Genetic diversity and population structure in a legacy collection of spring barley landraces adapted to a wide range of climates

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Pasam, Raj K ^a,d   Sharma, Rajiv ^a,e   Walther, Alexander ^b   Özkan, Hakan ^c   Graner, Andreas ^a   Kilian, Benjamin ^a,f  

^a Department of Genebank Leibniz Institute of Plant Genetics and Crop Plant Research ^*  (Germany)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c CUKUROVA UNIVERSITY   (Turkey)

^d Biosciences Research Division   (Australia)

^e UNIVERSITY OF DUNDEE   (United Kingdom)

^f Bayer Cropscience Belgium   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT DNA;

ALLELE; ARTICLE; BARLEY; CLIMATE; DOMESTICATION; ENVIRONMENTAL CHANGE; EVOLUTIONARY ADAPTATION; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC ORIGIN; GRAIN; HETEROZYGOSITY; LANDRACE; NONHUMAN; POPULATION STRUCTURE; QUANTITATIVE TRAIT; SIMPLE SEQUENCE REPEAT; ACCLIMATIZATION; ECOSYSTEM; GENETICS; HORDEUM; PHENOTYPE; PHYSIOLOGY; SEASON; TEMPERATURE;

ACCLIMATIZATION; ALLELES; CLIMATE; ECOSYSTEM; GENETIC VARIATION; GENOTYPE; HORDEUM; PHENOTYPE; SEASONS; TEMPERATURE;

EID: 84919912968     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0116164     Document Type: Article

References (109)

1. Zohary D, Hopf M, Weiss E (2012) Domestication of plants in the old world, 4th edition. Oxford: Oxford Univ Press. 264 p.
2. Nevo E, Ordentlich A, Beiles A, Raskin I (1992) Genetic divergence of heat production within and between the wild progenitors of wheat and barley: evolutionary and agronomical implications. Theor Appl Genet 84: 958-962.
3. Weltzien E (1988) Evaluation of barley (Hordeum vulgare L.) landrace populations originating from different growing regions in the Near East. Plant Breed 101: 95-106.
4. Graner A, Bjørnstad A˚, Konishi T, Ordon F (2003) Molecular diverisity of the barley genome. In: von Bothmer R, van Hintum T, Knüpffer H, Sato K, editors. Diversity in Barley (Hordeum vulgare). Elsevier Science B. V. Amsterdam, The Netherlands. pp. 121-141.
5. Ward DJ (1962) Some evolutionary aspects of certain morphological characters in a world collection of barley. USDA Technical Bulletin 1276. Washington, D.C.
6. Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127: 1309-1321.
7. Kilian B, Ozkan H, Kohl J, Haseler A Von, Barale F, et al. (2006) Haplotype structure at seven barley genes: relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication. Mol Genet Genom 276: 230-241.
8. Prada D (2009) Molecular population genetics and agronomic alleles in seed banks: Searching for a needle in a haystack? J Exp Bot 60: 2541-2552.
9. Saghai Maroof MA, Biyashev RM, Yang GP, Zhang Q, Allard RW (1994) Extraordinarily polymorphic microsatellite DNA in barley: species diversity, chromosomal locations, and population dynamics. Proc Natl Acad Sci USA 91: 5466-5470.
10. Fischbeck G (2003) Diversification through breeding. In: von Bothmer R, van Hintum T, Knüpffer H, Sato K, editors. Diversity in Barley (Hordeum vulgare). Elsevier Science B. V. Amsterdam, The Netherlands. pp. 29-52.
11. Jones H, Civáň P, Cockram J, Leigh FJ, Smith LM, et al. (2011) Evolutionary history of barley cultivation in Europe revealed by genetic analysis of extant landraces. BMC Evol Biol 11: 320.
12. Yahiaoui S, Cuesta-Marcos A, Gracia MP, Medina B, Lasa JM, et al. (2014) Spanish barley landraces outperform modern cultivars at low-productivity sites. Plant Breed 133: 218-226.
13. Anonymous (2008) Global strategy for the ex-situ conservation and use of barley germplasm. pp. 1-65.
14. Knüpffer H (2009) Triticeae genetic resources in ex situ genebank collections. In:, Muehlbauer G, Feuillet C, , editors., Genetics and Genomics of the Triticeae. Plant Genetics and Genomics: Crops and Models 7. Springer Science + Business Media LLC New York. pp. 31-80.
15. Kihara H (1983) Origin and history of "Daruma", a parental variety of Norin 10. In: Sakamoto S, ed. Proc. 6th Int. Wheat Genetics Symp. Kyoto University Press, Kyoto, Japan, Nov. 28 - Dec 3. pp, 13-19.
16. Hoisington D, Khairallah M, Reeves T, Ribaut JM, Skovmand B, et al. (1999) Plant genetic resources: what can they contribute toward increased crop productivity? Proc Natl Acad Sci U S A 96:5937-5943.
17. Newton AC, Akar T, Baresel JP, Bebeli PJ, Bettencourt E, et al. (2010) Cereal landraces for sustainable agriculture. A review. Agron Sustain Dev 30: 237-269.
18. Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, et al. (2010) Submergence tolerant rice: SUB1's journey from landrace to modern cultivar. Rice 3: 138-147.
19. Piffanelli P, Ramsay L, Waugh R, Benabdelmouna A, D'Hont A, et al. (2004) A barley cultivationassociated polymorphism conveys resistance to powdery mildew. Nature 430: 887-891.
20. Graner A, Bauer E (1993) RFLP mapping of the rym4 virus resistance gene in barley. Theor Appl Genet 86: 689-693.
21. Sutton T, Baumann U, Hayes J, Collins NC, Shi B-J, et al. (2007) Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 318: 1446-1449.
22. Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57-63.
23. 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. Nat Genet 38: 203-208.
24. Malosetti M, van der Linden CG, Vosman B, van Eeuwijk FA (2007) A mixed-model approach to association mapping using pedigree information with an illustration of resistance to Phytophthora infestans in potato. Genetics 175: 879-889.
25. Tanksley SD, McCouch SR (1997) Seed banks and molecular maps: Unlocking genetic potential from the wild. Science 277: 1063-1066.
26. Hamblin MT, Buckler ES, Jannink JL (2011) Population genetics of genomics-based crop improvement methods. Trends Genet 27: 98-106.
27. Waugh R, Jannink JL, Muehlbauer GJ, Ramsay L (2009) The emergence of whole genome association scans in barley. Curr Opin Plant Biol 12: 218-222.
28. Hamblin MT, Close TJ, Bhat PR, Chao SM, Kling JG, et al. (2010) Population structure and linkage disequilibrium in US barley germplasm: Implications for association mapping. Crop Sci 50: 556-566.
29. Mezaka I, Legzdina L, Waugh R, Close T, Rostoks N (2013) Genetic Diversity in Latvian spring barley association mapping population. In: Zhang G, Li C, Liu X, editors. Advance in Barley Sciences. Springer Netherlands. pp. 25-35.
30. Tondelli A, Xu X, Moragues M, Sharma R, Schnaithmann F, et al. (2013) Structural and temporal variation in genetic diversity of European spring two-row barley cultivars and association mapping of quantitative traits. Plant Genome 6: 1-14.
31. Yahiaoui S, Igartua E, Moralejo M, Ramsay L, Molina-Cano JL, et al. (2008) Patterns of genetic and eco-geographical diversity in Spanish barleys. Theor Appl Genet 116: 271-282.
32. Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA, Haseneyer G, et al. (2012) Genome-wide association studies for agronomical traits in a world-wide spring barley collection. BMC Plant Biol 12: 16.
33. Muñoz-Amatriaín M, Cuesta-Marcos A, Endelman JB, Comadran J, Bonman JM, et al. (2014) The USDA barley core collection: genetic diversity, population structure, and potential for genome-wide association studies. PLOS One 9: e94688.
34. Russell JR, Booth A, Fuller JD, Baum M, Ceccarelli S, et al. (2003) Patterns of polymorphism detected in the chloroplast and nuclear genomes of barley landraces sampled from Syria and Jordan. Theor Appl Genet 107: 413-421.
35. Pandey M, Wagner C, Friedt W, Ordon F (2006) Genetic relatedness and population differentiation of Himalayan hulless barley (Hordeum vulgare L.) landraces inferred with SSRs. Theor Appl Genet 113: 715-729.
36. Gong X, Westcott S, Li C, Yan G, Lance R, et al. (2009) Comparative analysis of genetic diversity between Qinghai-Tibetan wild and Chinese landrace barley. Genome 52: 849-861.
37. Comadran J, Russell JR, Booth A, Pswarayi A, Ceccarelli S, et al. (2011) Mixed model association scans of multi-environmental trial data reveal major loci controlling yield and yield related traits in Hordeum vulgare in Mediterranean environments. Theor Appl Genet 122: 1363-1373.
38. Rodriguez M, Rau D, O'Sullivan D, Brown AHD, Papa R, et al. (2012) Genetic structure and linkage disequilibrium in landrace populations of barley in Sardinia. Theor Appl Genet 125: 171-184.
39. Jilal A, Grando S, Henry RJ, Lee LS, Rice N, et al. (2008) Genetic diversity of ICARDA's worldwide barley landrace collection. Genet Resour Crop Evol 55: 1221-1230.
40. Mansfeld R (1950) Das morphologische System der Saatgerste, Hordeum vulgare L. s. l. Der Züchter 20: 8-24.
41. Russell J, Dawson IK, Flavell AJ, Steffenson B, Weltzien E, et al. (2011) Analysis of>1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome-level differences in diversity around domestication genes. New Phytol 191: 564-578.
42. Lehmann CO, Mansfeld R (1957) Zur Technik der Sortimentserhaltung. Die Kultpfl 5: 108-138.
43. Sackville Hamilton NR, Engels JMM, van Hintum T, Koo B, Smale M (2002) Accession management: combining or splitting accessions as a tool to improve germplasm management efficiency. IPGRI Tech.
44. Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106: 411-422.
45. Stein N, Prasad M, Scholz U, Thiel T, Zhang H, et al. (2007) A 1,000-loci transcript map of the barley genome: new anchoring points for integrative grass genomics. Theor Appl Genet 114: 823-839.
46. Haseneyer G, Stracke S, Paul C, Einfeldt C, Broda A, et al. (2010) Population structure and phenotypic variation of a spring barley world collection set up for association studies. Plant Breed 129: 271-279.
47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus Genotype Data. Genetics 155: 945-959.
48. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype gata: Linked loci and correlated cllele Frequencies. Genetics 164: 1567-1587.
49. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14: 2611-2620.
50. Jakob SS, Rodder D, Engler JO, Shaaf S, Ozkan H, et al. (2014) Evolutionary history of wild barley (Hordeum vulgare subsp. spontaneum) analyzed using multilocus sequence data and paleodistribution modeling. Genome Biol Evol 6: 685-702.
51. Hammer Ø, Harper DAT, Ryan PD (2001) Paleontological statistics software package for education and data analysis. Palaeontol Electron 4: 9.
52. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
53. Liu K, Muse S V (2005) PowerMarker: An integrated analysis environment for genetic marker analysis. Bioinformatics 21: 2128-2129.
54. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32: 314-331.
55. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564-567.
56. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the analysis of population structure. Evolution (NY) 38: 1358-1370.
57. Goudet J (1995) FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics. J Hered 86: 485-486.
58. Leberg PL (2002) Estimating allelic richness: Effects of sample size and bottlenecks. Mol Ecol 11: 2445-2449.
59. Weir BS (1996) Genetic data analysis II: Methods for discrete population genetic data. 376 p.
60. Chakraborty R, Jin L (1993) Determination of relatedness between individuals using DNA fingerprinting. Hum Biol an Int Rec Res 65: 875-895.
61. Escudero A (2003) Spatial analysis of genetic diversity as a tool for plant conservation. Biol Conserv 113: 351-365.
62. Rosenberg MS, Anderson CD (2011) PASSaGE: Pattern Analysis, Spatial Statistics and Geographic Exegesis. Version 2. Methods Ecol Evol 2: 229-232.
63. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of Köppen-Geiger climate classification. Meteorol Zeitschrift 15: 259-263.
64. Glaszmann JC, Kilian B, Upadhyaya HD, Varshney RK (2010) Accessing genetic diversity for crop improvement. Curr Opin Plant Biol 13: 167-173.
65. Acquaah G (2012) Principles of plant genetics and breeding, 2nd Edition. Wiley-Blackwell. 758 p.
66. Gouesnard B (2001) MSTRAT: An algorithm for building germplasm core collections by maximizing allelic or phenotypic richness. J Hered 92: 93-94.
67. Schoen DJ, Brown AH (1993) Conservation of allelic richness in wild crop relatives is aided by assessment of genetic markers. Proc Natl Acad Sci U S A 90: 10623-10627.
68. Keilwagen J, Kilian B, Ozkan H, Babben S, Perovic D, et al. (2014) Separating the wheat from the chaff - a strategy to utilize plant genetic resources from ex-situ genebanks. Sci Rep 4: 5231.
69. Backes G, Orabi J, Wolday A, Yahyaoui A, Jahoor A (2009) High genetic diversity revealed in barley (Hordeum vulgare) collected from small-scale farmer's fields in Eritrea. Genet Resour Crop Evol 56: 85-97.
70. Leino MW, Hagenblad J (2010) Nineteenth century seeds reveal the population genetics of landrace barley (Hordeum vulgare). Mol Biol Evol 27: 964-973.
71. Varshney RK, Baum M, Guo P, Grando S, Ceccarelli S, et al. (2010) Features of SNP and SSR diversity in a set of ICARDA barley germplasm collection. Mol Breed 26: 229-242.
72. Bellucci E, Bitocchi E, Rau D, Nanni L, Ferradini N, et al. (2013) Population structure of barley landrace populations and gene-flow with modern varieties. PLOS ONE 8: e83891
73. Malysheva-Otto LV, Ganal MW, Roder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genet 7: 6.
74. Long NV, Dolstra O, Malosetti M, Kilian B, Graner A, et al. (2013) Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 126: 2335-2351.
75. Abdel-Ghani AH, Neumann K, Wabila C, Sharma R, Dhanagond S, et al. (2014) Diversity of germination and seedling traits in a spring barley (Hordeum vulgare L.) collection under drought simulated conditions. Genet Resour Crop Evol. DOI 10.1007/s10722-014-0152-z
76. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLOS Genet 2: 2074-2093.
77. Castillo A, Dorado G, Feuillet C, Sourdille P, Hernandez P (2010) Genetic structure and ecogeographical adaptation in wild barley (Hordeum chilense Roemer et Schultes) as revealed by microsatellite markers. BMC Plant Biol 10: 266.
78. Cuesta-Marcos A, Szucs P, Close TJ, Filichkin T, Muehlbauer GJ, et al. (2010) Genome-wide SNPs and re-sequencing of growth habit and inflorescence genes in barley: implications for association mapping in germplasm arrays varying in size and structure. BMC Genomics 11: 707. doi:10.1186/1471-2164-11-707
79. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The Pseudo-Response Regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310: 1031-1034.
80. Comadran J, Kilian B, Russell J, Ramsay L, Stein N, et al. (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44: 1388-1392.
81. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, et al. (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100: 6263-6268.
82. Szucs P, Skinner JS, Karsai I, Cuesta-Marcos A, Haggard KG, et al. (2007) Validation of the VRN-H2/ VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity. Mol Genet Genomics 277: 249-261.
83. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, et al. (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303: 1640-1644.
84. Yan L, Fu D, Li C, Blechl A, Tranquilli G, et al. (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103: 19581-19586.
85. Stracke S, Haseneyer G, Veyrieras JB, Geiger HH, Sauer S, et al. (2009) Association mapping reveals gene action and interactions in the determination of flowering time in barley. Theor Appl Genet 118: 259-273.
86. Dubcovsky J, Chen C, Yan L (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15: 395-407.
87. Tanto Hadado T, Rau D, Bitocchi E, Papa R (2010) Adaptation and diversity along an altitudinal gradient in Ethiopian barley (Hordeum vulgare L.) landraces revealed by molecular analysis. BMC Plant Biol 10: 121.
88. Alderman PD, Quilligan E, Asseng S, Ewert F, Reynolds MP, editors (2013) Proceedings of the workshop Modeling Wheat Response to High Temperature. CIMMYT, Mexico June 19-21.
89. Semenov MA, Stratonovitch P (2013) Designing high-yielding wheat ideotypes for a changing climate. Food Energy Secur 2: 185-196.
90. Allard RW, Zhang Q, Saghai Maroof MA, Muona OM (1992) Evolution of multilocus genetic structure in an experimental barley population. Genetics 131: 957-969.
91. Bjørnstad A, Demissie A, Kilian A, Kleinhofs A (1997) The distinctness and diversity of Ethiopian barleys. Theor Appl Genet 94: 514-521.
92. Orabi J, Backes G, Wolday A, Yahyaoui A, Jahoor A (2007) The Horn of Africa as a centre of barley diversification and a potential domestication site. Theor Appl Genet 114: 1117-1127.
93. Igartua E, Moralejo M, Casas AM, Torres L, Molina-Cano JL (2013) Whole-genome analysis with SNPs from BOPA1 shows clearly defined groupings of Western Mediterranean, Ethiopian, and Fertile Crescent barleys. Genet Resour Crop Evol 60: 251-264.
94. Allard RW, Kahler AL, Weir BS (1972) The effect of selection on esterase allozymes in a barley population. Genetics 72: 489-503.
95. Schiemann E (1939) Gedanken zur Genzentrentheorie Vavilovs. Naturwissenschaften 27: 394-401.
96. Schiemann E (1951) New results on the history of cultivated cereals. J Hered 5: 305-320.
97. Bjørnstad A, Abay F (2010) Multivariate patterns of diversity in Ethiopian barleys. Crop Sci 50: 1579.
98. Tsehaye Y, Bjørnstad A˚, Abay F (2012) Phenotypic and genotypic variation in flowering time in Ethiopian barleys. Euphytica 188: 309-323.
99. Taketa S, Kikuchi S, Awayama T, Yamamoto S, Ichii M, et al. (2004) Monophyletic origin of naked barley inferred from molecular analyses of a marker closely linked to the naked caryopsis gene (nud). Theor Appl Genet 108: 1236-1242.
100. Pourkheirandish M, Komatsuda T (2007) The importance of barley genetics and domestication in a global perspective. Ann Bot 100: 999-1008.
101. Taketa S, Amano S, Tsujino Y, Sato T, Saisho D, et al. (2008) Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway. Proc Natl Acad Sci USA 105: 4062-4067.
102. Schiemann E (1943) Entstehung der Kulturpflanzen. Ergebn Biol 19: 409-452.
103. Kilian B, Knüpffer H, Hammer K (2014) Elisabeth Schiemann (1881-1972): a pioneer of crop plant research, with special reference to cereal phylogeny. Genet Resour Crop Evol 61: 89-106.
104. Bhullar NK, Street K, Mackay M, Yahiaoui N, Keller B (2009) Unlocking wheat genetic resources for the molecular identification of previously undescribed functional alleles at the Pm3 resistance locus. Proc Natl Acad Sci USA 106: 9519-9524.
105. Bhullar NK, Zhang Z, Wicker T, Keller B (2010) Wheat gene bank accessions as a source of new alleles of the powdery mildew resistance gene Pm3: a large scale allele mining project. BMC Plant Biol 10: 88.
106. B, Graner A (2012) NGS technologies for analyzing germplasm diversity in genebanks. Brief Funct Genomics 11: 38-50.
107. Mayer KFX, Waugh R, Brown JWS, Schulman A, Langridge P, et al. (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491: 711-716.
108. Mascher M, Richmond TA, Gerhardt DJ, Himmelbach A, Clissold L, et al. (2013) Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J 76: 494-505.
109. Varshney RK, Terauchi R, McCouch SR (2014) Harvesting the promising fruits of genomics: applying genome sequencing technologies to crop breeding. PLOS Biol 12: e1001883.