Skip to main content
Log in

Comparative assessment of genetic diversity in cytoplasmic and nuclear genome of upland cotton

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The importance of the cytoplasmic genome for many economically important traits is well documented in several crop species, including cotton. There is no report on application of cotton chloroplast specific SSR markers as a diagnostic tool to study genetic diversity among improved Upland cotton lines. The complete plastome sequence information in GenBank provided us an opportunity to report on 17 chloroplast specific SSR markers using a cost-effective data mining strategy. Here we report the comparative analysis of genetic diversity among a set of 42 improved Upland cotton lines using SSR markers specific to chloroplast and nuclear genome, respectively. Our results revealed that low to moderate level of genetic diversity existed in both nuclear and cytoplasm genome among this set of cotton lines. However, the specific estimation suggested that genetic diversity is lower in cytoplasmic genome compared to the nuclear genome among this set of Upland cotton lines. In summary, this research is important from several perspectives. We detected a set of cytoplasm genome specific SSR primer pairs by using a cost-effective data mining strategy. We reported for the first time the genetic diversity in the cytoplasmic genome within a set of improved Upland cotton accessions. Results revealed that the genetic diversity in cytoplasmic genome is narrow, compared to the nuclear genome within this set of Upland cotton accessions. Our results suggested that most of these polymorphic chloroplast SSRs would be a valuable complementary tool in addition to the nuclear SSR in the study of evolution, gene flow and genetic diversity in Upland cotton.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, Salakhutdinov IB, Buriev ZT, Saha S, Scheffler BE, Jenkins JN, Abdukarimov A (2008) Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics 92:478–487

    Article  CAS  PubMed  Google Scholar 

  • Abdurakhmonov IY, Saha S, Jenkins JN, Buriev ZT, Shermatov SE, Scheffler BE, Pepper AE, Yu JZ, Kohel RJ, Abdukarimov A (2009) Linkage disequilibrium based association mapping of fiber quality traits in G. hirsutum L. variety germplasm. Genetica 136:401–417

    Article  PubMed  Google Scholar 

  • Abdurakhmonov IY, Buriev ZT, Shermatov SE, Abdullaev AA, Urmonov K, Kushanov F, Egamberdiev SS, Shapulatov U, Abdukarimov A, Saha S, Jenkins JN, Kohel RJ, Yu JZ, Pepper AE, Kumpatla SP, Ulloa M (2011) Genetic diversity in Gossypium genus. In: Caliskan M (ed) Genetic diversity, InTech, Slavka Krautzeka 83/A. Open Access Publisher, Croatia, pp 313–336

    Google Scholar 

  • Allen JF, Puthiyaveetil S, Strom J, Allen CA (2005) Energy transduction anchors genes in organelles. BioEssays 27:426–435. doi:10.1002/bies.20194

    Article  CAS  PubMed  Google Scholar 

  • Arroyo-Garcia R, Lefort F, de Andres MT, Ibanez J, Borrego J, Jouve N, Cabello F, Martinez-Zapater JM (2002) Chloroplast microsatellite polymorphisms in Vitis species. Genome 45:1142–1149

    Article  CAS  PubMed  Google Scholar 

  • Badigannavar A, Myers GO, Jones DC (2012) Molecular diversity revealed by AFLP markers in upland cotton genotypes. J Crop Improv 26:627–640

    Article  CAS  Google Scholar 

  • Bechere E, Auld DL, Cantrell RG, Krifa EHM, Misra S, Smith CW (2007) Registration of TTU 0774-3-3 and TTU 0808-1-6-1 upland cotton germplasm lines with improved fiber length and strength. J Plant Regist 1:58–59

    Article  Google Scholar 

  • Bertini CM, Schuster I, Sediyama T, Barros EG, Moreira MA (2006) Characterization and genetic diversity analysis of cotton cultivars using microsatellites. Gene Mol Biol 29(2):321–329

    Article  Google Scholar 

  • Blenda A, Scheffler J, Scheffler B, Lacape J, Yu JZ, Jung S, Staton M, Palmer M, Jesudurai C, Muthukumar S, Yellambalase P, Ficklin S, Eschelman R, Ulloa M, Saha S, Feng D, Cantrell R, Main D (2006) CMD: a cotton microsatellite data base resource for Gossypium genomics. BMC Genom 7:132

    Article  Google Scholar 

  • Bowers J, Boursiquot JM, This P, Chu K, Johansson M, Meredith C (1999) Historical genetics: the parentage of Chardonnay, Gamay and other wine grapes of northeastern France. Science 285:1562–1565

    Article  CAS  PubMed  Google Scholar 

  • Buyyarapu R, Kantety RV, Saha S, Yu J, Sharma GC (2011) New candidate gene and EST-based molecular markers in Gossypium species. Int J Plant Genomics. doi:10.1155/2011/894598

    PubMed  PubMed Central  Google Scholar 

  • Cato SA, Richardson TE (1996) Inter- and intraspecific polymorphism at chloroplast SSR loci and the inheritance of plastids in Pinus radiata D. Don. Theor Appl Genet 93:587–592

    Article  CAS  PubMed  Google Scholar 

  • Chao S, Zhang W, Akhunov E, Sherman J, Ma Y, Luo MC, Dubcovsky J (2009) Analysis of gene-derived SNP marker polymorphism in US wheat (Triticum aestivum L.) cultivars. Mol Breed 23:23–33

    Article  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 89:707–725

    Article  CAS  PubMed  Google Scholar 

  • Cuenca A, Escalante AE, Piñero D (2003) Long-distance colonization, isolation by distance, and historical demography in a relictual Mexican pinyon pine (Pinus nelsonii Shaw) as revealed by paternally inherited genetic markers (cpSSRs). Mol Ecol 12:2087–2097

    Article  CAS  PubMed  Google Scholar 

  • Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62:1908–1920

    PubMed  Google Scholar 

  • Ebert D, Peakall R (2009) Chloroplast simple sequence repeats (cpSSRs) technical resources and recommendations for expanding cpSSR discovery and application to a wide array of plant species. Mol Econ Res 9:673–690

    Article  CAS  Google Scholar 

  • Erisen JA (1999) Mechanistic basis of microsatellite instability. In: Goldstein DB, Schlotterer C (eds) Microsatellite evolution and application. Oxford University Press, Oxford, pp 34–48

    Google Scholar 

  • Fang DD, Hinze LL, Percy RG, Li P, Deng D, Thyssen GA (2013) Microsatellite-based genome-wide analysis of genetic diversity and linkage disequilibrium in Upland cotton (Gossypium hirsutum L.) cultivars from major cotton-growing countries. Euphytica 191:391–401

    Article  CAS  Google Scholar 

  • Ferris C, King RA, Väinölä R, Hewitt GM (1998) Chloroplast DNA recognizes three refugial sources of European oaks and suggests independent eastern and western immigrations to Finland. Heredity (Edinb) 80:584–593

    Article  Google Scholar 

  • Fineschi S, Taurchini D, Grossoni P, Petit RJ, Vendramin GG (2002) Chloroplast DNA variation of white oaks in Italy. For Ecol Manage 156:103–114

    Article  Google Scholar 

  • Goloenko IM, Lukhanina NV, Shimkevich AM, Aksyonova EA, Danilenko NG, Davydenko OG (2002) The productivity characteristics of substituted barley lines with marked chloroplast and mitochondrial genomes. Cell Mol Biol Lett 7(2):4

    Google Scholar 

  • Guo W, Zhang TZ, Pan JJ, Wang XY (1997) A preliminary study on genetic diversity of Upland cotton cultivars in China. Acta Gossypii Sin 9:19–24

    Google Scholar 

  • Hamza NB (2010) Cytoplasmic and nuclear DNA markers as powerful tools in populations’ studies and in setting conservation strategies. Afr J Biotech 9(29):4510–4515

    CAS  Google Scholar 

  • Han L, Yang J, Zhu J (2007) Analysis of genetic effects of nuclear-cytoplasmic interaction on quantitative traits: genetic model for diploid plants. J Genet Genome 34(6):562–568

    Article  Google Scholar 

  • Hansen AK, Escobar LK, Gilbert LE, Jansen RK (2007) Paternal, maternal, and biparental inheritance of the chloroplast genome in Passifl ora (Passifl oraceae): implications for phylogenetic studies. Am J Bot 94:42–46

    Article  CAS  PubMed  Google Scholar 

  • Hinze LL, Dever JK, Percy RG (2012) Molecular variation among and within improved cultivars in the U.S. cotton germplasm collection. Crop Sci 52:222–230

    Article  Google Scholar 

  • Ibrahim RI, Azuma J, Sakamoto M (2006) Complete nucleotide sequence of the cotton (Gossypium barbadense L.) chloroplast genome with a comparative analysis of sequences among 9 dicot plants. Genes Genet Syst 81:311–321

    Article  CAS  PubMed  Google Scholar 

  • Karaca M, Saha S, Callahan FE, Jenkins JN, Read J, Percy RG (2004) Molecular and cytological characterization of a cytoplasmic-specific mutant in Pima cotton (Gossypium barbadense L.). Euphytica 139:187–197

    Article  CAS  Google Scholar 

  • Khan AI, Fu Y-B, Khan IA (2009) Genetic diversity of Pakistani cotton cultivars as revealed by simple sequence repeat markers. Commun Biom Crop Sci 4:21–30

    Google Scholar 

  • Lacape J-M, Dessauw D, Rajab M, Noyer J-L, Hau B (2007) Microsatellite diversity in tetraploid Gossypium germplasm: assembling a highly informative genotyping set of cotton SSRs. Mol Breed 19:45–58

    Article  CAS  Google Scholar 

  • Lee DJ, Blake TK, Smith SE (1998) Biparental inheritance of chloroplast DNA and the existence of heteroplasmic cells in alfalfa. Theor Appl Genet 76:545–549

    Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Leigh FJ, Mackay I, Oliveira HR, Gosman NE, Horsnell RA, Jones H, White J, Powell W, Brown TA (2013) Using diversity of the chloroplast genome to examine evolutionary history of wheat species. Genet Res Crop Evol 60:1831–1842

    Article  CAS  Google Scholar 

  • Levinson G, Gutman GA (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Bio Evol 4:205–221

    Google Scholar 

  • Li Y-C, Korol AB, Fahima T, Beiles A, Nevo E (2002) Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol 11:2453–2465

    Article  CAS  PubMed  Google Scholar 

  • Li P, Li Z, Liu H, Hua J (2014) Cytoplasmic diversity of the cotton genus as revealed by chloroplast microsatellite markers. Genet Resour Crop Evol 61:107–119

    Article  CAS  Google Scholar 

  • Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21:2128–2129

    Article  CAS  PubMed  Google Scholar 

  • Marchelli P, Gallo L, Scholz F, Ziegenhagen B (1998) Chloroplast DNA markers reveal a geographical divide across argentinean Southern Beech Nothofagus nervosa (Phil.) Dim. ET Mil. distribution area. Theor Appl Genet 97:642–646

    Article  CAS  Google Scholar 

  • Muir G, Filatov D (2007) A selective sweep in the chloroplast DNA of dioecious silene (Section Elisanthe). Genetics 177:1239–1247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navascués M, Emerson BC (2005) Chloroplast microsatellites: measures of genetic diversity and the effect of homoplasy. Mol Ecol 14:1333–1341

    Article  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Provan J (2000) Novel chloroplast microsatellites reveal cytoplasmic variation in Arabidopsis thaliana. Mol Ecol 9:2183–2185

    Article  CAS  PubMed  Google Scholar 

  • Provan J, Campanella JJ (2003) Patterns of cytoplasmic variation in Arabidopsis thaliana (Brassicaceae) revealed by polymorphic chloroplast microsatellites. Syst Bot 28(3):578–583

    Google Scholar 

  • Provan J, Powell W, Hollingsworth PM (2001) Chloroplast microsatellites: new tools for studies in plant ecology and evolution. Trends Ecol Evol 16:142–147

    Article  PubMed  Google Scholar 

  • Provan J, Biss PM, McMeel D, Mathews S (2004) Universal 394 primers for the amplification of chloroplast microsatellites in grasses (Poaceae). Mol Ecol Notes 4:262–264

    Article  CAS  Google Scholar 

  • Qin H, Guo W, Zhang Y, Zhang T (2008) QTL mapping of yield and fiber traits based on a four-way cross population in Gossypium hirsutum L. Theor Appl Genet 117:883–894

    Article  PubMed  Google Scholar 

  • Qureshi SN, Saha S, Kantety RV, Jenkins JN (2004) EST-SSR: a new class of genetic markers in cotton. J Cot Sci 8:112–123. http://www.jcotsci.org

  • Rao AP, Fleming AA (1978) Cytoplasmic–genetypic effect in the GT 112 maize inbred with four cytoplasms. Crop Sci 8(4):935–937

    Article  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols. Humana Press, Towota, pp 365–386

    Google Scholar 

  • Sapkal DR, Suter SR, Thakre PB, Patil BR, Paterson AH, Waghmare VN (2011) Genetic diversity analysis of maintainer and restorer accessions in upland cotton (Gossypium hirsutum L.). J Plant Biochem Biotechnol 20(1):20–28

    Article  Google Scholar 

  • Scotti N, Monti L, Cardi T (2004) Organelle DNA variation in pa-rental Solanum spp genotypes and nuclear-cytoplasmic inter-actions in Solanum tuberosum (+) S. commersonii somatic hybrid–backcross progeny. Theor Appl Genet 108(1):87–94

    Article  Google Scholar 

  • Sears BB (1980) Elimination of plastids during spermatogenesis and fertilization in the plant kingdom. Plasmid 4:233–255

    Article  CAS  PubMed  Google Scholar 

  • Shurtleff MC (ed) (1980) Compendium of corn diseases, 2nd edn. American Phytopathological Society, Minneapolis

    Google Scholar 

  • Smith CW, Cothren JT (1999) Cotton: origin, history, technology, and production. Wiley, New York

    Google Scholar 

  • Tao D, Hu F, Yang J, Yang G, Yang Y, Xu P, Li J, Ye C, Dai L (2004) Cytoplasm and cytoplasm–nucleus interactions affect agronomic traits in japonica rice. Euphytica 135(3):129–134

    Article  CAS  Google Scholar 

  • Tyagi P, Gore MA, Bowman DT, Campbell BT, Udall JA, Kuraparthy V (2014) Genetic diversity and population structure in the US Upland cotton (Gossypium hirsutum L.). Theor Appl Genet 127:283–295

    Article  PubMed  Google Scholar 

  • Ullstrup JA (1972) The impacts of the southern corn leaf blight epidemics of 1970-1971. Ann Rev Phytopath 10:37–50

    Article  Google Scholar 

  • Van Esbroeck GA, Bowman DT, May OL, Calhoun DS (1999) Genetic similarity indices for ancestral cotton cultivars and their impact on genetic diversity estimates of modern cultivars. Crop Sci 39:323–328

    Google Scholar 

  • Vendramin GG, Lelli L, Rossi P, Morgante M (1996) A set of primers for the amplification of 20 chloroplast microsatellites in Pinaceae. Mol Ecol 5(415):595–598

    Article  CAS  PubMed  Google Scholar 

  • Weising K, Gardner RC (1999) A set of conserved PCR primers for 416 the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome 42:9–19

    Article  CAS  PubMed  Google Scholar 

  • Wendel J (1989) New World tetraploid cotton contains Old World cytoplasm. Proc Natl Acad Sci 86(11):4132–4136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whatley JM (1982) Ultrastructure of plasmid inheritance: green algae to angiosperm. Bot Rev 57:527–569

    Google Scholar 

  • Wheeler GL, Dorman HE, Buchanan A, Challagundla L, Wallace LE (2014) A review of the prevalence, utility, and caveats of using chloroplast simple sequence repeats for studies of plant biology. Appl Plant Sci. 2:1400059

    Google Scholar 

  • Wu J, Gutierrez OA, Jenkins JN et al (2009) Quantitative analysis and QTL mapping for agronomic and fiber traits in an RI population of upland cotton. Euphytica 165:231–245

    Article  Google Scholar 

  • Xu Q, Xiong G, Li P, He F, Huang Y, Wang K, Li Z, Hua J (2012) Analysis of complete nucleotide sequences of 12 Gossypium chloroplast genomes: origin and evolution of allotetraploids. PLoS ONE. doi:10.1371/journal.pone.0037128

    Google Scholar 

  • Yu JZ, Kohel RJ, Fang DD, Cho J, Deynze AV, Ulloa M, Hoffman SM, Pepper AE, Stelly DM, Jenkins JN et al (2012) A high density simple sequence repeat and single nucleotide polymorphism genetic map of the tetraploid cotton genome. G3-Genes/Genomics/Genetics 2:43–58

    Article  CAS  Google Scholar 

  • Zhang J, Lu Y, Cantrell RG, Hughs E (2005) Molecular marker diversity and field Performance in commercial cotton cultivars evaluated in the Southwestern USA. Crop Sci 45:1483–1490

    Article  CAS  Google Scholar 

  • Zhang Y, Wang XF, Li ZK, Zhang GY, Ma ZY (2011) Assessing genetic diversity of cotton cultivars using genomic and newly developed expressed sequenced tag-derived microsatellite markers. Genet Mol Res 10:1462–1470

    Article  CAS  PubMed  Google Scholar 

  • Zhang T, Qian N, Zhu X, Chen H, Wang S, Mei H, Zhang Y (2013) Variations and transmission of QTL alleles for yield and fiber qualities in Upland Cotton cultivars developed in China. PLoS ONE. doi:10.1371/journal.pone.0057220

    Google Scholar 

Download references

Acknowledgments

The authors thank the Office of International Research Programs, U. S. Department of Agriculture (USDA) for providing funds for this study under research grant UZB2-31016-TA-09 and U.S. Civilian Research & Development Foundation (CRDF) and Cotton Incorporated, USA. We thank the Academy of Sciences of Uzbekistan for supporting this joint study within USDA-Uzbekistan cooperative programs. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U. S. Department of Agriculture. The U. S. Department of Agriculture is equal opportunity provider and employer. We acknowledge joint publication of USDA/ARS, and Mississippi Agricultural and Forestry Experiment Station, approved for publication as Journal Article of the Mississippi Agricultural and Forestry Experiment Station. We thank all of the public and private cotton breeders who provided seeds for this study. We would specifically like to acknowledge the help of Dr. Jack C. McCarty, Dr. Wayne Smith, Dr. Bill Meredith, Dr. Gerald O. Myers, Dr. Ted Wallace, Dr. Fred Bourland, Dr. Jack Jones, and Dr. Dick L. Auld for their help in this study by providing seeds of their released germplasm. Without their help and support we could not accomplished the goals of this research project. We also thank Dr. B. Todd Campbell and Dr. Mauricio Ulloa for their help in reviewing the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sukumar Saha.

Additional information

Disclaimer Mention of trademark or proprietary product does not constitute a guarantee or warranty of the product by the United States Department of Agriculture and does not imply its approval to the exclusion of other products that may also be suitable.

Sharof S. Egamberdiev and Sukumar Saha equally credited as the first author for their contribution in this research.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 51 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Egamberdiev, S.S., Saha, S., Salakhutdinov, I. et al. Comparative assessment of genetic diversity in cytoplasmic and nuclear genome of upland cotton. Genetica 144, 289–306 (2016). https://doi.org/10.1007/s10709-016-9898-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-016-9898-x

Keywords

Navigation