A primitive Y chromosome in papaya marks incipient sex chromosome evolution

Abstract

Many diverse systems for sex determination have evolved in plants and animals. One involves physically distinct (heteromorphic) sex chromosomes (X and Y, or Z and W) that are homozygous in one sex (usually female) and heterozygous in the other (usually male). Sex chromosome evolution is thought to involve suppression of recombination around the sex determination genes, rendering permanently heterozygous a chromosomal region that may then accumulate deleterious recessive mutations by Muller's ratchet, and fix deleterious mutations by hitchhiking as nearby favourable mutations are selected on the Y chromosome. Over time, these processes may cause the Y chromosome to degenerate and to diverge from the X chromosome over much of its length; for example, only 5% of the human Y chromosome still shows X-Y recombination. Here we show that papaya contains a primitive Y chromosome, with a male-specific region that accounts for only about 10% of the chromosome but has undergone severe recombination suppression and DNA sequence degeneration. This finding provides direct evidence for the origin of sex chromosomes from autosomes.

The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus)

“…These genes include 11 cellulose synthase (CesA) genes, the same number as in Arabidopsis but 7 fewer than in poplar. Putative cellulose orientation genes (COBRA) were more abundant in Arabidopsis (12) than in papaya (8).…”

“…Perhaps papaya has developed an alternative way of integrating light or timing information specific to day-neutral plants, such as a strict adherence to the diel light/dark cycle that is better served by the COPmediated system. Sex determination in papaya is controlled by a pair of primitive sex chromosomes, with a small male-specific region of the Y chromosome (MSY) 8 . The physical map of the MSY is currently estimated by chromosome walking to span about 8 Mb (ref.…”

“…It has a relatively small genome of 372 megabases (Mb) 6 , diploid inheritance with nine pairs of chromosomes, a well-established transformation system 7 , a short generation time (9-15 months), continuous flowering throughout the year and a primitive sex-chromosome system 8 . It is a member of the Brassicales, sharing a common ancestor with Arabidopsis about 72 million years ago 9 .…”

The obscure events contributing to the evolution of an incipient sex chromosome in Populus: a retrospective working hypothesis

“…The chromosomes of Populus are typically metacentric and small (Blackburn and Harrison 1924;Meurman 1925;Erlanson and Hermann 1927;Nakajima 1937;Islam-Faridi et al 2009), and based on cytological studies, there is no evidence of morphologically differentiated sex chromosomes in any Populus species (Peto 1938;Van Dillewijn 1940;van Buijtenen and Einspahr 1959). One generalized hypothesis is that sex chromosomes originate from autosomes, and dioecy almost certainly evolves from ancestral hermaphrodites that lacked sex chromosomes (Muller 1914;Liu et al 2004). Based on genetic mapping results, evidence of sex chromosomes has been reported in various species by Gaudet et al (2008), Yin et al (2008), Pakull et al (2009Pakull et al ( , 2011, and Paolucci et al (2010).…”

Is the Y chromosome disappearing?—Both sides of the argument

“…In some groups of animals, both ZW and XY systems are reported in the same groups (Organ and Janes 2008;Ross et al 2009) even at the level of the same genera (Campos-Ramos et al 2001;Griffin et al 2000;Harvey et al 2002;Takehana et al 2007) or species (Ogata et al 2007). While there are a number of examples of fish (Kondo et al 2004;Peichel et al 2004), insects (Bachtrog and Charlesworth 2002;Benatti et al 2010), and plants (Liu et al 2004;Filatov 2005) with novel sex chromosome systems close to the beginning of the degenerative process, neo-sex chromosomes have been identified in very few mammalian, avian or insect species (Zhou et al 2008;Pala et al 2011;Carvalho and Clark 2005).…”