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An integrated cytogenetic and physical map reveals unevenly distributed recombination spots along the papaya sex chromosomes

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Abstract

Papaya is a model system for the study of sex chromosome evolution in plants. However, the cytological structures of the papaya chromosomes remain largely unknown and chromosomal features have not been linked with any genetic or genomic data. We constructed a cytogenetic map of the papaya sex chromosome (chromosome 1) by hybridizing 16 microsatellite markers and 2 cytological feature-associated markers on pachytene chromosomes using fluorescence in situ hybridization (FISH). Except for three markers, the order of the markers was concordant to that of marker loci along the linkage map. This discrepancy was likely caused by skewed segregation in the highly heterochromatic or centromeric regions. The papaya sex chromosome is largely euchromatic, its heterochromatin spans about 15 % of the Y chromosome and is mostly restricted to the centromeric and pericentromeric regions. Analysis of the recombination frequency along the papaya sex chromosome revealed a complete suppression of recombination in the centromere and pericentromere region and 60 % higher recombination rate in the long arm than in the short arm. The uneven distribution of recombination events might be caused by differences in sequence composition. Sequence analysis of 18 scaffolds in total length of 15 Mb revealed higher gene density towards the telomeres and lower gene density towards the centromere, and a relatively higher gene density in the long arm than in the short arm. In an opposite trend, the centromeric and pericentromeric region contained the highest repetitive sequences and the long arm showed the lowest repetitive sequences. This cytogenetic map provides essential information for evolutionary study of sex chromosomes in Caricaceae and will facilitate the analysis of papaya sex chromosomes.

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Abbreviations

MSY:

Male-specific region of the Y chromosome

FISH:

Fluorescence in situ hybridization

AFLP:

Amplified fragment length polymorphism

HSY:

Hermaphrodite-specific region of the Y chromosome

MYA:

Million years ago

LG:

Linkage group

SSR:

Simple sequence repeat

CP:

Cytological position

FL:

Fraction length

SD:

Standard deviation

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Acknowledgments

This project was partially supported by a USDA T-STAR grant from the USDA-CSREES, Award # 2008-34135-19371, to the University of Hawaii at Manoa and a sub-award to the Hawaii Agriculture Research Center.

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Authors and Affiliations

  1. Department of Tropical Plant and Soil Sciences, University of Hawaii, Honolulu, HI, 96822, USA

    Ching Man Wai & Robert E. Paull

  2. Hawaii Agriculture Research Center, Waipahu, HI, 96797, USA

    Ching Man Wai, Paul H. Moore, Ray Ming & Qingyi Yu

  3. Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Ray Ming

  4. AgriLife Research Center, Department of Plant Pathology and Microbiology, Texas A&M University, Weslaco, TX, 78596-8344, USA

    Qingyi Yu

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  1. Ching Man Wai
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  2. Paul H. Moore
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  3. Robert E. Paull
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  4. Ray Ming
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  5. Qingyi Yu
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Correspondence to Qingyi Yu.

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Responsible Editor: Tatsuo Fukagawa

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Table S1

Distribution of euchromatin and heterochromatin on chromosome 1 (XLS 35 kb)

Table S2

Transposable element and gene content of scaffolds on chromosome 1 (XLS 25 kb)

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Wai, C.M., Moore, P.H., Paull, R.E. et al. An integrated cytogenetic and physical map reveals unevenly distributed recombination spots along the papaya sex chromosomes. Chromosome Res 20, 753–767 (2012). https://doi.org/10.1007/s10577-012-9312-1

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