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Comparative transmission genetics of introgressed chromatin in reciprocal advanced backcross populations in Gossypium (cotton) polyploids

Heredity volume 130, pages 209–222 (2023)Cite this article

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Abstract

Introgression is a potential source of valuable genetic variation and interspecific introgression lines are important resources for plant breeders to access novel alleles. Experimental advanced-generation backcross populations contain individuals with genomic compositions similar to those resulting from natural interspecific hybridization and provide opportunities to study the nature and transmission pattern of donor chromatin in recipient genomes. Here, we analyze transmission of donor chromatin in reciprocal backcrosses between G. hirsutum and G. barbadense. Across the genome, recurrent backcrossing in both backgrounds yielded donor chromatin at slightly higher frequencies than the Mendelian expectation in BC5F1 plants, while the average frequency of donor alleles in BC5F2 segregating families was less than expected. In the two subgenomes of polyploid cotton, the rate of donor chromatin introgression was similar. Although donor chromatin was tolerated over much of the recipient genomes, 21 regions recalcitrant to donor alleles were identified. Only limited correspondence is observed between the recalcitrant regions in the two backgrounds, suggesting the effect of species background on introgression of donor segments. Genetic breakdown was progressive, with floral abscission and seed inviability ongoing during backcrossing cycles. Regions of either high or low introgression tended to be in terminal chromosomal regions that are generally rich in both genes and crossover events, with long stretches around the centromere having limited crossover activity resulting in relatively constant low introgression frequencies. Constraints on fixation and selection of donor alleles highlights the challenges of utilizing introgression breeding in crop improvement.

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Fig. 1: Development of reciprocal set of advanced-backcross populations.
Fig. 2: Retention of donor alleles in reciprocal interspecific populations.
Fig. 3: Genomic composition of 190 BC5F1 lines in G. barbadense background.
Fig. 4: Genomic composition of 179 BC5F1 lines in G. hirsutum background.

Data availability

The raw data supporting the conclusions of this article has been included in the supplementary information (Dataset 1 and Dataset 2) and has also been deposited in the Dryad repository (https://doi.org/10.5061/dryad.kh189329v).

References

  • Adhikari J, Das S, Wang Z, Khanal S, Chandnani R, Patel JD et al. (2017) Targeted identification of association between cotton fiber quality traits and microsatellite markers. Euphytica 213(3):65

    Article  Google Scholar 

  • Anderson E (1949). Introgressive hybridization. J. Wiley

  • Andolfatto P, Davison D, Erezyilmaz D, Hu TT, Mast J, Sunayama-Morita T et al. (2011). Vol. 21. COLD SPRING HARBOR LABORATORY PRESS: United States, pp 610-617

  • Baack E, Melo MC, Rieseberg LH, Ortiz-Barrientos D (2015) The origins of reproductive isolation in plants. N Phytol 207(4):968–984

    Article  Google Scholar 

  • Beasley JO (1942) Meiotic chromosome behaviour in species, species hybrids, haploids, and induced polyploids of Gossypium. Genetics 27:25–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brubaker CL, Paterson AH, Wendel JF (1999) Comparative genetic mapping of allotetraploid cotton and its diploid progenitors. Genome 42(2):184–203

    Article  CAS  Google Scholar 

  • Chandnani R, Wang B, Draye X, Rainville LK, Auckland S, Zhuang Z et al. (2017) Segregation distortion and genome-wide digenic interactions affect transmission of introgressed chromatin from wild cotton species. Theor Appl Genet 130(10):2219

    Article  CAS  PubMed  Google Scholar 

  • Chee PW, Draye X, Jiang CX, Decanini L, Delmonte TA, Bredhauer R et al. (2005) Molecular dissection of phenotypic variation between Gossypium hirsutum and Gossypium barbadense (cotton) by a backcross-self approach: III. Fiber length. TAG Theor Appl Genet 111(4):772–781

    Article  CAS  PubMed  Google Scholar 

  • Desai A, Chee PW, Junkang R, May OL, Paterson AH, Gustafson JP (2006) Chromosome structural changes in diploid and tetraploid A genomes of Gossypium. Genome 49(4):336–345

    Article  PubMed  Google Scholar 

  • Draye X, Chee P, Jiang C-X, Decanini L, Delmonte TA, Bredhauer R et al. (2005) Molecular dissection of interspecific variation between Gossypium hirsutum and G. barbadense (cotton) by a backcross-self approach: II. Fiber fineness. Theor Appl Genet 111(4):764–771

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q et al. (2014) TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline. PLoS ONE 9(2):1–11

    Article  Google Scholar 

  • Grant V (1981). Plant speciation, 2nd edn. Columbia University Press

  • Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156(1):1–13

    Article  Google Scholar 

  • Heiser CB (1979) Hybrid Populations of Helianthus divaricatus and H. microcephalus after 22 Years. Taxon 28(1/3):71–75

    Article  Google Scholar 

  • Hu Y, Chen J, Fang L, Zhang Z, Ma W, Niu Y et al. (2019) Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet 51(4):739–748

    Article  CAS  PubMed  Google Scholar 

  • Jiang C-X, Chee PW, Draye X, Morrell PL, Smith CW, Paterson AH (2000) Multilocus interactions restrict gene introgression in interspecific populations of polyploid gossypium (cotton). Evolution 54(3):798–814

    CAS  PubMed  Google Scholar 

  • Kantartzi S, Roupakias DG (2008) Breeding barriers between Gossypium spp. and species of the Malvaceae family. Aust J Bot 56(3):241–245

    Article  Google Scholar 

  • Kelly S, Huihui L, Navarro JAR, Dong A, Maria Cinta R, Sarah H et al (2014). Novel methods to optimize genotypic imputation for low-coverage, next-generation sequence data in crop plants. The Plant Genome 7(3):1–12

  • Kim C, Guo H, Kong W, Rahul C, Shuang L, Paterson AH (2016) Application of genotyping by sequencing technology to a variety of crop breeding programs. Plant Sci 242:14–22

    Article  CAS  PubMed  Google Scholar 

  • Kumar P, Singh R, Lubbers EL, Shen X, Paterson AH, Campbell BT et al. (2019) Genetic evaluation of exotic chromatins from two obsolete interspecific introgression lines of upland cotton for fiber quality improvement. Crop Sci 59(3):1073–1084

    Article  CAS  Google Scholar 

  • Levi A, Ovnat L, Paterson AH, Saranga Y (2009) Photosynthesis of cotton near-isogenic lines introgressed with QTLs for productivity and drought related traits. Plant Sci 177(2):88–96

    Article  CAS  Google Scholar 

  • Li F, Fan G, Lu C, Xiao G, Zou C, Kohel RJ et al. (2015) Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol 33(5):524–530

    Article  PubMed  Google Scholar 

  • Meyn O, Emboden WA (1987) Parameters and consequences of introgression in salvia apiana x S. mellifera (Lamiaceae). Syst Bot 12(3):390–399

    Article  Google Scholar 

  • Paterson AH, Boman RK, Brown SM, Chee PW, Gannaway JR, Gingle AR et al. (2004) Reducing the genetic vulnerability of cotton. Crop Sci 44(6):1900

    Article  Google Scholar 

  • Paterson AH, Brubaker CL, Wendel JF (1993) A rapid method for extraction of cotton (Gossypium spp.) genomic DNA suitable for RFLP or PCR analysis. Plant Mol Biol Report 11(2):122–127

    Article  CAS  Google Scholar 

  • Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D et al. (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492(7429):423–427

    Article  CAS  PubMed  Google Scholar 

  • Rieseberg LH, Kim MJ, Seiler GJ (1999) Introgression between the cultivated sunflower and a sympatric wild relative, helianthus petiolaris (Asteraceae). Int J Plant Sci 160(1):102–108

    Article  Google Scholar 

  • Rong J, Wang X, Schulze SR, Compton RO, Williams-Coplin TD, Goff V et al. (2012) Types, levels and patterns of low-copy DNA sequence divergence, and phylogenetic implications, for Gossypium genome types. Heredity (Edinb) 108(5):500–506

    Article  CAS  PubMed  Google Scholar 

  • Rong JK, Abbey C, Bowers JE, Brubaker CL, Chang C, Chee PW et al. (2004) A 3347-locus genetic recombination map of sequence-tagged sites reveals features of genome organization, transmission and evolution of cotton (Gossypium). Genetics 166(1):389–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen X, Cao Z, Singh R, Lubbers EL, Xu P, Smith CW et al. (2011) Efficacy of qFL-chr1, a Quantitative Trait Locus for Fiber Length in Cotton (Gossypium spp.). Crop Sci 51(5):2005–2010

    Article  Google Scholar 

  • Stephens SG (1949) The cytogenetics of speciation in Gossypium I. Selective elimination of the donor parent genotype in interspecific backcrosses. Genetics 1949 34:627–637

    Google Scholar 

  • Tanksley SD, Nelson JC (1996) Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Theor Appl Genet 92(2):191–203

    Article  CAS  PubMed  Google Scholar 

  • Waghmare VN, Rong J, Rogers CJ, Bowers JE, Chee PW, Gannaway JR et al. (2016) Comparative transmission genetics of introgressed chromatin in Gossypium (cotton) polyploids. Am J Bot 103(4):719–729

    Article  CAS  PubMed  Google Scholar 

  • Waghmare VN, Rong J, Rogers CJ, Pierce GJ, Wendel JF, Paterson AH (2005) Genetic mapping of a cross between Gossypium hirsutum (cotton) and the Hawaiian endemic Gossypium tomentosum. Theor Appl Genet 111(4):665–676

    Article  CAS  PubMed  Google Scholar 

  • Wang GL, Dong JM, Paterson AH (1995) The distribution of Gossypium hirsutum chromatin in G. barbadense germ plasm: molecular analysis of introgressive plant breeding. Theor Appl Genet 91(6):1153–1161

    Article  CAS  PubMed  Google Scholar 

  • Wendel JF (1989) New world tetraploid cottons contain old world cytoplasm. Proc Natl Acad Sci USA 86(11):4132–4136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wendel JF, Schnabel A, Seelanan T (1995) Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). Proc Natl Acad Sci USA 92(1):280–284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Yu S, Lu C, Wang W, Fan S, Song M et al. (2007) High-density linkage map of cultivated allotetraploid cotton based on SSR, TRAP, SRAP and AFLP markers. J Integr Plant Biol 49(5):716–724

    Article  CAS  Google Scholar 

  • Yu Y, Yuan D, Liang S, Li X, Wang X, Lin Z et al. (2011) Genome structure of cotton revealed by a genome-wide SSR genetic map constructed from a BC1 population between gossypium hirsutum and G. barbadense. BMC Genomics 12(1):15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Stewart J (2004) Semigamy gene is associated with chlorophyll reduction in cotton. Crop Sci 44:2054–2062

    Article  Google Scholar 

  • Zhang JF, Percy RG, McCarty JC (2014) Introgression genetics and breeding between Upland and Pima cotton: a review. Euphytica 198:1–12

    Article  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J et al. (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33(5):531–537

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are thankful to the members of Plant Genome Mapping Laboratory for their help in DNA extractions and SSR genotyping.

Funding

Financial support is acknowledged from the US National Science Foundation (DBI 0817707, AIR 1127755), Cotton Incorporated (14–460), and a Regents Professorship to AHP.

Author information

Authors and Affiliations

  1. Plant Genome Mapping Laboratory, Department of Crop and Soil Sciences, University of Georgia, Athens, GA, USA

    Jeevan Adhikari, Deepak Vitrakoti, Wiriyanat Ployaram & Andrew H. Paterson

  2. Global Institute for Food Security, Saskatoon, SK, Canada

    Rahul Chandnani

  3. Institute of Plant Breeding Genetics and Genomics, Department of Crop and Soil Sciences, University of Georgia, Tifton, GA, USA

    Sameer Khanal

Authors
  1. Jeevan Adhikari
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  2. Rahul Chandnani
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  5. Wiriyanat Ployaram
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  6. Andrew H. Paterson
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Contributions

JA conceived, designed, and performed experiments, developed populations, conducted data analysis and interpretation, and drafted and revised the manuscript. RC performed initial crosses. DV and WP helped in DNA extraction and SSR genotyping, SK performed data analysis and revised manuscript. AHP conceived the project, acquired the funds, supervised the project, and revised the manuscript. All authors contributed to the article and approved the submitted version.

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Correspondence to Andrew H. Paterson.

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Adhikari, J., Chandnani, R., Vitrakoti, D. et al. Comparative transmission genetics of introgressed chromatin in reciprocal advanced backcross populations in Gossypium (cotton) polyploids. Heredity 130, 209–222 (2023). https://doi.org/10.1038/s41437-023-00594-w

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