Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system

doi:10.1073/pnas.0609054104

Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system

*Laboratory of Plant Molecular Biology, Division of Integrated Life Science, Graduate School of Biostudies, Kyoto University, Kyoto 606-8502, Japan;
^†Plant Genetic Engineering Research Unit, Division of Plant Sciences, National Institute of Agrobiological Sciences, Kannondai, Tsukuba 305-8602, Japan;
^‡Molekulare Botanik, Universität Ulm, 89069 Ulm, Germany;
^§Center for Genetic Resource Information, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan; and
^¶Laboratory of Plant Gene Technology, Research Institute for Bioresources and Biotechnology, Ishikawa Prefectural University, Ishikawa 921-8836, Japan

Edited by Dan L. Lindsley, University of California at San Diego, La Jolla, CA, and approved January 31, 2007 (received for review October 27, 2006)

Abstract

Y chromosomes are different from other chromosomes because of a lack of recombination. Until now, complete sequence information of Y chromosomes has been available only for some primates, although considerable information is available for other organisms, e.g., several species of Drosophila. Here, we report the gene organization of the Y chromosome in the dioecious liverwort Marchantia polymorpha and provide a detailed view of a Y chromosome in a haploid organism. On the 10-Mb Y chromosome, 64 genes are identified, 14 of which are detected only in the male genome and are expressed in reproductive organs but not in vegetative thalli, suggesting their participation in male reproductive functions. Another 40 genes on the Y chromosome are expressed in thalli and male sexual organs. At least six of these genes have diverged X-linked counterparts that are in turn expressed in thalli and sexual organs in female plants, suggesting that these X- and Y-linked genes have essential cellular functions. These findings indicate that the Y and X chromosomes share the same ancestral autosome and support the prediction that in a haploid organism essential genes on sex chromosomes are more likely to persist than in a diploid organism.

Footnotes

^‖To whom correspondence should be addressed. E-mail: kohyama{at}ishikawa-pu.ac.jp
Author contributions: K.T.Y., T.K., H.F., and K.O. designed research; K.T.Y., K.I., M. Fujisawa, S.O., S.N., M. Fujishita, H.B., K.Y., K.H., T.B., A.H., T. Nishio, R.S., M.Y., A.Y., M.K., T.Y., T. Nishide, S.-H.C., Y.S.-U., T.H., M.S., K.K., M.T., S.Y., C.K., Y. Kohzu, H.N., T.S.-i., Y. Kohara, T.K., and H.F. performed research; K.T.Y., K.I., M. Fujisawa, S.O., S.N., M. Fujishita, H.B., K.Y., K.H., T.B., A.H., T. Nishio, R.S., M.Y., A.Y., M.K., T.Y., T. Nishide, S.-H.C., Y.S.-U., T.H., M.S., K.K., A.B., H.F., and K.O. analyzed data; and K.T.Y., K.I., M. Fujisawa, S.O., S.N., A.B., and K.O. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. BJ840459–BJ873180).
This article contains supporting information online at www.pnas.org/cgi/content/full/0609054104/DC1.
Abbreviations:

PAC,

P1-derived artificial chromosome;

rDNA,

ribosomal DNA;

YR2,

Y chromosome region 2.