Expression of the Floral B-function Gene SLM2 in Female Flowers of Silene latifolia Infected with the Smut Fungus Microbotryum violaceum

Kazama, Yusuke; Koizumi, Ayako; Uchida, Wakana; Ageez, Amr; Kawano, Shigeyuki

doi:10.1093/pcp/pci080

Cited by 28 publications

(25 citation statements)

References 26 publications

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“…In females of dioecious host species, anther development is induced by the pathogen, and this remarkable symptom caught the attention of early researchers including Darwin (1863) to be followed by a series of studies using the pathogen to understand the host's sexual development (for example, Strasburger, Silene as a model system in ecology and evolution G Bernasconi et al 1900; Shull, 1910). Thus, utility of this disease for studying Silene continues to be shown and is enhanced by modern molecular approaches to gene expression during infection (Uchida et al, 2003;Kazama et al, 2005). Moreover, the smut diseases provide some of the strongest arguments for the value of 'model systems' in their own right.…”

Section: Biotic Interactions: Microbotryum and The Evolutionary Ecolomentioning

confidence: 99%

Silene as a model system in ecology and evolution

et al. 2009

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The genus Silene, studied by Darwin, Mendel and other early scientists, is re-emerging as a system for studying interrelated questions in ecology, evolution and developmental biology. These questions include sex chromosome evolution, epigenetic control of sex expression, genomic conflict and speciation. Its well-studied interactions with the pathogen Microbotryum has made Silene a model for the evolution and dynamics of disease in natural systems, and its interactions with herbivores have increased our understanding of multi-trophic ecological processes and the evolution of invasiveness. Molecular tools are now providing new approaches to many of these classical yet unresolved problems, and new progress is being made through combining phylogenetic, genomic and molecular evolutionary studies with ecological and phenotypic data. The model role of a non-model organismThe genus Silene (Caryophyllaceae), with a tradition of genetical and ecological studies dating back to Mendel and Darwin, has remarkably many interesting features. First, the species in the genus vary widely in their breeding systems and ecology. Second, several members of this mainly holarctic genus can be easily bred, and have short life cycles, and are thus convenient for experimental and field studies. Genomic resources are now becoming increasingly available in Silene, making genetic, quantitative genetic and molecular studies possible. A strength of Silene as a model system, compared with many classical model organisms, is that researchers can rely on a large number of ecological studies encompassing biotic interactions with sexually transmitted fungi, pollinators and herbivores. It is the wealth of ecological and other earlier knowledge that makes the genus Silene important for studying many biological questions, including the suppression of recombination during sex chromosome evolution, sexually antagonistic selection in an organism that is not an animal, epigenetic processes in flower development, speciation and reproductive isolation, multi-trophic interactions, disease ecology and biological invasions.Thanks to the classical genetic and ecological work on Silene, new progress can now be made in studying some of these important unresolved questions in biology with the aid of modern molecular tools. That new model systems with accessible and well-studied ecology open fruitful avenues for investigation is illustrated also by Mimulus (Wu et al., 2008) and the ongoing efforts to develop genomic resources in an increasing number of different systems. In the following, we outline the unique features of the Silene system, and describe active research areas and future directions, highlighting new advances and work in progress. Evolution of sexual systemsPlants show remarkable diversity in their sexual and mating systems, ranging from hermaphroditism to dioecy, from self-incompatible hermaphroditism to hermaphroditism in which individuals possess a capacity to self-fertilize, but which often show complex mechanisms to promote outcrossing (Darwin, 18...

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Section: Biotic Interactions: Microbotryum and The Evolutionary Ecolomentioning

confidence: 99%

Silene as a model system in ecology and evolution

et al. 2009

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“…Several floral identity genes along with the MADS box, SLM genes, are also known to function in floral development of S. latifolia (Hardenack et al, 1994;Kazama et al, 2005). Moreover, RT-PCR with degenerate primers from the conserved regions of Arabidopsis MADS box proteins amplified three novel MADS box genes, SlAP3, SlSEP1 and SlSEP3, from young S. latifolia male flower buds (Matsunaga et al , 2004b.…”

Section: A Mads Box Gene Linked To the Y Chromosomementioning

confidence: 99%

Sex chromosome-linked genes in plants

Matsunaga

2006

Genes Genet. Syst.

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Recent studies of plant sex chromosome-linked genes have revealed many interesting characteristics, although there are limited reports about heteromorphic sex chromosomes in flowering plants. Sex chromosome-linked genes in angiosperms have been characterized mainly in the dioecious plant Silene latifolia . Although all such genes were isolated from transcripts of male flower buds of S. latifolia , most seem to be housekeeping genes except for the petal-and stamen-specific MADS box gene on the Y chromosome ( SlAP3Y ) and the male reproductive organspecific gene on the X chromosome ( MROS3X ). Recent evolutionary studies have revealed at least three evolutionary strata on the X chromosome that are related to stepwise loss of recombination between the sex chromosomes. Moreover, genetic maps showed conservation of gene organization on the X chromosome in the genus Silene and substantial pericentric inversion between the X and Y chromosomes of S. latifolia during evolution. A comparison between paralogs on the sex chromosomes revealed that introns of the Y-linked genes are longer than those of X-linked paralogs. Although analyses of sex chromosome-linked genes suggest that degeneration of the Y chromosome has occurred, the Y chromosome in flowering plants remains the largest in the male genome, unlike that of mammals. Accumulation of repetitive sequences and the entire chloroplast genome on the Y chromosome appear to have contributed to this large size. However, more detailed studies will be required to help explain the basis for the fact that heteromorphic sex chromosomes in angiosperms are large.

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“…M. violaceum induced stamen development after this stage in infected females. Kazama et al, (2005) deteced the expression of the floral development gene, SLM2, in the induced stamens of the infected female. SLM2 was not expressed in the suppressed stamens of the healthy female, which confirms that the smut fungus can mimic the Y-chromosome domain responsible for stamen development.…”

Section: Discussionmentioning

confidence: 99%

“…In situ hybridization In situ hybridization was performed according to Kazama et al, (2005). DNA fragments used for genomic southern were cloned into the pBluescript II SK+ (Stratagen, LaJolla, CA) and used for in vitro transcription of the probes.…”

Section: Virtual Northern and Genomic Southern Blotsmentioning

confidence: 99%

Male-fertility genes expressed in male flower buds of Silene latifolia include homologs of anther-specific genes

et al. 2005

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When the female plant of Silene latifolia is infected with the smut fungus Microbotryum violaceum , its rudimentary stamens develop into anthers which contain fungus teliospores instead of pollen. To identify genes required for maturation of anthers in S. latifolia , we performed a cDNA subtraction approach with healthy male buds and female buds infected with M. violaceum . We isolated five cDNA clones, which were preferentially expressed in healthy male buds during stages associated with a burst in tapetal activity. These five cDNAs are predicted to encode a mandelonitrile lyase protein (SlMDL1), a strictosidine synthase protein (SlSs), a glycosyl hydrolase 17 protein ( SlGh17), a proline-rich protein APG precursor (SlAPG), and a chalcone-synthase-like protein (SlChs). All five genes showed expression in both healthy and fungus-infected male buds, but not expressed in either healthy or infected female buds. The first three genes were highly expressed in both tapetum and pollen grains while the last two genes were expressed only inside the tapetum of male flower buds. Phylogenetic analysis results showed that SlChs and SlGh17 belong to anther-specific subgroups of chalcone-synthase-like genes and glycosyl hydrolase 17 family genes, respectively. Our results suggest that the isolated five genes are related to the fertility of the anther leading to the development of fertile pollen. The smut fungus was not able to induce the expression of the five genes in the infected female buds. This raises the possibility that these genes are under the control of master gene(s) on the Y chromosome.

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Expression of the Floral B-function Gene SLM2 in Female Flowers of Silene latifolia Infected with the Smut Fungus Microbotryum violaceum

Cited by 28 publications

References 26 publications

Silene as a model system in ecology and evolution

Silene as a model system in ecology and evolution

Sex chromosome-linked genes in plants

Male-fertility genes expressed in male flower buds of Silene latifolia include homologs of anther-specific genes

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