High-throughput single nucleotide polymorphism genotyping reveals population structure and genetic diversity of tall fescue (Festuca arundinacea) populations
Zeynab Shahabzadeh A , Reza Darvishzadeh A * , Reza Mohammadi B , Morad Jafari A and Hadi Alipour A *A Department of Plant Production and Genetics, Faculty of Agriculture, Urmia University, Urmia, Iran.
B Branch for Northwest & West Region, Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO), Tabriz, Iran.
Handling Editor: Rajeev Varshney
Crop & Pasture Science 73(9) 1070-1084 https://doi.org/10.1071/CP21311
Submitted: 4 May 2021 Accepted: 2 February 2022 Published: 28 March 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Single nucleotide polymorphisms (SNPs) are the most abundant form of genetic variation in eukaryote genomes and may be useful for selection of genetically distant parents for crossing in breeding programs. In this study, genome-wide SNPs of tall fescue (Festuca arundinacea Schreb.) were genotyped by using double-digest restriction-site-associated DNA sequencing to determine the genetic variation and differentiation among and within forage, turf and hybrid populations. After filtering, 16 036 SNPs were used to investigate genetic diversity and for structure analysis. SNP markers clearly differentiated the populations from each other. However, the hybrid population had a higher genetic similarity with the turf population than with the forage population. The results were confirmed by genetic differentiation (fixation index, Fst) and gene flow (Nm) statistics, so that low Fst and high Nm were observed between turf and hybrid groups, indicating less genetic distance and a high similarity between them. Based on the results of the weighted pair group method with arithmetic mean clustering, discriminant analysis of principal components and analysis of molecular variance, greater genetic differentiations were found among diverse turf, forage and hybrid populations, especially between turf and forage ones. In conclusion, numerous informative SNPs, natural allelic diversity-led domestication patterns, basic genetic variation statistics (e.g. Fst and heterozygosity) and population structures have multidimensional applicability for tall fescue genomics-assisted breeding.
Keywords: AMOVA, ddRAD, fixation index, genetic differentiation, gene flow, genome-wide SNPs, structure, tall fescue.
References
Agrama HA, Yan WG, Lee F, Fjellstrom R, Chen MH, Jia M, McClung A (2009) Genetic assessment of a mini-core subset developed from the USDA rice genebank. Crop Science 49, 1336–1346.| Genetic assessment of a mini-core subset developed from the USDA rice genebank.Crossref | GoogleScholarGoogle Scholar |
Akhunov E, Nicolet C, Dvorak J (2009) Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay. Theoretical and Applied Genetics 119, 507–517.
| Single nucleotide polymorphism genotyping in polyploid wheat with the Illumina GoldenGate assay.Crossref | GoogleScholarGoogle Scholar | 19449174PubMed |
Alipour H, Bihamta MR, Mohammadi V, Peyghambari SA, Bai G, Zhang G (2017) Genotyping-by-sequencing (GBS) revealed molecular genetic diversity of Iranian wheat landraces and cultivars. Frontiers in Plant Science 8, 1293
| Genotyping-by-sequencing (GBS) revealed molecular genetic diversity of Iranian wheat landraces and cultivars.Crossref | GoogleScholarGoogle Scholar | 28912785PubMed |
Allen AM, Winfield MO, Burridge AJ, Downie RC, Benbow HR, Barker GL, Wilkinson PA, Coghill J, Waterfall C, Davassi A, Scopes G, Pirani A, Webster T, Brew F, Bloor C, Griffiths S, Bentley AR, Alda M, Jack P, Phillips AL, Edwards KJ (2017) Characterization of a wheat breeders’ array suitable for high-throughput SNP genotyping of global accessions of hexaploid bread wheat (Triticum aestivum). Plant Biotechnology Journal 15, 390–401.
| Characterization of a wheat breeders’ array suitable for high-throughput SNP genotyping of global accessions of hexaploid bread wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 27627182PubMed |
Amini F, Mirlohi A, Majidi MM, Shojaiefar S, Kölliker R (2011) Improved polycross breeding of tall fescue through marker-based parental selection. Plant Breeding 130, 701–707.
| Improved polycross breeding of tall fescue through marker-based parental selection.Crossref | GoogleScholarGoogle Scholar |
Asmamaw M, Keneni G, Tesfaye K (2019) Genetic diversity of Ethiopian durum wheat (Triticum durum Desf.) landrace collections as reveled by SSR markers. Advances in Crop Science and Technology 7, 413
| Genetic diversity of Ethiopian durum wheat (Triticum durum Desf.) landrace collections as reveled by SSR markers.Crossref | GoogleScholarGoogle Scholar |
Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3, e3376
| Rapid SNP discovery and genetic mapping using sequenced RAD markers.Crossref | GoogleScholarGoogle Scholar | 18852878PubMed |
Benfriha H, Mefti M, Robbins M, Thorsted K, Bushman S (2021) Molecular characterization of Algerian populations of cocksfoot and tall fescue: ploidy level determination and genetic diversity analysis. Grassland Science 67, 167–176.
| Molecular characterization of Algerian populations of cocksfoot and tall fescue: ploidy level determination and genetic diversity analysis.Crossref | GoogleScholarGoogle Scholar |
Berkman PJ, Lai K, Lorenc MT, Edwards D (2012) Next-generation sequencing applications for wheat crop improvement. American Journal of Botany 99, 365–371.
| Next-generation sequencing applications for wheat crop improvement.Crossref | GoogleScholarGoogle Scholar | 22268223PubMed |
Blair MW, Cortés AJ, Penmetsa RV, Farmer A, Carrasquilla-Garcia N, Cook DR (2013) A high-throughput SNP marker system for parental polymorphism screening, and diversity analysis in common bean (Phaseolus vulgaris L.). Theoretical and Applied Genetics 126, 535–548.
| A high-throughput SNP marker system for parental polymorphism screening, and diversity analysis in common bean (Phaseolus vulgaris L.).Crossref | GoogleScholarGoogle Scholar | 23124389PubMed |
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.
| Trimmomatic: a flexible trimmer for Illumina sequence data.Crossref | GoogleScholarGoogle Scholar | 24695404PubMed |
Bundock PC, Eliott FG, Ablett G, Benson AD, Casu RE, Aitken KS, Henry RJ (2009) Targeted single nucleotide polymorphism (SNP) discovery in a highly polyploid plant species using 454 sequencing. Plant Biotechnology Journal 7, 347–354.
| Targeted single nucleotide polymorphism (SNP) discovery in a highly polyploid plant species using 454 sequencing.Crossref | GoogleScholarGoogle Scholar | 19386042PubMed |
Byers DL, Meagher TR (1992) Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68, 353–359.
| Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility.Crossref | GoogleScholarGoogle Scholar |
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Molecular Ecology 22, 3124–3140.
| Stacks: an analysis tool set for population genomics.Crossref | GoogleScholarGoogle Scholar | 23701397PubMed |
Cavanagh CR, Chao S, Wang S, Huang BE, Stephen S, Kiani S, Forrest K, Saintenac C, Brown-Guedira GL, Akhunova A, See D, Bai G, Pumphrey M, Tomar L, Wong D, Kong S, Reynolds M, da Silva ML, Bockelman H, Talbert L, Anderson JA, Dreisigacker S, Baenziger S, Carter A, Korzun V, Morrell PL, Dubcovsky J, Morell MK, Sorrells ME, Hayden MJ, Akhunov E (2013) Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proceedings of the National Academy of Sciences of the United States of America 110, 8057–8062.
| Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars.Crossref | GoogleScholarGoogle Scholar | 23630259PubMed |
Chang LY, Toghiani S, Hay EH, Aggrey SE, Rekaya R (2019) A weighted genomic relationship matrix based on fixation index Fst prioritized SNPs for genomic selection. Genes 10, 922
| A weighted genomic relationship matrix based on fixation index Fst prioritized SNPs for genomic selection.Crossref | GoogleScholarGoogle Scholar |
Chapman SC (2008) Use of crop models to understand genotype by environment interactions for drought in real-world and simulated plant breeding trials. Euphytica 161, 195–208.
| Use of crop models to understand genotype by environment interactions for drought in real-world and simulated plant breeding trials.Crossref | GoogleScholarGoogle Scholar |
Chong Z, Ruan J, Wu CI (2012) Rainbow: an integrated tool for efficient clustering and assembling RAD-seq reads. Bioinformatics 28, 2732–2737.
| Rainbow: an integrated tool for efficient clustering and assembling RAD-seq reads.Crossref | GoogleScholarGoogle Scholar | 22942077PubMed |
Cuyeu R, Rosso B, Pagano E, Soto G, Fox R, Ayub ND (2013) Genetic diversity in a world germplasm collection of tall fescue. Genetics and Molecular Biology 36, 237–242.
| Genetic diversity in a world germplasm collection of tall fescue.Crossref | GoogleScholarGoogle Scholar | 23885206PubMed |
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R (2011) The variant call format and VCFtools. Bioinformatics 27, 2156–2158.
| The variant call format and VCFtools.Crossref | GoogleScholarGoogle Scholar | 21653522PubMed |
Ebrahimiyan M, Majidi MM, Mirlohi A, Noroozi A (2013) Physiological traits related to drought tolerance in tall fescue. Euphytica 190, 401–414.
| Physiological traits related to drought tolerance in tall fescue.Crossref | GoogleScholarGoogle Scholar |
Edae EA, Byrne PF, Haley SD, Lopes MS, Reynolds MP (2014) Genome-wide association mapping of yield and yield components of spring wheat under contrasting moisture regimes. Theoretical and Applied Genetics 127, 791–807.
| Genome-wide association mapping of yield and yield components of spring wheat under contrasting moisture regimes.Crossref | GoogleScholarGoogle Scholar | 24408378PubMed |
Edae EA, Bowden RL, Poland J (2015) Application of population sequencing (POPSEQ) for ordering and imputing genotyping-by-sequencing markers in hexaploid wheat. G3: Genes, Genomes, Genetics 5, 2547–2553.
| Application of population sequencing (POPSEQ) for ordering and imputing genotyping-by-sequencing markers in hexaploid wheat.Crossref | GoogleScholarGoogle Scholar |
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.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar | 15969739PubMed |
Feltus FA, Wan J, Schulze SR, Estill JC, Jiang N, Paterson AH (2004) An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments. Genome Research 14, 1812–1819.
| An SNP resource for rice genetics and breeding based on subspecies indica and japonica genome alignments.Crossref | GoogleScholarGoogle Scholar | 15342564PubMed |
Franchini P, Monné Parera D, Kautt AF, Meyer A (2017) quaddRAD: a new high-multiplexing and PCR duplicate removal ddRAD protocol produces novel evolutionary insights in a nonradiating cichlid lineage. Molecular Ecology 26, 2783–2795.
| quaddRAD: a new high-multiplexing and PCR duplicate removal ddRAD protocol produces novel evolutionary insights in a nonradiating cichlid lineage.Crossref | GoogleScholarGoogle Scholar | 28247584PubMed |
Goudet J (2005) Hierfstat, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes 5, 184–186.
| Hierfstat, a package for R to compute and test hierarchical F-statistics.Crossref | GoogleScholarGoogle Scholar |
Habier D, Fernando RL, Kizilkaya K, Garrick DJ (2011) Extension of the bayesian alphabet for genomic selection. BMC Bioinformatics 12, 186
| Extension of the bayesian alphabet for genomic selection.Crossref | GoogleScholarGoogle Scholar | 21605355PubMed |
Halász J, Pedryc A, Hegedűs A (2007) Origin and dissemination of the pollen-part mutated SC haplotype which confers self-compatibility in apricot (Prunus armeniaca). New Phytologist 176, 792–803.
| Origin and dissemination of the pollen-part mutated SC haplotype which confers self-compatibility in apricot (Prunus armeniaca).Crossref | GoogleScholarGoogle Scholar |
Hand ML, Cogan NO, Forster JW (2012) Genome-wide SNP identification in multiple morphotypes of allohexaploid tall fescue (Festuca arundinacea Schreb.). BMC Genomics 13, 219
| Genome-wide SNP identification in multiple morphotypes of allohexaploid tall fescue (Festuca arundinacea Schreb.).Crossref | GoogleScholarGoogle Scholar | 22672128PubMed |
Hasbún R, González J, Iturra C, Fuentes G, Alarcón D, Ruiz E (2016) Using genome-wide SNP discovery and genotyping to reveal the main source of population differentiation in Nothofagus dombeyi (Mirb.) Oerst. in Chile. International Journal of Genomics 2016, 3654093
| Using genome-wide SNP discovery and genotyping to reveal the main source of population differentiation in Nothofagus dombeyi (Mirb.) Oerst. in Chile.Crossref | GoogleScholarGoogle Scholar | 27446942PubMed |
Huo N, Zhang S, Zhu T, Dong L, Wang Y, Mohr T, Hu T, Liu Z, Dvorak J, Luo MC, Wang D, Lee JY, Altenbach S, Gu YQ (2018) Gene duplication and evolution dynamics in the homeologous regions harboring multiple prolamin and resistance gene families in hexaploid wheat. Frontiers in Plant Science 9, 673
| Gene duplication and evolution dynamics in the homeologous regions harboring multiple prolamin and resistance gene families in hexaploid wheat.Crossref | GoogleScholarGoogle Scholar | 29875781PubMed |
Iorizzo M, Senalik DA, Grzebelus D, Bowman M, Cavagnaro PF, Matvienko M, Ashrafi H, Van Deynze A, Simon PW (2011) De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity. BMC Genomics 12, 389
| De novo assembly and characterization of the carrot transcriptome reveals novel genes, new markers, and genetic diversity.Crossref | GoogleScholarGoogle Scholar | 21810238PubMed |
Ishikawa G, Saito M, Tanaka T, Katayose Y, Kanamori H, Kurita K, Nakamura T (2018) An efficient approach for the development of genome-specific markers in allohexaploid wheat (Triticum aestivum L.) and its application in the construction of high-density linkage maps of the D genome. DNA Research 25, 317–326.
| An efficient approach for the development of genome-specific markers in allohexaploid wheat (Triticum aestivum L.) and its application in the construction of high-density linkage maps of the D genome.Crossref | GoogleScholarGoogle Scholar |
(2014) A chromosome-based draft sequence of the hexaploid bread wheat Triticum aestivum genome. Science 345, 1251788
| A chromosome-based draft sequence of the hexaploid bread wheat Triticum aestivum genome.Crossref | GoogleScholarGoogle Scholar | 25035500PubMed |
Jia J, Zhao S, Kong X, et al. (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496, 91–95.
| Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation.Crossref | GoogleScholarGoogle Scholar | 23535592PubMed |
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11, 94
| Discriminant analysis of principal components: a new method for the analysis of genetically structured populations.Crossref | GoogleScholarGoogle Scholar | 20950446PubMed |
Jost L (2008) G(ST) and its relatives do not measure differentiation. Molecular Ecology 17, 4015–4026.
| G(ST) and its relatives do not measure differentiation.Crossref | GoogleScholarGoogle Scholar | 19238703PubMed |
Kaljund K, Jaaska V (2010) No loss of genetic diversity in small and isolated populations of Medicago sativa subsp. falcata. Biochemical Systematics and Ecology 38, 510–520.
| No loss of genetic diversity in small and isolated populations of Medicago sativa subsp. falcata.Crossref | GoogleScholarGoogle Scholar |
Kaur S, Francki MG, Forster JW (2012) Identification, characterization and interpretation of single-nucleotide sequence variation in allopolyploid crop species. Plant Biotechnology Journal 10, 125–138.
| Identification, characterization and interpretation of single-nucleotide sequence variation in allopolyploid crop species.Crossref | GoogleScholarGoogle Scholar | 21831136PubMed |
Legati A, Reyes A, Nasca A, Invernizzi F, Lamantea E, Tiranti V, Garavaglia B, Lamperti C, Ardissone A, Moroni I, Robinson A, Ghezzi D, Zeviani M (2016) New genes and pathomechanisms in mitochondrial disorders unraveled by NGS technologies. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1857, 1326–1335.
| New genes and pathomechanisms in mitochondrial disorders unraveled by NGS technologies.Crossref | GoogleScholarGoogle Scholar |
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659.
| Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences.Crossref | GoogleScholarGoogle Scholar | 16731699PubMed |
Li R, Fan W, Tian G, et al. (2010) The sequence and de novo assembly of the giant panda genome. Nature 463, 311–317.
| The sequence and de novo assembly of the giant panda genome.Crossref | GoogleScholarGoogle Scholar | 20010809PubMed |
Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21, 2128–2129.
| PowerMarker: an integrated analysis environment for genetic marker analysis.Crossref | GoogleScholarGoogle Scholar | 15705655PubMed |
Lorenc MT, Hayashi S, Stiller J, Lee H, Manoli S, Ruperao P, Visendi P, Berkman PJ, Lai K, Batley J, Edwards D (2012) Discovery of single nucleotide polymorphisms in complex genomes using SGSautoSNP. Biology 1, 370–382.
| Discovery of single nucleotide polymorphisms in complex genomes using SGSautoSNP.Crossref | GoogleScholarGoogle Scholar | 24832230PubMed |
Majidi MM, Mirlohi A, Amini F (2009) Genetic variation, heritability and correlations of agro-morphological traits in tall fescue (Festuca arundinacea Schreb.). Euphytica 167, 323–331.
| Genetic variation, heritability and correlations of agro-morphological traits in tall fescue (Festuca arundinacea Schreb.).Crossref | GoogleScholarGoogle Scholar |
Mammadov JA, Chen W, Ren R, Pai R, Marchione W, Yalçin F, Witsenboer H, Greene TW, Thompson SA, Kumpatla SP (2010) Development of highly polymorphic SNP markers from the complexity reduced portion of maize [Zea mays L.] genome for use in marker-assisted breeding. Theoretical and Applied Genetics 121, 577–588.
| Development of highly polymorphic SNP markers from the complexity reduced portion of maize [Zea mays L.] genome for use in marker-assisted breeding.Crossref | GoogleScholarGoogle Scholar | 20401646PubMed |
Man D, Bao YX, Han LB, Zhang X (2011) Drought tolerance associated with proline and hormone metabolism in two tall fescue cultivars. HortScience 46, 1027–1032.
| Drought tolerance associated with proline and hormone metabolism in two tall fescue cultivars.Crossref | GoogleScholarGoogle Scholar |
Manickavelu A, Jighly A, Ban T (2014) Molecular evaluation of orphan Afghan common wheat (Triticum aestivum L.) landraces collected by Dr. Kihara using single nucleotide polymorphic markers. BMC Plant Biology 14, 320
| Molecular evaluation of orphan Afghan common wheat (Triticum aestivum L.) landraces collected by Dr. Kihara using single nucleotide polymorphic markers.Crossref | GoogleScholarGoogle Scholar | 25432399PubMed |
Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M Marcussen T, Sandve SR, Heier L, Spannagl M, Pfeifer M (2014) Ancient hybridizations among the ancestral genomes of bread wheat. Science 345, 1250092
| Ancient hybridizations among the ancestral genomes of bread wheat.Crossref | GoogleScholarGoogle Scholar | 25035499PubMed |
Matsuoka Y (2011) Evolution of polyploid Triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification. Plant and Cell Physiology 52, 750–764.
| Evolution of polyploid Triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification.Crossref | GoogleScholarGoogle Scholar | 21317146PubMed |
Matus IA, Hayes PM (2002) Genetic diversity in three groups of barley germplasm assessed by simple sequence repeats. Genome 45, 1095–1106.
| Genetic diversity in three groups of barley germplasm assessed by simple sequence repeats.Crossref | GoogleScholarGoogle Scholar | 12502254PubMed |
McCouch S (2004) Diversifying selection in plant breeding. PLoS Biology e347
| Diversifying selection in plant breeding.Crossref | GoogleScholarGoogle Scholar |
Nasu S, Suzuki J, Ohta R, Hasegawa K, Yui R, Kitazawa N, Monna L, Minobe Y (2002) Search for and analysis of single nucleotide polymorphisms (SNPs) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers. DNA Research 9, 163–171.
| Search for and analysis of single nucleotide polymorphisms (SNPs) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers.Crossref | GoogleScholarGoogle Scholar | 12465716PubMed |
Novembre J (2016) Pritchard, Stephens, and Donnelly on population structure. Genetics 204, 391–393.
| Pritchard, Stephens, and Donnelly on population structure.Crossref | GoogleScholarGoogle Scholar | 27729489PubMed |
Nugroho Y, Tanjung Z, Yono D, Mulyana A, Simbolon H, Ardi A, Yong Y, Utomo C, Liwang T (2019) Genome-wide SNP-discovery and analysis of genetic diversity in oil palm using double digest restriction site associated DNA sequencing. IOP Conference Series: Earth and Environmental Science 293, 012041
| Genome-wide SNP-discovery and analysis of genetic diversity in oil palm using double digest restriction site associated DNA sequencing.Crossref | GoogleScholarGoogle Scholar |
Paradis E (2010) pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420.
| pegas: an R package for population genetics with an integrated–modular approach.Crossref | GoogleScholarGoogle Scholar | 20080509PubMed |
Parchman TL, Gompert Z, Mudge J, Schilkey FD, Benkman CW, Buerkle CA (2012) Genome-wide association genetics of an adaptive trait in lodgepole pine. Molecular Ecology 21, 2991–3005.
| Genome-wide association genetics of an adaptive trait in lodgepole pine.Crossref | GoogleScholarGoogle Scholar | 22404645PubMed |
Pasam RK, Sharma R, Malosetti M, van Eeuwijk FA, Haseneyer G, Kilian B, Graner A (2012) Genome-wide association studies for agronomical traits in a world wide spring barley collection. BMC Plant Biology 12, 16
| Genome-wide association studies for agronomical traits in a world wide spring barley collection.Crossref | GoogleScholarGoogle Scholar | 22284310PubMed |
Paszkiewicz K, Studholme DJ (2010) De novo assembly of short sequence reads. Briefings in Bioinformatics 11, 457–472.
| De novo assembly of short sequence reads.Crossref | GoogleScholarGoogle Scholar | 20724458PubMed |
Perrier X, Jacquemoud-Collet J (2006) DARwin: dissimilarity analysis and representation for windows. Version 5, 158. CIRAD, Montpellier, France. Available at http://darwin.cirad.fr/darwin
Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135
| Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species.Crossref | GoogleScholarGoogle Scholar | 22675423PubMed |
Pickup M, Young AG (2008) Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae). Heredity 100, 268–274.
| Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae).Crossref | GoogleScholarGoogle Scholar | 17940547PubMed |
Puritz JB, Matz MV, Toonen RJ, Weber JN, Bolnick DI, Bird CE (2014) Demystifying the RAD fad. Molecular Ecology 23, 5937–5942.
| Demystifying the RAD fad.Crossref | GoogleScholarGoogle Scholar | 25319241PubMed |
Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes & Development 20, 3407–3425.
| A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Reyes-Valdés MH, Santacruz-Varela A, Martínez O, Simpson J, Hayano-Kanashiro C, Cortés-Romero C (2013) Analysis and optimization of bulk DNA sampling with binary scoring for germplasm characterization. PLoS ONE 8, e79936
| Analysis and optimization of bulk DNA sampling with binary scoring for germplasm characterization.Crossref | GoogleScholarGoogle Scholar | 24260321PubMed |
Ross-Ibarra J, Morrell PL, Gaut BS (2007) Plant domestication, a unique opportunity to identify the genetic basis of adaptation. Proceedings of the National Academy of Sciences of the United States of America 104, 8641–8648.
| Plant domestication, a unique opportunity to identify the genetic basis of adaptation.Crossref | GoogleScholarGoogle Scholar | 17494757PubMed |
Rowe HC, Renaut S, Guggisberg A (2011) RAD in the realm of next-generation sequencing technologies. Molecular Ecology 20, 3499–3502.
| RAD in the realm of next-generation sequencing technologies.Crossref | GoogleScholarGoogle Scholar | 21991593PubMed |
Roy Choudhury D, Singh N, Singh AK, Kumar S, Srinivasan K, Tyagi R, Ahmad A, Singh N, Singh R (2014) Analysis of genetic diversity and population structure of rice germplasm from north-eastern region of India and development of a core germplasm set. PLoS ONE 9, e113094
| Analysis of genetic diversity and population structure of rice germplasm from north-eastern region of India and development of a core germplasm set.Crossref | GoogleScholarGoogle Scholar | 25412256PubMed |
Salas-Lizana R, Oono R (2018) Double-digest RADseq loci using standard Illumina indexes improve deep and shallow phylogenetic resolution of Lophodermium, a widespread fungal endophyte of pine needles. Ecology and Evolution 8, 6638–6651.
| Double-digest RADseq loci using standard Illumina indexes improve deep and shallow phylogenetic resolution of Lophodermium, a widespread fungal endophyte of pine needles.Crossref | GoogleScholarGoogle Scholar | 30038763PubMed |
Salehi M, Salehi H, Niazi A, Ghobadi C (2014) Convergence of goals: phylogenetical, morphological, and physiological characterization of tolerance to drought stress in tall fescue (Festuca arundinacea Schreb.). Molecular Biotechnology 56, 248–257.
| Convergence of goals: phylogenetical, morphological, and physiological characterization of tolerance to drought stress in tall fescue (Festuca arundinacea Schreb.).Crossref | GoogleScholarGoogle Scholar | 24078217PubMed |
Shahabzadeh Z, Darvishzadeh R, Mohammadi R, Jafari M (2019) Isolation, characterization, and expression profiling of nucleoside diphosphate kinase gene from tall fescue (Festuca arundinaceous Schreb.) (FaNDPK) under salt stress. Plant Molecular Biology Reporter 38, 175–186.
| Isolation, characterization, and expression profiling of nucleoside diphosphate kinase gene from tall fescue (Festuca arundinaceous Schreb.) (FaNDPK) under salt stress.Crossref | GoogleScholarGoogle Scholar |
Shahabzadeh Z, Mohammadi R, Darvishzadeh R, Jaffari M (2020) Genetic structure and diversity analysis of tall fescue populations by EST-SSR and ISSR markers. Molecular Biology Reports 47, 655–669.
| Genetic structure and diversity analysis of tall fescue populations by EST-SSR and ISSR markers.Crossref | GoogleScholarGoogle Scholar | 31707600PubMed |
Shavrukov Y, Suchecki R, Eliby S, Abugalieva A, Kenebayev S, Langridge P (2014) Application of next-generation sequencing technology to study genetic diversity and identify unique SNP markers in bread wheat from Kazakhstan. BMC Plant Biology 14, 258
| Application of next-generation sequencing technology to study genetic diversity and identify unique SNP markers in bread wheat from Kazakhstan.Crossref | GoogleScholarGoogle Scholar | 25928569PubMed |
Sokal R, Sneath PH (1963) ‘Principles of numerical taxonomy’, (WH Friedman and Company: San Francisco, CA, USA)
Sun X, Xie Y, Bi Y, Liu J, Amombo E, Hu T, Fu J (2015) Comparative study of diversity based on heat tolerant-related morpho-physiological traits and molecular markers in tall fescue accessions. Scientific Reports 5, 18213
| Comparative study of diversity based on heat tolerant-related morpho-physiological traits and molecular markers in tall fescue accessions.Crossref | GoogleScholarGoogle Scholar | 26666506PubMed |
Toonen RJ, Puritz JB, Forsman ZH, Whitney JL, Fernandez-Silva I, Andrews KR, Bird CE (2013) ezRAD: a simplified method for genomic genotyping in non-model organisms. PeerJ 1, e203
| ezRAD: a simplified method for genomic genotyping in non-model organisms.Crossref | GoogleScholarGoogle Scholar | 24282669PubMed |
Trebbi D, Maccaferri M, de Heer P, Sørensen A, Giuliani S, Salvi S, Sanguineti MC, Massi A, van der Vossen EA, Tuberosa R (2011) High-throughput SNP discovery and genotyping in durum wheat (Triticum durum Desf.). Theoretical and Applied Genetics 123, 555–569.
| High-throughput SNP discovery and genotyping in durum wheat (Triticum durum Desf.).Crossref | GoogleScholarGoogle Scholar | 21611761PubMed |
Turuspekov Y, Ormanbekova D, Rsaliev A, Abugalieva S (2016) Genome-wide association study on stem rust resistance in Kazakh spring barley lines. BMC Plant Biology 16, 6
| Genome-wide association study on stem rust resistance in Kazakh spring barley lines.Crossref | GoogleScholarGoogle Scholar | 26821649PubMed |
Van Inghelandt D, Reif JC, Dhillon BS, Flament P, Melchinger AE (2011) Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theoretical and Applied Genetics 123, 11–20.
| Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm.Crossref | GoogleScholarGoogle Scholar | 21404061PubMed |
Würschum T, Langer SM, Longin CFH, Korzun V, Akhunov E, Ebmeyer E, Schachschneider R, Schacht J, Kazman E, Reif JC (2013) Population structure, genetic diversity and linkage disequilibrium in elite winter wheat assessed with SNP and SSR markers. Theoretical and Applied Genetics 126, 1477–1486.
| Population structure, genetic diversity and linkage disequilibrium in elite winter wheat assessed with SNP and SSR markers.Crossref | GoogleScholarGoogle Scholar | 23429904PubMed |
Xu P, Xu S, Wu X, Tao Y, Wang B, Wang S, Qin D, Lu Z, Li G (2014) Population genomic analyses from low-coverage RAD-Seq data: a case study on the non-model cucurbit bottle gourd. The Plant Journal 77, 430–442.
| Population genomic analyses from low-coverage RAD-Seq data: a case study on the non-model cucurbit bottle gourd.Crossref | GoogleScholarGoogle Scholar | 24320550PubMed |
Xu X, Sharma R, Tondelli A, Russell J, Comadran J, Schnaithmann F, Pillen K, Kilian B, Cattivelli L, Thomas WT (2018) Genome-wide association analysis of grain yield-associated traits in a pan-European barley cultivar collection. The Plant Genome 11, 170073
| Genome-wide association analysis of grain yield-associated traits in a pan-European barley cultivar collection.Crossref | GoogleScholarGoogle Scholar |
Young A, Miller C, Gregory E, Langston A (2000) Sporophytic self-incompatibility in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae). Australian Journal of Botany 48, 667–672.
| Sporophytic self-incompatibility in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae).Crossref | GoogleScholarGoogle Scholar |
Zhou Y, He ZH, Sui XX, Xia XC, Zhang XK, Zhang GS (2007) Genetic improvement of grain yield and associated traits in the northern China winter wheat region from 1960 to 2000. Crop Science 47, 245–253.
| Genetic improvement of grain yield and associated traits in the northern China winter wheat region from 1960 to 2000.Crossref | GoogleScholarGoogle Scholar |