Inter-generational nuclear crosstalk links the control of gene expression to programmed genome rearrangements during the Paramecium sexual cycle

Multinucleate cells exist in many eukaryotes, but how multiple nuclei coordinate their functions is still poorly understood. In the cytoplasm of the ciliate Paramecium tetraurelia, two micronuclei (MIC) serving sexual reproduction coexist with a somatic macronucleus (MAC) dedicated to gene expression. During sexual processes, the MAC is progressively destroyed while still ensuring transcription and new MACs develop from copies of the zygotic MIC. Several gene clusters are induced successively, and switched off before vegetative growth resumes. Concomitantly, programmed genome rearrangements (PGR) remove transposons and their relics from the new MAC. Development of the new MAC is under control of the old MAC since the latter expresses genes involved in PGR, including the PGM gene encoding the essential PiggyMac endonuclease that cleaves the ends of eliminated sequences. Using RNA sequencing data, we show that impairing PGR up-deregulates 628 genes potentially involved in genome rearrangements. A subset of these, including 180 genes co-expressed with PGM, are no longer induced when new MACs are missing. We conclude that a bi-directional crosstalk between the two coexisting generations of MACs links gene expression to the progression of MAC development and propose that a signal from the new MACs activates the transcription of PGM co-regulated genes.