Skip to main content
SpringerLink
Log in

Demographic dynamics and molecular evolution of the rare and endangered subsect. Gerardianae of Pinus: insights from chloroplast genomes and mitochondrial DNA markers

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main Conclusion

The divergence of subsect. Gerardianae was likely triggered by the uplift of the Qinghai–Tibetan Plateau and adjacent mountains. Pinus bungeana might have probably experienced expansion since Last Interglacial period.

Abstract

Historical geological and climatic oscillations have profoundly affected patterns of nucleotide variability, evolutionary history, and species divergence in numerous plants of the Northern Hemisphere. However, how long-lived conifers responded to geological and climatic fluctuations in East Asia remain poorly understood. Here, based on paternally inherited chloroplast genomes and maternally inherited mitochondrial DNA markers, we investigated the population demographic history and molecular evolution of subsect. Gerardianae (only including three species, Pinus bungeana, P. gerardiana, and P. squamata) of Pinus. A low level of nucleotide diversity was found in P. bungeana (π was 0.00016 in chloroplast DNA sequences, and 0.00304 in mitochondrial DNAs). The haplotype-based phylogenetic topology and unimodal distributions of demographic analysis suggested that P. bungeana probably originated in the southern Qinling Mountains and experienced rapid population expansion since Last Interglacial period. Phylogenetic analysis revealed that P. gerardiana and P. squamata had closer genetic relationship. The species divergence of subsect. Gerardianae occurred about 27.18 million years ago (Mya) during the middle to late Oligocene, which was significantly associated with the uplift of the Qinghai–Tibetan Plateau and adjacent mountains from the Eocene to the mid-Pliocene. The molecular evolutionary analysis showed that two chloroplast genes (psaI and ycf1) were under positive selection, the genetic lineages of P. bungeana exhibited higher transition and nonsynonymous mutations, which were involved with the strongly environmental adaptation. These findings shed light on the population evolutionary history of white pine species and provide striking insights for comprehension of their species divergence and molecular evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The authors do not have permission to share data.

Abbreviations

cpDNA:

Chloroplast DNA

cp genome:

Chloroplast genome

mtDNA:

Mitochondrial DNA

Mya:

Million years ago

QTP:

Qinghai–Tibetan Plateau

RMSD:

Root-mean-square deviation

SNP:

Single-nucleotide polymorphism

References

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Logse M, Usadel B (2014) Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci USA 101:15255–15260

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WE, Wetter T, Suhai S (2004) Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14:1147–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crampton-Platt A, Timmermans MJ, Gimmel ML, Kutty SN, Cockerill TD, Khen CV, Vogler AP (2015) Soup to tree: the phylogeny of beetles inferred by mitochondrial metagenomics of a bornean rainforest sample. Mol Biol Evol 32:2302–2316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denisov G, Walenz B, Halpern AL, Miller J, Axelrod N, Levy S, Sutton G (2008) Consensus generation and variant detection by celera assembler. Bioinformatics 24:1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Ding L, Liao JC, Liu NF (2020) The uplift of the Qinghai-Tibet Plateau and glacial oscillations triggered the diversification of Tetraogallus (Galliformes, Phasianidae). Ecol Evol 10:1722–1736

    Article  PubMed  PubMed Central  Google Scholar 

  • Donath A, Jühling F, Al-Arab M, Bernhart SH, Reinhardt F, Stadler PF, Middendorf M, Bernt M (2019) Improved annotation of protein-coding genes boundaries in metazoan mitochondrial genomes. Nucleic Acids Res 47:10543–10552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1990) Isolation of plant DNA from plant tissue. Focus 12:13–15

    Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with beauti and the beast 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earl DA, vonHoldt BM (2012) Structure harvester: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Eveno E, Collada C, Guevara MA, Léger V, Soto A, Díaz L, Léger P, González-Martínez SC, Cervera MT, Plomin C, Garnier-Géré PH (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2007) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  PubMed Central  Google Scholar 

  • Fay JC, Wu CI (2000) Hitchhiking under positive darwinian selection. Genetics 155:1405–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu LG, Li N, Mill RR (1999) Pinaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China. Science Press, Missouri Botanical Garden Press, Beijing, St. Louis, pp 25–32

    Google Scholar 

  • Gernandt DS, Liston A, Piñero D (2003) Phylogenetics of Pinus subsections Cembroides and Nelsoniae inferred from cpDNA sequences. Syst Bot 28:657–673

    Google Scholar 

  • Gernandt DS, López GG, García SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42

    Article  Google Scholar 

  • Grant WS, Bowen BW (1998) Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J Hered 89:415–426

    Article  Google Scholar 

  • Guo J-F, Wang BS, Liu Z-L, Mao JF, Wang XR, Zhao W (2021) Low genetic diversity and population connectivity fuel vulnerability to climate change for the Tertiary relict pine Pinus bungeana. J Syst Evol 61:143–156

    Article  Google Scholar 

  • Haddrill PR, Thornton KR, Charlesworth B, Andolfatto P (2005) Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations. Genome Res 15:790–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hahn C, Bachmann L, Chevreux B (2013) Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads-abaiting and iterative mapping approach. Nucleic Acids Res 41:e129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall D, Olsson J, Zhao W, Kroon J, Wennström U, Wang XR (2021) Divergent patterns between phenotypic and genetic variation in Scots pine. Plant Commun 2:100139

    Article  CAS  PubMed  Google Scholar 

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467

    Article  PubMed  Google Scholar 

  • Hao ZZ, Liu YY, Nazaire M, Wei XX, Wang XQ (2015) Molecular phylogenetics and evolutionary history of sect. Quinquefoliae (Pinus): implications for Northern Hemisphere biogeography. Mol Phylogenet Evol 87:65–79

    Article  PubMed  Google Scholar 

  • Hu CY, Zheng XY, Teng YW (2011) Characterization and phylogenetic utility of non-coding chloroplast regions trnL-trnF and accD-psaI in Pyrus. Acta Horticulturae Sinica 38:2261–2272

    CAS  Google Scholar 

  • Huang JH, Huang JH, Liu CR, Zhang JL, Lu XH, Ma KP (2016) Diversity hotspots and conservation gaps for the Chinese endemic seed flora. Biol Conserv 198:104–112

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332

    Article  PubMed  PubMed Central  Google Scholar 

  • IUCN (2012) Guidelines for application of IUCN red list criteria at regional and national levels: Version 4.0. IUCN

  • Jiang XZ, Yu HY, Xiang MC, Liu XY, Liu XZ (2011) Echinochlamydosporium variabile, a new genus and species of Zygomycota from soil nematodes. Fungal Divers 46:43–51

    Article  Google Scholar 

  • Jin W-T, Gernandt DS, Wehenkel C, Xia XM, Wei XX, Wang XQ (2021) Phylogenomic and ecological analyses reveal the spatiotemporal evolution of global pines. Proc Natl Acad Sci USA 118:e2022302118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software versions 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Stur-rock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim KJ, Lee HL (2004) Complete chloroplast genome sequences from Korean ginseng (Panax schinseng Nees) and comparative analysis of sequence evolution among 17 vascular plants. DNA Res 11:247–261

    Article  CAS  PubMed  Google Scholar 

  • Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candiate genes in Douglas fir. Genetics 171:2029–2041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  PubMed  Google Scholar 

  • Laslett D, Canback B (2004) ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Stocks M, Hemmilä S, Källman T, Zhu HT, Zhou Y, Chen J, Liu JQ, Lascoux M (2009) Demographic histories of four spruce (Picea) species of the Qinghai-Tibetan Plateau and neighboring areas inferred from multiple nuclear loci. Mol Biol Evol 27:1001–1014

    Article  PubMed  Google Scholar 

  • Li Y, Gao QB, Gengji ZM, Jia L-K, Wang Z-H, Chen S-L (2018) Rapid intraspecific diversification of the alpine species Saxifraga sinomontana (Saxifragaceae) in the Qinghai-Tibetan Plateau and Himalayas. Front Genet 9:381

    Article  PubMed  PubMed Central  Google Scholar 

  • Librado P, Rozas J (2009) Dnasp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu YY, Jin WT, Wei XX, Wang XQ (2019) Cryptic speciation in the Chinese white pine (Pinus armandii): implications for the high species diversity of conifers in the Hengduan Mountains, a global biodiversity hotspot. Mol Phylogenet Evol 138:114–125

    Article  PubMed  Google Scholar 

  • Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma XF, Szmidt AE, Wang XR (2006) Genetic structure and evolutionary history of a diploid hybrid pine Pinus densata inferred from the nucleotide variation at seven gene loci. Mol Biol Evol 23:807–816

    Article  CAS  PubMed  Google Scholar 

  • Meng ZL, Zaykin DV, Xu CF, Wagner M, Ehm MG (2003) Selection of genetic markers for association analyses, using linkage disequilibrium and haplotypes. Am J Hum Genet 73:115–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell C (1993) MultAlin–multiple sequence alignment. Bioinformatics 9:614

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  ADS  Google Scholar 

  • Nachman MW, Crowell SL (2000) Estimate of the mutation rate per nucleotide in humans. Genetics 156:297–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa T, Ishii C, Kagawa D, Muramoto K, Kamiya H (1999) Accelerated evolution in the protein-coding region of galectin cDNAs, congerin I and congerin II, from skin mucus of conger eel (Conger myriaster). Biosci Biotechnol Biochem 63:1203–1208

    Article  CAS  PubMed  Google Scholar 

  • Palmer JD, Herbon LA (1988) Plant mitochondrial DNA evolves rapidly in structure, but slowly in sequence. J Mol Evol 28:87–97

    Article  CAS  PubMed  ADS  Google Scholar 

  • Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Potter KM, Hipkins VD, Mahalovich MF, Means RE (2015) Nuclear genetic variation across the range of ponderosa pine (Pinus ponderosa): phylogeographic, taxonomic and conservation implications. Tree Genet Genomes 11:38

    Article  Google Scholar 

  • Price RA, Liston A, Strauss SH (1998) Phylogeny and systematics of Pinus. In: Richardson D (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 49–68

    Google Scholar 

  • Pyhäjärvi T, Salmela MJ, Savolainen O (2008) Colonization routes of Pinus sylvestris inferred from distribution of mitochondrial DNA variation. Tree Genet Genom 4:247–254

    Article  Google Scholar 

  • Qian H, Ricklefs RE (2000) Large-scale processes and the Asian bias in species diversity of temperate plants. Nature 407:180–182

    Article  CAS  PubMed  ADS  Google Scholar 

  • Rodríguez-Ezpeleta N, Brinkmann H, Roure B, Lartillot N, Lang BF, Philippe H (2007) Detecting and overcoming systematic errors in genome-scale phylogenies. Syst Biol 56:389–399

    Article  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Saitou N, Ueda S (1994) Evolutionary rates of insertion and deletion in noncoding nucleotide sequences of primates. Mol Biol Evol 11:504–512

    CAS  PubMed  Google Scholar 

  • Sloan DB, Taylor DR (2012) Evolutionary rate variation in organelle genomes: the role of mutational processes. In: Bullerwell CE (ed) Organelle genetics. Springer, Berlin Heidelberg, pp 123–146

    Chapter  Google Scholar 

  • Sobel JM, Chen GF, Watt LR, Schemske DW (2010) The biology of speciation. Evolution 64:295–315

    Article  PubMed  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Straub SCK, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot 99:349–364

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Twyford AD, Ness RW (2017) Strategies for complete plastid genome sequencing. Mol Ecol Resour 17:858–868

    Article  PubMed  Google Scholar 

  • Umar Z, Dong WL, Zhang TT, Wang R-N, Shahzad K, Ma X-F, Li Z-H (2020) Comparative plastid genomics of Pinus species: insights into sequence variations and phylogenetic relationships. J Syst Evol 58:118–132

    Article  Google Scholar 

  • Walker JF, Walker-Hale N, Vargas OM, Larson DA, Stull GW (2019) Characterizing gene tree conflict in plastome-inferred phylogenies. PeerJ 7:e7747

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang B, Mao JF, Gao J, Zhao W, Wang XR (2011) Colonization of the Tibetan Plateau by the homoploid hybrid pine Pinus densata. Mol Ecol 20:3796–3811

    Article  PubMed  Google Scholar 

  • Wang S, Shi C, Gao LZ (2013) Plastid genome sequence of a wild woody oil species, Prinsepia utilis, provides insights into evolutionary and mutational patterns of Rosaceae chloroplast genomes. PLoS One 8:e73946

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Wang W, Chen X, Wolin SL, Xiong Y (2018a) Structural basis for tRNA mimicry by a bacterial Y RNA. Structure 26:1635–1644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang YC, Liao L, Li ZZ (2018b) Genetic differentiation of Actinidia chinensis and analysis of gene flow barriers in the Qinling Mountains, the species’ northern distribution boundary. Genet Resour Crop Evol 65:881–895

    Article  Google Scholar 

  • Wang N, Dong W-L, Zhang X-J, Zhou T, Huang X-J, Li B-G, Liu J-N, Ma X-F, Li Z-H (2021) Evolutionary characteristics and phylogeny of cotton chloroplast tRNAs. Planta 254:116

    Article  CAS  PubMed  Google Scholar 

  • Weber F, Dietrich A, Weil J-H, Maréchal-Drouard L (1990) A potato mitochondrial isoleucine tRNA is coded for by a mitochondrial gene possessing a methionine anticodon. Nucl Acids Res 18:5027–5030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu SD, Wang Y, Wang ZF, Shrestha N, Liu JQ (2022) Species divergence with gene flow and hybrid speciation on the Qinghai–Tibet Plateau. New Phytol 234:392–404

    Article  CAS  PubMed  Google Scholar 

  • Yang ZH (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Nielsen R (2002) Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19:908–917

    Article  CAS  PubMed  Google Scholar 

  • Yang YX, Zhi LQ, Jia Y, Zhong Q-Y, Liu Z-L, Yue M, Li Z-H (2020) Nucleotide diversity and demographic history of Pinus bungeana, an endangered conifer species endemic in China. J Syst Evol 58:282–294

    Article  Google Scholar 

  • Yin A, Harrison TM (2000) Geologic evolution of the Himalayan–Tibetan orogen. Annu Rev Earth Planet Sci 28:211–280

    Article  CAS  ADS  Google Scholar 

  • Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693

    Article  CAS  PubMed  ADS  Google Scholar 

  • Zhang ZY, Yang JB, Li DZ (2003) Phylogenetic relationship of an extremely endangered species, Pinus squamata (Pinaceae) inferred from four sequences of the chloroplast genome and ITS of the nuclear ribosomal DNA. Acta Bot Sin 45:530–535

    CAS  Google Scholar 

  • Zhang TT, Liu H, Gao QY, Yang T, Liu JN, Ma XF, Li Z-H (2020a) Gene transfer and nucleotide sequence evolution by Gossypium cytoplasmic genomes indicates novel evolutionary characteristics. Plant Cell Rep 39:765–777

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Wang J, Xiao Y (2020b) 3dRNA: Building RNA 3D structure with improved template library. Comput Struct Biotechnol J 18:2416–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao W, Sun YQ, Pan J, Sullivan AR, Arnold ML, Mao JF, Wang XR (2020) Effects of landscapes and range expansion on population structure and local adaptation. New Phytol 228:330–343

    Article  CAS  PubMed  Google Scholar 

  • Zhong QY, Fu XG, Zhang TT, Zhou T, Yue M, Liu JN, Li ZH (2021) Phylogeny and evolution of chloroplast tRNAs in Adoxaceae. Ecol Evol 11:1294–1309

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou YF, Zhang LR, Liu JQ, Wu GL, Savolainen O (2014) Climatic adaptation and ecological divergence between two closely related pine species in Southeast China. Mol Ecol 23:3504–3522

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (31970359) and the Key Program of Research and Development of Shaanxi Province (2022ZDLSF06-02).

Author information

Authors and Affiliations

  1. Key Laboratory of Resource Biology and Biotechnology in Western China (Ministry of Education), College of Life Sciences, Northwest University, Xi’an, 710069, China

    Ting-Ting Zhang, Chun-Li Yan, Jin-Xia Qiao, Ao-Shuang Yang, Mi-Li Liu & Zhong-Hu Li

  2. Laboratory of Subtropical Biodiversity, Jiangxi Agricultural University, Nanchang, 330045, China

    Yi-Xuan Kou

Authors
  1. Ting-Ting Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chun-Li Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin-Xia Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ao-Shuang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mi-Li Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yi-Xuan Kou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhong-Hu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZHL and YXK designed the research and contributed the materials. JXQ and ASY performed the experiments. TTZ and CLY carried out data analysis. MLL contributed analysis tools. TTZ wrote the first draft of the manuscript. ZHL revised the paper. All authors have approved the final paper.

Corresponding author

Correspondence to Zhong-Hu Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Dorothea Bartels.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Fig. S1 Geographical distribution of the samples used in the study (PDF 12417 kb)

Fig. S2 Mantel test based on the cpDNA sequences of P. bungeana (PDF 410 kb)

Fig. S3 Mantel test based on the mtDNA sequences of P. bungeana (PDF 425 kb)

425_2023_4316_MOESM4_ESM.pdf

Fig. S4 LnP(D) and ΔK test based on the cpDNA sequences for the 18 populations of P. bungeana. a LnP(D) for K from 1 to 15. b ΔK for K from 1 to 15 (PDF 123 kb)

425_2023_4316_MOESM5_ESM.pdf

Fig. S5 Results of structure based on the cpDNA sequences for the 18 populations of P. bungeana (when K was 2, 3, and 4) (PDF 353 kb)

425_2023_4316_MOESM6_ESM.pdf

Fig. S6 LnP(D) and ΔK test based on the mtDNA sequences for the 18 populations of P. bungeana. a LnP(D) for K from 1 to 15. b ΔK for K from 1 to 15 (PDF 125 kb)

425_2023_4316_MOESM7_ESM.pdf

Fig. S7 Results of structure based on the mtDNA sequences for the 18 populations of P. bungeana (when K was 2, 3, and 4) (PDF 365 kb)

425_2023_4316_MOESM8_ESM.pdf

Fig. S8 Secondary structure of typical clover and unconventional structures for chloroplast genomic tRNAs. a The typical clover structure for tRNAArg. b tRNASer with unconventional structure. c tRNALeu with unconventional structure. d tRNATyr with unconventional structure (PDF 408 kb)

425_2023_4316_MOESM9_ESM.pdf

Fig. S9 Tertiary structures of typical and unconventional chloroplast genomic tRNAs. a The typical tertiary structure for tRNAArg. b tRNASer with unconventional tertiary structure. c tRNALeu with unconventional tertiary structure. d tRNATyr with unconventional tertiary structure (PDF 20991 kb)

425_2023_4316_MOESM10_ESM.pdf

Fig. S10 The root-mean-square deviation (RMSD) of the same tRNAs molecules between P. bungeana (red) and P. squamata (blue). a The RMSD of tRNAArg (0.172) between P. bungeana (red) and P. squamata (blue). b The RMSD of tRNATrp (1.748) between P. bungeana (red) and P. squamata (blue). c The RMSD of tRNAMet (10.542) between P. bungeana (red) and P. squamata (blue). d The RMSD of tRNAGlu (0.578) between P. bungeana (red) and P. squamata (blue) (PDF 6516 kb)

425_2023_4316_MOESM11_ESM.pdf

Fig. S11 The root-mean-square deviation (RMSD) of the same tRNAs molecules between P. bungeana (red) and P. gerardiana (blue). a The RMSD of tRNAArg (0.185) between P. bungeana (red) and P. gerardiana (blue). b The RMSD of tRNATrp (0.018) between P. bungeana (red) and P. gerardiana (blue). c The RMSD of tRNAMet (8.172) between P. bungeana (red) and P. gerardiana (blue). d The RMSD of tRNAGlu (0.297) between P. bungeana (red) and P. gerardiana (blue) (PDF 7341 kb)

425_2023_4316_MOESM12_ESM.pdf

Fig. S12 The root-mean-square deviation (RMSD) of the same tRNA molecules between P. squamata (red) and P. gerardiana (blue). a The RMSD of tRNAArg (0.036) between P. squamata (red) and P. gerardiana (blue). b The RMSD of tRNATrp (1.734) between P. squamata (red) and P. gerardiana (blue). c The RMSD of tRNAMet (8.173) between P. squamata (red) and P. gerardiana (blue). d The RMSD of tRNAGlu (0.571) between P. squamata (red) and P. gerardiana (blue) (PDF 6315 kb)

Supplementary file13 (DOC 1191 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, TT., Yan, CL., Qiao, JX. et al. Demographic dynamics and molecular evolution of the rare and endangered subsect. Gerardianae of Pinus: insights from chloroplast genomes and mitochondrial DNA markers. Planta 259, 45 (2024). https://doi.org/10.1007/s00425-023-04316-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-023-04316-8

Keywords

Search

Navigation