Molecular mimicry and the hijacking of sex determination mechanisms in dioecious Silene dioica by the anther smut fungus Microbotryum violaceum.

Investigators

Phil Gilmartin (UEA), Sophien Kamoun (TSL)

Background

Silene dioica (red campion) and Silene latifolia (white campion) are two dioecious species with the Caryophyllaceaea that share a common XY sex determination mechanism that evolved prior to speciation.   Males are the heterogametic sex and possess a dominant Y chromosome.  Females are homogametic and possess two X chromosomes.  This system superficially is similar, although of independent origin, to the XY sex chromosome system in mammals. However, in mammals, the default program is female, with the dominant Y chromosome switching the reproductive destiny of the germ line in favour of male development.  In most plants the default program is hermaphroditism.  However, in dioecious Silene species female plants develop carpels as programmed by the pair of X chromosomes and diploid autosome complement, but stamen development is arrested at an early stage due to the absence of a Y chromosome.   In male flowers, the presence of a male determining Y chromosome provides the cue to enable the stamen primordia to continue to develop into functional stamens.  A second Y chromosome locus is responsible for pollen production in the resulting anthers.   The Y chromosome carries a third locus that suppresses carpel development to yield male rather than hermaphrodite flowers.  This reproductive development system is remarkable in itself, but what is truly astonishing is the species-specific interaction between the anther smut fungus Microbotryum violaceum and S. dioica and S. latifolia.  Infection of these species by the anther smut fungus leads to the triggering of stamen development in the genetically female flowers. The fungus can therefore mimic the reproductive developmental signal, provided by the Y chromosome in males, to promote mature stamen development from pre-formed anther primorida in genetically female flowers.  When the anthers of these parasitized flowers dehisce, they release fungal spores in place of pollen.  The parasitism has not only hijacked male reproductive development within the flower, but has also exploited the pollen dissemination mechanism.  Nothing is known about the molecular mimicry that underpins this remarkable plant fungal interaction; this project will change that.

Objectives

The key objectives of this ELSA supported project are to:

  1. Generate transcriptome data sets from male, female and smut infected female flowers of S. dioica.
  2. Use the available genome sequence to identify M. violaceum transcripts within the flower transcriptomes.
  3. Use male-specific S. dioica and M. violaceum transcripts to predict genes encoding common regulators.

Scientific program

This collaboration between the Kamoun lab at The Sainsbury laboratory and the Gilmartin Lab at UEA/John Innes Centre, will generate transcriptome data sets for male and female S.dioica flower buds, and M. violaceum infected male and female S. dioica flower buds. Bioinformatic comparisons will be used to identify those transcripts within infected flower buds that derive from M. Violaceum.   Similar analyses will be used to identify transcripts present uniquely within the male flower buds. Comparison of the M. violaceum transcriptome and male flower transcriptome will identify Microbotryum genes that share homology with the male specific genes. These in silico comparisons will be used to predict potential candidates for the Y chromosome-encoded gene that triggers maturation of stamen primordia and the M. violaceum-encoded gene that mimics this function in infected plants.   This project provides an approach to predict candidate genes for subsequent functional analyses from M. violaceum and S. dioica that have, through convergent evolution, acquired the same role in promoting stamen development.

Flowers of Silene latifolia

Dissected flowers of Silene latifolia

Female flower (XX) showing carpels but no stamens (left), female flower (XX) showing reduced carpels and U. violaceum induced stamens with purple spores (middle), male flower (XY) showing stamens but no carpels.

 


Earlham institute
Quadram Institute Bioscience
John Innes Centre
The Sainsbury Laboratory
NHS NNUH
University of East Anglia

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