High-resolution genome assembly and population genetic study of the endangered maple Acer pentaphyllum (Sapindaceae): implications for conservation strategies

Xiong Li , Li-Sha Jiang , Heng-Ning Deng , Qi Yu , Wen-Bin Ju , Xiao-Juan Chen , Yu Feng , Bo Xu

Horticulture Research ›› 2025, Vol. 12 ›› Issue (4) : 357

PDF (2934KB)
Horticulture Research ›› 2025, Vol. 12 ›› Issue (4) :357 DOI: 10.1093/hr/uhae357
ARTICLES
High-resolution genome assembly and population genetic study of the endangered maple Acer pentaphyllum (Sapindaceae): implications for conservation strategies
Author information +
History +
PDF (2934KB)

Abstract

Acer pentaphyllum Diels (Sapindaceae), a highly threatened maple endemic to the dry-hot valleys of the Yalong River in western Sichuan, China, represents a valuable resource for horticulture and conservation. This study presents the first chromosomal-scale genome assembly of A. pentaphyllum (~626 Mb, 2n = 26), constructed using PacBio HiFi and Hi-C sequencing technologies. Comparative genomic analyses revealed significant recent genomic changes through rapid amplification of transposable elements, particularly long terminal repeat retrotransposons, coinciding with the dramatic climate change during recent uplift of the Hengduan Mountains. Genes involved in photosynthesis, plant hormone signal transduction, and plant-pathogen interaction showed expansion and/or positive selection, potentially reflecting adaptation to the species’ unique dry-hot valley habitat. Population genomic analysis of 227 individuals from 28 populations revealed low genetic diversity (1.04 ± 0.97 × 10−3) compared to other woody species. Phylogeographic patterns suggest an unexpected upstream colonization along the Yalong River, while Quaternary climate fluctuations drove its continuous lineage diversification and population contraction. Assessment of genetic diversity, inbreeding, and genetic load across populations revealed concerning levels of inbreeding and accumulation of deleterious mutations in small, isolated populations, particularly those at range edges (TKX, CDG, TES). Based on these results, we propose conservation strategies, including the identification of management units and recommendations for genetic rescue. These findings not only facilitate the conservation of A. pentaphyllum but also serve as a valuable resource for future horticultural development and as a model for similar studies on other endangered plant species adapted to extreme environments.

Cite this article

Download citation ▾
Xiong Li, Li-Sha Jiang, Heng-Ning Deng, Qi Yu, Wen-Bin Ju, Xiao-Juan Chen, Yu Feng, Bo Xu. High-resolution genome assembly and population genetic study of the endangered maple Acer pentaphyllum (Sapindaceae): implications for conservation strategies. Horticulture Research, 2025, 12(4): 357 DOI:10.1093/hr/uhae357

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

We thank Min Liao, Junyi Zhang, Yushan Zhou, Shuo Tan, Cier Zhongyang, and Pianchu for assistance with sample collection. We thank Yongling Qiu for her help with writing. We also gratefully thank Wentai Dai for providing transcriptome data of leaves. This work was supported by the National Natural Science Foundation of China (NSFC Grant No. 32400304), the Wild Plants Sharing and Service Platform of Sichuan Province, and the Western China Youth Scholars Project.

Author contributions

B.X. conceived the project. B.X. and Y.F. designed the research. X.L., Q.Y., H.N.D., L.S.J., Y.F., and W.B.J. collected the materials. X.L. and Y.F. analyzed the data. X.J.C. performed species distribution modeling. X.L., Y.F., B.X., and W.B.J. contributed to the interpretation of results. X.L., Y.F., and L.S.J. wrote the manuscript, B.X. and Y.F. revised the manuscript. All authors read and approved the manuscript.

Data availability

All data that support the findings of this study, including sequencing data, reference genome, and gene annotations, have been deposited into CNGB Sequence Archive (CNSA; [110]) of China National GeneBank DataBase (CNGBdb) with accession number CNP0006021 (reviewer link: http://db.cngb.org/cnsa/project/CNP0006021_715ecb62/reviewlink/).

Conflict of interests

All authors declare no conflict of interest.

Supplementary Data

Supplementary data is available at Horticulture Research online.

References

[1]

Stevens PF. Angiosperm Phylogeny Website. Version 14. Angiosperm Phylogeny Website. Version 13. 2016.

[2]

Xu TZ, Chen YS, de Jong PC. et al. Aceraceae. In: Wu ZY, Raven PH, Hong DY, eds. FloraofChina: Science Press St. Louis, USA: Missouri Botanical Garden Press: Beijing, China, 2008,515-53

[3]

Bi W, Gao Y, Shen J. et al. Traditional uses, phytochemistry, and pharmacology of the genus Acer (maple): a review. J Ethnophar-macol. 2016; 189:31-60

[4]

González-Sarrías A, Li L, Seeram NP. Effects of maple (Acer) plant part extracts on proliferation, apoptosis and cell cycle arrest of human tumorigenic and non-tumorigenic colon cells. Phytother Res. 2012; 26:995-1002

[5]

Sun ZY, Li MF, Li BJ. et al. Rare and endangered plant Acer pen-taphyllum in Yajiang County, Sichuan. Journal of Sichuan Forestry Science and Technology. 2010; 31:86-7

[6]

Yin KP. A rare photograph—a field record of Acer pentaphyllum. Plant J. 1997; 05:2

[7]

McNamara WA. 708. Acer pentaphyllum: Sapindaceae. Curtis’s Botanical Magazine. 2011; 28:128-40

[8]

Pan HL, Feng QH, Long TL. et al. Discussion on resource condi-tion and protection technique for rare endangered species in Sichuan Province. Journal of Sichuan Forestry Science and Technol-ogy. 2014; 35:41-6

[9]

Hao YQ, Luo XB, Wang XL. Genetic diversity of the endangered Acer pentaphyllum Diels by ISSR analysis. Journal of Sichuan Uni-versity (Natural Science Edition). 2019; 56:161-6

[10]

Luo XB, Wang XL, Hao YQ. et al. A study of species diversity and dominant species niche characteristics of Acer pentaphyllum community. Journal of Sichuan Forestry Science and Technology. 2017; 38:79-83

[11]

Roh MS, McNamara WA, Barnes C. et al. Genetic variations of Acer pentaphyllum based on AFLP analysis, seed germination, and seed morphology Kaipu Yin and Qian Wang Chengdu institute of biology. Acta Hortic. 2010; 885:305-12

[12]

Li DQ, Peng YS, Zhang ZX. et al. Research overview and devel-opment strategy analysis of rare and endangered plant Acer pentaphyllum Diels. Jiangxi Science. 2019; 37:190-192+220

[13]

Yang J, Wariss HM, Tao LD. et al. De novo genome assembly of the endangered Acer yangbiense, a plant species with extremely small populations endemic to Yunnan Province, China. Giga-science. 2019; 8:giz085

[14]

Liang Q, Li H, Li S. et al. The genome assembly and annota-tion of yellowhorn (Xanthoceras sorbifolium Bunge). Gigascience. 2019; 8:giz071

[15]

Yu T, Hu YH, Zhang YY. et al. Whole-genome sequencing of Acer catalpifolium reveals evolutionary history of endangered species. Genome Biol Evol. 2021; 13:evab271

[16]

McEvoy SL, Sezen UU, Trouern-Trend A. et al. Strategies of tolerance reflected in two North American maple genomes. Plant J. 2022; 109:1591-613

[17]

Li X, Cai K, Han ZM. et al. Chromosome-level genome assem-bly for Acer pseudosieboldianum and highlights to mechanisms for leaf color and shape change. Front Plant Sci. 2022; 13: 850054

[18]

Lu XY, Chen Z, Liao BY. et al. The chromosome-scale genome provides insights into pigmentation in Acer rubrum. Plant Physiol Biochem. 2022; 186:322-33

[19]

Chen Z, Lu XY, Zhu L. et al. Chromosomal-level genome and multi-omics dataset provides new insights into leaf pigmenta-tion in Acer palmatum. Int J Biol Macromol. 2023; 227:93-104

[20]

Yang Y, Ma T, Wang ZF. et al. Genomic effects of population col-lapse in a critically endangered ironwood tree Ostrya rehderiana. Nat Commun. 2018; 9:5449

[21]

Feng Y, Comes HP, Chen J. et al. Genome sequences and popu-lation genomics provide insights into the demographic history, inbreeding, and mutation load of two ‘living fossil’ tree species of Dipteronia. Plant J. 2024; 117:177-92

[22]

Chen Y, Ma T, Zhang LS. et al. Genomic analyses of a "liv-ing fossil": the endangered dove-tree. Mol Ecol Resour. 2020; 20: 756-69

[23]

Vurture GW, Sedlazeck FJ, Nattestad M. et al. GenomeScope: fast reference-free genome profiling from short reads. Bioinfor-matics. 2017; 33:2202-4

[24]

Li Z, Barker MS. Inferring putative ancient whole-genome duplications in the 1000 plants (1KP) initiative: access to gene family phylogenies and age distributions. Gigascience. 2020; 9:giaa004

[25]

Ma H, Liu YB, Liu DT. et al. Chromosome-level genome assembly and population genetic analysis of a critically endangered rhododendron provide insights into its conservation. Plant J. 2021; 107:1533-45

[26]

Zhu S, Chen J, Zhao J. et al. Genomic insights on the contribu-tion of balancing selection and local adaptation to the long-term survival of a widespread living fossil tree, Cercidiphyllum japonicum. New Phytol. 2020; 228:1674-89

[27]

Cai L, Liu DT, Yang FM. et al. The chromosome-scale genome of Magnolia sinica (Magnoliaceae) provides insights into the con-servation of plant species with extremely small populations (PSESP). Gigascience. 2024; 13:giad110

[28]

Chen ZY, Ai FD, Zhang JL. et al. Survival in the tropics despite isolation, inbreeding and asexual reproduction: insights from the genome of the world’s southernmost poplar (Populus ilicifo-lia). Plant J. 2020; 103:430-42

[29]

Ceballos FC, Joshi PK, Clark DW. et al. Runs of homozygosity: windows into population history and trait architecture. Nat Rev Genet. 2018; 19:220-34

[30]

Excoffier L, Dupanloup I, Huerta-Sánchez E. et al. Robust demo-graphic inference from genomic and SNP data. PLoS Genet. 2013; 9:e1003905

[31]

Xing Y, Ree RH. Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc Natl Acad Sci USA. 2017; 114:E3444-51

[32]

Ding WN, Ree RH, Spicer RA. et al. Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora. Science. 2020; 369:578-81

[33]

Belyayev A. Bursts of transposable elements as an evolutionary driving force. J Evol Biol. 2014; 27:2573-84

[34]

Canapa A, Barucca M, Biscotti MA. et al. Transposons, genome size, and evolutionary insights in animals. Cytogenet Genome Res. 2015; 147:217-39

[35]

Kinoshita N, Wang H, Kasahara H. et al. IAA-ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidop-sis root architecture changes during high osmotic stress. Plant Cell. 2012; 24:3590-602

[36]

Yang T, Wang Y, Teotia S. et al. The interaction between miR160 and miR165/ 166 in the control of leaf development and drought tolerance in Arabidopsis. Sci Rep. 2019; 9:2832

[37]

Jones JDG, Dangl JL. The plant immune system. Nature. 2006; 444:323-9

[38]

Sun H, Zhang J, Deng T. et al. Origins and evolution of plant diversity in the Hengduan Mountains, China. Plant Divers. 2017; 39:161-6

[39]

Yue LL, Chen G, Sun WB. et al. Phylogeography of Buddleja crispa (Buddlejaceae) and its correlation with drainage sys-tem evolution in southwestern China. Am J Bot. 2012; 99: 1726-35

[40]

Feng B, Zhao Q, Xu J. et al. Drainage isolation and climate change-driven population expansion shape the genetic struc-tures of tuber indicum complex in the Hengduan Mountains region. Sci Rep. 2016; 6:21811

[41]

Tessier JT. Evidence of capacity for water dispersal in Acer saccharum. Ecosphere. 2019; 14:1267714

[42]

Wu H, Yan LP, Li CZ. et al. Morphological characteristics and wind dispersal characteristics of samara of common Acer species. J Nanjing For Univ. 2021; 45:103

[43]

Ma HC, McConchie JA. The dry-hot valleys and forestation in Southwest China. JForRes. 2001; 12:35-9

[44]

Ou X, Replumaz A. Landscape modelling of the Yalong River catchment during the uplift of Southeast Tibet. Earth Planet Sci Lett. 2024; 637:118721

[45]

Rohrmann A, Kirby E, Schwanghart W. Accelerated Miocene incision along the Yangtze River driven by headward drainage basin expansion. Sci Adv. 2023; 9:eadh1636

[46]

Huang YJ, Su T, Zhu H. et al. Vegetation diversity and distri-bution in the Pliocene of the southern Hengduan Mountains region. Biodivers Sci. 2022; 30:22295

[47]

Gao J, Liao PC, Huang BH. et al. Historical biogeography of Acer L. (Sapindaceae): genetic evidence for out-of-Asia hypothesis with multiple dispersals to North America and Europe. Sci Rep. 2020; 10:21178

[48]

Li J, Stukel M, Bussies P. et al. Maple phylogeny and biogeog-raphy inferred from phylogenomic data. J Syst Evol. 2019; 57: 594-606

[49]

Henrot AJ, Utescher T, Erdei B. et al. Middle Miocene climate and vegetation models and their validation with proxy data. Palaeogeogr Palaeoclimatol Palaeoecol. 2017; 467:95-119

[50]

Hui Z, Zhou X, Chevalier M. et al. Miocene East Asia summer monsoon precipitation variability and its possible driving forces. Palaeogeogr Palaeoclimatol Palaeoecol. 2021; 581: 110609

[51]

Yao YF, Bruch AA, Cheng YM. et al. Monsoon versus uplift in southwestern China-late Pliocene climate in Yuanmou Basin, Yunnan. PLoS One. 2012; 7:e37760

[52]

Ge J, Dai Y, Zhang Z. et al. Major changes in east Asian climate in the mid-Pliocene: triggered by the uplift of the Tibetan plateau or global cooling? J Asian Earth Sci. 2013; 69:48-59

[53]

Liu FL, Gao HS, Pan BT. et al. The genesis, age and its pale-oclimatic significance of loess-like sediments in the Huatan section of the dry-hot valley of the Jinsha River. J Desert Res. 2020; 42:60-70

[54]

Wei XY, Wang T, Zhou J. et al. Simplified genomic data revealing the decline of Aleuritopteris grevilleoides population accompa-nied by the uplift of dry-Hot Valley in Yunnan, China. Plants. 2023; 12:1579

[55]

Li YC, Zhang Z, Ding GQ. et al. Late Pliocene and early Pleistocene vegetation and climate change revealed by a pollen record from Nihewan Basin, North China. Quat Sci Rev. 2019c; 222:105905

[56]

Legrain E, Parrenin F, Capron E. A gradual change is more likely to have caused the mid-Pleistocene transition than an abrupt event. Commun Earth Environ. 2023; 4:90

[57]

Ma YP, Liu DT, Wariss HM. et al. Demographic history and iden-tification of threats revealed by population genomic analysis provide insights into conservation for an endangered maple. Mol Ecol. 2021; 31:767-79

[58]

Liu Y, Cai L, Sun WB. Transcriptome data analysis pro-vides insights into the conservation of Michelia lacei, a plant species with extremely small populations distributed in Yun-nan province, China. BMC Plant Biol. 2024; 24:200

[59]

Hu WJ, Hao ZQ, Du PY. et al. Genomic inference of a severe human bottleneck during the Early to Middle Pleistocene tran-sition. Science. 2023; 381:979-84

[60]

Ferchaud AL, Perrier C, April J. et al. Making sense of the rela-tionships between Ne, Nb and Nc towards defining conservation thresholds in Atlantic salmon (Salmo salar). Heredity. 2016; 117: 268-78

[61]

Agrawal AF, Whitlock MC. Mutation load: the fitness of indi-viduals in populations where deleterious alleles are abundant. Annu Rev Ecol Evol Syst. 2012; 43:115

[62]

Höglund J. Evolutionary Conservation Genetics. Oxford University Press; 2009:

[63]

Lynch M, Burger R, Butcher D. et al. The mutational meltdown in asexual populations. J Hered. 1993; 84:339-44

[64]

Robinson J, Kyriazis CC, Yuan SC. et al. Deleterious variation in natural populations and implications for conservation genet-ics. Ann Rev Anim Biosci. 2023; 11:93-114

[65]

Teixeira JC, Huber CD. The inflated significance of neutral genetic diversity in conservation genetics. Proc Natl Acad Sci USA. 2021; 118:e2015096118

[66]

Xie HX, Liang XX, Chen ZQ. et al. Ancient demographics determine the effectiveness of genetic purging in endangered lizards. MolBiolEvol. 2021; 39:msab359

[67]

Caughley G. Directions in conservation biology. JAnimEcol. 1994; 63:215-44

[68]

Frankham R. Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv. 2010; 143: 1919-27

[69]

Porebski S, Bailey LG, Baum BR. Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Report. 1997; 15:8-15

[70]

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

[71]

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

[72]

Walker BJ, Abeel T, Shea T. et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014; 9:e112963

[73]

Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. 2013; arXiv e-prints

[74]

Burton JN, Adey A, Patwardhan RP. et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol. 2013; 31:1119-25

[75]

Li H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics. 2016; 32: 2103-10

[76]

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

[77]

Simão F, Waterhouse RM, Panagiotis I. et al. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015; 31:3210-2

[78]

Cheng CY, Krishnakumar V, Chan AP. et al. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 2017; 89:789-804

[79]

Wang X, Xu YT, Zhang SQ. et al. Genomic analyses of primitive, wild and cultivated citrus provide insights into asexual repro-duction. Nat Genet. 2017; 49:765-72

[80]

Myburg AA, Grattapaglia D, Tuskan GA. et al. The genome of Eucalyptus grandis. Nature. 2014; 510:356-62

[81]

Zhang WP, Lin JS, Li JG. et al. Rambutan genome revealed gene networks for spine formation and aril development. Plant J. 2021; 108:1037-52

[82]

Canaguier A, Grimplet J, Di Gaspero G. et al. A new version of the grapevine reference genome assembly (12X.v2) and of its annotation (VCost.v3). Genom Data. 2017; 14:56-62

[83]

Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015; 16:157

[84]

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

[85]

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

[86]

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

[87]

McClain AM, Manchester SR. Dipteronia (Sapindaceae) from the tertiary of North America and implications for the phytogeo-graphic history of the Aceroideae. Am J Bot. 2001; 88:1316-25

[88]

De Bie T, Cristianini N, Demuth JP. et al. CAFE: a computa-tional tool for the study of gene family evolution. Bioinformatics. 2006; 22:1269-71

[89]

Tang H, Bowers JE, Wang X. et al. Synteny and collinearity in plant genomes. Science. 2008; 320:486-8

[90]

Sun PC, Jiao BB, Yang YZ. et al. WGDI: a user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. Mol Plant. 2022; 15:1841-51

[91]

Edgar RC. Muscle5: high-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny. Nat Commun. 2022; 13:6968

[92]

Hu TT, Pattyn P, Bakker EG. et al. The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet. 2011; 43:476-81

[93]

Slotte T, Hazzouri KM, Agren JA. et al. The Capsella rubella genome and the genomic consequences of rapid mating sys-tem evolution. Nat Genet. 2013; 45:831-5

[94]

Van der Auwera GA, Carneiro MO, Hartl C. et al. From FastQ data to high confidence variant calls: the genome analy-sis toolkit best practices pipeline. Curr Protoc Bioinformatics. 2013; 43:11.10.1-33

[95]

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

[96]

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

[97]

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

[98]

Manichaikul A, Mychaleckyj JC, Rich SS. et al. Robust relation-ship inference in genome-wide association studies. Bioinformat-ics. 2010; 26:2867-73

[99]

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

[100]

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

[101]

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

[102]

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

[103]

Liu X, Fu YX. Stairway plot 2: demographic history inference with folded SNP frequency spectra. Genome Biol. 2020; 21:280

[104]

Hartl DL, Clark AG. Principles of Population Genetics.4th ed.Los Angeles: Sinauer Associates; 2007

[105]

Grantham R. Amino acid difference formula to help explain protein evolution. Science. 1974; 185:862-4

[106]

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

[107]

Cingolani P, Platts A, Wang le L. 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. 2012; 6:80-92

[108]

Do R, Balick D, Li H. et al. No evidence that selection has been less effective at removing deleterious mutations in Europeans than in Africans. Nat Genet. 2015; 47:126-31

[109]

Feng Y.Phylogenetic and conservation genomic study of dipteronia. PhD dissertation, Zhejiang University; 2021

[110]

Guo XQ, Chen FZ, Gao F. et al. CNSA: a data repository for archiving omics data. Database (Oxford). 2020; 2020:baaa055

PDF (2934KB)

1127

Accesses

0

Citation

Detail

Sections
Recommended

/