Abstract
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Development of the first consensus genetic map of intermediate wheatgrass gives insight into the genome and tools for molecular breeding.
Abstract
Intermediate wheatgrass (Thinopyrum intermedium) has been identified as a candidate for domestication and improvement as a perennial grain, forage, and biofuel crop and is actively being improved by several breeding programs. To accelerate this process using genomics-assisted breeding, efficient genotyping methods and genetic marker reference maps are needed. We present here the first consensus genetic map for intermediate wheatgrass (IWG), which confirms the species’ allohexaploid nature (2n = 6x = 42) and homology to Triticeae genomes. Genotyping-by-sequencing was used to identify markers that fit expected segregation ratios and construct genetic maps for 13 heterogeneous parents of seven full-sib families. These maps were then integrated using a linear programming method to produce a consensus map with 21 linkage groups containing 10,029 markers, 3601 of which were present in at least two populations. Each of the 21 linkage groups contained between 237 and 683 markers, cumulatively covering 5061 cM (2891 cM––Kosambi) with an average distance of 0.5 cM between each pair of markers. Through mapping the sequence tags to the diploid (2n = 2x = 14) barley reference genome, we observed high colinearity and synteny between these genomes, with three homoeologous IWG chromosomes corresponding to each of the seven barley chromosomes, and mapped translocations that are known in the Triticeae. The consensus map is a valuable tool for wheat breeders to map important disease-resistance genes within intermediate wheatgrass. These genomic tools can help lead to rapid improvement of IWG and development of high-yielding cultivars of this perennial grain that would facilitate the sustainable intensification of agricultural systems.
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References
Armstead IP, Turner LB, Marshall AH, Humphreys MO, King IP, Thorogood D (2008) Identifying genetic components controlling fertility in the outcrossing grass species perennial ryegrass (Lolium perenne) by quantitative trait loci analysis and comparative genetics. New Phytol 178:559–571
Baumann U, Juttner J, Bian X, Langridge P (2000) Self-incompatibility in the grasses. Ann Bot 85:203–209
Buetow KH (1991) Influence of aberrant observations on high-resolution linkage analysis outcomes. Am J Hum Genet 49:985–994
Cattani D (2014) Perennial grains around the world: II. ASA, CSSA, & SSA, Long Beach
Chen Q, Conner RL, Laroche A, Thomas JB (1998) Genome analysis of Thinopyrum intermedium and Thinopyrum ponticum using genomic in situ hybridization. Genome 41:580–586
Cornish MA, Hayward MD, Lawrence MJ (1980) Self-incompatibility in ryegrass. Heredity 44:333–340
DeHaan LR, Wang S, Larson SR, Cattani DJ, Zhang X, Kantarski TR (2014) Current efforts to develop perennial wheat and domesticate Thinopyrum intermedium as a perennial grain. In: Batello C, Wade L, Cox S, Pogna N, Bozzini A, Choptiany J (eds) Perennial crops for food security proceedings of the FAO expert workshop. FAO of the UN, Rome, pp 72–89
Devos KM, Atkinson M, Chinoy C, Francis H, Harcourt R, Koebner R, Liu C, Masojć P, Xie D, Gale M (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85:673–680
Devos KM, Dubcovsky J, Dvořák J, Chinoy CN, Gale MD (1995) Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet 91:282–288
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379
Endelman JB, Plomion C (2014) LPmerge: an R package for merging genetic maps by linear programming. Bioinformatics 30:1623–1624
FAO (2014) Perennial crops for food security proceedings of the FAO expert workshop. FAO of the UN, Rome
Fedak G, Han F (2005) Characterization of derivatives from wheat-Thinopyrum wide crosses. Cytogenet Genome Res 109:360–367
Friebe B, Gill KS, Tuleen NA, Geill BS (1996) Transfer of wheat streak mosaic virus resistance from Agropyron intermedium into wheat. Crop Sci 36:857–861
Glover JD (2014) Perennial grains for food security in a changing world: gene to farm innovations. AAAS, Chicago
Hackett CA, Broadfoot LB (2002) Effects of genotyping errors, missing values and segregation distortion in molecular marker data on the construction of linkage maps. Heredity 90:33–38
Hao M, Luo J, Zhang L, Yuan Z, Zheng Y, Zhang H, Liu D (2013) In situ hybridization analysis indicates that 4AL–5AL–7BS translocation preceded subspecies differentiation of Triticum turgidum. Genome 56:303–305
Iehisa JCM, Ohno R, Kimura T, Enoki H, Nishimura S, Okamoto Y, Nasuda S, Takumi S (2014) A high-density genetic map with array-based markers facilitates structural and quantitative trait locus analyses of the common wheat genome. DNA Res 21:555–567
Jensen KB, Dewey DR, Zhang YF (1990) Mode of pollination of perennial species of the Triticeae in relation to genomically defined genera. Can J Plant Sci 70:215–225
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106
King I, Purdie K, Liu C, Reader S, Pittaway T, Orford S, Miller T (1994) Detection of interchromosomal translocations within the Triticeae by RFLP analysis. Genome 37:882–887
Klaas M, Yang B, Bosch M, Thorogood D, Manzanares C, Armstead IP, Franklin FCH, Barth S (2011) Progress towards elucidating the mechanisms of self-incompatibility in the grasses: further insights from studies in Lolium. Ann Bot 108:677–685
Larson SR, Kishii M, Tsujimoto H, Qi L, Chen P, Lazo GR, Jensen KB, Wang RRC (2012) Leymus EST linkage maps identify 4NsL–5NsL reciprocal translocation, wheat-Leymus chromosome introgressions, and functionally important gene loci. Theor Appl Genet 124:189–206
Li HJ, Wang XM (2009) Thinopyrum ponticum and Th. intermedium: the promising source of resistance to fungal and viral diseases of wheat. J Genet Genom 36(9):557–565
Li H, Vikram P, Singh RP, Kilian A, Carling J, Song J, Burgueno-Ferreira JA, Bhavani S, Huerta-Espino J, Payne T, Sehgal D, Wenzl P, Singh S (2015) A high density GBS map of bread wheat and its application for dissecting complex disease resistance traits. BMC Genom 16:1–15
Liu X, Guo L, You J, Liu X, He Y, Yuan J, Liu G, Feng Z (2010) Progress of segregation distortion in genetic mapping of plants. Res J Agron 4:78–83
Liu W, Seifers DL, Qi LL, Friebe B, Gill BS (2011) A compensating wheat–Thinopyrum intermedium robertsonian translocation conferring resistance to wheat streak mosaic virus and Triticum mosaic virus. Crop Sci 51:2382–2390
Liu W, Danilova T, Rouse M, Bowden R, Friebe B, Gill B, Pumphrey M (2013) Development and characterization of a compensating wheat-Thinopyrum intermedium Robertsonian translocation with Sr44 resistance to stem rust (Ug99). Theor Appl Genet 126:1167–1177
Lu H, Romero-Severson J, Bernardo R (2002) Chromosomal regions associated with segregation distortion in maize. Theor Appl Genet 105:622–628
Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9:e1003215
Luo L, Xu S (2003) Mapping viability loci using molecular markers. Heredity 90:459–467
Luo MC, Gu YQ, You FM, Deal KR, Ma Y, Hu Y, Huo N, Wang Y, Wang J, Chen S, Jorgensen CM, Zhang Y, McGuire PE, Pasternak S, Stein JC, Ware D, Kramer M, McCombie WR, Kianian SF, Martis MM, Mayer KFX, Sehgal SK, Li W, Gill BS, Bevan MW, Šimková H, Doležel J, Weining S, Lazo GR, Anderson OD, Dvorak J (2013) A 4-gigabase physical map unlocks the structure and evolution of the complex genome of Aegilops tauschii, the wheat D-genome progenitor. Proc Natl Acad Sci USA 110:7940–7945
Mahelka V, Kopecky D, Pastova L (2011) On the genome constitution and evolution of intermediate wheatgrass (Thonopyrum intermedium: Poaceae, Triticeae). BMC Evol Biol 11:127. doi:10.1186/1471-2148-11-127
Morgan MT (2001) Consequences of life history for inbreeding depression and mating system evolution in plants. Proc R Soc Lond B Biol 268:1817–1824
Ohm H, Anderson J (2007) Utilization and performance in wheat of yellow dwarf virus resistance transferred from Thinopyrum intermedium. In: Buck HT, Nisi JE, Salomón N (eds) Wheat production in stressed environments. Springer, Netherlands, pp 149–152
Pew J, Muir PH, Wang J, Frasier TR (2015) Related: an R package for analysing pairwise relatedness from codominant molecular markers. Mol Ecol Resour 15:557–561
Poland JA, Rife TW (2012) Genotyping-by-sequencing for plant breeding and genetics. Plant Genome 5:92–102
Poland JA, Brown PJ, Sorrells ME, Jannink JL (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PLoS One 7:e32253
R_Core_Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Robins JG (2010) Cool-season grasses produce more total biomass across the growing season than do warm-season grasses when managed with an applied irrigation gradient. Biomass Bioenergy 34:500–505
Runck BC, Kantar MB, Jordan NR, Anderson JA, Wyse DL, Eckberg JO, Barnes RJ, Lehman CL, DeHaan LR, Stupar RM, Sheaffer CC, Porter PM (2014) The reflective plant breeding paradigm: a robust system of germplasm development to support strategic diversification of agroecosystems. Crop Sci 54:1939–1948
Sharma H, Ohm H, Goulart L, Lister R, Appels R, Behlhabib O (1995) Introgression and characterization of barley yellow dwarf virus resistance from Thinopyrum intermedium into wheat. Genome 38:406–413
Tang S, Li Z, Jia X, Larkin PJ (2000) Genomic in situ hybridization (GISH) analyses of Thinopyrum intermedium, its partial amphiploid Zhong 5, and disease-resistant derivatives in wheat. Theor Appl Genet 100:344–352
Taylor DR, Ingvarsson PK (2003) Common features of segregation distortion in plants and animals. Genetica 117:27–35
The_International_Barley_Genome_Sequencing_Consortium (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491:711–716
Thorogood D, Kaiser WJ, Jones JG, Armstead I (2002) Self-incompatibility in ryegrass 12. Genotyping and mapping the S and Z loci of Lolium perenne L. Heredity 88:385–390
Tsvelev NN (1983) Grasses of the Soviet Union. Oxonian Press Pvt. Ltd., New Delhi, India, pp 196–298
Van Ooijen J (2006) JoinMap 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen
Vogel KP, Jensen KJ (2001) Adaptation of perennial Triticeae to the eastern central great plains. J Range Manag 54:674–679
Vogel KP, Arumuganathan K, Jensen KB (1999) Nuclear DNA content of perennial grasses of the Triticeae. Crop Sci 39:661–667
Wagoner P (1990) Perennial grain new use for intermediate wheatgrass. J Soil Water Conserv 45:81–82
Wagoner PS, Jurgen R (1990) Perennial grain development: past efforts and potential for the future. CRC Crit Rev Plant Sci 9:381–408
Wang RRC, Larson SR, Jensen KB, Bushman BS, DeHaan LR, Wang S, Yan X (2015) Genome evolution of intermediate wheatgrass as revealed by EST-SSR markers developed from its three progenitor diploid species. Genome 58:63–70
Yang J, Zhao X, Cheng K, Du H, Ouyang Y, Chen J, Qiu S, Huang J, Jiang Y, Jiang L, Ding J, Wang J, Xu C, Li X, Zhang Q (2012) A killer-protector system regulates both hybrid sterility and segregation distortion in rice. Science 337:1336–1340
Zhang X, Sallam A, Gao L, Kantarski T, Poland J, DeHaan LR, Wyse DL, Anderson JA (2016) Establishment and optimization of genomic selection to accelerate the domestication and improvement of intermediate wheatgrass. Plant Genome 9. doi:10.3835/plantgenome2015.07.0059
Zhou G, Zhang Q, Zhang XQ, Tan C, Li C (2015) Construction of high-density genetic map in barley through restriction-site associated DNA sequencing. PLoS One 10:e0133161
Acknowledgments
This work was supported by the Malone Family Land Preservation Foundation and The Land Institute through The Perennial Agriculture Project, The Initiative of Renewable Energy & The Environment, University of Minnesota, grant number RL_0015-12, and The Forever Green Initiative, University of Minnesota. The work at Kansas State University was done under the auspices of the Wheat Genetics Resource Center (WGRC) Industry/University Collaborative Research Center (I/UCRC) supported by NSF grant contract (IIP-1338897) and industry partners. Trevor Rife (Kansas State University) provided great assistance with combining the Ion and Illumina data and Jonathan Mitchell (University of Michigan/The Field Museum) provided assistance with early versions of the R scripts for custom genotype calling.
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Communicated by P. Heslop-Harrison.
Traci Kantarski, Steve Larson and Xiaofei Zhang contributed equally to the findings.
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Kantarski, T., Larson, S., Zhang, X. et al. Development of the first consensus genetic map of intermediate wheatgrass (Thinopyrum intermedium) using genotyping-by-sequencing. Theor Appl Genet 130, 137–150 (2017). https://doi.org/10.1007/s00122-016-2799-7
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DOI: https://doi.org/10.1007/s00122-016-2799-7