Premature arrest of the male flower meristem precedes sexual dimorphism in the dioecious plant Silene latifolia

Abstract

Most dioecious plant species are believed to derive from hermaphrodite ancestors. The regulatory pathways that have been modified during evolution of the hermaphrodite ancestors and led to the emergence of dioecious species still remain unknown. Silene latifolia is a dioecious plant species harboring XY sex chromosomes. To identify the molecular mechanisms involved in female organ suppression in male flowers of S. latifolia, we looked for genes potentially involved in the establishment of floral organ and whorl boundaries. We identified homologs of Arabidopsis thaliana SHOOTMERISTEMLESS (STM) and CUP SHAPED COTYLEDON (CUC) 1 and CUC2 genes in S. latifolia. Our phylogenetic analyses suggest that we identified true orthologs for both types of genes. Detailed expression analyses showed a conserved expression pattern for these genes between S. latifolia and A. thaliana, suggesting a conserved function of the corresponding proteins. Comparative in situ hybridization experiments between male, female, and hermaphrodite individuals reveal that these genes show a malespecific pattern of expression before any morphological difference become apparent. Our results make SlSTM and SlCUC strong candidates for being involved in sex determination in S. latifolia.

Plant sex chromosomes: molecular structure and function

“…By using homeotic mutants of C. sativus , Kater et al (2001) demonstrated that the abortion of floral organs in the third and fourth whorl of female or male flowers of cucumber was not dependent on their floral organ identity but on their position in the floral meristem. The S. latifolia orthologues to Arabidopsis thaliana SHOOT-MERISTEMLESS ( STMS ) and CUP SHAPED COTYLEDON ( CUC ) have recently been isolated that participate not only in the establishment and maintenance of the shoot meristem but also in the proper proliferation of cells in the floral meristem that lead to the correct position of the organ primordial (Zluvova et al, 2006). Although these genes are not specifically expressed in males, their expression patterns in female, male and hermaphrodite flowers of S. latifolia by RT-PCR and in situ hybridization suggest that they represent a regulatory pathway involved in sex determination of this species (Zluvova et al, 2006).…”

“…The S. latifolia orthologues to Arabidopsis thaliana SHOOT-MERISTEMLESS ( STMS ) and CUP SHAPED COTYLEDON ( CUC ) have recently been isolated that participate not only in the establishment and maintenance of the shoot meristem but also in the proper proliferation of cells in the floral meristem that lead to the correct position of the organ primordial (Zluvova et al, 2006). Although these genes are not specifically expressed in males, their expression patterns in female, male and hermaphrodite flowers of S. latifolia by RT-PCR and in situ hybridization suggest that they represent a regulatory pathway involved in sex determination of this species (Zluvova et al, 2006). By using a cDNA subtractive hybridization approach we have recently isolated a gene from R. acetosa ( RAFSM-32 ) that has a flower-specific expression, and its expression is higher in female than in male flowers, particularly around the aborted stamen primordia.…”

Analyses of SORTING NEXINs Reveal Distinct Retromer-Subcomplex Functions in Development and Protein Sorting inArabidopsis thaliana

“…In situ hybridization on sections was performed as described (Zluvova et al, 2006). To produce the probes, we cloned in pGEMTeasy (Promega) the entire open reading frame (ORF) of SNX1 (amplified with Nex12F/ Nex39R) and the N-terminal region upstream of the PX domain of SNX2a (amplified with Nex2a1/Nex2aR3) and SNX2b ORF (amplified with Nex2bF4/Nex2bR3), respectively.…”

Independent Origin of Sex Chromosomes in Two Species of the Genus Silene

“…For example, sex chromosomes in S. latifolia have evolved from a single pair of autosomes (Filatov 2005) that have undergone a stepwise reduction of recombination, as shown by a stepwise-gradient of silent site divergence between X-and Y-linked copies of genes from the pseudoautosomal region toward the distal end of the X chromosome Bergero et al 2007). In addition, the mechanism of sex determination in S. latifolia has started to be elucidated (Westergaard 1958;Zluvova et al 2006). Sex determination in S. latifolia is based on the active role of the Y chromosome that possesses genes for malepromoting functions necessary for anther development, genes necessary for male fertility, and genes for the gynoecium-suppressing function, which prevents the development of female sex organs in males.…”