Nostoc talks back: Temporal patterns of differential gene expression during establishment of the Anthoceros-Nostoc symbiosis

Abstract

Endosymbiotic association between hornworts and dinitrogen-fixing cyanobacteria form when the plant is limited for combined nitrogen (N). We generated RNA-Seq data to examine the temporal gene expression patterns during culture of N-starved Anthoceros punctatus in the absence and presence of the symbiotically competent cyanobacterium Nostoc punctiforme. Symbiotic nitrogenase activity commenced within 5 days of coculture reaching a maximal by 14 days. In symbiont-free gametophytes, chlorophyll content, chlorophyll fluorescence characteristics and transcription of genes encoding light harvesting and reaction center proteins, as well as the small subunit of ribulose-bisphosphate-carboxylase/oxygenase, were downregulated. The downregulation was complemented in a temporal pattern corresponding to the N. punctiforme provision of N2-derived ammonium. The impairment and complementation of photosynthesis was the most distinctive response of A. punctatus to N-starvation. Increases in transcription of ammonium and nitrate transporters and their N. punctiforme-dependent complementation was also observed. The temporal patterns of differential gene expression indicated N. punctiforme transmits signals to A. punctatus both prior to, and after its provision of fixed N. This is the only known temporal transcriptomic study during establishment of a symbiotic nitrogen-fixing association in this monophyletic evolutionary lineage of land plants. HighlightsTemporal RNA-Seq analysis revealed how symbiotic cyanobacteria impact plant partners global gene expression and elucidated the nature of bidirectional communications between the partners