Skip to main content
SpringerLink
Log in

Gene transfer and nucleotide sequence evolution by Gossypium cytoplasmic genomes indicates novel evolutionary characteristics

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

The DNA fragments transferred among cotton cytoplasmic genomes are highly differentiated. The wild D group cotton species have undergone much greater evolution compared with cultivated AD group.

Abstract

Cotton (Gossypium spp.) is one of the most economically important fiber crops worldwide. Gene transfer, nucleotide evolution, and the codon usage preferences in cytoplasmic genomes are important evolutionary characteristics of high plants. In this study, we analyzed the nucleotide sequence evolution, codon usage, and transfer of cytoplasmic DNA fragments in Gossypium chloroplast (cp) and mitochondrial (mt) genomes, including the A genome group, wild D group, and cultivated AD group of cotton species. Our analyses indicated that the differences in the length of transferred cytoplasmic DNA fragments were not significant in mitochondrial and chloroplast sequences. Analysis of the transfer of tRNAs found that trnQ and nine other tRNA genes were commonly transferred between two different cytoplasmic genomes. The Codon Adaptation Index values showed that Gossypium cp genomes prefer A/T-ending codons. Codon preference selection was higher in the D group than the other two groups. Nucleotide sequence evolution analysis showed that intergenic spacer sequences were more variable than coding regions and nonsynonymous mutations were clearly more common in cp genomes than mt genomes. Evolutionary analysis showed that the substitution rate was much higher in cp genomes than mt genomes. Interestingly, the D group cotton species have undergone much faster evolution compared with cultivated AD groups, possibly due to the selection and domestication of diverse cotton species. Our results demonstrate that gene transfer and differential nucleotide sequence evolution have occurred frequently in cotton cytoplasmic genomes.

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

Similar content being viewed by others

References

  • Adams KL, Wendel JF (2004) Exploring the genomic mysteries of polyploidy in cotton. Biol J Linnean Soc 82(4):573–581

    Article  Google Scholar 

  • Agris PF (2004) Decoding the genome: a modified view. Nucleic Acids Res 32(1):223–238

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Amaral-Zettler LA, Dragone NB, Schell J, Slikas B, Murphy LG, Morrall CE, Zettler ER (2017) Comparative mitochondrial and chloroplast genomics of a genetically distinct form of sargassum contributing to recent "golden tides" in the western Atlantic. Ecol Evol 7(2):516–525

    Article  PubMed  Google Scholar 

  • Beasley JO (1940) The origin of American tetraploid Gossypium species. Am Nat 74(752):285–286

    Article  Google Scholar 

  • Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69(2):313–319

    Article  PubMed  Google Scholar 

  • Braukmann T, Kuzmina M, Stefanović S (2013) Plastid genome evolution across the genus Cuscuta (Convolvulaceae): two clades within subgenus grammica exhibit extensive gene loss. J Exp Bot 64(4):977–989

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bright SW, Wood EA, Miflin BJ (1978) The effect of aspartate-derived amino acids (Lysine, Threonine, Methionine) on the growth of excised embryos of wheat and barley. Planta 139(2):113–117

    Article  PubMed  CAS  Google Scholar 

  • Buschiazzo E, Ritland C, Bohlmann J, Ritland K (2012) Slow but not low: genomic comparisons reveal slower evolutionary rate and higher dN/dS in conifers compared to angiosperms. BMC Evol Biol 12:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai CP, Zhang XY, Niu E, Zhao L, Li N, Wang LM, Ding LY, Guo WZ (2014) GhPSY, a phytoene synthase gene, is related to the red plant phenotype in upland cotton (Gossypium hirsutum L.). Mol Biol Rep 41(8):4941–4952

    Article  PubMed  CAS  Google Scholar 

  • Cai XY, Liu F, Zhou ZL, Wang XX, Wang CY, Wang YH, Wang KB (2015) Characterization and development of chloroplast microsatellite markers for Gossypium hirsutum, and cross-species amplification in other Gossypium species. Genet Mol Res 14(4):11924–11932

    Article  PubMed  CAS  Google Scholar 

  • Chen ZW, Grover CE, Li PB, Wang YM, Nie HS, Zhao YP, Wang MY, Liu F, Zhou ZL, Wang XX, Cai XY, Wang KB, Wendel JF, Hua JP (2017a) Molecular evolution of the plastid genome during diversification of the cotton genus. Mol Phylogenet Evol 112:268–276

    Article  PubMed  CAS  Google Scholar 

  • Chen ZW, Nie HS, Wang YM, Pei HL, Li SS, Zhang LD, Hua JP (2017b) Rapid evolutionary divergence of diploid and allotetraploid Gossypium mitochondrial genomes. BMC Genom 18:876

    Article  CAS  Google Scholar 

  • Collins DW, Jukes TH (1994) Rates of transition and transversion in coding sequences since the human-rodent divergence. Genomics 20(3):386–396

    Article  PubMed  CAS  Google Scholar 

  • Cronn RC, Small RL, Haselkorn T, Wendel JF (2002) Rapid diversification of the cotton genus (Gossypium: Malvaceae) revealed by analysis of sixteen nuclear and chloroplast genes. Am J Bot 89(4):707–725

    Article  PubMed  CAS  Google Scholar 

  • Daniell H, Lee SB, Grevich J, Saski C, Quesada-Vargas T, Guda C, Tomkins J, Jansen RK (2006) Complete chloroplast genome sequences of Solanum bulbocastanum, Solanum lycopersicum and comparative analyses with other Solanaceae genomes. Theor Appl Genet 112(8):1503–1518

    Article  PubMed  CAS  Google Scholar 

  • De Camargo GM, Porto-Neto LR, Kelly MJ, Bunch RJ, Mcwilliam SM, Tonhati H, Lehnert SA, Fortes MR, Moore SS (2015) Non-synonymous mutations mapped to chromosome X associated with andrological and growth traits in beef cattle. BMC Genom 16:384

    Article  CAS  Google Scholar 

  • Dong WL, Wang RN, Zhang NY, Fan WB, Fang MF, Li ZH (2018) Molecular evolution of chloroplast genomes of orchid species: insights into phylogenetic relationship and adaptive evolution. Int J Mol Sci 19(3):716

    Article  PubMed Central  CAS  Google Scholar 

  • Fan WB, Wu Y, Yang J, Shahzad K, Li ZH (2018) Comparative chloroplast genomics of dipsacales species: insights into sequence variation, adaptive evolution, and phylogenetic relationships. Front Plant Sci 9:689

    Article  PubMed  PubMed Central  Google Scholar 

  • Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186(1):184–193

    Article  PubMed  CAS  Google Scholar 

  • Foster PG, Jermiin LS, Hickey DA (1997) Nucleotide composition bias affects amino acid content in proteins coded by animal mitochondria. J Mol Evol 44(3):282–288

    Article  PubMed  CAS  Google Scholar 

  • Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19(12):2226–2238

    Article  PubMed  CAS  Google Scholar 

  • Gray MW (1989) Origin and evolution of mitochondrial DNA. Annu Rev Cell Biol 5:25–50

    Article  PubMed  CAS  Google Scholar 

  • Grover CE, Gallagher JP, Jareczek JJ, Page JT, Udall JA, Gore MA, Wendel JF (2015) Re-evaluating the phylogeny of allopolyploid Gossypium L. Mol Phylogenet Evol 92:45–52

    Article  PubMed  Google Scholar 

  • Gruenstaeudl M, Nauheimer L, Borsch T (2017) Plastid genome structure and phylogenomics of Nymphaeales: conserved gene order and new insights into relationships. Plant Syst Evol 303(9):1251–1270

    Article  CAS  Google Scholar 

  • Hao J, Sun YQ (2015) Applied plant genomics and biotechnology. In: Poltronieri P (ed) Cotton genomics and biotechnology, 13th Woodhead Publishing, pp 213–227.

  • Hasenöhrl D, Fabbretti A, Londei P, Gualerzi CO, Bläsi U (2009) Translation initiation complex formation in the crenarchaeon Sulfolobus solfataricus. RNA 15(12):2288–2298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoang CV, Wessler HG, Local A, Turley RB, Benjamin RC, Chapman KD (1999) Identification and expression of cotton (Gossypium hirsutum L.) plastidial carbonic anhydrase. Plant Cell Physiol 40(12):1262–1270

    Article  PubMed  CAS  Google Scholar 

  • Joy KW, Ireland RJ, Lea PJ (1983) Asparagine synthesis in pea leaves, and the occurrence of an asparagine synthetase inhibitor. Plant Physiol 73(1):165–168

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ke X, Cardon LR (2003) Efficient selective screening of haplotype tag SNPs. Bioinformatics 19(2):287–288

    Article  PubMed  CAS  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock 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(12):1647–1649

    Article  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(4):299–306

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lane N (2011) Plastids, genomes, and the probability of gene transfer. Genome Biol Evol 3:372–374

    Article  PubMed  PubMed Central  Google Scholar 

  • Larson SR, Doebley J (1994) Restriction site variation in the chloroplast genome of Tripsacum (Poaceae): phylogeny and rates of sequence evolution. Syst Bot 19(1):21–34

    Article  Google Scholar 

  • Lee S-B, Kaittanis C, Jansen RK, Hostetler JB, Tallon LJ, Town CD, Daniell H (2006) The complete chloroplast genome sequence of Gossypium hirsutum: organization and phylogenetic relationships to other angiosperms. BMC Genom 7:61

    Article  CAS  Google Scholar 

  • Lei BB, Li SS, Liu GZ, Chen ZW, Su AG, Li PB, Li ZH, Hua JP (2013) Evolution of mitochondrial gene content: loss of genes, tRNAs and introns between Gossypium harknessii and other plants. Plant Syst Evol 299(10):1889–1897

    Article  CAS  Google Scholar 

  • Liao BY, Scott NM, Zhang JZ (2006) Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol Biol Evol 23(11):2072–2080

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Liu GZ, Cao DD, Li SS, Su AG, Geng JN, Grover CE, Hu SN, Hua JP (2013) The complete mitochondrial genome of Gossypium hirsutum and evolutionary analysis of higher plant mitochondrial genomes. PLoS ONE 8(8):e69476

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Logacheva MD, Samigullin TH, Dhingra A, Penin AA (2008) Comparative chloroplast genomics and phylogenetics of Fagopyrum esculentum ssp. Ancestrale—a wild ancestor of cultivated buckwheat. BMC Plant Biol 8:59

    Article  PubMed  PubMed Central  CAS  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(5):955–964

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma PF, Zhang YX, Guo ZH, Li DZ (2015) Evidence for horizontal transfer of mitochondrial DNA to the plastid genome in a bamboo genus. Sci Rep 5:11608

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin W (2003) Gene transfer from organelles to the nucleus: frequent and in big chunks. Proc Natl Acad Sci USA 100(15):8612–8614

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsuoka Y, Yamazaki Y, Ogihara Y, Tsunewaki K (2002) Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals. Mol Biol Evol 19(12):2084–2091

    Article  PubMed  CAS  Google Scholar 

  • Mcbain CJ, Mayer ML (1994) N-methyl-d-aspartic acid receptor structure and function. Physiol Rev 4(3):723–760

    Article  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(1):115–130

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mes THM, Kuperus P, Kirschner J, Stepanek J, Oosterveld P, Storchova H, den Nijs JCM (2000) Hairpins involving both inverted and direct repeats are associated with homoplasious indels in non-coding chloroplast DNA of Taraxacum, (Lactuceae: Asteraceae). Genome 43(4):634–641

    Article  PubMed  CAS  Google Scholar 

  • Miyata S, Nakazono M, Hirai A (1998) Transcription of plastid-derived tRNA genes in rice mitochondria. Curr Genet 34(3):216–220

    Article  PubMed  CAS  Google Scholar 

  • Morton BR (1993) chloroplast DNA codon use: Evidence for selection at the psbA locus based on tRNA availability. J Mol Evol 37(3):273–280

    Article  PubMed  CAS  Google Scholar 

  • Nachman MW, Crowell SL (2000) Estimate of the mutation rate per nucleotide in humans. Genetics 156(1):297–304

    PubMed  PubMed Central  CAS  Google Scholar 

  • Percudani R, Ottonello S (1999) Selection at the wobble position of codons read by the same tRNA in Saccharomyces cerevisiae. Mol Biol Evol 16(12):1752–1762

    Article  PubMed  CAS  Google Scholar 

  • Rota-Stabelli O, Lartillot N, Philippe H, Pisani D (2013) Serine codon-usage bias in deep phylogenomics: Pancrustacean relationships as a case study. Syst Biol 62(1):121–133

    Article  PubMed  CAS  Google Scholar 

  • Saha S, Karaca M, Jenkins JN, Zipf AE, Reddy OUK, Kantety RV (2003) Simple sequence repeats as useful resources to study transcribed genes of cotton. Euphytica 130(3):355–364

    Article  CAS  Google Scholar 

  • Saini AK, Nanda JS, Lorsch JR, Hinnebusch AG (2010) Regulatory elements in eIF1A control the fidelity of start codon selection by modulating tRNA(i)(Met) binding to the ribosome. Genes Dev 24(1):97–110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saitou N, Ueda S (1994) Evolutionary rates of insertion and deletion in noncoding nucleotide sequences of primates. Mol Biol Evol 11(3):504–512

    PubMed  CAS  Google Scholar 

  • Sancho R, Cantalapiedra CP, López-Alvarez D, Gordon SP, Vogel JP, Catalán P, Contreras-Moreira B (2017) Comparative plastome genomics and phylogenomics of Brachypodium: flowering time signatures, introgression and recombination in recently diverged ecotypes. New Phytol 218(4):1631–1644

    Article  PubMed  CAS  Google Scholar 

  • Saski C, Lee SB, Fjellheim S, Guda C, Jansen RK, Luo H, Tomkins J, Rognli OA, Daniell H, Clarke JL (2007) Complete chloroplast genome sequences of Hordeum vulgare, Sorghum bicolor and Agrostis stolonifera, and comparative analyses with other grass genomes. Theor Appl Genet 115(4):571–590

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharp PM, Cowe E (1991) Synonymous codon usage in Saccharomyces cerevisiae. Yeast 7(7):657–678

    Article  PubMed  CAS  Google Scholar 

  • Sharp PM, Li WH (1987) The codon adaptation index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15(3):1281–1295

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sloan DB, Alverson AJ, Wu M, Palmer JD, Taylor DR (2012) Recent acceleration of plastid sequence and structural evolution coincides with extreme mitochondrial divergence in the angiosperm genus silene. Genome Biol Evol 4(3):294–306

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith DR (2011) Extending the limited transfer window hypothesis to inter-organelle DNA migration. Genome Biol Evol 3:743–748

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Talat F, Wang KB (2015) Comparative bioinformatics analysis of the chloroplast genomes of a wild diploid Gossypium and two cultivated allotetraploid species. Iran J Biotechnol 13(3):47–56

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang DT, Glazov EA, McWilliam SM, Barris WC, Dalrymple BP (2009) Analysis of the complement and molecular evolution of tRNA genes in cow. BMC Genom 10:188

    Article  CAS  Google Scholar 

  • Tang MY, Chen ZW, Grover CE, Wang YM, Li SS, Liu GZ, Ma ZY, Wendel JF, Hua JP (2015) Rapid evolutionary divergence of Gossypium barbadense and G. hirsutum mitochondrial genomes. BMC Genom 16:770

    Article  CAS  Google Scholar 

  • Treangen TJ, Rocha EPC (2011) Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 7(1):e1001284

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsai CT, Lin CH, Chang CY (2007) Analysis of codon usage bias and base compositional constraints in iridovirus genomes. Virus Res 126(1–2):196–206

    Article  PubMed  CAS  Google Scholar 

  • Turmel M, Otis C, Lemieux C (2016) Mitochondrion-to-chloroplast dna transfers and intragenomic proliferation of chloroplast group ii introns in Gloeotilopsis green algae (Ulotrichales, Ulvophyceae). Genome Biol Evol 8(9):2789–2805

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang YH, Huang CL, Jia JF (2009) Construction of multicistron expression vector by using plastid homologous sequences of sweet potato. Genom Appl Biol 28(4):659–667

    Google Scholar 

  • Wang Y, Zhu FC, He LS, Danchin A (2018) Unique tRNA gene profile suggests paucity of nucleotide modifications in anticodons of a deep-sea symbiotic spiroplasma. Nucleic Acids Res 46(5):2197–2203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186

    Article  Google Scholar 

  • Wolfe KH, Sharp PM (1988) Identification of functional open reading frames in chloroplast genomes. Gene 66(2):215–222

    Article  PubMed  CAS  Google Scholar 

  • Wolfe KH, Li WH, Sharp PM (1987) Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proc Natl Acad Sci USA 84(24):9054–9058

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wu Y, Liu F, Yang DG, Li W, Zhou XJ, Pei XY, Liu YG, He KL, Zhang WS, Ren ZY, Zhou KH, Ma XF, Li ZH (2018) Comparative chloroplast genomics of Gossypium species: insights into repeat sequence variations and phylogeny. Front Plant Sci 9:376

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia X, Luan LL, Qin G, Yu LF, Wang ZW, Dong WC, Song Y, Qiao Y, Zhang XS, Sang YL, Yang L (2017) Genome-wide analysis of SSR and ILP markers in trees: diversity profiling, alternate distribution, and applications in duplication. Sci Rep 7(1):17902

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu Q, Xiong GJ, Li PB, He F, Huang Y, Wang KB, Li ZH, Hua JP (2012) Analysis of complete nucleotide sequences of 12 Gossypium chloroplast genomes: origin and evolution of allotetraploids. PLoS ONE 7(8):e37128

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang L, Gaut BS (2011) Factors that contribute to variation in evolutionary rate among Arabidopsis genes. Mol Biol Evol 28(8):2359–2369

    Article  PubMed  CAS  Google Scholar 

  • Zhang G, Hubalewska M, Ignatova Z (2009) Transient ribosomal attenuation coordinates protein synthesis and co-translational folding. Nat Struct Mol Biol 16(3):274–280

    Article  PubMed  CAS  Google Scholar 

  • Zhang MY, Fritsch PW, Ma PF, Wang H, Lu L, Li DZ (2017) Plastid phylogenomics and adaptive evolution of Gaultheria series Trichophyllae (Ericaceae), a clade from sky islands of the Himalaya-Hengduan mountains. Mol Phylogenet Evol 110:7–18

    Article  PubMed  CAS  Google Scholar 

  • Zhou M, Long W, Li X (2008) Patterns of synonymous codon usage bias in chloroplast genomes of seed plants. For Stud China 11(4):235–242

    Article  CAS  Google Scholar 

Download references

Funding

This research was funded by grants from National Key R & D Program for Crop Breeding (2016YFD0100306), National Natural Science Foundation of China (No. 31401431), and the Shaanxi Science and Technology Innovation Team (2019TD‐012), the Public health specialty in the Department of traditional Chinese Medicine (Grant nos. 2017-66 and 2018-43) and the Open Foundation of Key Laboratory of Resource Biology and Biotechnology in Western China (Ministry of Education) (Grant nos. ZSK2017007 and ZSK2019008).

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, Heng Liu, Qi-Yuan Gao, Ting Yang & Zhong-Hu Li

  2. State Key Laboratory of Continental Dynamics, Department of Geology, Early Life Institute, Northwest University, Xi’an, 710069, China

    Jian-Ni Liu & Zhong-Hu Li

  3. State Key Laboratory of Cotton Biology, Institute of Cotton Research, Chinese Academy of Agricultural Sciences, Anyang, 455000, China

    Xiong-Feng Ma & Zhong-Hu Li

Authors
  1. Ting-Ting Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qi-Yuan Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ting Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jian-Ni Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiong-Feng Ma
    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

Corresponding authors

Correspondence to Xiong-Feng Ma or Zhong-Hu Li.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Amit Dhingra .

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

299_2020_2529_MOESM1_ESM.tif

Supplementary file1 Secondary structures inferred for the tRNAs present in the Gossypium chloroplast genomes (TIF 1960 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, TT., Liu, H., Gao, QY. et al. Gene transfer and nucleotide sequence evolution by Gossypium cytoplasmic genomes indicates novel evolutionary characteristics. Plant Cell Rep 39, 765–777 (2020). https://doi.org/10.1007/s00299-020-02529-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02529-9

Keywords

Search

Navigation