The Evolution of Reproductive Systems and Sex-Determining Mechanisms Within Rumex (Polygonaceae) Inferred from Nuclear and Chloroplastidial Sequence Data

Abstract

The genus Rumex includes hermaphroditic, polygamous, gynodioecious, monoecious, and dioecious species, with the dioecious species being represented by different sex-determining mechanisms and sex-chromosome systems. Therefore, this genus represents an exceptional case study to test several hypotheses concerning the evolution of both mating systems and the genetic control of sex determination in plants. Here, we compare nuclear intergenic transcribed spacers and chloroplast intergenic sequences of 31 species of Rumex. Our phylogenetic analysis supports a systematic classification of the genus, which differs from that currently accepted. In contrast to the current view, this new phylogeny suggests a common origin for all Eurasian and American dioecious species of Rumex, with gynodioecy as an intermediate state on the way to dioecy. Our results support the contention that sex determination based on the balance between the number of X chromosomes and the number of autosomes (X/A balance) has evolved secondarily from male-determining Y mechanisms and that multiple sex-chromosome systems, XX/XY1Y2, were derived twice from an XX/XY system. The resulting phylogeny is consistent with a classification of Rumex species according to their basic chromosome number, implying that the evolution of Rumex species might have followed a process of chromosomal reduction from x = 10 toward x = 7 through intermediate stages (x = 9 and x = 8).

The Birds and the Bees and the Flowers and the Trees: Lessons from Genetic Mapping of Sex Determination in Plants and Animals

“…Among the best studied dioecious taxa, male heterogamety has evolved twice in the genus Silene (Mrackova et al 2008), twice more in the Hawaiian genus Schiedia in the same family, Caryophyllaceae (Sakai et al 2006), and twice yet again in the genus Rumex in another family (Navajas-Perez et al 2005). In all these cases, dioecy probably evolved within the past 10-15 million years (dioecy in Silene is estimated to have evolved more recently than in Rumex, and dioecious Schiedia evolved more recently still).…”

“…XY 1 Y 2 neosex chromosome systems have arisen in Humulus japonicus (Kihara and Hirayoshi 1932;Kim et al 2008), and Silene diclinis (Howell et al 2009), and twice independently in Rumex (Smith 1963(Smith , 1969Navajas-Perez et al 2005), and Viscum fischeri has a multiple Y system (Barlow and Wiens 1976). These situations probably evolved by X-autosome translocations (Figure 1; changing the ancestrally autosomal element into a chromosome that segregates from the new arm of the X, denoted by Y 2 , while Y 1 denotes the ancestral Y), although fission of the Y cannot yet be ruled out in Rumex; genetic maps using genic markers might be able to establish whether the Y chromosomes still carry functional genes (as in Silene; see for instance Marais et al 2008), in which case their gene content could be compared and this possibility tested.…”

“…Given our wide taxonomic scope, it is important to note, first, that the terms X and Y chromosomes (or Z and W) do not necessarily mean a chromosome pair carrying the genes giving the earliest sex-determining signal to the developmental system. In some systems, the sex chromosomes and autosomes jointly determine sex, such as the X-autosome balance systems of Drosophila, C. elegans, and the plant Rumex (Navajas-Perez et al 2005). Cases such as these probably evolved from ancestors whose sex chromosomes did carry such genes.…”

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

“…The diagram to the left uses the same color-coding and further illustrates the chimeric nature and origin of most chromosomes. Chromosome XIX contains high homology with chromosome XIII expected for the peritelomeric end of XIX which contains the segment related to gender determination Numbers of flowering trees with male and female flowers are presented *p≤0.05; **p≤0.01; ***p≤0.001; ****p≤0.0001; values are significant at their respective levels; *****p>0.5; values are nonsignificant at this level a Populus x canadensis, P. deltoides × P. nigra; P. x generosa, P. deltoides × P. trichocarpa; P. x wettsteinii, P. tremula × P. tremuloides determination based on the X/A (autosome) ratio (e.g., Rumex acetosa) (Navajas-Pérez et al 2005). There is also a species, Rumex hastatulus, which has two chromosomal races: the Texas race with XX/XY and the North Carolina race with XX/XY1Y2.…”

Comparative Genetic Mapping Points to Different Sex Chromosomes in Sibling Species of Wild Strawberry (Fragaria)

“…Furthermore, sex chromosomes have diverged within one section of the genus, with species Silene diclinis possessing neo-sex chromosomes, while two sister species (S. latifolia and S. dioica) have only the ancestral state (Howell et al 2009). Despite the wide phylogenetic distribution of dioecy and sex chromosomes in flowering plants (Charlesworth 2002), only a handful have been the subject of genetic mapping studies (grape: Telgmann-Rauber et al 2007; papaya: Sondur et al 1996;Ma et al 2004;Chen et al 2007; kiwifruit: Testolin et al 2001), and even fewer have been the subject of comparative analyses that can inform on other evolutionary dynamics (e.g., Rumex: Navajas- Perez et al 2005;Cunado et al 2007; Silene: Howell et al 2009;papaya: Yu et al 2008a;Wu et al 2010).…”