Identification and sequencing of chimpanzee BACs
We screened high-density filters from the RPCI-43 male chimpanzee BAC library
22
(BACPAC resources) using hybridization probes designed to detect sequences (1) near the
inner boundaries of palindromes P1–P6 and P8; (2) near P7; and (3) from a non-
ampliconic region of the human MSY. STS content and BAC-end sequences confirmed
that, among the candidate BACs identified by hybridization, six contained the central
portions of orthologues to human MSY palindromes. The BACs were sequenced as
previously described
2
. Supplementary Table 4 provides descriptions of the sequenced
BACs and their GenBank accession numbers.
Sequence analysis
Sequences were aligned with CLUSTAL W using default parameters
23
. In a few cases, the
resulting alignments were adjusted manually. All alignments are provided as
Supplementary Information.
Typing nucleotide variants in palindrome arms
The sites studied were CDY1þ381 (Fig. 2 and Supplementary Fig. 1), CDY1284
(Supplementary Fig. 2), and sY586 (Supplementary Fig. 3). sY586 was genotyped as
previously described
24
. PCR primers and conditions for amplifying CDY1þ381 (sY1313)
and CDY1284 (sY1314) have been deposited in GenBank (accession numbers G73596 and
G73597, respectively). When typing CDY1þ381 by sequencing, ‘primer A’ in GenBank
G73596 served as the sequencing primer. CDY1284 was typed by sequencing using
‘primer B’ in GenBank G73597.
For the samples that showed evidence of gene conversion (Fig. 2 and Supplementary
Figs 1–3), we excluded the possibility of deletion of one copy of the variant site as discussed
in Supplementary Note 1.
Steady-state balance between mutations and gene-conversion
To show that the combined action of mutation and gene conversion results in a steady-
state level of arm-to-arm divergence, we use the following recursion: d
nþ1
¼ð1 2 c
g
Þd
n
þ
2m
g
where d
n
is the sequence divergence between repeat copies at generation n, m
g
is the
mutation rate per nucleotide per generation, and c
g
is the gene conversion rate per
duplicated nucleotide per generation. We presume that d
0
¼ 0, corresponding to no
differences between sequence copies immediately after the initial duplication event.
However, as 1 2 c
g
, 1, lim
n!1
d
n
¼ 2m
g
/c
g
, for any value of d
0
small enough to support
c
g
. Because m
g
and d are very small, mutations almost never occur at sites that already
differ between the two palindrome arms, and this possibility can be ignored. As shown in
Supplementary Note 2, our analysis is a special case of Ohta’s analysis
25
.
Received 10 March; accepted 7 April 2003; doi:10.1038/nature01723.
1. Skaletsky, H. et al. The male-specific region of the human Y chromosome is a mosaic of discrete
sequence classes. Nature 423, 825–837 (2003).
2. Kuroda-Kawaguchi, T. et al. The AZFc region of the Y chromosome features massive palindromes and
uniform recurrent deletions in infertile men. Nature Genet. 29, 279–286 (2001).
3. Agulnik, A. I. et al. Evolution of the DAZ gene family suggests that Y-linked DAZ plays little, or a
limited, role in spermatogenesis but underlines a recent African origin for human populations. Hum.
Mol. Genet. 7, 1371–1377 (1998).
4. Reijo, R. et al. Diverse spermatogenic defects in humans caused by Y chromosome deletions
encompassing a novel RNA-binding protein gene. Nature Genet. 10, 383–393 (1995).
5. Glaser, B. et al. Simian Y chromosomes: species-specific rearrangements of DAZ, RBM, and TSPY
versus contiguity of PAR and SRY . Mamm. Genome 9, 226–231 (1998).
6. Makova, K. D. & Li, W. H. Strong male-driven evolution of DNA sequences in humans and apes.
Nature 416, 624–626 (2002).
7. Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J. & Stahl, F. W. The double-strand-break repair model
for recombination. Cell 33, 25–35 (1983).
8. Jackson, J. A. & Fink, G. R. Gene conversion between duplicated genetic elements in yeast. Nature 292,
306–311 (1981).
9. Underhill, P. A. et al. The phylogeography of Y chromosome binary haplotypes and the origins of
modern human populations. Ann. Hum. Genet. 65, 43–62 (2001).
10. Murti, J. R., Bumbulis, M. & Schimenti, J. C. High-frequency germ line gene conversion in transgenic
mice. Mol. Cell. Biol. 12, 2545–2552 (1992).
11. Johnson, R. D. & Jasin, M. Sister chromatid gene conversion is a prominent double-strand break
repair pathway in mammalian cells. EMBO J. 19, 3398–3407 (2000).
12. Bailey, J. A. et al. Recent segmental duplications in the human genome. Science 297, 1003–1007 (2002).
13. International Human Genome Sequencing Consortium Initial sequencing and analysis of the human
genome. Nature 409, 860–921 (2001).
14. Small, K., Iber, J. & Warren, S. T. Emerin deletion reveals a common X-chromosome inversion
mediated by inverted repeats. Nature Genet. 16, 95–99 (1997).
15. Aradhya, S. et al. Multiple pathogenic and benign genomic rearrangements occur at a 35 kb
duplication involving the NEMO and LAGE2 genes. Hum. Mol. Genet. 10, 2557–2567 (2001).
16. Rochette, C. F., Gilbert, N. & Simard, L. R. SMN gene duplication and the emergence of the SMN2
gene occurred in distinct hominids: SMN2 is unique to Homo sapiens. Hum. Genet. 108, 255–266
(2001).
17. Deeb, S. S., Jorgensen, A. L., Battisti, L., Iwasaki, L. & Motulsky, A. G. Sequence divergence of the red
and green visual pigments in great apes and humans. Proc. Natl Acad. Sci. USA 91, 7262–7266 (1994).
18. Zhou, Y.-H. & Li, W.-H. Gene conversion and natural selection in the evolution of X-linked color
vision genes in higher primates. Mol. Biol. Evol. 18, 780–783 (1996).
19. Charlesworth, B. & Charlesworth, D. The degeneration of Y chromosomes. Phil. Trans. R. Soc. Lond. B
355, 1563–1572 (2000).
20. Bohossian, H. B., Skaletsky, H. & Page, D. C. Unexpectedly similar rates of nucleotide substitution
found in male and female hominids. Nature 406, 622–625 (2000).
21. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917–920
(1998).
22. Fujiyama, A. et al. Construction and analysis of a human-chimpanzee comparative clone map. Science
295, 131–134 (2002).
23. Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTALW: improving the sensitivity of progressive
multiple sequence alignment through sequence weighting, position-specific gap penalties and weight
matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).
24. Saxena, R. et al. Four DAZ genes in two clusters found in AZFc region of human Y chromosome.
Genomics 67, 256–267 (2000).
25. Ohta, T. Allelic and nonallelic homology of a supergene family. Proc. Natl Acad. Sci. USA 79,
3251–3254 (1982).
26. Casanova, M. et al. A human Y-linked DNA polymorphism and its potential for estimating genetic
and evolutionary distance. Science 230, 1403–1406 (1985).
27. Underhill, P. A. et al. Detection of numerous Y chromosome biallelic polymorphisms by denaturing
high-performance liquid chromatography. Genome Res. 7, 996–1005 (1997).
28. Shen, P. et al. Population genetic implications from sequence variation in four Y chromosome genes.
Proc. Natl Acad. Sci. USA 97, 7354–7359 (2000).
Supplementary Information accompanies the paper on www.nature.com/nature.
Acknowledgements We thank R. K. Alagappan and L. G. Brown for technical contributions;
N. A. Ellis, M. F. Hammer, T. Jenkins and P. A. Underhill for assistance with genealogical studies;
H. M. McClure and Yerkes Regional Primate Research Center for samples; C. Disteche,
A. E. Donnenfeld, J. H. Hersh, T. Jenkins, P. G. McDonough, B. McGillivray, R. D. Oates,
P. Patrizio, R. Rosenfield, L. Shapiro, S. Silber, M. C. Summers, J. Weissenbach, B. Whitmire and
S. Yang for patient samples; and J. E. Alfoldi, B.Charlesworth, A. G. Clark, J. Koubova, J. Lange,
B. Levy, T. L. Orr-Weaver, S. Repping, W. R. Rice and J. Saionz for comments on the manuscript.
This work was supported by the National Institutes of Health and the Howard Hughes Medical
Institute.
Competing interests statement The authors declare that they have no competing financial
interests.
Correspondence and requests for materials should be addressed to D.C.P.
(page_admin@wi.mit.edu). All new DNA sequences and STSs were submitted to GenBank with
accession numbers AC139189–AC139194 (chimpanzeeBACs), AY090860–AY090881
(palindrome boundary sequences in apes), and G73582–G73595 (STS for amplifying palindrome
boundaries); see Supplementary Information for details.
..............................................................
Fibronectin requirement in
branching morphogenesis
Takayoshi Sakai, Melinda Larsen & Kenneth M. Yamada
Craniofacial Developmental Biology and Regeneration Branch, National Institute
of Dental and Craniofacial Research, National Institutes of Health, Bethesda,
Maryland 20892-4370, USA
.............................................................................................................................................................................
Many organs, including salivary glands, lung and kidney, are
formed during embryonic development by epithelial branching.
In branching morphogenesis, repetitive epithelial cleft and bud
formation create the complex three-dimensional branching
structures characteristic of many organs
1–3
. Although the mech-
anisms are poorly understood, one might involve the site-specific
accumulation of some regulatory protein. Here we show that the
extracellular matrix protein fibronectin
4,5
is essential for cleft
formation during the initiation of epithelial branching. Fibro-
nectin messenger RNA and fibrils appeared transiently and
focally in forming cleft regions of submandibular salivary-
gland epithelia, accompanied by an adjacent loss of cadherin
localization. Decreasing the fibronectin concentration by using
small interfering RNA and inhibition by anti-fibronectin or anti-
integrin antibodies blocked cleft formation and branching.
Exogenous fibronectin accelerated cleft formation and branch-
ing. Similar effects of fibronectin suppression and augmentation
were observed in developing lung and kidney. Mechanistic
studies revealed that fibrillar fibronectin can induce cell–matrix
adhesions on cultured human salivary epithelial cells with a
local loss of cadherins at cell–cell junctions. Thus, fibro-
nectin expression is required for cleft formation in branching
letters to nature
NATURE | VOL 423 | 19 JUNE 2003 | www.nature.com/nature 876 © 2003 Nature Publishing Group