Orchid seed germination through auto-activation of mycorrhizal symbiosis signaling regulated by gibberellin

Orchids parasitically depend on external nutrients from mycorrhizal fungi for seed germination. Previous findings suggest that orchids utilize a genetic system of mutualistic arbuscular mycorrhizal (AM) symbiosis to establish parasitic symbiosis. In AM symbiosis, recent studies have revealed that the plant hormone gibberellin (GA) negatively affects fungal colonization and development. Although previous studies imply that GA is important for orchid mycorrhizal symbiosis, the molecular mechanism of seed germination in which mycorrhizal symbiosis co-occurs remains unclear because, in AM plants, GA regulates seed germination and symbiosis positively and negatively, respectively. To elucidate this conflict, we investigated the effect of GA on Bletilla striata seed germination and mycorrhizal symbiosis using asymbiotic and symbiotic germination methods. Additionally, we compared the transcriptome profiles between asymbiotically and symbiotically germinated seeds. Exogenous GA negatively affected seed germination and fungal colonization, and endogenous bioactive GA was actively converted to the inactive form during seed germination. Transcriptome analysis showed that B. striata shared many of the induced genes between asymbiotically and symbiotically germinated seeds, including GA metabolism- and signaling-related genes and AM-specific marker homologs. Our study suggests that orchids have evolved in a manner that they do not use bioactive GA as a positive regulator of seed germination and instead, auto-activate the mycorrhizal symbiosis pathway through GA inactivation to accept the fungal partner immediately during seed germination.