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Homoeologous recombination in the presence of Ph1 gene in wheat

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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.

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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.

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Authors and Affiliations

  1. Wheat Genetics Resource Center, Department of Plant Pathology, Throckmorton Plant Sciences Center, Kansas State University, Manhattan, KS, 66506-5502, USA

    Dal-Hoe Koo, Wenxuan Liu, Bernd Friebe & Bikram S. Gill

  2. Laboratory of Cell and Chromosome Engineering, College of Life Sciences, Henan Agricultural University, Zhengzhou, 450002, China

    Wenxuan Liu

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  1. Dal-Hoe Koo
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Correspondence to Bernd Friebe.

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

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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)

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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

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