Genetic diversity, population structure, and genome-wide association analysis of ginkgo cultivars

Yaping Hu , Zhaoyan Yu , Xiaoge Gao , Ganping Liu , Yun Zhang , Petr Šmarda , Qirong Guo

Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) : 136

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Horticulture Research ›› 2023, Vol. 10 ›› Issue (8) :136 DOI: 10.1093/hr/uhad136
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Genetic diversity, population structure, and genome-wide association analysis of ginkgo cultivars
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Abstract

Ginkgo biloba is an economically valuable tree worldwide. The species has nearly become extinct during the Quaternary, which has likely resulted in reduction of its genetic variability. The genetic variability is now conserved in few natural populations in China and a number of cultivars that are, however, derived from a few ancient trees, helping the species survive in China through medieval times. Despite the recent interest in ginkgo, however, detailed knowledge of its genetic diversity, conserved in cultivated trees and cultivars, has remained poor. This limits efficient conservation of its diversity as well as efficient use of the existing germplasm resources. Here we performed genotyping-by-sequencing (GBS) on 102 cultivated germplasms of ginkgo collected to explore their genetic structure, kinship, and inbreeding prediction. For the first time in ginkgo, a genome-wide association analysis study (GWAS) was used to attempt gene mapping of seed traits. The results showed that most of the germplasms did not show any obvious genetic relationship. The size of the ginkgo germplasm population expanded significantly around 1500 years ago during the Sui and Tang dynasties. Classification of seed cultivars based on a phylogenetic perspective does not support the current classification criteria based on phenotype. Twenty-four candidate genes were localized after performing GWAS on the seed traits. Overall, this study reveals the genetic basis of ginkgo seed traits and provides insights into its cultivation history. These findings will facilitate the conservation and utilization of the domesticated germplasms of this living fossil plant.

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Yaping Hu, Zhaoyan Yu, Xiaoge Gao, Ganping Liu, Yun Zhang, Petr Šmarda, Qirong Guo. Genetic diversity, population structure, and genome-wide association analysis of ginkgo cultivars. Horticulture Research, 2023, 10 (8) : 136 DOI:10.1093/hr/uhad136

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Acknowledgements

This research was funded by the National Natural Science Foundation of China (31971648), the China Scholarship Council (202108320301), and the Czech Science Foundation (19-18545S).

Author Contributions

Y.H. and Q.G. designed the experiments; Y.H., Z.Y., X.G., Y.Z. and G.L. performed experiments; Y.H., Z.Y.,X.G. and P.L. analyzed data; Y.H. and Q.G. wrote the manuscript; P. Š. reviewed the manuscript.

Data availability

The high-throughput sequencing data in this study are all open access and have been uploaded to the National Genomics Data Center (NGDC, https://ngdc.cncb.ac.cn/) with the accession number CRA006613.

Conflict of interest

The authors declare no competing interests.

References

[1]

Tang CQ, Yang Y, Ohsawa M et al. Evidence for the persistence of wild Ginkgo biloba (Ginkgoaceae) populations in the Dalou Mountains, southwestern China . Am J Bot. 2012; 99: 1408-14

[2]

Zhao Y, Paule J, Fu C et al. Out of China: distribution history of Ginkgo biloba L. Taxon. 2010; 59: 495-504

[3]

Zhao YP, Fan G, Yin PP et al. Resequencing 545 ginkgo genomes across the world reveals the evolutionary history of the living fossil. Nat Commun. 2019; 10: 4201

[4]

Forest F, Moat J, Baloch E et al. Gymnosperms on the EDGE. Sci Rep. 2018; 8: 6053.

[5]

Purohit VK, Phondani PC, Dhyani D et al. Ginkgo biloba a living fossil: need conservation initiatives . Natl Acad Sci Lett. 2007; 30: 31-3

[6]

Sadaf HM, Bibi Y, Arshad M et al. Status of maiden hair tree - Ginkgo biloba; living fossils becoming endangered . Nova J Med Biol Sci. 2014; 2: 1-5

[7]

Crane PR . Ginkgo: The Tree that Time Forgot. London: Yale University Press, 2013

[8]

Tredici P . Ginkgos and people - a thousand years of interaction. Arnoldia (Boston). 1991; 51: 2-15

[9]

Gong W, Zeng Z, Chen YY et al. Glacial refugia of Ginkgo biloba and human impact on its genetic diversity: evidence from chloroplast DNA . J Integr Plant Biol. 2008; 50: 368-74

[10]

Crane PR . An evolutionary and cultural biography of ginkgo. Plants People Planet. 2019; 1: 32-7

[11]

Zhou Q, Mu KM, Ni ZX et al. Analysis of genetic diversity of ancient ginkgo populations using SSR markers. Ind Crop Prod. 2020; 145: 111942

[12]

Fan XX, Shen L, Zhang X et al. Assessing genetic diversity of Ginkgo biloba L. (Ginkgoaceae) populations from China by RAPD markers . Biochem Genet. 2004; 42: 269-78

[13]

Elshire RJ, Glaubitz JC, Sun Q et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011; 6: e19379

[14]

Chung YS, Choi SC, Jun TH et al. Genotyping-by-sequencing: a promising tool for plant genetics research and breeding. Hortic Environ Biotechnol. 2017; 58: 425-31

[15]

Riangwong K, Wanchana S, Aesomnuk W et al. Mining and validation of novel genotyping-by-sequencing (GBS)-based simple sequence repeats (SSRs) and their application for the estimation of the genetic diversity and population structure of coconuts (Cocos nucifera L.) in Thailand . Hortic Res. 2020; 7: 156

[16]

Pavan S, Delvento C, Mazzeo R et al. Almond diversity and homozygosity define structure, kinship, inbreeding, and linkage disequilibrium in cultivated germplasm, and reveal genomic associations with nut and seed weight. Hortic Res. 2021; 8: 15

[17]

Wang X, Bao K, Reddy UK et al. The USDA cucumber (Cucumis sativus L.) collection: genetic diversity, population structure, genome-wide association studies, and core collection development . Hortic Res. 2018; 5: 64

[18]

Blanca J, Canizares J, Cordero L et al. Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato. PLoS One. 2012; 7: e48198

[19]

Migicovsky Z, Gardner KM, Richards C et al. Genomic consequences of apple improvement. Hort Res. 2021; 8: 9

[20]

Fu PN, Wu W, Lai GT et al. Identifying Plasmopara viticola resistance loci in grapevine (Vitis amurensis) via genotyping-by-sequencing-based QTL mapping . Plant Physiol Biochem. 2020; 154: 75-84

[21]

Liu H, Wang X, Wang G et al. The nearly complete genome of Ginkgo biloba illuminates gymnosperm evolution . Nat Plants. 2021; 7: 748-56

[22]

Xu X, Liu X, Ge S et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol. 2012; 30: 105-11

[23]

Lam HM, Xu X, Liu X et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet. 2010; 42: 1053-9

[24]

Zhang MY, Xue C, Hu H et al. Genome-wide association studies provide insights into the genetic determination of fruit traits of pear. Nat Commun. 2021; 12: 1144

[25]

Duan N, Bai Y, Sun H et al. Genome re-sequencing reveals the history of apple and supports a two-stage model for fruit enlargement. Nat Commun. 2017; 8: 1-11

[26]

Forutan M, Ansari Mahyari S, Baes C et al. Inbreeding and runs of homozygosity before and after genomic selection in North American Holstein cattle. BMC Genomics. 2018; 19: 98

[27]

Pemberton TJ, Absher D, Feldman MW et al. Genomic patterns of homozygosity in worldwide human populations. Am J Hum Genet. 2012; 91: 275-92

[28]

Hu Y, Šmarda P, Liu G et al. High-depth transcriptome reveals differences in natural haploid Ginkgo biloba L. due to the effect of reduced gene dosage . Int J Mol Sci. 2022; 23: 8958

[29]

Terhorst J, Kamm JA, Song YS . Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat Genet. 2017; 49: 303-9

[30]

Hamrick JL, Godt MJW . Allozyme diversity in cultivated crops. Crop Sci. 2002; 37: 26-30

[31]

Šmarda P, Horová L, Knápek O et al. Multiple haploids, triploids, and tetraploids found in modern-day ‘living fossil’ Ginkgo biloba. Hortic Res. 2018; 5: 55

[32]

Šmarda P, Veselý P, Šmerda J et al. Polyploidy in a ‘living fossil’ Ginkgo biloba. New Phytol. 2016; 212: 11-4

[33]

De Vladar HP, Santos M, Szathmary E . Grand views of evolution. Trends Ecol Evol. 2017; 32: 324-34

[34]

Kumar S, Deng CH, Hunt M et al. Homozygosity mapping reveals population history and trait architecture in self-incompatible pear (Pyrus spp.). Front Plant Sci. 2021; 11: 590846.

[35]

Yang XP, Luo ZL, Todd J et al. Genome-wide association study of multiple yield traits in a diversity panel of polyploid sugarcane (Saccharum spp.). Plant Genome. 2020; 13: e20006.

[36]

Liu S, Zhang Y, Feng Q et al. Tomato AUXIN RESPONSE FACTOR 5 regulates fruit set and development via the mediation of auxin and gibberellin signaling. Sci Rep. 2018; 8: 2971

[37]

Luna CM, Pastori GM, Driscoll S et al. Drought controls on H2O2 accumulation, catalase (CAT) activity and CAT gene expression in wheat . J Exp Bot. 2005; 56: 417-23

[38]

Boateng ID . A critical review of current technologies used to reduce ginkgotoxin, ginkgotoxin-5′-glucoside, ginkgolic acid, allergic glycoprotein, and cyanide in Ginkgo biloba L. seed . Food Chem. 2022; 382: 132408

[39]

Muller BSF, de Almeida JE, Lima BM et al. Independent and joint-GWAS for growth traits in Eucalyptus by assembling genome-wide data for 3373 individuals across four breeding populations . New Phytol. 2019; 221: 818-33

[40]

Minamikawa MF, Takada N, Terakami S et al. Genome-wide association study and genomic prediction using parental and breeding populations of Japanese pear (Pyrus pyrifolia Nakai). Sci Rep. 2018; 8: 11994

[41]

Lee SJ, Ban SH, Kim GH et al. Identification of potential gene-associated major traits using GBS-GWAS for Korean apple germplasm collections. Plant Breed. 2017; 136: 977-86

[42]

Yu BY, Boyle K, Zhang WT et al. Multi-trait and multi-environment QTL analysis reveals the impact of seed colour on seed composition traits in Brassica napus. Mol Breed. 2016; 36: 111.

[43]

Doyle JJ . Isolation of plant DNA from fresh tissue. Focus. 1990; 12: 13-5

[44]

Chen SF, Zhou YQ, Chen YR et al. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34: i884-90

[45]

Li H, Durbin R . Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009; 25: 1754-60

[46]

Van der Auwera GA, Carneiro MO, Hartl C et al. From FastQ data to high-confidence variant calls: the genome analysis toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013; 43: 11.10.11-11.10.33

[47]

Wang K, Li M, Hakonarson H . ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010; 38: e164-4

[48]

Alexander DH, Novembre J, Lange K . Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009; 19: 1655-64

[49]

Chang CC, Chow CC, Tellier L et al. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015; 4: 7

[50]

Francis RM . POPHELPER: an R package and web app to analyse and visualize population structure. Mol Ecol Resour. 2017; 17: 27-32

[51]

Price AL, Patterson NJ, Plenge RM et al. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet. 2006; 38: 904-9

[52]

Yang JA, Lee SH, Goddard ME et al. GCTA: a tool for genome-wide complex trait analysis. Am J Hum Genet. 2011; 88: 76-82

[53]

Zhang C, Dong SS, Xu JY et al. PopLDdecay: a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics. 2019; 35: 1786-8

[54]

Purcell S, Neale B, Todd-Brown K et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007; 81: 559-75

[55]

Danecek P, Auton A, Abecasis G et al. The variant call format and VCFtools. Bioinformatics. 2011; 27: 2156-8

[56]

Bates D, Mächler M, Bolker B et al. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015; 67: 1-48

[57]

Massey FJ Jr. The Kolmogorov-Smirnov test for goodness of fit. J Am Stat Assoc. 1951; 46: 68-78

[58]

Villanueva RAM, Chen ZJ ggplot2: Elegant Graphics for Data Analysis. Measurement: Interdisciplinary Research and Perspectives. 2019; 17: 160-167

[59]

Jiang L, Zheng Z, Qi T et al. A resource-efficient tool for mixed model association analysis of large-scale data. Nat Genet. 2019; 51: 1749-55

[60]

Mbatchou J, Barnard L, Backman J et al. Computationally efficient whole-genome regression for quantitative and binary traits. Nat Genet. 2021; 53: 1097-103

[61]

Dey R, Schmidt EM, Abecasis GR et al. A fast and accurate algorithm to test for binary phenotypes and its application to PheWAS. Am J Hum Genet. 2017; 101: 37-49

[62]

Zhou W, Nielsen JB, Fritsche LG et al. Efficiently controlling for case-control imbalance and sample relatedness in large-scale genetic association studies. Nat Genet. 2018; 50: 1335-41

[63]

Chen H, Huffman JE, Brody JA et al. Efficient variant set mixed model association tests for continuous and binary traits in large-scale whole-genome sequencing studies. Am J Hum Genet. 2019; 104: 260-74

[64]

Wu MC, Lee S, Cai T et al. Rare-variant association testing for sequencing data with the sequence kernel association test. Am J Hum Genet. 2011; 89: 82-93

[65]

Lee S, Wu MC, Lin X . Optimal tests for rare variant effects in sequencing association studies. Biostatistics. 2012; 13: 762-75

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