Genomic population structure and local adaptation of the wild strawberry Fragaria nilgerrensis

Yuxi Hu , Chao Feng , Lihua Yang , Patrick P. Edger , Ming Kang

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhab059

PDF (860KB)
Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhab059 DOI: 10.1093/hr/uhab059
Article
research-article
Genomic population structure and local adaptation of the wild strawberry Fragaria nilgerrensis
Author information +
History +
PDF (860KB)

Abstract

The crop wild relative Fragaria nilgerrensis is adapted to a variety of diverse habitats across its native range in China. Thus, discoveries made in this species could serve as a useful guide in the development of new superior strawberry cultivars that are resilient to new or variable environments. However, the genetic diversity and genetic architecture of traits in this species underlying important adaptive traits remain poorly understood. Here, we used whole-genome resequencing data from 193 F. nilgerrensis individuals spanning the distribution range in China to investigate the genetic diversity, population structure and genomic basis of local adaptation. We identified four genetic groups, with the western group located in Hengduan Mountains exhibiting the highest genetic diversity. Redundancy analysis suggested that both environment and geographic variables shaped a significant proportion of the genomic variation. Our analyses revealed that the environmental difference explains more of the observed genetic variation than geographic distance. This suggests that adaptation to distinct habitats, which present a unique combination of abiotic factors, likely drove genetic differentiation. Lastly, by implementing selective sweep scans and genome–environment association analysis throughout the genome, we identified the genetic variation associated with local adaptation and investigated the functions of putative candidate genes in F. nilgerrensis.

Cite this article

Download citation ▾
Yuxi Hu, Chao Feng, Lihua Yang, Patrick P. Edger, Ming Kang. Genomic population structure and local adaptation of the wild strawberry Fragaria nilgerrensis. Horticulture Research, 2022, 9 (1) : uhab059 DOI:10.1093/hr/uhab059

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Hajjar R, Hodgkin T . The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica. 2007; 156: 1-13.

[2]

Vincent H, Wiersema J, Kell S et al. A prioritized crop wild relative inventory to help underpin global food security. Biol Conserv 2013; 167: 265-75.

[3]

Dempewolf H, Baute G, Anderson JE et al. Past and future use of wild relatives in crop breeding. Crop Sci 2017; 57: 1070-82.

[4]

Vollbrecht E, Sigmon B . Amazing grass: developmental genetics of maize domestication. Biochem Soc Trans. 2005; 33: 1502-6.

[5]

Pimentel D, Wilson C, McCullum C et al. Economic and environmental benefits of biodiversity. Bioscience 1997; 47: 747-57.

[6]

Jarvis A, Lane A, Hijmans RJ . The effect of climate change on crop wild relatives. Agric Ecosyst Environ. 2008; 126: 13-23.

[7]

Bilz M, Kell SP, Maxted N et al. European Red List of Vascular Plants . Luxembourg: Publications Office of the European Union; 2011.

[8]

Giampieri F, Tulipani S, Alvarez-Suarez JM et al. The strawberry: composition, nutritional quality, and impact on human health. Nutrition. 2012; 28: 9-19.

[9]

Romandini S, Mazzoni L, Giampieri F et al. Effects of an acute strawberry (Fragaria × ananassa) consumption on the plasma antioxidant status of healthy subjects . J Berry Res. 2013; 3: 169-79.

[10]

Environmental Working Group . EWG’s 2013 Shopper’s Guide to Pesticides in Produce . http://www.ewg.org/foodnews/summary. 2013. (last accessed June 15, 2021)

[11]

Luo G, Xue L, Guo R et al. Creating interspecific hybrids with improved cold resistance in Fragaria . Sci Hortic 2018; 234: 1-9.

[12]

Liston A, Cronn R, Ashman TL . Fragaria: a genus with deep historical roots and ripe for evolutionary and ecological insights . Am J Bot 2014; 101: 1686-99.

[13]

Lei JJ, Xue L, Guo RX et al. The Fragaria species native to China and their geographical distribution. Acta Hortic 2017; 1156: 37-46.

[14]

Staudt G . The species of Fragaria, their taxonomy and geographical distribution. Acta Hortic. 1989; 265: 23-34.

[15]

Guo R, Xue L, Luo G et al. Investigation and taxonomy of wild Fragaria resources in Tibet. Kulturpflanze. 2018; 65: 405-15.

[16]

Hancock J, Luby J . Genetic resources at our doorstep: the wild strawberries. Bioscience. 1993; 43: 141-7.

[17]

Noguchi Y. “Tokun”: a new decaploid interspecific hybrid strawberry having the aroma of the wild strawberry. J Jpn Assoc Odor Environ. 2011; 42: 122-8.

[18]

Davey JW, Hohenlohe PA, Etter PD et al. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet. 2011; 12: 499-510.

[19]

Bickhart DM, Hou Y, Schroeder SG et al. Copy number variation of individual cattle genomes using next-generation sequencing. Genome Res. 2012; 22: 778-90.

[20]

Hou Z, Li A, Zhang J . Genetic architecture, demographic history, and genomic differentiation of Populus davidiana revealed by whole-genome resequencing. Evol Appl 2020; 13: 2582-96.

[21]

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: 5230.

[22]

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.

[23]

McKinney GJ, Larson WA, Seeb LW et al. RADseq provides unprecedented insights into molecular ecology and evolutionary genetics: comment on breaking RAD by Lowry et al. (2016). Mol Ecol Resour. 2017; 17: 356-61.

[24]

McCormack JE, Hird SM, Zellmer AJ et al. Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogenet Evol 2013; 66: 526-38.

[25]

Ellegren H. Genome sequencing and population genomics in non-model organisms. Trends Ecol Evol. 2014; 29: 51-63.

[26]

Seehausen O, Butlin RK, Keller I et al. Genomics and the origin of species. Nat Rev Genet. 2014; 15: 176-92.

[27]

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

[28]

Gibson MJS, Moyle LC . Regional differences in the abiotic environment contribute to genomic divergence within a wild tomato species. Mol Ecol. 2020; 29: 2204-17.

[29]

Wang J, Ding J, Tan B et al. A major locus controls local adaptation and adaptive life history variation in a perennial plant. Genome Biol. 2018; 19: 72.

[30]

Zou YP, Hou XH, Wu Q et al. Adaptation of Arabidopsis thaliana to the Yangtze River basin. Genome Biol 2017; 18: 239.

[31]

Morin PA, Luikart G, Wayne RK . SNPs in ecology, evolution and conservation. Trends Ecol Evol. 2004; 19: 208-16.

[32]

Garvin MR, Saitoh K, Gharrett AJ . Application of single nucleotide polymorphisms to non-model species: a technical review. Mol Ecol Resour 2010; 10: 915-34.

[33]

Atwell S, Huang YS, Vilhjalmsson BJ et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines . Nature. 2010; 465: 627-31.

[34]

Exposito-Alonso M, Vasseur F, Ding W et al. Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana . Nat Ecol Evol. 2018; 2: 352-8.

[35]

Nelson JT, Motamayor JC, Cornejo OE . Environment and pathogens shape local and regional adaptations to climate change in the chocolate tree. Mol Ecol. 2021; 30: 656-69.

[36]

Todesco M, Owens GL, Bercovich N et al. Massive haplotypes underlie ecotypic differentiation in sunflowers. Nature. 2020; 584: 602-7.

[37]

Feng C, Wang J, Harris AJ et al. Tracing the diploid ancestry of the cultivated octoploid strawberry. Mol Biol Evol. 2021; 38: 478-85.

[38]

Janes JK et al. The K = 2 conundrum. Mol Ecol 2017; 26: 3594-602.

[39]

Rizzini L, Favory JJ, Cloix C. et al. Perception of UV-B by the Arabidopsis UVR8 protein. Science 2011; 332: 103-6.

[40]

Sebastián D, Fernando FD, Raul DG et al. Overexpression of Arabidopsis aspartic protease APA1 gene confers drought tolerance. Plant Sci. 2020; 292: 110406.

[41]

Deng W, Liu CY, Pei YX et al. Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis . Plant Physiol 2007; 143: 1660-8.

[42]

Han SK, Song JD, Noh YS et al. Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J 2007; 49: 103-14.

[43]

Ahmad M, Jarillo JA, Cashmore AR . Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell. 1998; 10: 197-207.

[44]

Moon JY, Belloeil C, Ianna ML et al. Arabidopsis CNGC family members contribute to heavy metal ion uptake in plants . Int J Mol Sci 2019; 20: 413.

[45]

Kim H, Yu SI, Jung SH et al. The F-box protein SAGL1 and ECERIFERUM3 regulate cuticular wax biosynthesis in response to changes in humidity in Arabidopsis . Plant Cell 2019; 31: 2223-40.

[46]

Zhang M, Wu F, Shi J et al. ROOT HAIR DEFECTIVE3 family of dynamin-like GTPases mediates homotypic endoplasmic reticulum fusion and is essential for Arabidopsis development. Plant Physiol. 2013; 163: 713-20.

[47]

Rodriguez-Hernandez AA, Muro MCV, Ramirez-Alonso JI et al. Modification of AtGRDP1 gene expression affects silique and seed development in Arabidopsis thaliana . Biochem Biophys Res Commun. 2017; 486: 252-6.

[48]

Pokotylo I, Premysl P, Potacky M et al. The plant non-specific phospholipase C gene family. Novel competitors in lipid signalling. Prog Lipid Res. 2013; 52: 62-79.

[49]

Weraduwage SM, Kim SJ, Renna L et al. Pectin methylesterification impacts the relationship between photosynthesis and plant growth. Plant Physiol. 2016; 171: 833-48.

[50]

Mialoundama AS, Jadid N, Brunel J et al. Arabidopsis ERG28 tethers the sterol C4-demethylation complex to prevent accumulation of a biosynthetic intermediate that interferes with polar auxin transport. Plant Cell 2013; 25: 4879-93.

[51]

Fu L, Liu YL, Qin G et al. The TOR-EIN2 axis mediates nuclear signalling to modulate plant growth. Nature. 2021; 591: 288-92.

[52]

Du FK, Hou M, Wang W et al. Phylogeography of Quercus aquifolioides provides novel insights into the Neogene history of a major global hotspot of plant diversity in south-west China. J Biogeogr 2017; 44: 294-307.

[53]

Liu J, Moller M, Provan J et al. Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot. New Phytol. 2013; 199: 1093-108.

[54]

Zhang X, Sun Y, Landis JB et al. Genomic insights into adaptation to heterogeneous environments for the ancient relictual Circaeaster agrestis (Circaeasteraceae, Ranunculales) . New Phytol. 2020; 228: 285-301.

[55]

Wang J, Street NR, Scofield DG et al. Variation in linked selection and recombination drive genomic divergence during allopatric speciation of European and American aspens. Mol Biol Evol. 2016; 33: 1754-67.

[56]

Sun J, Sun R, Liu H et al. Complete chloroplast genome sequencing of ten wild Fragaria species in China provides evidence for phylogenetic evolution of Fragaria . Genomics. 2021; 113: 1170-9.

[57]

Joshi J, Schmid B, Caldeira MC et al. Local adaptation enhances performance of common plant species. Ecol Lett 2001; 4: 536-44.

[58]

Savolainen O, Pyhäjärvi T, Knürr T . Gene flow and local adaptation in trees. Annu Rev Ecol Evol Syst. 2007; 38: 595-619.

[59]

Johnson AL, Govindarajulu R, Ashman TL . Bioclimatic evaluation of geographical range in Fragaria (Rosaceae): consequences of variation in breeding system, ploidy and species age. Bot J Linn Soc 2014; 176: 99-114.

[60]

Yang J, Su D, Wei S et al. Current and future potential distribution of wild strawberry species in the biodiversity hotspot of Yunnan Province. Agronomy. 2020; 10: 959.

[61]

Yan HF, Zhang CY, Wang FY et al. Population expanding with the phalanx model and lineages split by environmental heterogeneity: a case study of Primula obconica in subtropical China. PLoS One 2012; 7: e41315.

[62]

Ye Z, Zhu G, Chen P et al. Molecular data and ecological niche modelling reveal the Pleistocene history of a semi-aquatic bug (Microvelia douglasi douglasi) in East Asia . Mol Ecol 2014; 23: 3080-96.

[63]

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

[64]

Jia KH, Zhao W, Maier PA et al. Landscape genomics predicts climate change-related genetic offset for the widespread Platycladus orientalis (Cupressaceae) . Evol Appl. 2020; 13: 665-76.

[65]

Kondou Y, Miyagi Y, Morito T et al. Physiological function of photoreceptor UVR8 in UV-B tolerance in the liverwort Marchantia polymorpha . Planta. 2019; 249: 1349-64.

[66]

Hamala T, Savolainen O . Genomic patterns of local adaptation under gene flow in Arabidopsis lyrata . Mol Biol Evol 2019; 36: 2557-71.

[67]

Singh A, Roy S . High altitude population of Arabidopsis thaliana is more plastic and adaptive under common garden than controlled condition. BMC Ecol. 2017; 17: 39.

[68]

Li H . Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. https://arxiv.org/abs/1303.3997. 2013. (last accessed January 8, 2020)

[69]

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

[70]

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

[71]

Pritchard JK, Stephans M, Donnelly P . Inference of population structure using multilocus genotype data. Genetics 2000; 155: 945-59.

[72]

Earl DA, Vonholdt BM . STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour. 2012; 4: 359-61.

[73]

Evanno G, Regnaut S, Goudet J . Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005; 14: 2611-20.

[74]

Jakobsson M, Rosenberg NA . CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007; 23: 1801-6.

[75]

Rosenberg NA . DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes. 2004; 4: 137-8.

[76]

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

[77]

Kumar S, Stecher G, Li M et al. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35: 1547-9.

[78]

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

[79]

Schiffels S, Durbin R . Inferring human population size and separation history from multiple genome sequences. Nat Genet 2014; 46: 919-25.

[80]

Browning BL, Browning SR . A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals. Am J Hum Genet. 2009; 84: 210-23.

[81]

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.

[82]

Oksanen J, Kindt, R, Legendre, P. et al. Vegan: Community Ecology Package. R Package Version 2.5-4 (2019). http://CRAN.R-project.org/package=vegan. (last accessed September 10, 2020)

[83]

Hijmans RJ, Williams E, Vennes C . Geosphere: Spherical Trigonometry R package version 1.5-10 . 2019. https://CRAN.R-project.org/package=geosphere. (last accessed September 10, 2020)

[84]

Fick SE, Hijmans RJ . WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol 2017; 37: 4302-15.

[85]

Dray S, Bauman D, Blanchet G et al. Adespatial: Multivariate Multiscale Spatial Analysis R Package Version 0.3-2 . 2018. http://cran.r-project.org/package=adespatial. (last accessed February 26, 2021)

[86]

Rellstab C, Gugerli F, Eckert AJ et al. R. a practical guide to environmental association analysis in landscape genomics. Mol Ecol. 2015; 24: 4348-70.

[87]

Borcard D, Gillet F, Legendre P . Numerical Ecology with R . 2nd ed. Cham, Switzerland: Springer; 2018.

[88]

Alachiotis N, Pavlidis P . RAiSD detects positive selection based on multiple signatures of a selective sweep and SNP vectors. Commun Biol. 2018; 1: 79.

[89]

Szpiech ZA, Novak TE, Bailey NP et al. Application of a novel haplotype-based scan for local adaptation to study high-altitude adaptation in rhesus macaques. Evolution Letters. 2021; 5: 408-421.

[90]

Szpiech ZA, Hernandez RD . Selscan: an efficient multithreaded program to perform EHH-based scans for positive selection. Mol Biol Evol 2014; 31: 2824-7.

[91]

Leroy T, Louvet JM, Lalanne C et al. Adaptive introgression as a driver of local adaptation to climate in European white oaks. New Phytol 2020; 226: 1171-82.

[92]

Gautier M. Genome-wide scan for adaptive divergence and association with population-specific covariates. Genetics. 2015; 201: 1555-79.

[93]

Meirmans PG . The trouble with isolation by distance. Mol Ecol 2012; 21: 2839-46.

[94]

Förstner W, Moonen B . A Metric for Covariance Matrices , in Geodesy - The Challenge of the 3rd Millennium, eds Grafarend EW, Krumm FW, and Schwarze VS, Geodesy - The Challenge of the 3rd Millennium.Berlin: Springer, 2003, 299-309.

[95]

Forester BR, Lasky JR, Wagner HH et al. Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations. Mol Ecol. 2018; 27: 2215-33.

[96]

Alexa A, Rahnenführer J . Gene set enrichment analysis with topGO. Bioconductor Improv. 2009; 27: 1-26.

PDF (860KB)

47

Accesses

0

Citation

Detail

Sections
Recommended

/