Association and linkage analysis of aluminum tolerance genes in maize

PLoS ONE

Volumn 5, Issue 4, 2010, Pages

  Krill, Allison M ^a,b   Kirst, Matias ^b,c   Kochian, Leon V ^a,b   Buckler, Edward S ^a,b   Hoekenga, Owen A ^a,b  

^a ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSYLHOMOCYSTEINASE; ALUMINUM ACTIVATED MALATE TRANSPORTER 1; ALUMINUM ACTIVATED MALATE TRANSPORTER 2; MALIC ACID; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ALUMINUM;

ALUMINUM TOLERANCE; ARTICLE; CONTROLLED STUDY; DNA POLYMORPHISM; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HAPLOTYPE; HYDROPONICS; LINKAGE ANALYSIS; MAIZE; NONHUMAN; NUTRIENT SOLUTION; PH; PLANT BREEDING; PLANT GENETICS; QUANTITATIVE TRAIT LOCUS; BREEDING; CROP; DRUG EFFECT; DRUG TOLERANCE; GENETIC LINKAGE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METHODOLOGY; PHYSIOLOGY; PLANT GENE; PLANT ROOT;

ZEA MAYS;

ALUMINUM; BREEDING; CROPS, AGRICULTURAL; DRUG TOLERANCE; GENES, PLANT; GENETIC ASSOCIATION STUDIES; GENETIC LINKAGE; PLANT ROOTS; ZEA MAYS;

EID: 77956312123     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009958     Document Type: Article

References (60)

1. Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. In Date RA, Grundon NJ, Raymet GE, Probert ME, eds. Plant-Soil Interactions at Low pH: Principles and Management. Dordrecht: Kluwer Academic Publishers. pp 5-19.
2. Pandey S, Ceballos H, Magnavaca R, Bahia Filho AFC, Duque-Vargas J, et al. (1994) Genetics of Tolerance to Soil Acidity in Tropical Maize. Crop Science 34: 1511-1514.
3. Welcker C, The C, Andreau B, De Leon C, Parentoni SN, et al. (2005) Heterosis and Combining Ability for Maize Adaptation to Tropical Acid Soils: Implications for Future Breeding Strategies. Crop Science 45: 2405-2413.
4. Rao IM, Zeigler RS, Vera R, Sarkarung S (1993) Selection and Breeding for Acid-Soil Tolerance in Crops. BioScience 43: 454.
5. Vargas-Duque J, Pandey S, Granados G, Ceballos H, Knapp E (1994) Inheritance of Tolerance to Soil Acidity in Tropical Maize. Crop Science 34: 50-54.
6. Granados G, Pandey S, Ceballos H (1993) Response to Selection for Tolerance to Acid Soils in a Tropical Maize Population. Crop Science 33: 936-940.
7. Kochian LV (1995) Cellular Mechanisms of Aluminum Toxicity and Resistance in Plants. Annual Reviews of Plant Physiology and Plant Molecular Biology 46: 237-260.
8. Poschenrieder C, Gunse B, Corrales I, Barcelo J (2008) A glance into aluminum toxicity and resistance in plants. Science of the Total Environment 400: 356-368.
9. Delhaize E, Ryan PR (1995) Aluminum Toxicity and Tolerance in Plants. Plant Physiology 107: 315-321.
10. Ryan PR, Shaff JE, Kochian LV (1992) Aluminum Toxicity in Roots: Correlation among Ionic Currents, Ion Fluxes, and Root Elongation in Aluminum-Sensitive and Aluminum-Tolerant Wheat Cultivars. Plant Physiology 99: 1193-1200.
11. Kollmeier M, Felle HH, Horst WJ (2000) Genotypical Differences in Aluminum Resistance of Maize Are Expressed in the Distal Part of the Transition Zone. Is Reduced Basipetal Auxin Flow Involved in Inhibition of Root Elongation by Aluminum? Plant Physiology 122: 945-956.
12. Jones DL, Blancaflor EB, Kochian LV, Gilroy S (2006) Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots. Plant, Cell and Environment 29: 1309-1318.
13. Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Reviews of Plant Biology 55: 459-493.
14. Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid Peroxidation Is an Early Symptom Triggered by Aluminum, But Not the Primary Cause of Elongation Inhibition in Pea Roots. Plant Physiology 125: 199-208.
15. Jones DL, Shaff JE, Kochian LV (1995) Role of calcium and other ions in directing root hair tip growth in Limnobium stoloniferum. Planta 197: 672-680.
16. Ma JF, Ryan PR, Delhaize E (2001) Aluminum tolerance in plants and the complexing role of organic acids. Trends in Plant Science 6: 273-8.
17. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annual Reviews of Plant Physiology and Plant Molecular Biology 52: 527-560.
18. Hoekenga OA, Maron LG, Piñeros MA, Cançado GMA, Shaff JE, et al. (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Acad Natl Sci USA 103: 9738-9743.
19. Delhaize E, Gruber B, Ryan PR (2007) The roles of organic anion permeases in aluminium resistance and mineral nutrition. FEBS Letters 581: 2255-2262.
20. Magalhaes JV, Liu J, Guimaraes CT, Lana UG, Alves VM, et al. (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nature Genetics 39: 1156-61.
21. Piñeros MA, Shaff JE, Manslank HS, Alves VM, Kochian LV (2005) Aluminum Resistance in Maize Cannot Be Solely Explained by Root Organic Acid Exudation. A Comparative Physiological Study. Plant Physiology 137: 231-241.
22. Eticha D, Stass A, Horst WJ (2005) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance Plant. Cell & Environment 28: 1410-1420.
23. Edmeades G, Beck D (1995) Physiology and Stress Resistant Maize Subprogram Accessed from: http://www.cimmyt.org/Research/Maize/Revisar/htm/MFSSRB.HTM (Verified November 10, 2009).
24. Pandey S, Alberto L, Leon N, Keith D, Stephen F, et al. (2007) Breeding Maize for Tolerance to Soil Acidity. Plant Breeding Reviews 28: 59-100.
25. Garvin D, Carver B (2003) Role of the genotype in tolerance to acidity and aluminum toxicity. In Rengel Z, ed. Handbook of Soil Acidity. New York: Marcel Dekker. pp 387-406.
26. Sibov ST, Gaspar MJ, Ottoboni LMM, Arruda P, Souza AP (1999) Two genes controlling aluminum tolerance in maize: genetic and molecular mapping analyses. Genome 42: 475-482.
27. Ninamango-Cárdenas F, Guimaraes CT, Martins P, Parentoni SN, Carneiro NP, et al. (2003) Mapping QTLs for aluminum tolerance in maize. Euphytica 130: 223-232.
28. Mason PA (2005) Molecular and genetic investigations of aluminum tolerance in wheat and maize. Ithaca NY: Cornell University Ph.D. dissertation. 141 p.
29. Holland JB (2007) Genetic architecture of complex traits in plants. Current Opinion in Plant Biology 10: 156-161.
30. Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Current Opinion in Plant Biology 5: 107-11.
31. Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38: 203-8.
32. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, et al. (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nature Genetics 28: 286-9.
33. Whitt SR, Buckler ES (2003) Using natural allelic diversity to evaluate gene function. Methods in Molecular Biology 236: 123-40.
34. Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, et al. (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. The Plant Journal 44: 1054-64.
35. Urrea-Gomez R, Ceballos H, Pandey S, Bahia Filho AFC, Leon LA (1996) A Greenhouse Screening Technique for Acid Soil Tolerance in Maize. The Agronomy Journal 88: 806-812.
36. Magnavaca R, Gardner C, Clark R (1987) Evaluation of inbred maize lines for aluminum tolerance in nutrient solution. In Gabelman H, Loughman BC, eds. Genetic Aspects of Plant Mineral Nutrition. Dordrecht: Martinus Nijhoff. pp 255-265.
37. Piñeros MA, Magalhaes JV, Alves VM, Kochian LV (2002) The physiology and biophysics of an aluminum tolerance mechanism based on root citrate exudation in maize. Plant Physiology 129: 1194-206.
38. Maron LG, Kirst M, Mao C, Milner MJ, Menossi M, et al. (2008) Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytologist 179: 116-128.
39. Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, et al. (2004) A wheat gene encoding an aluminum-activated malate transporter. The Plant Journal 37: 645-653.
40. Magalhaes JV, Garvin DF, Wang Y, Sorrells ME, Klein PE, et al. (2004) Comparative mapping of a major aluminum tolerance gene in sorghum and other species in the poaceae. Genetics 167: 1905-14.
41. Fontecha G, Silva-Navas J, Benito C, Mestres MA, Espino FJ, et al. (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: 249-60.
42. 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: 389-99.
43. Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, et al. (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminum tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115: 265-76.
44. The Maize Genome Sequencing Project accessed from http://www.maizesequence.org (Verified November 10, 2009).
45. Fu Y, Emerich SJ, Guo L, Wen TJ, Ashlock DA, et al. (2005) Quality assessment of maize assembled genomic islands (MAGIs) and experimental verification of predicted novel genes. Proc Acad Natl Sci USA 102: 12282-12287.
46. Softberry, Inc. Prediction of protein secondary structure using Markov chains. Accessed from http://linux1.softberry.com/berry.phtml?topic=pps&group=programs&subgroup=propt (Verified November 10, 2009).
47. Ravanel S, Gakiare B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Acad Natl Sci USA 95: 7805-7812.
48. Detarsio E, Maurino V, Alvarez C, Müller C, Andreo C, et al. (2008) Maize cytosolic NADP-malic enzyme (ZmCytNADP-ME): a phylogenetically distant isoform specifically expressed in embryo and emerging roots. Plant Molecular Biology 68: 355-367.
49. Li CH, Yu N, Jiang Sm, Shangguan XX, Wang JL, et al. (2008) Downregulation of S-adenosyl-L-homocysteine hydrolase reveals a role of cytokinin in promoting transmethylation reactions. Planta 228: 125-36.
50. Weretilnyk EA, Alexander KJ, Drebenstedt M, Snider JD, Summer PS, et al. (2001) Maintaining Methylation Activities during Salt Stress: The Involvement of Adenosine Kinase. Plant Physiology 125: 856-865.
51. Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, et al. (2008) Cell Wall Polysaccharides Are Specifically Involved in the Exclusion of Aluminum from the Rice Root Apex. Plant Physiology 146: 602-611.
52. Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, et al. (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-3.
53. 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 Physiology 142: 1294-1303.
54. Piñeros MA, Cançado GMA, Maron LG, Lyi SM, Menossi M, et al. (2008) Not all ALMT1-type transporters mediate aluminum-activated organic acid responses: the case of ZmALMT1-an anion-selective transporter. The Plant Journal 53: 352-67.
55. Piñeros MA, Cançado GMA, Kochian LV (2008) 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.
56. Kovermann P, Meyer S, Hörtensteiner, Picco C, Scholz-Starke J, et al. (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. The Plant Journal 52: 1169-1180.
57. Saghai-Maroof MA, Soliman K, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81: 8014-8018.
58. Hall T, Biolign 4.0.7 (computer program). Accessed from http://www2.maizegenetics.net/bioinformatics (Verified November 10, 2009).
59. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, et al. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23: 2633-5.
60. Yamasaki M, Tenaillon MI, Vroh Bi I, Schroeder SG, Sanchez-Villeda H, et al. (2005) A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17: 2859-72.