Fungal infection induces sex-specific transcriptional changes and alters sexual dimorphism in the dioecious plant Silene latifolia. Silene latifolia strain:U11

Sexual dimorphism, including differences in morphology, behavior and physiologybetween males and females, is widespread in animals and plants and is shaped bygene expression differences between the sexes. Such expression differences may alsounderlie sex-specific responses of hosts to pathogen infections, most notably whenpathogens induce partial sex reversal in infected hosts. The genetic changesassociated with sexual dimorphism, on the one hand, and sex-specific responses topathogen infections, on the other hand, remain poorly understood. The dioeciousWhite Campion (Silene latifolia) displays strong sexual dimorphism in floral traits andinfection with the smut fungus Microbotryum violaceum induces a partial sex reversal infemales, rendering them more male-like. We find strong sex-specific responses topathogen infection in S. latifolia. This allows for the first time to link pathogen-mediatedchanges in sex-biased gene expression to altered sexual dimorphism in the host. Infemales, expression changes following infection led to transcriptome defeminizationand masculinization, whereas in males, infection caused widespread down-regulationof contigs with male-biased expression in healthy plants, leading to opposite changesof expression patterns, and thus to feminization and demasculinization of thetranscriptome in response to smut infection. These transcriptional changes includedactivation of sex-specific genes in the opposite sex and were associated with a partialsex reversal in females and reduced sexual dimorphism between infected male andfemale hosts. Our results reveal strong sex-specific responses to pathogen infection ina dioecious plant and provide a link between changes in sex-biased gene expressionand sexual dimorphism.

雌雄异型（Sexual dimorphism）指雄性与雌性在形态、行为及生理层面的差异，该现象广泛分布于动植物界，其形成受两性间基因表达差异的调控。此类表达差异同样可能是宿主对病原体感染产生性别特异性响应的基础，尤其当病原体诱导受感染宿主发生部分性逆转时，这一关联更为显著。目前，与雌雄异型相关的遗传变化，以及宿主针对病原体感染的性别特异性响应这两类问题，均尚未得到充分解析。雌雄异株（dioecious）植物白玉草（Silene latifolia）在花部性状上表现出显著的雌雄异型特征；当其感染黑粉菌（smut fungus, Microbotryum violaceum）后，雌性个体将发生部分性逆转，呈现出更接近雄性的表型。本研究在白玉草中观测到宿主针对病原体感染的强烈性别特异性响应，这一发现首次将病原体介导的性别偏向性基因表达（sex-biased gene expression）变化与宿主雌雄异型状态的改变建立了直接关联。受感染的雌性个体中，感染引发的基因表达变化导致其转录组（transcriptome）发生去雌性化与雄性化转变；而受感染的雄性个体中，健康植株中原本呈现雄性偏向性表达的重叠群（contigs）出现广泛的表达下调，进而引发表达模式的反向改变，最终使染菌雄性的转录组呈现雌性化与去雄性化特征。此类转录变化还包括激活异性特异性基因，这与雌性个体的部分性逆转以及染菌雌雄宿主间雌雄异型程度的降低密切相关。本研究结果揭示了雌雄异株植物中宿主针对病原体感染的强烈性别特异性响应，并为性别偏向性基因表达变化与雌雄异型之间的关联提供了直接证据。