Abstract
The Philippines is situated in the geographic region regarded as the center of diversity of banana and its wild relatives (Musa spp.). It holds the most extensive collection of B-genome germplasm in the world along with A-genome groups and several natural hybrids with A- and B-genome combinations. Management of this germplasm resource has relied immensely on identification using local names and morphological characters, and the extent of genetic diversity of the collection has not been achieved with molecular markers. A high-throughput and reliable genotyping method for banana and its relatives will facilitate germplasm management and support breeding initiatives toward a marker-based approach. Here, we developed a 1 K SNP genotyping panel based on filtering of high-quality genome-wide SNPs from the Musa Germplasm Information System and used it to assess the genetic diversity and population structure of 183 accessions from a Musa spp. germplasm collection containing Philippine and foreign accessions. Targeted GBS using SeqSNP™ technology generated 70,376,284 next-generation sequencing (NGS) reads with an average effective target SNP coverage of 340 × . Bioinformatics pipeline revealed 971 polymorphic SNPs containing 76.9% homozygous calls, 23.1% heterozygous calls and 4% with missing data. A final set of 952 SNPs detected 2,092 alleles. Pairwise genetic distance varied from 0.0021 to 0.3325 with most pairs of accessions distinguished with 250 to 300 loci. The SNP panel was able to detect seven (k = 7) genetically differentiated groups and its composition through Principal Component Analysis (PCA) with k-means clustering algorithm and Discriminant Analysis of Principal Components (DAPC). Accession-specific SNPs were also identified. The 1 K SNP panel effectively distinguishes between genomic groups and provides relatively good resolution of genome-wide nucleotide diversity of Musa spp. This panel is recommended for low-density genotyping for application in marker-assisted breeding and germplasm management, and could be further enhanced to increase marker density for other applications like genetic association and genomic selection in bananas.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The raw next-generation sequencing datasets generated and/or analyzed during the current study are publicly available in the DDBJ/ENA/GenBank database under BioProject Accession number PRJNA850853.
References
Ahmad F, Megia R, Poerba YS (2014) Genetic diversity of Musa balbisiana Colla in Indonesia based on AFLP marker. HAYATI J Biosci 21:39–47. https://doi.org/10.4308/hjb.21.1.39
Bhattacharjee R, Agre P, Bauchet G et al (2020) Genotyping-by-Sequencing to Unlock Genetic Diversity and Population Structure in White Yam (Dioscorea rotundata Poir). Agronomy 10:1437. https://doi.org/10.3390/agronomy10091437
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
Dacumos CN, Lalusin AG, Namuco LO et al (2011) Diversity analysis of Philippine bananas using Simple sequence repeats markers. Philip J Crop Sci 36:1–10
Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158
Danecek P, Bonfield JK, Liddle J (2021) Twelve years of SAMtools and BCFtools. Gigascience 10(2):008
de Jesus ON, de Silva S et al (2013) Genetic diversity and population structure of Musa accessions in ex situ conservation. BMC Plant Biol 13:41. https://doi.org/10.1186/1471-2229-13-41
Dela Cruz FMR, Laude RP, Sandoval CMC et al (2020) Genetic characterization of Philippine Saba germplasm collection using microsatellite markers. Phil J Sci 149:169–197
Dela Cueva FM, Perez NAM, Benjamin AFA et al (2023) Resistance of Musa balbisiana accessions of the Philippines to banana bunchy top virus. Plant Dis. https://doi.org/10.1094/PDIS-10-22-2427-SC
Deperi SI, Tagliotti ME, Bedogni MC et al (2018) Discriminant analysis of principal components and pedigree assessment of genetic diversity and population structure in a tetraploid potato panel using SNPs. PLoS ONE 13:0194398. https://doi.org/10.1371/journal.pone.0194398
Doloiras-Laraño AD, Garcia RN, Sandoval CMC et al (2018) DNA fingerprinting and genetic diversity analysis of Philippine Saba and other cultivars of Musa balbisiana Colla using simple sequence repeat markers. Philipp J Crop Sci 43:1–11
Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:19379. https://doi.org/10.1371/journal.pone.0019379
Eltaher S, Sallam A, Belamkar V et al (2018) Genetic diversity and population structure of F3:6 Nebraska winter wheat genotypes using genotyping-by-sequencing. Front Genet 9:76. https://doi.org/10.3389/fgene.2018.00076
Horry JP (2000) Status and characterization of banana genetic resources. In: Singh HP, Chadha KL (eds) Banana: improvement, production and utilization. AIUPB, ICAR-NRC for Banana, Tiruchirapalli, India
Janssens SB, Vandelook F, De Langhe E et al (2016) Evolutionary dynamics and biogeography of Musaceae reveal a correlation between the diversification of the banana family and the geological and climatic history of Southeast Asia. New Phytol 210:1453–1465. https://doi.org/10.1111/nph.13856
Jombart T (2008) Adegenet package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Ahmed I (2011) Adegenet new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. https://doi.org/10.1186/1471-2156-11-94
Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. Peer J. 2:281. https://doi.org/10.7717/peerj.281
Knaus BJ, Grünwald NJ (2017) A package to manipulate and visualize variant call format data in R. Mol Ecol Resour 17:44–53. https://doi.org/10.1111/1755-0998.12549
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods 9(4):357–359. https://doi.org/10.1038/nmeth.1923
Martin G, Baurens F-C, Droc G et al (2016) Improvement of the banana “Musa acuminata” reference sequence using NGS data and semi-automated bioinformatics methods. BMC Genomics 17:243. https://doi.org/10.1186/s12864-016-2579-4
Mertens A, Bawin Y, Vanden Abeele S et al (2021) Genetic diversity and structure of Musa balbisiana populations in Vietnam and its implications for the conservation of banana crop wild relatives. PLoS ONE 16:0253255. https://doi.org/10.1371/journal.pone.0253255
Nei M (1990) Heterozygosity and genetic-distance - a citation classic commentary on estimation of average heterozygosity and genetic-distance from a small number of individuals. Genetics 89:583–590
Ngatat S, Hanna R, Lienou J et al (2022) Musa germplasm A and B genomic composition differentially affects their susceptibility to Banana bunchy top virus and its aphid vector, Pentalonia nigronervosa Plants 11:9. https://doi.org/10.3390/plants11091206
Nocum JDL, Manohar ANC, Mendoza JVS et al (2022) Identification of suitable internal control genes for gene expression analysis of banana in response to BBTV infection. Plant Gene. 32:100383. https://doi.org/10.1016/j.plgene.2022.100383
Nyine M, Uwimana B, Swennen R et al (2017) Trait variation and genetic diversity in a banana genomic selection training population. PLoS ONE 12:0178734. https://doi.org/10.1371/journal.pone.0178734
Nyine M, Uwimana B, Blavet N et al (2018) Genomic prediction in a multiploid crop: genotype by environment interaction and allele dosage effects on predictive ability in banana. Plant Genome. 11:170090. https://doi.org/10.3835/plantgenome2017.10.0090
Nyine M, Uwimana B, Akech V et al (2019) Association genetics of bunch weight and its component traits in East African highland banana (Musa spp. AAA group). Theor Appl Genet 132:3295–3308. https://doi.org/10.1007/s00122-019-03425-x
Paradis E, Claude J, Strimmer K (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20:289–290. https://doi.org/10.1093/bioinformatics/btg412
Perrier X, De Langhe E, Donohue M et al (2011) Multidisciplinary perspectives on banana (Musa spp) domestication. Proc Natl Acad Sci USA 108(28):11311–11318. https://doi.org/10.1073/pnas.1102001108
PSA (2020) OpenSTAT. IMT Philippine Exports and Imports by Commodity Groups: Bananas (Fresh)
Purcell S, Neale B, Todd-Brown K et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Amer J Human Gene 81(3):559–575. https://doi.org/10.1086/519795
Roncallo PF, Larsen AO, Achilli AL et al (2021) Linkage disequilibrium patterns, population structure and diversity analysis in a worldwide durum wheat collection including Argentinian genotypes. BMC Genomics 22:233. https://doi.org/10.1186/s12864-021-07519-z
Rosyara UR, De Jong WS, Douches DS, Endelman JB (2016) Software for genome-wide association studies in autopolyploids and its application to potato. Plant Genome. https://doi.org/10.3835/plantgenome2015.08.0073
RStudio Team (2020) RStudio: Integrated Development for R. RStudio PBC, Boston, MA
Ruas M, Guignon V, Sempere G et al (2017) MGIS: managing banana (Musa spp) genetic resources information and high-throughput genotyping data. Database. https://doi.org/10.1093/database/bax046
Salem KFM, Sallam A (2016) Analysis of population structure and genetic diversity of Egyptian and exotic rice (Oryza sativa L.) genotypes. C R Biol 339:1–9. https://doi.org/10.1016/j.crvi.2015.11.003
Sales EK, Butardo NG, Paniagua HG et al (2011) Assessment of ploidy and genome constitution of some Musa balbisiana cultivars using DArT markers. Philippine J Crop Sci 36:11–18
Sardos J, Rouard M, Hueber Y et al (2016) A Genome-wide association study on the seedless phenotype in banana (Musa spp) reveals the potential of a selected panel to detect candidate genes in a vegetatively propagated crop. PLoS ONE 11:0154448. https://doi.org/10.1371/journal.pone.0154448
Sardos J, Christelová P, Čížková J et al (2018) Collection of new diversity of wild and cultivated bananas (Musa spp.) in the Autonomous Region of Bougainville, Papua New Guinea. Genet Resour Crop Evol 65:2267–2286. https://doi.org/10.1007/s10722-018-0690-x
Shete S, Tiwari H, Elston RC (2000) On estimating the heterozygosity and polymorphism information content value. Theor Popul Biol 57:265–271. https://doi.org/10.1006/tpbi.2000.1452
Valmayor RV (2004) Musa alinsanaya RVValmayor. Philipp Agric Sci. 87(1):117
Acknowledgements
We gratefully acknowledge the Institute of Plant Breeding, College of Agriculture and Food Science at the University of the Philippines Los Baños for the use of facilities, equipment, and human resources counterpart. We also thank Ronilo M. Bajaro, Rodelio R. Pia and Wilermie D. Hernandez for technical assistance. Finally, the principal author would like to acknowledge the UPLB Graduate School and her advisory committee Dr. Consorcia E. Reaño, National Scientist Dolores A. Ramirez, Dr. Fe M. Dela Cueva, Dr. Hayde F. Galvez and Dr. Antonio C. Laurena for their technical advice in the doctoral dissertation.
Funding
This research was supported by the Philippine Department of Agriculture—Biotechnology Program Office (DA-BIOTECH) through the project entitled “DA-BIOTECH-R1902: Fast-tracking the Development of BBTV-resistant Banana Cultivars through Modern Biotech Tools: Molecular Profiling toward Marker Development and Diagnostics (Phase I)”.
Author information
Authors and Affiliations
Contributions
RRG, FMDC and DVL conceived and designed the study. JSM, JDLN and GCL carried out the experimental work. RRG and DVL developed the SNP panel and performed data analysis and interpretation. MST and LSG managed the germplasm and supplied the plant materials. RRG, ANCM and DVL wrote the manuscript with input from all authors. DVL secured the project funds. All authors have approved the submission of this manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no relevant financial or non-financial interests.
Ethical approval
This research does not involve any studies conducted on human or animal subjects.
Additional information
Communicated by Bing yang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gardoce, R.R., Manohar, A.N.C., Mendoza, JV.S. et al. A novel SNP panel developed for targeted genotyping-by-sequencing (GBS) reveals genetic diversity and population structure of Musa spp. germplasm collection. Mol Genet Genomics 298, 857–869 (2023). https://doi.org/10.1007/s00438-023-02018-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-023-02018-0