Skip to main content
Log in

Homoeologous recombination in the presence of Ph1 gene in wheat

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

Abstract

A crossover (CO) and its cytological signature, the chiasma, are major features of eukaryotic meiosis. The formation of at least one CO/chiasma between homologous chromosome pairs is essential for accurate chromosome segregation at the first meiotic division and genetic recombination. Polyploid organisms with multiple sets of homoeologous chromosomes have evolved additional mechanisms for the regulation of CO/chiasma. In hexaploid wheat (2n = 6× = 42), this is accomplished by pairing homoeologous (Ph) genes, with Ph1 having the strongest effect on suppressing homoeologous recombination and homoeologous COs. In this study, we observed homoeologous COs between chromosome 5Mg of Aegilops geniculata and 5D of wheat in plants where Ph1 was fully active, indicating that chromosome 5Mg harbors a homoeologous recombination promoter factor(s). Further cytogenetic analysis, with different 5Mg/5D recombinants, showed that the homoeologous recombination promoting factor(s) may be located in proximal regions of 5Mg. In addition, we observed a higher frequency of homoeologous COs in the pericentromeric region between chromosome combination of rec5Mg#2S·5Mg#2L and 5D compared to 5Mg#1/5D, which may be caused by a small terminal region of 5DL homology present in chromosome rec5Mg#2. The genetic stocks reported here will be useful for analyzing the mechanism of Ph1 action and the nature of homoeologous COs.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aghaee-Sarbarzeh M, Ferrahi M, Singh S, Singh H, Friebe B et al (2002) PhI-induced transfer of leaf and stripe rust-resistance genes from Aegilops triuncialis and Ae. geniculata to bread wheat. Euphytica 127:377–382

    Article  CAS  Google Scholar 

  • Al-Kaff N, Knight E, Bertin I, Foote T, Hart N, Griffiths S, Moore G (2008) Detailed dissection of the chromosomal region containing the Ph1 locus in wheat, Triticum aestivm: with deletion mutants and expression profiling. Ann Bot 101:863–872

    Article  CAS  PubMed  Google Scholar 

  • Bhullar R, Nagarajan R, Bennypaul H, Sidhu G, Rustgi S, Wettstein DV et al (2014) Silencing of a metaphase I-specific gene results in a phenotype similar to that of the pairing homoeologous 1 (Ph1) gene mutations. Proc Natl Acad Sci 111:14187–14192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cifuentes M, Benavente E (2009) Wheat-alien metaphase I pairing of individual wheat genomes and D genome chromosomes in interspecific hybrids between Triticum aestivum L. and Aegilops geniculata Roth. Theor Appl Genet 119:805–813

    Article  CAS  PubMed  Google Scholar 

  • Colas I, Shaw P, Prieto P, Wanous M, Spielmeyer W, Mago R, Moore G (2008) Effective chromosome pairing requires chromatin remodeling at the onset of meiosis. Proc Natl Acad Sci 105:6075–6080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM (1998) Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 94:387–398

    Article  CAS  PubMed  Google Scholar 

  • Dover GA, Riley R (1972) Prevention of pairing of homoeologous meiotic chromosomes of wheat by an activity of supernumerary chromosomes of Aegilops. Nature 240:159–161

    Article  Google Scholar 

  • Driscoll CJ (1972) Genetic suppression of homoeologous chromosome pairing in hexaploid wheat. Can J Genet Cytol 14:39–42

    Article  Google Scholar 

  • Dvorak J (1987) Chromosomal distribution of genes in diploid Elytriga elongata that promote or suppress pairing of wheat homoeologous chromosomes. Genome 29:34–40

    Article  Google Scholar 

  • Dvorak J, Deal KR, Luo M-C (2006) Discovery and mapping of wheat Ph1 suppressors. Genetics 174:17–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farooq S, Shah TM, Asghar M (1996) Intergeneric hybridization for wheat improvement. 5. Production of and metaphase 1 chromosome analysis in F1 hybrids of wheat (Triticum aestivum) with Aegilops ovata L. Cereal Res Commun 24:155–161

    Google Scholar 

  • Friebe B, Gill BS, Tuleen NA (1999) Development and cytogenetic identification of a set of Triticum aestivum-Aegilops geniculata chromosome addition lines. Genome 42:374–380

    Article  Google Scholar 

  • Friebe B, Heun M (1989) C-banding pattern and powdery mildew resistance of Triticum ovatum and four T. aestivum-T. ovatum chromosome addition lines. Theor Appl Genet 78:417–424

    CAS  PubMed  Google Scholar 

  • Gill BS, Sharma HC, Raupp WJ, Browder LE, Hatchett JH, Harvey TL et al (1985) Evaluation of Aegilops species for resistance to wheat powdery mildew, wheat leaf rust, Hessian fly, and greenbug. Plant Dis 69:314–316

    Google Scholar 

  • Giorgi B (1978) A homoeologous pairing mutant isolated in Triticum durum cv. Cappelli. Mutat Breed Newsl 11:4–5

    Google Scholar 

  • Greer E, Martin AC, Pendle A, Colas I, Jones AM, Moore G, Shaw P (2012) The Ph1 locus suppresses Cdk2-type activity during premeiosis and meiosis in wheat. Plant Cell 24:152–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20:589–600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Griffiths S, Sharp R, Foote TN, Bertin I, Wanous M, Reader SM et al (2006) Molecular characterization of Ph1 as a major chromosome pairing locus in polyploidy wheat. Nature 439:749–752

    Article  CAS  PubMed  Google Scholar 

  • Higgins JD, Perry RM, Barakat A, Ramsay L, Waugh R et al (2012) Spatiotemporal asymmetry of the meiotic program underlies the predominantly distal distribution of meiotic crossovers in barley. Plant Cell 24:4096–4109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones GH (1984) The control of chiasma distribution. Sym Soc Exp Biol 38:293–320

    CAS  Google Scholar 

  • Jones GH, Franklin FC (2006) Meiotic crossing-over: obligation and interference. Cell 126:246–248

    Article  CAS  PubMed  Google Scholar 

  • Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384

    Article  CAS  PubMed  Google Scholar 

  • Knight E, Greer E, Draeger T, Thole V, Reader S, Shaw P, Moore G (2010) Inducing chromosome pairing through premature condensation: analysis of wheat interspecific hybrids. Funct Integr Genomics 10:603–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koo D-H, Jiang JM (2009) Super-stretched pachytene chromosomes for fluorescence in situ hybridization mapping and immunodetection of DNA methylation. Plant J 59:509–516

    Article  CAS  PubMed  Google Scholar 

  • Koo D-H, Han F, Birchler JA, Jiang JM (2011) Distinct DNA methylation patterns associated with active and inactive centromeres of the maize B chromosome. Genome Res 21:908–914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kota RS, Dvorak J (1986) Mapping of a chromosome pairing gene and 5S rRNA genes in Triticum aestivum L. by a spontaneous deletion in chromosome arm 5Bp. Can J Genet Cytol 28:266–271

    Article  CAS  Google Scholar 

  • Kuraparthy V, Chhuneja P, Dhaliwal HS, Kaur S, Bowden RL, Gill BS (2007) Characterization and mapping of cryptic introgression from Ae. geniculata with new leaf rust and stripe rust resistance genes Lr57 and Yr40 in wheat. Theor Appl Genet 114:1379–1389

    Article  CAS  PubMed  Google Scholar 

  • Kuraparthy V, Sood S, Gill BS (2009) Molecular genetic description of the cryptic wheat–Aegilops geniculata introgression carrying rust resistance genes Lr57 and Yr40 using wheat ESTs and synteny with rice. Genome 52:1025–1036

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Rouse M, Friebe B, Jin Y, Gill BS, Pumphrey MO (2011) Discovery and molecular mapping of a new gene conferring resistance to stem rust, Sr53, derived from Aegilops geniculata and characterization of spontaneous translocation stocks with reduced alien chromatin. Chromosom Res 19:669–682

    Article  CAS  Google Scholar 

  • Lukaszewski AJ, Lpinski B, Rybka K (2005) Limitations of in situ hybridization with total genomic DNA in routine screening for alien introgressions in wheat. Cytogenet Genome Res 109:373–377

    Article  CAS  PubMed  Google Scholar 

  • MacQueen AJ, Phillips CM, Bhalla N, Weiser P, Villeneuve AM, Dernburg AF (2005) Chromosome sites play dual roles to establish homologous synapsis during meiosis in C. elegans. Cell 123:1037–1050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahadevaiah SK, Turner JMA, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J et al (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 27:271–276

    Article  CAS  PubMed  Google Scholar 

  • Martin AC, Shaw P, Phillips D, Reader S, Moore G (2014) Licensing MLH1 sites for crossover during meiosis. Nat Commun 5:4580

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez M, Cuando N, Carcelen N, Romero C (2001) The Ph1 and Ph2 loci play different roles in the synaptic behavior of hexaploid wheat Triticum aestivum. Theor Appl Genet 103:398–405

    Article  CAS  Google Scholar 

  • McKim KS (2005) When size does not matter: pairing sites during meiosis. Cell 123:989–992

    Article  CAS  PubMed  Google Scholar 

  • McKim KS, Green-Marroquin BL, Sekelsky JJ, Chin G, Steinberg C, Khodosh R et al (1998) Meiotic synapsis in the absence of recombination. Science 279:876–878

    Article  CAS  PubMed  Google Scholar 

  • Mello-Sampayo T (1971) Genetic regulation of meiotic chromosome pairing by chromosome 3D of Triticum aestivum. Nat New Biol 230:23–24

    Article  Google Scholar 

  • Orellana J (1985) Most of the homoeologous pairing at metaphase I in wheat-rye hybrids is not chiasmatic. Genetics 111:917–931

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prieto P, Shaw P, Moore G (2004) Homologue recognition during meiosis is associated with a change in chromatin conformation. Nat Cell Biol 6:906–908

    Article  CAS  PubMed  Google Scholar 

  • Qi LL, Friebe B, Gill BS (2007) Homoeologous recombination, chromosome engineering and crop improvement. Chromosom Res 15:3–19

    Article  CAS  Google Scholar 

  • Riley R (1960) The diploidization of polyploid wheat. Heredity 15:407–429

    Article  Google Scholar 

  • Riley R, Chapman V (1958) Genetic control of the cytologically diploid behavior of hexaploid wheat. Nature 182:713–715

    Article  Google Scholar 

  • Riley R, Chapman V, Miller TE (1973) The determination of meiotic chromosome pairing. Proc. 4th Int. Wheat Genet. Symp. Columbia, Mo., USA. pp. 713–738

  • Sears ER (1976) Genetic control of chromosome pairing in wheat. Ann Rev Genet 10:31–51

    Article  CAS  PubMed  Google Scholar 

  • Sears ER (1977) An induced mutant with homoeologous pairing in common wheat. Can J Genet Cytol 19:585–593

    Article  Google Scholar 

  • Shen Y, Tang D, Wang K, Wang M, Huang J, Luo W, Luo Q, Hong L, Li M, Cheng Z (2012) ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J Cell Sci 125:2581–2591

    Article  CAS  PubMed  Google Scholar 

  • Sutton T, Whitford R, Baumann U, Dong C, Able JA, Langridge P (2003) The Ph2 pairing homoeologous locus of wheat (Triticum aestivum): identification of candidate meiotic genes using a comparative genetics approach. Plant J 36:443–456

    Article  CAS  PubMed  Google Scholar 

  • Zhang P, Friebe B, Lukazewski AJ, Gill BS (2001) The centromere structure in Robertsonian wheat-rye translocation chromosomes indicates that centric breakage-fusion can occur at different positions within the primary constriction. Chromosoma 110:335–344

    Article  CAS  PubMed  Google Scholar 

  • Zickler D (2006) From early homologue recognition to synaptonemal complex formation. Chromosoma 115:158–174

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank W. John Raupp for critical review of the manuscript and Duane Wilson for technical assistance. We also thank Dr. A. J. Lukaszewski, University of California, Riverside for providing seeds of the wheat-rye recombinant stocks. This research was supported by the WGRC I/UCRC NSF contract 1338897. This is contribution number 16-186-J from the Kansas Agricultural Experiment Station, Kansas State University, Manhattan, KS 66506-5502, U.S.A.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bernd Friebe.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights and informed consent

This article does not contain any studies with human participants or animals performed by any of the authors.

Funding

This research was supported by grants from the Kansas Wheat Commission, the Kansas Crop Improvement Association and WGRC I/UCRC NSF contract 1,338,897.

Electronic supplementary material

Fig. S1.

GISH patterns of mitotic metaphase cell of plants double monosomic for 5Mg#1 and 5D (a), and double monosomic for rec5Mg2 and 5D (b), labeled with genomic Ae. comosa DNA (visualized in green) and Ae. tauschii DNA (visualized in red). Arrows indicate the 5Mg chromosome. Bars =10 μm. (JPEG 421 kb)

Fig. S2.

GISH pattern of mitotic metaphase (a) and meiotic pachytene chromosomes (b) of the wheat plants double monosomic wheat-Ae. speltoides translocation chromosome T7SL·7SS-7AS and 7A; b: complete synaptic association (98%, n = 100) between 7A (visualized in green) and T7SL·7SS-7AS (red); c: ideogram showing chromosome 7A and T7SL·7SS-7AS. The white arrowhead points to the centromere and the red arrow to 7A-7S translocation point. (JPEG 603 kb)

Fig. S3.

a: Recombinants recovered in the progeny of plants double monosomic for rec5Mg#2 (R5) and 5D. Nineteen recombinants (24.3%, n = 78) were recovered. 5Mg chromatin was visualized in green and 5D chromatin as red. b: Crossover distribution in recombinants derived from R5/5D (blue bars) and from 5Mg#2/5D plants (orange bars). (JPEG 446 kb)

Fig. S4.

Homoeologous pairing between chromosomes rec5Mg#2 and 5Ss of Ae. searsii (a and b), and recombinant chromosomes recovered in the progeny (c). a: 5Mg#2 and 5Ss univalents (91%); b: chiasmate association (9.0%) at MI; c: recombinants (6.7%, n = 56) derived from homoeologous recombination of rec5Mg#2 (visualized in green) and 5Ss (visualized in red) in a-1 left, and vice versa in b-1 right. d: MI of meiosis of plants double monosomic for chromosomes 5D and 5Ss of Ae. searsii , no chiasmata association was observed (0.0%, n = 120). e: meiotic metaphase I of plants double monosomic for chromosomes 7Mg of Ae. geniculata and 7D of wheat showing univalent and very few chiasmate association (0.4%, n = 237). (JPEG 624 kb)

Fig. S5.

Metaphase I pairing in a F1 plant [DS5Mg#1(5D) x Secale cereale, 2n = 2× = 14, RR]. a: mitotic chromosome constitution showing seven rye chromosomes (red), 20 A-, B-, and D-genome wheat chromosomes (blue), and one 5Mg#1 chromosome (green); b: chiasmate metaphase I association (1.5%, n = 130) between chromosome 5Mg#1 and chromosome 5R of rye; c: chiasmate association between chromosome 5Mg#1 and a chromosome (5A or 5B) of wheat; d: chiasmate association (3.8%, n = 130) between one rye chromosome and one wheat chromosome. W and R represent the wheat and rye chromosomes, respectively. (JPEG 673 kb)

Fig. S6.

Homoeologous pairing in the F1 plants of (Chinese Spring wheat x Ae. geniculata). a-b: A-, B-, and U-genome chromosomes are visualized in blue and wheat D-genome and Ae. geniculata M-genome chromosome in red and green, respectively, in a and b. Sequential GISH/FISH using genomic DNA of Ae. umbellulata and the D-genome specific repetitive DNA probe pAs1 were used to identify U- and D-genome chromosomes (c-d). a: homoeologous pairing between 5Mg#1 and 5D (3.4%, n = 114) (white signal marked by green arrow identifies repetitive DNA that is abundant in chromosome 5Mg#1, unpublished). Four different types of chiasmate associations were identified type a: wheat-wheat (W-W), type b: wheat-M genome (W-M), type c: M genome-U genome (M-U), and type d: U genome-wheat (U-W). (JPEG 716 kb)

Table S1

(DOCX 13 kb)

Table S2

(DOCX 14 kb)

Table S3

(DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koo, DH., Liu, W., Friebe, B. et al. Homoeologous recombination in the presence of Ph1 gene in wheat. Chromosoma 126, 531–540 (2017). https://doi.org/10.1007/s00412-016-0622-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-016-0622-5

Keywords

Navigation