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Chromosome-anchored QTL conferring aluminum tolerance in hexaploid oat

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Abstract

Aluminum (Al) toxicity is a major constraint on crop production in acid soils around the world. Hexaploid oat (Avena sativa L.) possesses significant Al tolerance making it a good candidate for production in these environments. Genetic improvement for Al tolerance in oat has traditionally been achieved through conventional plant breeding and could be enhanced by marker-assisted selection. The objectives of this study were to develop a chromosome-anchored genetic map for an oat recombinant inbred population and to identify SNP markers linked to quantitative trait loci (QTL) affecting root growth response to Al. Three QTL on chromosomes 7C-17A, 13A, and 19A conferring Al tolerance were identified using primary root regrowth of recombinant inbred lines derived from the cross between UFRGS 17 (Al tolerant) and UFRGS 930598-6 (Al sensitive). Localization of each QTL onto the sequenced rice genome revealed the genetic region on chromosome 13A might be associated with a putative malate transporter locus (LOC_Os06g15779). Studies of root apex tissue indicated that exudation of malate was increased in the Al-tolerant parent UFRGS17 and not in the sensitive parent. Based on these data, the malate transporter might be a candidate gene responsible for one of the Al tolerance QTL identified in this study.

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References

  • Archambault DJ, Zhang GC, Taylor GJ (1997) Spatial variation in the kinetics of aluminum (Al) uptake in roots of wheat (Triticum aestivum L.) exhibiting differential resistance to Al—evidence for metabolism-dependent exclusion of Al. J Plant Physiol 151:668–674

    Article  CAS  Google Scholar 

  • Arumuganathan K, Earle ED (1991) Nuclear DNA content of some important plant species. Plant Mol Biol Rep 9:208–219

    Article  CAS  Google Scholar 

  • Basu U, Good AG, Taing-Aung T, Slaski J, Basu A, Briggs KG, Taylor GJ (1999) A 23 kDa protein root exudates polypeptide co-segregates with aluminium resistance in Triticum aestivum. Physiol Plant 106:53–61

    Article  CAS  Google Scholar 

  • Bian M et al (2013) Development of gene-specific markers for acid soil/aluminium tolerance in barley (Hordeum vulgare L.). Mol Breed 32:155–164. doi:10.1007/s11032-013-9859-3

    Article  CAS  Google Scholar 

  • Bianchi-Hall CM et al (2000) Aluminum tolerance associated with quantitative trait loci derived from soybean PI 416937 in hydroponics. Crop Sci 40:538–545. doi:10.2135/cropsci2000.402538x

    Article  CAS  Google Scholar 

  • Bryan GJ, Stephenson P, Collins A, Kirby J, Smith JB, Gale MD (1999) Low levels of DNA sequence variation among adapted genotypes of hexaploid wheat. Theor Appl Genet 99:192–198. doi:10.1007/s001220051224

  • Castilhos G, Farias JG, de Bernardi Schneider A, de Oliveira PH, Nicoloso FT, Chitolina Schetinger MR, Delatorre CA (2011) Aluminum-stress response in oat genotypes with monogenic tolerance. Environ Exp Bot 74:114–121. doi:10.1016/j.envexpbot.2011.05.007

  • Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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. doi:10.1534/genetics.107.083451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Consortium TRCS (2005) Sequence, annotation, and analysis of synteny between rice chromosome 3 and diverged grass species. Genome Res 15:1284–1291. doi:10.1101/gr.3869505

    Article  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. doi:10.1016/j.febslet.2007.03.057

    Article  CAS  PubMed  Google Scholar 

  • Foy CD, Chaney RL, White MC (1978) The physiology of metal toxicity in plants. Annu Rev Plant Physiol 29:511–566. doi:10.1146/annurev.pp.29.060178.002455

    Article  CAS  Google Scholar 

  • Fujii M et al (2012) Acquisition of aluminium tolerance by modification of a single gene in barley. Nat Commun 3:713. http://www.nature.com/ncomms/journal/v3/n3/suppinfo/ncomms1726_S1.html

  • Genome sequencing and analysis of the model grass Brachypodium distachyon (2010). Nature 463:763–768. http://www.nature.com/nature/journal/v463/n7282/suppinfo/nature08747_S1.html

  • Gustafsson JP (2010) Visual MINTEQ ver. 3.0

  • Hervé CB, Calai FA, Nava IC, Delatorre CA (2013) Tolerância ao alumínio tóxico em germoplasma brasileiro elite de aveia. Ciência Rural 43:1364–1370

    Article  Google Scholar 

  • Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21:655–667. doi:10.1105/tpc.108.064543

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huan-Xin J, Ning T, Jin-Gui Z, Yan L, Li-Song C (2009) Phosphorus alleviates aluminum-induced inhibition of growth and photosynthesis in Citrus grandis seedlings. Physiol Plant 137:298–311

    Article  Google Scholar 

  • Jellen E, Beard J (2000) Geographical distribution of a chromosome 7C and 17 intergenomic translocation in cultivated oat. Crop Sci 40:256–263

    Article  Google Scholar 

  • Jellen EN, Gill BS, Cox TS (1994) Genomic in situ hybridization differentiates between A/D- and C-genome chromatin and detects intergenomic translocations in polyploid oat species (genus Avena). Genome 37:613–618. doi:10.1139/g94-087

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y et al (2013) Molecular and physiological analysis of Al3+ and H+ rhizotoxicities at moderately acidic conditions. Plant Physiol 163:180–192. doi:10.1104/pp.113.222893

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kochian LV, Piñeros MA, Hoekenga OA (2005) Physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195

    Article  CAS  Google Scholar 

  • Kulcheski FR, Graichen FAS, Martinelli JA, Locatelli AB, Federizzi LC, Delatorre CA (2010) Molecular mapping of Pc68, a crown rust resistance gene in Avena sativa. Euphytica 175:423–432

    Article  CAS  Google Scholar 

  • Lander E, Green P, Abrahamson J, Barlow A, Daly M, Lincoln S, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Li CD, Rossnagel BG, Scoles GJ (2000) The development of oat microsatellite markers and their use in identifying relationships among Avena species and oat cultivars. Theor Appl Genet 101:1259–1268. doi:10.1007/s001220051605

    Article  CAS  Google Scholar 

  • Liu J, Magalhães 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. doi:10.1111/j.1365-313X.2008.03696.x

    PubMed Central  Google Scholar 

  • Ma H-X, Bai G-H, Lu W-Z (2006) Quantitative trait loci for aluminum resistance in wheat cultivar Chinese Spring. Plant Soil 283:239–249. doi:10.1007/s11104-006-0008-1

    Article  CAS  Google Scholar 

  • Magalhães JV et al (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminium tolerance in sorghum. Nat Genet 39:1156–1161

    Article  PubMed  Google Scholar 

  • Maron LG et al (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 61:728–740. doi:10.1111/j.1365-313X.2009.04103.x

    Article  CAS  PubMed  Google Scholar 

  • Merino-Gergichevic C, Alberdi M, Ivanov AG, Reyes-Diaz M (2010) Al+3–Ca+2 interaction in plants growing in acid soils: Al-phytotoxicity response to calcareous amendments. J Soil Sci Plant Nutr 10:217–243

    Google Scholar 

  • Minella E, Sorrells ME (1997) Inheritance and chromosome location of Alp, a gene controlling aluminum tolerance in ‘Dayton’ barley. Plant Breed 116:465–469. doi:10.1111/j.1439-0523.1997.tb01032.x

    Article  CAS  Google Scholar 

  • Murphy JP, Hoffman LA (1992) The origin, history, and production of oat. In: Marshall HG, Sorrells ME (eds) Oat science and technology. ASA, CSSA Publishers, Madison, pp 1–28

    Google Scholar 

  • Nava IC, Delatorre CA, Duarte I, Pacheco MT, Federizzi LC (2006) Inheritance of aluminum tolerance and its effects on grain yield and grain quality in oats (Avena sativa L.). Euphytica 148:353–358

    Article  Google Scholar 

  • Nava IC, Delatorre CA, Pacheco MT, Scheeren PL, Federizzi LC (2015) Aluminum tolerance of oat cultivars under hydroponic and acid soil conditions. Exp Agric. doi:10.1017/S0014479715000046

  • Navakode S, Weidner A, Lohwasser U, Röder MS, Börner A (2009) Molecular mapping of quantitative trait loci (QTLs) controlling aluminium tolerance in bread wheat. Euphytica 166:283–290. doi:10.1007/s10681-008-9845-8

    Article  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. doi:10.1007/s001220000472

    Article  CAS  Google Scholar 

  • O’Donoughue LS et al (1995) A molecular linkage map of cultivated oat. Genome 38:368–380. doi:10.1139/g95-048

    Article  PubMed  Google Scholar 

  • Ofei-manu P, Wagatsuma T, Ishikawa S, Tawaraya K (2001) The plasma membrane strength of the root-tip cells ans root phenolic compounds are correlated with Al tolerance in several common woody plants. Soil Sci Plant Nutr 47:359–375

    Article  CAS  Google Scholar 

  • Oliveira PH, Federizzi LC, Milach SCK, Gotuzzo C, Sawasato JT (2005) Inheritance in oat (Avena sativa L.) of tolerance to soil aluminum toxicity. Crop Breed Appl Biotechnol 5:125–133

    Article  Google Scholar 

  • Oliver RE et al (2013) SNP discovery and chromosome anchoring provide the first physically-anchored hexaploid oat map and reveal synteny with model species. PLoS ONE 8:e58068. doi:10.1371/journal.pone.0058068

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pellet DM, Papernik LA, Kochian LV (1996) Multiple aluminum-resistance mechanisms in wheat: roles of root apical phosphate and malate exudation. Plant Physiol 112:591–597

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peng J, Ronin Y, Fahima T, Röder MS, Li Y, Nevo E, Korol A (2003) Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat. Proc Natl Acad Sci 100:2489–2494. doi:10.1073/pnas.252763199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pereira LB et al (2013) Differential speed of activation in antioxidant system in three oat genotypes. J Inorg Biochem 128:202–207. doi:10.1016/j.jinorgbio.2013.07.025

    Article  CAS  PubMed  Google Scholar 

  • Portyanko VA, Hoffman DL, Lee M, Holland JB (2001) A linkage map of hexaploid oat based on grass anchor DNA clones and its relationship to other oat maps. Genome 44:249–265

    Article  CAS  PubMed  Google Scholar 

  • Project RA (2008) The rice annotation project database (RAP-DB): 2008 update. Nucleic Acids Res 36:D1028–D1033. doi:10.1093/nar/gkm978

    Article  Google Scholar 

  • Radmer L, Tesfaye M, Somers D, Temple S, Vance C, Samac D (2012) Aluminum resistance mechanisms in oat (Avena sativa L.). Plant Soil 351:121–134. doi:10.1007/s11104-011-0937-1

    Article  CAS  Google Scholar 

  • Raman H et al (2005) Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). Genome 48:781–791. doi:10.1139/g05-054

    Article  CAS  PubMed  Google Scholar 

  • Rines H, Molnar S, Tinker N, Phillips R (2006) Oat. Genome mapping and molecular breeding in plants. Cereals Millets 1:211–242

  • Rossiello RO, Netto JJ (2006) Toxidez de alumínio em plantas: novos enfoques para um velho problema. In: Fernandes MS (ed) Nutrição mineral de plantas. Sociedade Brasileira de Ciência do Solo, Viçosa, pp 375–418

    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. doi:10.1093/jxb/erq272

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Chacon CD, Federizzi LC, Milach SCK, Pacheco MT (2000) Viabilidade genética e herança da tolerância à toxicidade do aluminio em aveia. Pesqui Agropecu Bras 35:1797–1808

    Article  Google Scholar 

  • Sasaki T et al (2006) Sequence upstream of the wheat (Triticum aestivum L.) ALMT1 gene and its relationship to aluminum resistance. Plant Cell Physiol 47:1343–1354. doi:10.1093/pcp/pcl002

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s11032-011-9668-5

    Article  CAS  Google Scholar 

  • Sivaguru M et al (2000) Aluminum-induced 1-3-B-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 2:991–1006

    Article  Google Scholar 

  • Sorrells ME et al (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827. doi:10.1101/gr.1113003

    PubMed Central  CAS  PubMed  Google Scholar 

  • Soto-Cerda B, Peñaloza E, Montenegro A, Rupayan A, Gallardo M, Salvo-Garrido H (2013) An efficient marker-assisted backcrossing strategy for enhancing barley (Hordeum vulgare L.) production under acidity and aluminium toxicity. Mol Breed 31:855–866. doi:10.1007/s11032-013-9839-7

    Article  CAS  Google Scholar 

  • Tan YD, Wan C, Zhu Y, Lu C, Xiang Z, Deng HW (2001) An amplified fragment length polymorphism map of the silkworm. Genetics 157:1277–1284  

  • Tinker NA, Mather DE (1995) MQTL: software for simplified composite interval mapping of QTL in multiple environments. J Agric Genomics 1:1–4

    Google Scholar 

  • Tinker NA et al (2014) A SNP genotyping array for hexaploid oat. Plant Genome. doi:10.3835/plantgenome2014.03.0010

  • Vogl C, Xu S (2000) Multipoint mapping of viability and segregation distorting loci using molecular markers. Genetics 155:1439–1447

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wagner CW, Milach SCK, Federizzi LC (2001) Genetic inheritance of aluminum tolerance in oat. Crop Breed Appl Biotechnol 1:22–26

    Google Scholar 

  • Wang J et al (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. doi:10.1007/s00122-007-0562-9

    Article  CAS  PubMed  Google Scholar 

  • Wang J et al (2009) High-throughput single nucleotide polymorphism genotyping using nanofluidic Dynamic Arrays. BMC Genomics 10:561    

  • Wight CP et al (2003) A molecular marker map in ‘Kanota’ x ‘Ogle’ hexaploid oat (Avena spp.) enhanced by additional markers and a robust framework. Genome 46:28–47

    Article  CAS  PubMed  Google Scholar 

  • Yokosho K, Yamaji N, Ma JF (2011) An Al-inducible MATE gene is involved in external detoxification of Al in rice. Plant J 68:1061–1069. doi:10.1111/j.1365-313X.2011.04757.x

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Herrmann M (2006) Inheritance and mapping of a powdery mildew resistance gene introgressed from Avena macrostachya in cultivated oat. Theor Appl Genet 25:329–335

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Zheng SJ, Yang JL, He YF, Yu XH et al (2005) Immobilization of aluminum with phosphorus in roots is associated with high aluminum resistance in buckwheat. Plant Physiol 138:297–303

    Article  PubMed Central  CAS  PubMed  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. doi:10.1093/aob/mct135

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Dr. Eric Jellen and Dr. Jeff Maughan from Brigham Young University for the support during the SNP analysis; Dr. Marcelo T. Pacheco for the heritability analysis, and Mauricio D. Salomon for figure preparation. This study was supported by grants, scholarships, and fellowships from the Brazilian National Council for Scientific and Technological Development (CNPq), the Coordination for the Improvement of Higher Education Personnel (CAPES) from Brazil, The Prairie Oat Growers Association, and the US Department of Agriculture.

Conflict of interest

The authors declare that they have no conflict of interest and the experiments complied with the current laws of Brazil and USA, where they were performed.

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Author notes

  1. Emerson Limberger

    Present address: Pioneer Hi-Bred International Inc., 7300 N.W. 62nd Avenue, P.O. Box 1004, Johnston, IA, 50131, USA

  2. Emir Islamovic

    Present address: BASF, 26 Davis Dr, Research Triangle Park, NC, 27709, USA

Authors and Affiliations

  1. Department of Crop Science, Federal University of Rio Grande do Sul (UFRGS), Av. Bento Gonçalves, 7712, P.O. Box 15100, Porto Alegre, RS, 91501-970, Brazil

    Adriano de Bernardi Schneider, Itamar Cristiano Nava, Cássio Barcellos Hervé, Emerson Limberger & Carla Andrea Delatorre

  2. Small Grains and Potato Germplasm Research Unit, United States Department of Agriculture-Agricultural Research Service (USDA-ARS), 1691 S. 2700 W., Aberdeen, ID, 83210, USA

    Emir Islamovic

  3. General Mills Crop Bioscience, 1990 Kimball Avenue, Manhattan, KS, 66502, USA

    Eric W. Jackson

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  1. Adriano de Bernardi Schneider
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Correspondence to Carla Andrea Delatorre.

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Schneider, A.B., Nava, I.C., Hervé, C.B. et al. Chromosome-anchored QTL conferring aluminum tolerance in hexaploid oat. Mol Breeding 35, 121 (2015). https://doi.org/10.1007/s11032-015-0315-4

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