Genomic evidence for evolutionary history and local adaptation of two endemic apricots: Prunus hongpingensis and P. zhengheensis

Xiaokang Dai , Songzhu Xiang , Yulin Zhang , Siting Yang , Qianqian Hu , Zhihao Wu , Tingting Zhou , Jingsong Xiang , Gongyou Chen , Xiaohua Tan , Jing Wang , Jihua Ding

Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) : 215

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (4) :215 DOI: 10.1093/hr/uhad215
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Genomic evidence for evolutionary history and local adaptation of two endemic apricots: Prunus hongpingensis and P. zhengheensis
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Abstract

Apricot, belonging to the Armeniaca section of Rosaceae, is one of the economically important crop fruits that has been extensively cultivated. The natural wild apricots offer valuable genetic resources for crop improvement. However, some of them are endemic, with small populations, and are even at risk of extinction. In this study we unveil chromosome-level genome assemblies for two southern China endemic apricots, Prunus hongpingensis (PHP) and P. zhengheensis (PZH). We also characterize their evolutionary history and the genomic basis of their local adaptation using whole-genome resequencing data. Our findings reveal that PHP and PZH are closely related to Prunus armeniaca and form a distinct lineage. Both species experienced a decline in effective population size following the Last Glacial Maximum (LGM), which likely contributed to their current small population sizes. Despite the observed decrease in genetic diversity and heterozygosity, we do not observe an increased accumulation of deleterious mutations in these two endemic apricots. This is likely due to the combined effects of a low inbreeding coefficient and strong purifying selection. Furthermore, we identify a set of genes that have undergone positive selection and are associated with local environmental adaptation in PHP and PZH, respectively. These candidate genes can serve as valuable genetic resources for targeted breeding and improvement of cultivated apricots. Overall, our study not only enriches our comprehension of the evolutionary history of apricot species but also offers crucial insights for the conservation and future breeding of other endemic species amidst rapid climate changes.

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Xiaokang Dai, Songzhu Xiang, Yulin Zhang, Siting Yang, Qianqian Hu, Zhihao Wu, Tingting Zhou, Jingsong Xiang, Gongyou Chen, Xiaohua Tan, Jing Wang, Jihua Ding. Genomic evidence for evolutionary history and local adaptation of two endemic apricots: Prunus hongpingensis and P. zhengheensis. Horticulture Research, 2024, 11 (4) : 215 DOI:10.1093/hr/uhad215

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Acknowledgements

This work was supported by Science and Technology Projects of Shennongjia Academy of Forestry (SAF202104), the National Natural Science Foundation of China (32271824 and 31971676), and the Fundamental Research Funds for the Central Universities (2662019PY007). We would like to thank Dr Xiang Li (Plant Biology Graduate Program and Department of Biology, University of Massachusetts Amherst) for his kind suggestions in bioinformatic analysis. The computations in this paper were run on the bioinformatics computing platform of the National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University.

Author contributions

J.D. and J.W. conceived and designed the research. S.X., S.Y., Z.W., Q.H., X.T., J.X., G.C., and X.D. performed the sampling and collected the materials. Y.Z. performed the genome assembly and annotation. T.Z. prepared DNA for sequencing. X.D. and S.X. conducted all bioinformatic analyses. X.D. wrote the manuscript, with input from J.D. and J.W. All authors read and edited the manuscript prior to publication.

Data availability statement

All Illumina sequence data of DNA raw data used in this study have been submitted to NCBI SRA, with accession number PRJNA957263. The whole-genome sequence and RNA data reported in this paper have been deposited in the Genome Warehouse at the National Genomics Data Center, Beijing Institute of Genomics (China National Center for Bioinformation), Chinese Academy of Sciences, under accession number PRJCA019885.

Conflict of interests

The authors declare no competing interests.

Supplementary information

Supplementary data is available at Horticulture Research online.

References

[1]

Kafkaletou M, Kalantzis I, Karantzi A. et al. Phytochemical characterization in traditional and modern apricot (Prunus armeniaca L.) cultivars - nutritional value and its relation to origin. Sci Hortic. 2019; 253:195-202

[2]

Zhang Q, Liu W. Advances of the apricot resources collection, evaluation and germplasm enhancement. Acta Hortic Sin. 2018; 45:1642-60

[3]

Liu ZE, Wang CH, Liu WQ. et al. Molecular phylogeny of Armeniaca based on nuclear and chloroplast gene sequences: exploring the origin and genetic relationship of Armeniaca hongpingensis. Plant Sci J. 2018; 36:633-41

[4]

Huang X, Tan W, Li F. et al. The chloroplast genome of Prunus zhengheensis: genome comparative and phylogenetic relationships analysis. Gene. 2021; 793:145751

[5]

Groppi A, Liu S, Cornille A. et al. Population genomics of apricots unravels domestication history and adaptive events. Nat Commun. 2021; 12:1-16

[6]

Zhang QX, Zhang H, Sun L. et al. The genetic architecture of floral traits in the woody plant Prunus mume. Nat Commun. 2018; 9:1-12

[7]

Numaguchi K, Akagi T, Kitamura Y. et al. Interspecific introgression and natural selection in the evolution of Japanese apricot (Prunus mume). Plant J. 2020; 104:1551-67

[8]

Zhang Q, Zhang D, Yu K. et al. Frequent germplasm exchanges drive the high genetic diversity of Chinese-cultivated common apricot germplasm. Hortic Res. 2021; 8:215

[9]

Jiang F, Zhang J, Wang S. et al. The apricot (Prunus armeniaca L.) genome elucidates Rosaceae evolution and beta-carotenoid synthesis. Hortic Res. 2019; 6:128

[10]

Li W, Liu L, Wang Y. et al. Genetic diversity, population structure, and relationships of apricot (Prunus) based on restriction site-associated DNA sequencing. Hortic Res. 2020; 7:69

[11]

Wang JQ, Wu B, Cui D. et al. Taxonomic study on Armeniaca Scop. species in China based on thirty morphological characters. J Plant Resour Environ. 2016; 25:103-11

[12]

Burlakova LE, Karatayev AY, Karatayev VA. et al. Endemic species: contribution to community uniqueness, effect of habitat alteration, and conservation priorities. Biol Conserv. 2011; 144:155-65

[13]

Mooney JA, Marsden CD, Yohannes A. et al. Long-term small population size, deleterious variation, and altitude adaptation in the Ethiopian wolf, a severely endangered canid. Mol Biol Evol. 2023; 40:msac277

[14]

Xie H-X, Liang XX, Chen ZQ. et al. Ancient demographics determine the effectiveness of genetic purging in endangered lizards. Mol Biol Evol. 2022; 39:msab359

[15]

Zhang M, Chen X, Lou X. et al. Identification of WUSCHEL-related homeobox (WOX) gene family members and determination of their expression profiles during somatic embryogenesis in Phoebe bournei. Forestry Res. 2023; 3:0.

[16]

Long X, Zhang J, Wang D. et al. Expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Liriodendron hybrids. Forestry Res. 2023; 3:0.

[17]

Liu S, Cornille A, Decroocq S. et al. The complex evolutionary history of apricots: species divergence, gene flow and multiple domestication events. Mol Ecol. 2019; 28:5299-314

[18]

Zhang Q, Zhang H, Sun L. et al. The genetic architecture of floral traits in the woody plant Prunus mume. Nat Commun. 2018; 9:1702

[19]

Alonge M, Lebeigle L, Kirsche M. et al. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol. 2022; 23:258

[20]

Goel M, Sun H, Jiao W-B. et al. SyRI: finding genomic rearrangements and local sequence differences from whole-genome assemblies. Genome Biol. 2019; 20:1-13

[21]

Liu XM, Fu YX. Stairway plot 2: demographic history inference with folded SNP frequency spectra. Genome Biol. 2020; 21:1-9

[22]

Hewitt G. The genetic legacy of the quaternary ice ages. Nature. 2000; 405:907-13

[23]

Pekkala N, Knott KE, Kotiaho JS. et al. The effect of inbreeding rate on fitness, inbreeding depression and heterosis over a range of inbreeding coefficients. Evol Appl. 2014; 7:1107-19

[24]

Yan CC, Song MH, Jiang DC. et al. Genomic evidence reveals intraspecific divergence of the hot-spring snake (Thermophis baileyi), an endangered reptile endemic to the Qinghai-Tibet plateau. Mol Ecol. 2022; 32:1335-50

[25]

Vaser R, Adusumalli S, Leng SN. et al. SIFT missense predictions for genomes. Nat Protoc. 2016; 11:1-9

[26]

Neff MM, Nguyen SM, Malancharuvil EJ. et al. BAS1: a gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. Proc Natl Acad Sci USA. 1999; 96:15316-23

[27]

Turk EM, Fujioka S, Seto H. et al. BAS1 and SOB7 act redundantly to modulate Arabidopsis photomorphogenesis via unique brassinosteroid inactivation mechanisms. Plant J. 2005; 42:23-34

[28]

Taji T, Ohsumi C, Iuchi S. et al. Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 2002; 29:417-26

[29]

Martins CP, Fernandes D, Guimarães VM. et al. Comprehensive analysis of the GALACTINOL SYNTHASE (GolS) gene family in citrus and the function of CsGolS 6 in stress tolerance. PLoS One. 2022; 17:e0274791

[30]

Salvi P, Kamble NU, Majee M. Ectopic over-expression of ABA-responsive chickpea galactinol synthase (CaGolS) gene results in improved tolerance to dehydration stress by modulating ROS scavenging. Environ Exp Bot. 2020; 171:103957

[31]

Sang YP, Long Z, Dan X. et al. Genomic insights into local adaptation and future climate-induced vulnerability of a keystone forest tree in East Asia. Nat Commun. 2022; 13:6541

[32]

Yang YY, Qu XJ, Zhang R. et al. Plastid phylogenomic analyses of Fagales reveal signatures of conflict and ancient chloroplast capture. Mol Phylogenet Evol. 2021; 163:107232

[33]

Muñoz-Rodríguez P, Carruthers T, Wood JRI. et al. Reconciling conflicting phylogenies in the origin of sweet potato and dispersal to Polynesia. Curr Biol. 2018; 28:1246-1256.e12

[34]

Acosta MC, Premoli AC. Evidence of chloroplast capture in south American Nothofagus (subgenus Nothofagus, Nothofagaceae). Mol Phylogenet Evol. 2010; 54:235-42

[35]

Carstens BC, Knowles LL. Shifting distributions and speciation: species divergence during rapid climate change. Mol Ecol. 2007; 16:619-27

[36]

Li J, Shu Q, Zhou S. et al. Review and prospects of quaternary glaciation research in China. J Glaciol Geocryol. 2004; 26:235-43

[37]

Qi XS, Chen C, Comes HP. et al. Molecular data and ecological niche modelling reveal a highly dynamic evolutionary history of the east Asian tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytol. 2012; 196:617-30

[38]

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

[39]

Harrison SP, Yu G, Takahara H. et al. Diversity of temperate plants in East Asia. Nature. 2001; 413:129-30

[40]

Yu G, Chen X, Ni J. et al. Palaeovegetation of China: a pollen data-based synthesis for the mid-Holocene and last glacial maximum. J Biogeogr. 2000; 27:635-64

[41]

Pamilo P, Pálsson S. Associative overdominance, heterozygosity and fitness. Heredity. 1998; 81:381-9

[42]

Lande R. Genetics and demography in biological conservation. Science. 1988; 241:1455-60

[43]

Ji F, Ma Q, Zhang W. et al. A genome variation map provides insights into the genetics of walnut adaptation and agronomic traits. Genome Biol. 2021; 22:1-22

[44]

Gilpin ME. Minimum viable populations:processes of species extinction. In:Soulé ME, ed. Conservation Biology: The Science of Scarcity and Diversity. Sinauer: Sunderland, 1986, 19-34

[45]

Rendón-Anaya M, Wilson J, Sveinsson S. et al. Adaptive introgression facilitates adaptation to high latitudes in European aspen (Populus tremula L.). Mol Biol Evol. 2021; 38:5034-50

[46]

Branco S, Bi K, Liao HL. et al. Continental-level population differentiation and environmental adaptation in the mushroom Suillus brevipes. Mol Ecol. 2017; 26:2063-76

[47]

Ries G, Heller W, Puchta H. et al. Elevated UV-B radiation reduces genome stability in plants. Nature. 2000; 406:98-101

[48]

Zhang J, Tian Y, Yan L. et al. Genome of plant maca (Lepidium meyenii) illuminates genomic basis for high-altitude adaptation in the Central Andes. Mol Plant. 2016; 9:1066-77

[49]

Zhang TC, Qiao Q, Novikova PY. et al. Genome of Crucihimalaya himalaica, a close relative of Arabidopsis, shows ecological adaptation to high altitude. Proc Natl Acad Sci USA. 2019; 116:7137-46

[50]

Geng Y, Guan Y, Qiong L. et al. Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation. BMC Biol. 2021; 19:1-14

[51]

Wang X, Liu S, Zuo H. et al. Genomic basis of high-altitude adaptation in Tibetan Prunus fruit trees. Curr Biol. 2021; 31:3848-3860.e8

[52]

Frohnmeyer H, Staiger D. Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physio. 2003; 133:1420-8

[53]

Tranquillini W. The physiology of plants at high altitudes. Annu Rev Plant Physiol. 1964; 15:345-62

[54]

Carvalho LC, Vilela BJ, Mullineaux PM. et al. Comparative transcriptomic profiling of Vitis vinifera under high light using a custom-made array and the Affymetrix GeneChip. Mol Plant. 2011; 4:1038-51

[55]

Foyer CH, Shigeoka S. Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol. 2011; 155:93-100

[56]

Liu J, Last RL. A land plant-specific thylakoid membrane protein contributes to photosystem II maintenance in Arabidopsis thaliana. Plant J. 2015; 82:731-43

[57]

Zhang M, Zeng Y, Peng R. et al. N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants. Nat Commun. 2022; 13:7441

[58]

Takahashi S, Sakamoto A, Sato S. et al. Roles of Arabidopsis AtREV1 and AtREV7 in translesion synthesis. Plant Physiol. 2005; 138:870-81

[59]

Doyle JJ, Doyle JL. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 1987; 19:11-5

[60]

Xu M, Zang B, Yao H. et al. Isolation of high quality RNA and molecular manipulations with various tissues of Populus. Russ J Plant Physiol. 2009; 56:716-9

[61]

Cheng H, Concepcion GT, Feng X. et al. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. Nat Methods. 2021; 18:170-5

[62]

Durand NC, Shamim MS, Machol I. et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016; 3:95-8

[63]

Dudchenko O, Batra SS, Omer AD. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017; 356:92-5

[64]

Dudchenko O, Shamim M, Batra S. et al. The Juicebox Assembly Tools module facilitates de novo assembly of mammalian genomes with chromosome-length scaffolds for under $1000. BioRxiv. 2018;254797

[65]

Simao FA, Waterhouse RM, Ioannidis P. et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31:3210-2

[66]

Huang X, Wang W, Gong T. et al. The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence. Nat. Plants. 2022; 8:500-12

[67]

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018; 34:3094-100

[68]

Goel M, Schneeberger K. plotsr: visualizing structural similarities and rearrangements between multiple genomes. Bioinformatics. 2022; 38:2922-6

[69]

Wang Y, Tang H, DeBarry JD. et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40:e49

[70]

Wang D, Zhang Y, Zhang Z. et al. KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics. 2010; 8:77-80

[71]

Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019; 20:238

[72]

Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30:772-80

[73]

Minh BQ, Schmidt HA, Chernomor O. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020; 37:1530-4

[74]

Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007; 24:1586-91

[75]

Mendes FK, Vanderpool D, Fulton B. et al. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics. 2021; 36:5516-8

[76]

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

[77]

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

[78]

Kendig KI, Baheti S, Bockol MA. et al. Sentieon DNASeq variant calling workflow demonstrates strong computational performance and accuracy. Front Genet. 2019; 10:736

[79]

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

[80]

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

[81]

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

[82]

Ortiz E. vcf2phylip v2.0: convert a VCF matrix into several matrix formats for phylogenetic analysis. Zenodo. 2019.

[83]

Lewis PO. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol. 2001; 50:913-25

[84]

Bouckaert R, Heled J, Kühnert D. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 2014; 10:e1003537

[85]

Bryant D, Bouckaert R, Felsenstein J. et al. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Mol Biol Evol. 2012; 29:1917-32

[86]

Korneliussen TS, Albrechtsen A, Nielsen R. ANGSD: analysis of next generation sequencing data. BMC Bioinformatics. 2014; 15:1-13

[87]

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 w1118; iso-2; iso-3. Fly (Austin). 2012; 6:80-92

[88]

Pickrell J, Pritchard J. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012;e1002967

[89]

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

[90]

Portik DM, Leaché AD, Rivera D. et al. Evaluating mechanisms of diversification in a Guineo-Congolian tropical forest frog using demographic model selection. Mol Ecol. 2017; 26:5245-63

[91]

Charles KL, Bell RC, Blackburn DC. et al. Sky, sea, and forest islands: diversification in the African leaf-folding frog Afrixalus paradorsalis (Anura: Hyperoliidae) of the lower Guineo-Congolian rain forest. J Biogeogr. 2018; 45:1781-94

[92]

Martin SH, Davey JW, Jiggins CD. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Mol Biol Evol. 2015; 32:244-57

[93]

Zhang XT, Chen S, Shi L. et al. Haplotype-resolved genome assembly provides insights into evolutionary history of the tea plant Camellia sinensis. Nat Genet. 2021; 53:1250-9

[94]

Pavlidis P, Živković D, Stamatakis A. et al. SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol Biol Evol. 2013; 30:2224-34

[95]

Sabeti PC, Varilly P, Fry B. et al. Genome-wide detection and characterization of positive selection in human populations. Nature. 2007; 449:913-8

[96]

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

[97]

Yu GC, Wang LG, Han YY. et al. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics. 2012; 16:284-7

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