Genome-wide association of drought-related and biomass traits with HapMap SNPs in Medicago truncatula

Plant Cell and Environment

Volumn 38, Issue 10, 2015, Pages 1997-2011

  Kang, Yun ^a   Sakiroglu, Muhammet ^b   Krom, Nicholas ^a   Stanton Geddes, John ^c   Wang, Mingyi ^a   Lee, Yi Ching ^a   Young, Nevin D ^d   Udvardi, Michael ^a  

^a PLANT BIOLOGY DIVISION   (United States)

^b KAFKAS UNIVERSITY   (Turkey)

^c UNIVERSITY OF VERMONT   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Biomass; Compressed mixed linear model; Drought; GWAS; Medicago truncatula; Single nucleotide polymorphisms

Indexed keywords

CARBON ISOTOPE; CHROMOSOME; DICOTYLEDON; DROUGHT; GENOME; PERFORMANCE ASSESSMENT; PHYTOMASS; PLANT BREEDING; PROTEIN;

ARABIDOPSIS; MEDICAGO; MEDICAGO TRUNCATULA;

ALDEHYDE DEHYDROGENASE; GLUTAMATE CYSTEINE LIGASE; VEGETABLE PROTEIN;

BARREL MEDIC; BIOMASS; CYTOLOGY; DROUGHT; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION STUDY; GENETICS; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; GROWTH, DEVELOPMENT AND AGING; PHENOTYPE; PHYSIOLOGY; PLANT LEAF; PLANT STOMA; SHOOT; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL MODEL;

ALDEHYDE DEHYDROGENASE; BIOMASS; DROUGHTS; GENETIC ASSOCIATION STUDIES; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; GLUTAMATE-CYSTEINE LIGASE; LINEAR MODELS; LINKAGE DISEQUILIBRIUM; MEDICAGO TRUNCATULA; PHENOTYPE; PLANT LEAVES; PLANT PROTEINS; PLANT SHOOTS; PLANT STOMATA; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84941880820     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12520     Document Type: Article

References (88)

1. Aharon R., Shahak Y., Wininger S., Bendov R., Kapulnik Y. & Galili G. (2003) Overexpression of a plasma membrane aquaporin in transgenic tobacco improves plant vigor under favorable growth conditions but not under drought or salt stress. The Plant Cell 15, 439-447.
2. Albrecht V., Ingenfeld A. & Apel K. (2008) Snowy cotyledon 2: the identification of a zinc finger domain protein essential for chloroplast development in cotyledons but not in true leaves. Plant Molecular Biology 66, 599-608.
3. Altshuler D., Brooks L.D., Chakravarti A., Collins F.S., Daly M.J., Donnelly P. & Stewart J. (2005) A haplotype map of the human genome. Nature 437, 1299-1320.
4. Araus J.L., Amaro T., Casadesus J., Asbati A. & Nachit M.M. (1998) Relationships between ash content, carbon isotope discrimination and yield in durum wheat. Australian Journal of Plant Physiology 25, 835-842.
5. Atwell S., Huang Y.S., Vilhjalmsson B.J., Willems G., Horton M., Li Y. & Nordborg M. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627-631.
6. Barker D.G., Bianchi S., Blondon F., Dattee Y., Duc G., Essad S. & Huguet T. (1990) Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis. Plant Molecular Biology Reporter 8, 40-49.
7. Baum M., Grando S., Backes G., Jahoor A., Sabbagh A. & Ceccarelli S. (2003) QTLs for agronomic traits in the Mediterranean environment identified in recombinant inbred lines of the cross 'Arta' x H-spontaneum 41-1. Theoretical and Applied Genetics 107, 1215-1225.
8. Bhargava S. & Sawant K. (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breeding 132, 21-32.
9. Bradbury P.J., Zhang Z., Kroon D.E., Casstevens T.M., Ramdoss Y. & Buckler E.S. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics (Oxford, England) 23, 2633-2635.
10. Branca A., Paape T.D., Zhou P., Briskine R., Farmer A.D., Mudge J. & Tiffin P. (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proceedings of the National Academy of Sciences of the United States of America 108, E864-E870.
11. Broughton W.J. & Dilworth M.J. (1971) Control of leghaemoglobin synthesis in snake beans. The Biochemical Journal 125, 1075-1080.
12. Buckler E. & Gore M. (2007) An Arabidopsis haplotype map takes root. Nature Genetics 39, 1056-1057.
13. Cai S., Wu D., Jabeen Z., Huang Y., Huang Y. & Zhang G. (2013a) Genome-wide association analysis of aluminum tolerance in cultivated and Tibetan wild barley. PLoS ONE 8, e69776.
14. Cai S., Yu G., Chen X., Huang Y., Jiang X., Zhang G. & Jin X. (2013b) Grain protein content variation and its association analysis in barley. BMC Plant Biology 13, 35.
15. Cardon L.R. & Abecasis G.R. (2003) Using haplotype blocks to map human complex trait loci. Trends in Genetics 19, 135-140.
16. Chaves M.M., Maroco J.P. & Pereira J.S. (2003) Understanding plant responses to drought - from genes to the whole plant. Functional Plant Biology 30, 239-264.
17. Chiu C.C., Lin C.S., Hsia A.P., Su R.C., Lin H.L. & Tsay Y.F. (2004) Mutation of a nitrate transporter, AtNRT1: 4, results in a reduced petiole nitrate content and altered leaf development. Plant and Cell Physiology 45, 1139-1148.
18. Condon A.G. & Richards R.A. (1992) Broad sense heritability and genotype × environment interaction for carbon isotope discrimination in field-grown wheat. Australian Journal of Agricultural Research 43, 921-934.
19. Dai A. (2011) Drought under global warming: a review. Wiley Interdisciplinary Reviews-Climate Change 2, 45-65.
20. Dai X., Wang G., Yang D.S., Tang Y., Broun P., Marks M.D. & Zhao P.X. (2010) TrichOME: a comparative omics database for plant trichomes. Plant Physiology 152, 44-54.
21. De Micco V. & Aronne G. (2012) Morpho-anatomical traits for plant adaptation to drought. In Plant Responses to Drought Stress (ed. R. Aroca), pp. 37-61. Springer-Verlag GmbH, Berlin, Heidelberg, Germany.
22. Evanno G., Regnaut S. & Goudet J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611-2620.
23. Farquhar G.D. & Richards R.A. (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat triticum-aestivum genotypes. Australian Journal of Plant Physiology 11, 539-552.
24. Foley J.A., Ramankutty N., Brauman K.A., Cassidy E.S., Gerber J.S., Johnston M. & Zaks D.P.M. (2011) Solutions for a cultivated planet. Nature 478, 337-342.
25. Futamura N., Kouchi H. & Shinohara K. (2002) A gene for pectate lyase expressed in elongating and differentiating tissues of a Japanese willow (Salix gilgiana). Journal of Plant Physiology 159, 1123-1130.
26. Gaudin A.C.M., Henry A., Sparks A.H. & Slamet-Loedin I.H. (2013) Taking transgenic rice drought screening to the field. Journal of Experimental Botany 64, 109-117.
27. Gibbs R.A., Belmont J.W., Hardenbol P., Willis T.D., Yu F.L., Yang H.M. & Stein L.D. (2003) The international HapMap project. Nature 426, 789-796.
28. Golldack D., Lueking I. & Yang O. (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Reports 30, 1383-1391.
29. Gomez L.D., Casano L.M., Braga M.R. & Buckeridge M.S. (1995) Changes in extracellular beta-galactosidase and protease activities during bean hypocotyl growth. Revista Brasileira de Fisiologia Vegetal 7, 1-6.
30. Gore M.A., Chia J.-M., Elshire R.J., Sun Q., Ersoz E.S., Hurwitz B.L. & Buckler E.S. (2009) A first-generation haplotype map of maize. Science 326, 1115-1117.
31. Gurian-Sherman D. (2012) High and dry: why genetic engineering is not solving agriculture's drought problem in a thirsty world. High and dry: why genetic engineering is not solving agriculture's drought problem in a thirsty world, iv + 34 pp.-iv + 34 pp.
32. 2 assimilation in the leaves of transgenic rice plants. Plant and Cell Physiology 45, 521-529.
33. Hao D., Chao M., Yin Z. & Yu D. (2012) Genome-wide association analysis detecting significant single nucleotide polymorphisms for chlorophyll and chlorophyll fluorescence parameters in soybean (Glycine max) landraces. Euphytica 186, 919-931.
34. Hirschhorn J.N. & Daly M.J. (2005) Genome-wide association studies for common diseases and complex traits. Nature Reviews. Genetics 6, 95-108.
35. Hubick K.T., Farquhar G.D. & Shorter R. (1986) Correlation between water-use efficiency and carbon isotope discrimination in diverse peanut (Arachis) germplasm. Australian Journal of Plant Physiology 13, 803-816.
36. Hwang E.-Y., Song Q., Jia G., Specht J.E., Hyten D.L., Costa J. & Cregan P.B. (2014) A genome-wide association study of seed protein and oil content in soybean. BMC Genomics 15, 1.
37. Joukhadar R., El-Bouhssini M., Jighly A. & Ogbonnaya F.C. (2013) Genome-wide association mapping for five major pest resistances in wheat. Molecular Breeding 32, 943-960.
38. Juenger T.E. (2013) Natural variation and genetic constraints on drought tolerance. Current Opinion in Plant Biology 16, 274-281.
39. Kang Y., Han Y., Torres-Jerez I., Wang M., Tang Y., Monteros M. & Udvardi M. (2011) System responses to long-term drought and re-watering of two contrasting alfalfa varieties. Plant Journal 68, 871-889.
40. Khan H.U.R., Link W., Hocking T.J. & Stoddard F.L. (2007) Evaluation of physiological traits for improving drought tolerance in faba bean (Vicia faba L.). Plant and Soil 292, 205-217.
41. Korte A. & Farlow A. (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9, 29.
42. Koziol L., Rieseberg L.H., Kane N. & Bever J.D. (2012) Reduced drought tolerance during domestication and the evolution of weediness results from tolerance-growth trade-offs. Evolution 66, 3803-3814.
43. Kumar S., Garrick D.J., Bink M.C.A.M., Whitworth C., Chagne D. & Volz R.K. (2013) Novel genomic approaches unravel genetic architecture of complex traits in apple. BMC Genomics 14, 393.
44. Lagunes Espinoza L.D.C., Huguet T. & Julier B. (2012) Multi-population QTL detection for aerial morphogenetic traits in the model legume Medicago truncatula. Theoretical and Applied Genetics 124, 739-754.
45. Leonhardt N., Kwak J.M., Robert N., Waner D., Leonhardt G. & Schroeder J.I. (2004) Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell 16, 596-615.
46. Lipiec J., Doussan C., Nosalewicz A. & Kondracka K. (2013) Effect of drought and heat stresses on plant growth and yield: a review. International Agrophysics 27, 463-477.
47. Liu C., Weng J., Zhang D., Zhang X., Yang X., Shi L. & Zhang S. (2014) Genome-wide association study of resistance to rough dwarf disease in maize. European Journal of Plant Pathology 139, 205-216.
48. Lobell D.B., Burke M.B., Tebaldi C., Mastrandrea M.D., Falcon W.P. & Naylor R.L. (2008) Prioritizing climate change adaptation needs for food security in 2030. Science 319, 607-610.
49. Lynch J.P. (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiology 156, 1041-1049.
50. Manolio T.A., Brooks L.D. & Collins F.S. (2008) A HapMap harvest of insights into the genetics of common disease. Journal of Clinical Investigation 118, 1590-1605.
51. Merah O., Deleens E., Souyris I., Nachit M. & Monneveux P. (2001) Stability of carbon isotope discrimination and grain yield in durum wheat. Crop Science 41, 677-681.
52. Morris G.P., Ramu P., Deshpande S.P., Hash C.T., Shah T., Upadhyaya H.D. & Kresovich S. (2013a) Population genomic and genome-wide association studies of agroclimatic traits in sorghum. Proceedings of the National Academy of Sciences of the United States of America 110, 453-458.
53. Morris G.P., Rhodes D.H., Brenton Z., Ramu P., Thayil V.M., Deshpande S. & Kresovich S. (2013b) Dissecting genome-wide association signals for loss-of-function phenotypes in sorghum flavonoid pigmentation traits. G3-Genes Genomes Genetics 3, 2085-2094.
54. Nir I., Moshelion M. & Weiss D. (2014) The Arabidopsis gibberellin methyl transferase 1 suppresses gibberellin activity, reduces whole-plant transpiration and promotes drought tolerance in transgenic tomato. Plant, Cell & Environment 37, 113-123.
55. Paape T., Bataillon T., Zhou P., Kono T.J.Y., Briskine R., Young N.D. & Tiffin P. (2013) Selection, genome-wide fitness effects and evolutionary rates in the model legume Medicago truncatula. Molecular Ecology 22, 3525-3538.
56. Popper Z.A. & Fry S.C. (2008) Xyloglucan-pectin linkages are formed intra-protoplasmically, contribute to wall-assembly, and remain stable in the cell wall. Planta 227, 781-794.
57. Pritchard J.K., Stephens M. & Donnelly P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945-959.
58. Rana R.M., Dong S., Ali Z., Huang J. & Zhang H.S. (2012) Regulation of ATG6/Beclin-1 homologs by abiotic stresses and hormones in rice (Oryza sativa L.). Genetics and Molecular Research 11, 3676-3687.
59. Rebetzke G.J., Condon A.G., Richards R.A. & Farquhar G.D. (2002) Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat. Crop Science 42, 739-745.
60. Rebetzke G.J., Condon A.G., Farquhar G.D., Appels R. & Richards R.A. (2008) Quantitative trait loci for carbon isotope discrimination are repeatable across environments and wheat mapping populations. Theoretical and Applied Genetics 118, 123-137.
61. Riedelsheimer C., Lisec J., Czedik-Eysenberg A., Sulpice R., Flis A., Grieder C. & Melchinger A.E. (2012) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. Proceedings of the National Academy of Sciences of the United States of America 109, 8872-8877.
62. Rytter R.M. (2005) Water use efficiency, carbon isotope discrimination and biomass production of two sugar beet varieties under well-watered and dry conditions. Journal of Agronomy and Crop Science 191, 426-438.
63. SAS Institute Inc. (2004) SAS/STAT® 9.1 User's Guide. Cary, NC: SAS Institute Inc.
64. Shimada H., Mochizuki M., Ogura K., Froehlich J.E., Osteryoung K.W., Shirano Y. & Takamiya K.-I. (2007) Arabidopsis cotyledon-specific chloroplast biogenesis factor CYO1 is a protein disulfide isomerase. The Plant Cell 19, 3157-3169.
65. Sinclair T.R. (2011) Challenges in breeding for yield increase for drought. Trends in Plant Science 16, 289-293.
66. Singh B., Chauhan H., Khurana J.P., Khurana P. & Singh P. (2013) Evidence for the role of wheat eukaryotic translation initiation factor 3 subunit g (TaeIF3g) in abiotic stress tolerance. Gene 532, 177-185.
67. Slavov G.T., Nipper R., Robson P., Farrar K., Allison G.G., Bosch M. & Jensen E. (2014) Genome-wide association studies and prediction of 17 traits related to phenology, biomass and cell wall composition in the energy grass Miscanthus sinensis. The New Phytologist 201, 1227-1239.
68. Stanton-Geddes J., Paape T., Epstein B., Briskine R., Yoder J., Mudge J. & Tiffin P. (2013) Candidate genes and genetic architecture of symbiotic and agronomic traits revealed by whole-genome, sequence-based association genetics in Medicago truncatula. PLoS ONE 8, e65688.
69. Sun L. & van Nocker S. (2010) Analysis of promoter activity of members of the pectate lyase-like (PLL) gene family in cell separation in Arabidopsis. BMC Plant Biology 10, 152.
70. Tanimoto E. & Igari M. (1976) Correlation between beta-galactosidase and auxin-induced elongation growth in etiolated pea stems. Plant and Cell Physiology 17, 673-682.
71. Tanksley S.D. & Nelson J.C. (1996) Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theoretical and Applied Genetics 92, 191-203.
72. Tanz S.K., Kilian J., Johnsson C., Apel K., Small I., Harter K. & Albrecht V. (2012) The SCO2 protein disulphide isomerase is required for thylakoid biogenesis and interacts with LCHB1 chlorophyll a/b binding proteins which affects chlorophyll biosynthesis in Arabidopsis seedlings. Plant Journal 69, 743-754.
73. Thapa G., Dey M., Sahoo L. & Panda S.K. (2011) An insight into the drought stress induced alterations in plants. Biologia Plantarum 55, 603-613.
74. Tian F., Bradbury P.J., Brown P.J., Hung H., Sun Q., Flint-Garcia S. & Buckler E.S. (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nature Genetics 43, 159-162.
75. Verslues P.E., Lasky J.R., Juenger T.E., Liu T.-W. & Kumar M.N. (2014) Genome-wide association mapping combined with reverse genetics identifies new effectors of low water potential-induced proline accumulation in Arabidopsis. Plant Physiology 164, 144-159.
76. Vogel J.P., Raab T.K., Schiff C. & Somerville S.C. (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. The Plant Cell 14, 2095-2106.
77. Wagner T.A. & Kohorn B.D. (2001) Wall-associated kinases are expressed throughout plant development and are required for cell expansion. The Plant Cell 13, 303-318.
78. Wang M., Jiang N., Jia T., Leach L., Cockram J., Waugh R. & Luo Z. (2012) Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theoretical and Applied Genetics 124, 233-246.
79. Wang W.Y.S., Barratt B.J., Clayton D.G. & Todd J.A. (2005) Genome-wide association studies: theoretical and practical concerns. Nature Reviews. Genetics 6, 109-118.
80. Weng J., Xie C., Hao Z., Wang J., Liu C., Li M. & Li X. (2011) Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS ONE 6, e29229.
81. Yang J., Benyamin B., McEvoy B.P., Gordon S., Henders A.K., Nyholt D.R. & Visscher P.M. (2010) Common SNPs explain a large proportion of the heritability for human height. Nature Genetics 42, 565-569.
82. Yoder J.B., Stanton-Geddes J., Zhou P., Briskine R., Young N.D. & Tiffin P. (2014) Genomic signature of adaptation to climate in Medicago truncatula. Genetics 196, 1263-1275.
83. Yokota K., Fukai E., Madsen L.H., Jurkiewicz A., Rueda P., Radutoiu S., Stougaard J. (2009) Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell 21, 267-284.
84. Young N.D. & Udvardi M. (2009) Translating Medicago truncatula genomics to crop legumes. Current Opinion in Plant Biology 12, 193-201.
85. Yu J.M., Pressoir G., Briggs W.H., Bi I.V., Yamasaki M., Doebley J.F. & Buckler E.S. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38, 203-208.
86. Zhang J.-Y., de Carvalho M.H.C., Torres-Jerez I., Kang Y., Allen S.N., Huhman D.V., Udvardi M.K. (2014) Global reprogramming of transcription and metabolism in Medicago truncatula during progressive drought and after rewatering. Plant Cell and Environment 37, 2553-2576.
87. Zhang Z., Ersoz E., Lai C.-Q., Todhunter R.J., Tiwari H.K., Gore M.A. & Buckler E.S. (2010) Mixed linear model approach adapted for genome-wide association studies. Nature Genetics 42, 355-360.
88. Zhou S., Hu W., Deng X., Ma Z., Chen L., Huang C. & He G. (2012) Overexpression of the wheat aquaporin gene, TaAQP7, enhances drought tolerance in transgenic tobacco. PLoS ONE 7, e52439.