tolerance in maize. Euphytica 130:223–232

    Article  Google Scholar 

  • de Oliveira AC, Richter T, Bennetzen JL (1996) Regional and racial specificities in sorghum germplasm assessed with DNA markers. Genome 39:579–587

    PubMed  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 

  • Papernik LA, Bethea AS, Singleton TE, Magalhaes JV, Garvin DF, Kochian LV (2001) Physiological basis of reduced Al tolerance in ditelosomic lines of Chinese Spring wheat. Planta 212:829–834

    Article  PubMed  CAS  Google Scholar 

  • Parker DR, Norvell WA, Chaney RL (1995) GEOCHEM-PC: a chemical speciation program for IBM and compatible computers. In: Loeppert RH, Schwab AP, Goldberg S (eds) Chemical equilibrium and reaction models. Soil Science Society of America, Madison, pp 253–269

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Rhue RD, Grogan CO, Stockmeyer EW, Everett HL (1978) Genetic control of aluminum tolerance in corn. Crop Sci 18:1063–1067

    Article  Google Scholar 

  • Riede CR, Anderson JA (1996) Linkage of RFLP markers to an aluminum tolerance gene in wheat. Crop Sci 36:905–909

    Article  Google Scholar 

  • Saghai-Maroof MA, Soliman KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer length polymorphism in barley: Mendelian inheritance, chromosomal location and population dynamics. Proc Natl Acad Sci USA 81:8014–8018

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Scott AJ, Knott M (1974) A cluster analysis method for grouping means in the analysis of variance. Biometrics 30:507–512

    Article  Google Scholar 

  • Sibov ST, Gaspar M, Silva MJ, Ottoboni LMM, Arruda P, Souza AP (1999) Two genes control aluminum tolerance in maize: genetic and molecular mapping analyses. Genome 42:475–482

    Article  CAS  Google Scholar 

  • Smith JSC, Kresovich S, Hopkins MS, Mitchell SE, Dean RE, Woodman WL, Lee M, Porter K (2000) Genetic diversity among elite sorghum inbred lines assessed with simple sequence repeats. Crop Sci 40:226–232

    Article  CAS  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy. Freeman, New York

    Google Scholar 

  • Sun Y, Skinner DZ, Liang GH, Hulbert SH (1994) Phylogenetic analysis of Sorghum and related taxa using internal transcribed spacers of nuclear ribosomal DNA. Theor Appl Genet 89:26–32

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tang Y, Garvin DF, Kochian LV, Sorrells ME, Carver BF (2002) Physiological genetics of aluminum tolerance in the wheat cultivar Atlas 66. Crop Sci 42:1541–1546

    Article  Google Scholar 

  • Tao Y, Manners JM, Ludlow MM, Henzell RG (1993) DNA polymorphisms in grain sorghum (Sorghum bicolor (L) Moench). Theor Appl Genet 86:679–688

    Article  CAS  Google Scholar 

  • Tukey JW (1953) The problem of multiple comparisons. Mimeographs Princeton University, Princeton

    Google Scholar 

  • Wight CP, Kibite S, Tinker NA, Molnar SJ (2006) Identification of molecular markers for aluminium tolerance in diploid oat through comparative mapping and QTL analysis. Theor Appl Genet 112:222–231

    Article  PubMed  CAS  Google Scholar 

  • Wu P, Liao CY, Hu B, Yi KK, Jin WZ, Ni JJ, He C (2000) QTLs and epistasis for aluminum tolerance in rice (Oryza sativa L.) at different seedling stages. Theor Appl Genet 100:1295–1303

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Dr. Fredolino G dos Santos and Dr. José Avelino S Rodrigues for useful suggestions on germplasm selection. We also acknowledge the financial support from The Generation Challenge Programme, the McKnight Foundation Collaborative Crop Research Program, the International Foundation for Science (IFS), and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). F.F. Caniato gratefully acknowledges the Fundação Coordenação de Pessoal de Nível Superior (CAPES) for providing financial support for her M.S. program.

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Authors and Affiliations

  1. Embrapa Maize and Sorghum, Rod. MG 424, Km 65, 35701-970, Sete Lagoas, MG, Brazil

    F. F. Caniato, C. T. Guimarães, R. E. Schaffert, V. M. C. Alves & J. V. Magalhaes

  2. U.S. Plant Soil and Nutrition Laboratory, USDA-ARS, Cornell University, Ithaca, NY, 14853, USA

    L. V. Kochian

  3. Federal University of Viçosa, Viçosa, MG, 36570-000, Brazil

    A. Borém

  4. Institute for Plant Genomics and Biotechnology and Department of Horticulture, Texas A&M University, College Station, TX, 77843, USA

    P. E. Klein

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  1. F. F. Caniato
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  2. C. T. Guimarães
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  3. R. E. Schaffert
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  4. V. M. C. Alves
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  5. L. V. Kochian
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  6. A. Borém
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  7. P. E. Klein
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  8. J. V. Magalhaes
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Correspondence to J. V. Magalhaes.

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Communicated by I. Romagosa.

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Table S1: Sorghum accessions evaluated in this study (DOC 106 KB)

Table S2: Standard errors of the means for the data presented in Table 1 (DOC 61 KB)

122_2006_485_MOESM3_ESM.doc

Table S3: Root growth in response to increasing Al3+ activities for the near-isogenic lines (NILs) BR012, 3DX/012, 225/012, and donors 3DX and CMS225. Percent Relative Net Root Growth (RNRG) values are means of three replications (seven plants per replication). RNRG means followed by the same letters within each of the four Al activities are significantly different by the Tukey test (P < 0.05). CV coefficient of variation (DOC 36 KB)

122_2006_485_MOESM4_ESM.doc

Table S4: Percent Relative Net Root Growth (RNRG) means and standard errors of the means for sorghum accessions subjected to {27} µM Al3+, {37} µM Al3+ and {58} µM Al3+ in nutrient solution. Values are the means of three replications for the Al activity of {27} µM Al3+ and two replications for the other Al activities. Seven plants per replication were used for all Al treatments. Accessions whose RNRG means are followed by the same lower-case letters within each of the three Al activities constitute homogeneous RNRG groups by the Scott–Knott test (P < 0.05) (DOC 167 KB)

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Caniato, F.F., Guimarães, C.T., Schaffert, R.E. et al. Genetic diversity for aluminum tolerance in sorghum. Theor Appl Genet 114, 863–876 (2007). https://doi.org/10.1007/s00122-006-0485-x

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