Candidate Genes and Genetic Architecture of Symbiotic and Agronomic Traits Revealed by Whole-Genome, Sequence-Based Association Genetics in Medicago truncatula

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Stanton Geddes, John ^a   Paape, Timothy ^a   Epstein, Brendan ^a   Briskine, Roman ^b   Yoder, Jeremy ^a   Mudge, Joann ^c   Bharti, Arvind K ^c   Farmer, Andrew D ^c   Zhou, Peng ^a   Denny, Roxanne ^a   May, Gregory D ^c   Erlandson, Stephanie ^a   Yakub, Mohammed ^a   Sugawara, Masayuki ^a   Sadowsky, Michael J ^a   Young, Nevin D ^a   Tiffin, Peter ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b University of Minnesota   (United States)

^c NATIONAL CENTER FOR GENOME RESOURCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGRONOMY; ARTICLE; BARREL MEDIC; CAML3 GENE; COMPUTER MODEL; CONTROLLED STUDY; DENSITY; FLOWERING; GENE IDENTIFICATION; GENE SEQUENCE; GENE STRUCTURE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC TRAIT; MTFD GENE; MTMMPL1 GENE; MTNODGRP3 GENE; MTNODGRP3A GENE; NFP GENE; NODULATION; NONHUMAN; PHENOTYPIC VARIATION; PLANT GENE; PLANT HEIGHT; SERK2 GENE; SINGLE NUCLEOTIDE POLYMORPHISM; SYMBIOSIS; TRICHOME;

GENOME, PLANT; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LINKAGE DISEQUILIBRIUM; MEDICAGO TRUNCATULA; PLANT ROOT NODULATION; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

MEDICAGO TRUNCATULA;

EID: 84878526220     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065688     Document Type: Article

References (59)

1. Smil V, (1999) Nitrogen in crop production. Global Biogeochem Cy 13: 647-662.
2. Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, et al. (1999) Global patterns of terrestrial biological nitrogn (N2) fixation in natural ecosystems. Global Biogeochem Cy 13: 623-645.
3. Oldroyd GE, Downie JA, (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5: 566-576.
4. Young ND, Debellé F, Oldroyd GED, Geurts R, Cannon SB, et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.
5. Young ND, Udvardi M, (2009) Translating Medicago truncatula genomics to crop legumes. Current Opinion Plant Biology 12: 193-201.
6. Rafalski JA, (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13: 174-180.
7. Clark AG, (2005) Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15: 1496-1502.
8. Long AD, Langley CH, (1999) The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res 9: 720-731.
9. Yang J, Benyamin B, McEvoy BP, Gordon S, Henders AK, et al. (2010) Common SNPs explain a large proportion of the heritability for human height. Nat Genet 42: 565-569.
10. Dickson SP, Wang K, Krantz I, Hakonarson H, Goldstein DB, (2010) Rare variants create synthetic genome-wide associations. PLoS Biol 8: e1000294.
11. Branca A, Paape TD, Zhou P, Briskine R, Farmer AD,et al. (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci USA 108.
12. Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465: 627-631.
13. Chan EKF, Rowe HC, Corwin JA, Joseph B, Kliebenstein DJ, (2011) Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana. PLoS Biol 9: e1001125.
14. DeRose-Wilson L, Gaut BS, (2011) Mapping salinity tolerance during Arabidopsis thaliana germination and seedling growth. PloS ONE 6: e22832.
15. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173-178.
16. Huang X, Zhao Y, Wei X, Li C, Wang A,et al. (2011) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet: 1-10.
17. Krill AM, Kirst M, Kochian LV, Buckler ES, Hoekenga Oa, (2010) Association and linkage analysis of aluminum tolerance genes in maize. PloS ONE 5: e9958.
18. Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, et al. (2012) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proc Natl Acad Sci USA 109: 8872-8877.
19. Gubry-Rangin C, Garcia M, Béna G, (2010) Partner choice in Medicago truncatula-Sinorhizobium symbiosis. Proc R Soc B 277: 1947-1951.
20. Heath KD, Tiffin P, (2007) Context dependence in the coevolution of plant and rhizobial mutualists. Proc R Soc B 274: 1905-1912.
21. Triplett EW, Sadowsky MJ, (1992) Genetics of competition for nodulation of legumes. Annu Rev Microbiol 46: 399-428.
22. Bhuvaneswari TV, Bhagwat AA, Bauer WD, (1981) Transient susceptibility of root cells in four common legumes to nodulation by rhizobia. Plant Physiol 68: 1144-1149.
23. Kang HM, Sul JH, Service SK, Zaitlen Na, Kong SY, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42: 348-354.
24. Yu J, Pressoir G, Briggs W, Vroh BI, Yamasaki M, et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38: 203-208.
25. Zhang Z, Ersoz E, Lai C-Q, Todhunter RJ, Tiwari HK, et al. (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42: 355-360.
26. 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: 2633-2635.
27. Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, et al. (2005) Genome-Wide Association Mapping in Arabidopsis Identifies Previously Known Flowering Time and Pathogen Resistance Genes. PLoS Genet 1: e60.
28. Pritchard JK, Pickrell JK, Coop G, (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20: R208-215.
29. Barton NH, Turelli M, (1989) Evolutionary quantitative genetics: how little do we know? Annu Rev Genet 23: 337-370.
30. Beavis WD (1998) QTL analyses: power, precision and accuracy. In: Pateron AH, editor. Molecular Dissection of Complex Traits. Boca Raton, Florida: CRC Press. 145-162.
31. Xu S, (2003) Theoretical basis of the Beavis effect. Genetics 165: 2259-2268.
32. Fisher RA (1930) The Genetical Theory of Natural Selection. Oxford, England: Clarendon Press.
33. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, et al. (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309: 1052-1056.
34. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, et al. (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309: 1056-1059.
35. Hudson M, Ringli C, Boylan MT, Quail PH, (1999) The FAR1 locus encodes a novel nuclear protein specific to phytochrome A signaling. Genes Dev 13: 2017-2027.
36. Pierre J-B, Bogard M, Herrman D, Huyghe C, Julier B, (2011) A CONSTANS-like gene candidate that could explain most of the genetic variation for flowering date in Medicago truncatula. Mol Breeding 28: 25-35.
37. Ferrario S, Busscher J, Franken J, Gerats T, Vandenbussche M, et al. (2004) Ectopic expression of the petunia MADS box gene UNSHAVEN accelerates flowering and confers leaf-like characteristics to floral organs in a dominant-negative manner. Plant Cell 16: 1490-1505.
38. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, et al. (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302: 630-633.
39. Kevei Z, Vinardell JM, Kiss GB, Kondorosi A, Kondorosi E, (2002) Glycine-rich proteins encoded by a nodule-specific gene family are implicated in different stages of symbiotic nodule development in Medicago spp. Mol Plant Microbe Interact 15: 922-931.
40. Elshire RJ, Glaubitz JC, Sun Q, Poland Ja, Kawamoto K, et al. (2011) A Robust, Simple genotyping-by-sequencing (GBS) approach for high diversity species. PloS ONE 6: e19379.
41. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, et al. (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3: e3376.
42. Ronfort J, Bataillon T, Santoni S, Delalande M, David JL, et al. (2006) Microsatellite diversity and broad scale geographic structure in a model legume: building a set of nested core collection for studying naturally occurring variation in Medicago truncatula. BMC Plant Biology 6: 28.
43. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456: 53-59.
44. Wu TD, Nacu S, (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873-881.
45. Bonnin I, Ronfort J, Wozniak F, Olivieri I, (2001) Spatial effects and rare outcrossing events in Medicago truncatula (Fabaceae). Mol Ecol 10: 1371-1383.
46. Siol M, Prosperi JM, Bonnin I, Ronfort J, (2008) How multilocus genotypic pattern helps to understand the history of selfing populations: a case study in Medicago truncatula. Heredity 100: 517-525.
47. Cregan PB, Keyser HH, Sadowsky MJ, (1989) Host plant effects on nodulation and competitiveness of the Bradyrhizobium japonicum serotype strains constituting serocluster 123. Appl Environ Microbiol 55: 2532-2536.
48. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100: 9440-9445.
49. Venables WN, Ripley BD (2002) Modern Applied Statistics with S. New York, NY: Springer.
50. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. 2.10 ed. Vienna, Austria: R Foundation for Statistical Computing.
51. Fedorova M, van de Mortel J, Matsumoto PA, Cho J, Town CD, et al. (2002) Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol 130: 519-537.
52. Arrighi J-F, Barre A, Ben Amor B, Bersoult A, Campos Soriano L, et al. (2006) The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
53. Nolan KE, Kurdyukov S, Rose RJ, (2011) Characterisation of the legume SERK-NIK gene superfamily including splice variants: implications for development and defence. BMC Plant Biol 11: 44.
54. Salzer P, Feddermann N, Wiemken A, Boller T, Staehelin C, (2004) Sinorhizobium meliloti-induced chitinase gene expression in Medicago truncatula ecotype R108-1: a comparison between symbiosis-specific class V and defence-related class IV chitinases. Planta 219: 626-638.
55. Gamas P, de Carvalho-Niebel F, Lescure N, Cullimore JV, (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol Plant Microbe Interact 9: 233-242.
56. Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, et al. (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci USA 108: 14348-14353.
57. Morère-Le Paven MC, Viau L, Hamon A, Vandecasteele C, Pellizzaro A, et al. (2011) Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula. Journal of Experimental Botany 62: 5595-5605.
58. Kevei Z, Lougnon G, Mergaert P, Horvath GV, Kereszt A, et al. (2007) 3-hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19: 3974-3989.
59. Combier JP, Vernié T, de Billy F, El Yahyaoui F, Mathis R, et al. (2007) The MtMMPL1 early nodulin is a novel member of the matrix metalloendoproteinase family with a role in Medicago truncatula infection by Sinorhizobium meliloti. Plant Physiol 144: 703-716.