A Fungal Parasite Regulates a Putative Female-Suppressor Gene Homologous to Maize Tasselseed2 and Causes Induced Hermaphroditism in Male Buffalograss

Parasitically induced hermaphroditism is a fascinating illustration of floral sex organ modification; however, knowledge of how parasites induce hermaphroditism in plants is limited. Here, we show the fungal parasite pistil smut induces development of female sex organs (pistils) in flowers of male buffalograss, potentially by downregulating a putative female-suppressor gene, BdTs2, homologous to maize Tasselseed2 (ZmTs2). Full-length BdTs2, isolated using rapid amplification of cDNA ends, exhibits 89% nucleotide sequence similarity with ZmTs2 and 85% amino acid sequence homology with ZmTs2 protein. Scanning electron micrographs demonstrate that unisexual buffalograss flowers develop through a process of selective abortion of opposite sex organs within hermaphroditic floral primordia. Quantitative real-time polymerase chain reaction showed that high expression levels of BdTs2 within male inflorescences correlate with the selective abortion of gynoecium, leading to the development of unisexual male flowers. RNA in situ hybridization confirmed the expression of BdTs2 precisely within vestigial gynoeciums of male flowers and not in other floral organs of the inflorescence. Furthermore, we show that BdTs2 expression is downregulated by pistil smut infection, which corresponds to the presence of pistils in flowers otherwise destined to become unisexual male. This study provides a potential molecular basis for pistil smut-induced hermaphroditism in male buffalograss.