Low X/Y divergence in four pairs of papaya sex-linked genes

doi:10.1111/j.1365-313X.2007.03329.x

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Wiley InterScience

The Plant Journal

Volume 53 Issue 1, Pages 124 - 132

Published Online: 27 Sep 2007

Published in association with the Society for Experimental Biology

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Low X/Y divergence in four pairs of papaya sex-linked genes

Qingyi Yu ¹ , Shaobin Hou ² , F. Alex Feltus ³ , Meghan R. Jones ¹ , Jan E. Murray ¹ , Olivia Veatch ^1,4 , Cornelia Lemke ³ , Jimmy H. Saw ² , Richard C. Moore ⁵ , Jyothi Thimmapuram ⁶ , Lei Liu ⁶ , Paul H. Moore ⁷ , Maqsudul Alam ² , Jiming Jiang ⁸ , Andrew H. Paterson ³ and Ray Ming ^1,9,*

¹ Hawaii Agriculture Research Center, Aiea, HI 96701, USA,
² Center for Advanced Studies in Genomics, Proteomics and Bioinformatics, University of Hawaii, Honolulu, HI 96822, USA,
³ Plant Genome Mapping Laboratory, University of Georgia, Athens, GA 30602, USA,
⁴ Department of Molecular Bioscience and Bioengineering, University of Hawaii, Honolulu, HI 96822, USA,
⁵ Department of Botany, Miami University, Oxford, OH 45056, USA,
⁶ W.M. Keck Center for Comparative and Functional Genomics, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA,
⁷ USDA-ARS, Pacific Basin Agricultural Research Center, Hilo, HI 96720, USA , ⁸ Department of Horticulture, University of Wisconsin, Madison, WI 53706, USA, and
⁹ Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA

Correspondence to *(fax +1 217 244 1336; e-mail rming@life.uiuc.edu).

KEYWORDS

Carica papaya • chromosomal rearrangements • molecular evolution • male-specific region of the Y chromosome (MSY) • sex chromosomes

ABSTRACT

Sex chromosomes in flowering plants, in contrast to those in animals, evolved relatively recently and only a few are heteromorphic. The homomorphic sex chromosomes of papaya show features of incipient sex chromosome evolution. We investigated the features of paired X- and Y-specific bacterial artificial chromosomes (BACs), and estimated the time of divergence in four pairs of sex-linked genes. We report the results of a comparative analysis of long contiguous genomic DNA sequences between the X and hermaphrodite Y (Y^h) chromosomes. Numerous chromosomal rearrangements were detected in the male-specific region of the Y chromosome (MSY), including inversions, deletions, insertions, duplications and translocations, showing the dynamic evolutionary process on the MSY after recombination ceased. DNA sequence expansion was documented in the two regions of the MSY, demonstrating that the cytologically homomorphic sex chromosomes are heteromorphic at the molecular level. Analysis of sequence divergence between four X and Y^h gene pairs resulted in a estimated age of divergence of between 0.5 and 2.2 million years, supporting a recent origin of the papaya sex chromosomes. Our findings indicate that sex chromosomes did not evolve at the family level in Caricaceae, and reinforce the theory that sex chromosomes evolve at the species level in some lineages.

Received 21 July 2007; revised 15 August 2007; accepted 11 September 2007.

DIGITAL OBJECT IDENTIFIER (DOI)

10.1111/j.1365-313X.2007.03329.x About DOI