Population genomics reveals demographic history and selection signatures of hazelnut (Corylus)

Zhen Yang , Wenxu Ma , Lujun Wang , Xiaohong Yang , Tiantian Zhao , Lisong Liang , Guixi Wang , Qinghua Ma

Horticulture Research ›› 2023, Vol. 10 ›› Issue (5) : 065

PDF (1382KB)
Horticulture Research ›› 2023, Vol. 10 ›› Issue (5) :065 DOI: 10.1093/hr/uhad065
Article
research-article
Population genomics reveals demographic history and selection signatures of hazelnut (Corylus)
Author information +
History +
PDF (1382KB)

Abstract

Hazelnut (Corylus spp.) is known as one of the four famous tree nuts in the world due to its pleasant taste and nutritional benefits. However, hazelnut promotion worldwide is increasingly challenged by global climate change, limiting its production to a few regions. Focusing on the eurytopic Section Phyllochlamys, we conducted whole-genome resequencing of 125 diverse accessions from five geo-ecological zones in Eurasia to elucidate the genomic basis of adaptation and improvement. Population structure inference outlined five distinct genetic lineages corresponding to climate conditions and breeding background, and highlighted the differentiation between European and Asian lineages. Demographic dynamics and ecological niche modeling revealed that Pleistocene climatic oscillations dominantly shaped the extant genetic patterns, and multiple environmental factors have contributed to the lineage divergence. Whole-genome scans identified 279, 111, and 164 selective sweeps that underlie local adaptation in Corylus heterophylla, Corylus kweichowensis, and Corylus yunnanensis, respectively. Relevant positively selected genes were mainly involved in regulating signaling pathways, growth and development, and stress resistance. The improvement signatures of hybrid hazelnut were concentrated in 312 and 316 selected genes, when compared to C. heterophylla and Corylus avellana, respectively, including those that regulate protein polymerization, photosynthesis, and response to water deprivation. Among these loci, 22 candidate genes were highly associated with the regulation of biological quality. Our study provides insights into evolutionary processes and the molecular basis of how sibling species adapt to contrasting environments, and offers valuable resources for future climate-resilient breeding.

Cite this article

Download citation ▾
Zhen Yang, Wenxu Ma, Lujun Wang, Xiaohong Yang, Tiantian Zhao, Lisong Liang, Guixi Wang, Qinghua Ma. Population genomics reveals demographic history and selection signatures of hazelnut (Corylus). Horticulture Research, 2023, 10 (5) : 065 DOI:10.1093/hr/uhad065

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32101541) and the Key Research and Development Program of Hebei Province (21326804D).

Author contributions

Z.Y. and Q.M. conceived the study; Z.Y. and W.M. performed molecular experiments and analyzed the data; X.Y., L.W., T.Z., and G.W. collected materials; L.L. contributed to data analysis; Z.Y. and Q.M. wrote the paper. All authors contributed to revisions and gave final approval for publication.

Data availability

The raw sequencing data of 125 accessions have been submitted to the NCBI BioProject database under accession number PRJNA899594. The unfiltered variant call format (VCF) file relative to the resequencing experiment is publicly available at the Figshare repository (10.6084/m9.figshare.22306681).

Conflict of interest

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Yang Z, Ma WX, He X et al. Species divergence and phylogeography of Corylus heterophylla Fisch. Complex (Betulaceae): inferred from molecular, climatic and morphological data . Mol Phylogenet Evol. 2022; 168: 107413.

[2]

Holstein N, el Tamer S, Weigend M . The nutty world of hazel names - a critical taxonomic checklist of the genus Corylus (Betulaceae). Eur J Taxon. 2018; 409: 1-45.

[3]

Lu Z, Sun Y, Li Y et al. Species delimitation and hybridization history of a hazel species complex. Ann Bot. 2021; 127: 875-86.

[4]

Botta R, Molnar TJ, Erdogan V et al. Hazelnut (Corylus spp.) breeding . In: Al-Khayri J, Jain S, Johnson D, eds. Advances in Plant Breeding Strategies: Nut and Beverage Crops: Volume 4. Springer: Cham, 2019, 157-219.

[5]

Whitcher IN, Wen J . Phylogeny and biogeography of Corylus (Betulaceae): inferences from ITS sequences . Syst Bot. 2001; 26: 283-98.

[6]

Chen ZD, Manchester SR, Sun HY . Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology and paleobotany. Am J Bot. 1999; 86: 1168-81.

[7]

Zhao T, Wang GX, Ma QH et al. Multilocus data reveal deep phylogenetic relationships and intercontinental biogeography of the Eurasian-north American genus Corylus (Betulaceae). Mol Phylogenet Evol. 2020; 142: 106658.

[8]

Yang Z, Zhao TT, Ma QH et al. Resolving the speciation patterns and evolutionary history of the intercontinental disjunct genus Corylus (Betulaceae) using genome-wide SNPs . Front Plant Sci. 2018; 9: 1386.

[9]

Forest F, Savolainen V, Chase MW et al. Teasing apart molecular-versus fossil-based error estimates when dating phylogenetic trees: a case study in the birch family (Betulaceae). Syst Bot. 2005; 30: 118-33.

[10]

Thompson MM, Lagerstedt HB, Mehlenbacher SA . Hazelnuts. In: Janick J, Moore JN, eds. Fruit Breeding: Nuts. Wiley: New York, 1996, 125-84.

[11]

Liang WJ, Zhang YM . Investigation and study of filbert resources in China. In: Chinese Society for Horticultural Science. Proceedings of the International Symposium on Horticultural Germplasm. Cultivated and Wild: Beijing, 1988, 5-9.

[12]

Ma QH, Huo HL, Chen X et al. Study on the taxonomy, distribution, development and utilization of Corylus kweichowensis Hu . J Plant Genet Resour. 2014; 15: 1223-31.

[13]

Qi JZ . Study on taxonomy of Corylus kweichowensis. J Nanjing Forestry Univ. 1996; 20: 71-4.

[14]

Helmstetter AJ, Buggs RJ, Lucas SJ . Repeated long-distance dispersal and convergent evolution in hazel. Sci Rep. 2019; 9: 1-12.

[15]

Liang WJ, Dong DF, Wang GX et al. Progresses on the hazelnut cross breeding of Corylus heterophylla Fisch. × Corylus avellana L. in China . Acta Hortic. 2012; 940: 233-8.

[16]

Erdogan V, Mehlenbacher SA . Interspecific hybridization in hazelnut (Corylus). J Am Soc Hortic Sci. 2000; 125: 489-97.

[17]

Miller AJ, Gross BL . From forest to field: perennial fruit crop domestication. Am J Bot. 2011; 98: 1389-414.

[18]

Petit RJ, Hampe A . Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst. 2006; 37: 187-214.

[19]

Hedrick PW . Genetic polymorphism in heterogeneous environments: the age of genomics. Annu Rev Ecol Syst. 2006; 37: 67-93.

[20]

Kawecki TJ, Ebert D . Conceptual issues in local adaptation. Ecol Lett. 2004; 7: 1225-41.

[21]

Zhang YH, Liu L, Liang WJ et al. Chinese Fruit Tree. In: Volume Chestnut and Hazelnut. Beijing: China Forestry Publishing House, 2005.

[22]

Wang GX . Progress in cultivation and utilization of Corylus L. resources in China (I)- Corylus Germplasm resources . For Res. 2018; 31: 105-12.

[23]

Funk WC, McKay JK, Hohenlohe PA et al. Harnessing genomics for delineating conservation units. Trends Ecol Evol. 2012; 27: 489-96.

[24]

Hedrick PW . Recent developments in conservation genetics. For Ecol Manag. 2004; 197: 3-19.

[25]

Peery MZ, Kirby R, Reid BN et al. Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol. 2012; 21: 3403-18.

[26]

Li J, Milne RI, Ru D et al. Allopatric divergence and hybridization within Cupressus chengiana (Cupressaceae), a threatened conifer in the northern Hengduan Mountains of western China . Mol Ecol. 2020; 29: 1250-66.

[27]

Fennessy J, Bidon T, Reuss F et al. Multi-locus analyses reveal four giraffe species instead of one. Curr Biol. 2016; 26: 2543-9.

[28]

Ma Y, Wang JI, Hu Q et al. Ancient introgression drives adaptation to cooler and drier mountain habitats in a cypress species complex. Commun Biol. 2019; 2: 213.

[29]

Ren G, Zhang X, Li Y et al. Large-scale whole-genome resequencing unravels the domestication history of Cannabis sativa. Sci Adv. 2021; 7: eabg2286.

[30]

Fu R, Zhu Y, Liu Y et al. Genome-wide analyses of introgression between two sympatric Asian oak species. Nat Ecol Evol. 2022; 6: 924-35.

[31]

Zhou BF, Yuan S, Crowl AA et al. Phylogenomic analyses highlight innovation and introgression in the continental radiations of Fagaceae across the northern hemisphere. Nat Commun. 2022; 13: 1-14.

[32]

Zhou Y, Massonnet M, Sanjak JS et al. Evolutionary genomics of grape (Vitis vinifera ssp. vinifera) domestication . Proc Natl Acad Sci. 2017; 114: 11715-20.

[33]

Weigel D, Nordborg M . Population genomics for understanding adaptation in wild plant species. Annu Rev Genet. 2015; 49: 315-38.

[34]

Yu Y, Guan J, Xu Y et al. Population-scale peach genome analyses unravel selection patterns and biochemical basis underlying fruit flavor. Nat Commun. 2021; 12: 1-13.

[35]

Zhao T, Ma W, Yang Z et al. A chromosome-level reference genome of the hazelnut, Corylus heterophylla Fisch . GigaScience. 2021; 10: giab027.

[36]

Liu J, Wei H, Zhang X et al. Chromosome-level genome assembly and HazelOmics database construction provides insights into unsaturated fatty acid synthesis and cold resistance in hazelnut (Corylus heterophylla). Front Plant Sci. 2021; 2912: 3604.

[37]

Lucas SJ, Kahraman K, Avşar B et al. A chromosome-scale genome assembly of European hazel (Corylus avellana L.) reveals targets for crop improvement . Plant J. 2021; 105: 1413-30.

[38]

Li Y, Sun P, Lu Z et al. The Corylus mandshurica genome provides insights into the evolution of Betulaceae genomes and hazelnut breeding . Hort Res. 2021; 8: 54.

[39]

Editorial Board of the Flora of China of Chinese Academy of Sciences. Flora of China. Beijing: Science Press; 2013, Vol. 21.

[40]

Zhao T, Ma W, Ma Q et al. Genetic diversity and population structure of Chinese Corylus heterophylla and Corylus kweichowensis using simple sequence repeat markers . J Am Soc Hortic Sci. 2020; 145: 289-98.

[41]

Ma YP, Wariss HM, Liao RL et al. Genome-wide analysis of butterfly bush (Buddleja alternifolia) in three uplands provides insights into biogeography, demography and speciation . New Phytol. 2021; 232: 1463-76.

[42]

Li JL, Zhong LL, Wang J et al. Genomic insights into speciation history and local adaptation of an alpine aspen in the Qinghai-Tibet plateau and adjacent highlands. J Syst Evol. 2021; 59: 1220-31.

[43]

Chen JH, Huang Y, Brachi B et al. Genome-wide analysis of cushion willow provides insights into alpine plant divergence in a biodiversity hotspot. Nat Commun. 2019; 10: 1-12.

[44]

Wang Z, Jiang Y, Bi H et al. Hybrid speciation via inheritance of alternate alleles of parental isolating genes. Mol Plant. 2021; 14: 208-22.

[45]

Liu Z, Zhu H, Zhou J et al. Resequencing of 296 cultivated and wild lotus accessions unravels its evolution and breeding history. Plant J. 2020; 104: 1673-84.

[46]

Hancock AM, Brachi B, Faure N et al. Adaptation to climate across the Arabidopsis thaliana genome . Science. 2011; 334: 83-6.

[47]

Fournier-Level A, Korte A, Cooper MD et al. A map of local adaptation in Arabidopsis thaliana. Science. 2011; 334: 86-9.

[48]

Kevin LC, Wang HL, Joseph RE . Ethylene biosynthesis and signaling networks. Plant Cell. 2002; 14: S131-51.

[49]

Manel S, Gugerli F, Thuiller W et al. Broad-scale adaptive genetic variation in alpine plants is driven by temperature and precipitation. Mol Ecol. 2012; 21: 3729-38.

[50]

Norsang G, Kocbach L, Stamnes J et al. Spatial distribution and temporal variation of solar UV radiation over the Tibetan plateau. Appl Phys Res. 2011; 3: 37.

[51]

Körner C. Alpine Plant Life: Functional Plant Ecology of High Mountain Ecosystems. Verlag Berlin, Heidelberg: Springer Science & Business Media; 2003.

[52]

Britt AB . Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 1999; 4: 20-5.

[53]

Belostotsky DA, Sieburth LE . Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol. 2009; 12: 96-102.

[54]

Xu J, Chua NH . Processing bodies and plant development. Curr Opin Plant Biol. 2011; 14: 88-93.

[55]

Rius M, Darling JA . How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol. 2014; 29: 233-42.

[56]

Abbott RJ, Albach D, Ansell S et al. Hybridization and speciation. J Evol Biol. 2013; 26: 229-46.

[57]

Bolger AM, Lohse M, Usadel B . Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30: 2114-20.

[58]

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

[59]

Li H, Handsaker B, Wysoker A et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009; 25: 2078-9.

[60]

DePristo MA, Banks E, Poplin R et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet. 2011; 43: 491-8.

[61]

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.

[62]

Cingolani P, Platts A, Wang LL et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain. Fly. 2012; 6: 80-92.

[63]

Stamatakis A . RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30: 1312-3.

[64]

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

[65]

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

[66]

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

[67]

Shannon P, Markiel A, Ozier O et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003; 13: 2498-504.

[68]

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. 2018; 35: 1786-8.

[69]

Li H, Durbin R . Inference of human population history from individual whole-genome sequences. Nature. 2011; 475: 493-6.

[70]

Zheng Z, Li Y, Li M et al. Whole-genome diversification analysis of the hornbeam species reveals speciation and adaptation among closely related species. Front Plant Sci. 2021; 12: 581704.

[71]

Gutenkunst RN, Hernandez RD, Williamson SH et al. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 2009; 5: e1000695.

[72]

Malinsky M, Matschiner M, Svardal H . Dsuite-fast D-statistics and related admixture evidence from VCF files . Mol Ecol Resour. 2021; 21: 584-95.

[73]

Dormann CF, Elith J, Bacher S et al. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography. 2013; 36: 27-46.

[74]

Phillips SJ, Anderson RP, Schapire RE . Maximum entropy modeling of species geographic distributions. Ecol Model. 2006; 190: 231-59.

[75]

Esri. ArcGIS. v. 10. Redlands, CA: ESRI, 2010.

[76]

Warren DL, Glor RE, Turelli M . Enmtools: a toolbox for comparative studies of environmental niche models. Ecography. 2010; 33: 607-11.

[77]

Ashburner M, Ball CA, Blake JA et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000; 25: 25-9.

[78]

Conesa A, Götz S, García-Gómez JM . Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21: 3674-6.

PDF (1382KB)

45

Accesses

0

Citation

Detail

Sections
Recommended

/