Four-dimensional omics data reveals ribosome heterogeneity, regulation of translation efficacy, and nonsense-mediated decay in the differentiation of spermatocyte to round spermatid

A protein expression is regulated by transcription, translation, and sequential processing. However, well correlated RNA and protein abundance just only proportionate 40%, and even poorer when cell was stressed, differentiated, or tumorigenic transformed. Here, we discovered spermatocyte (SP) differentiated to round spermatid (RS) had equal regulation extent which may related to ribosomal behavior alteration. The change of ribosome occupancy was related to SP and RS specific function in spermatogenesis. Interactome of functional ribosome in SP and RS revealed the activated ribosome in SP but stalled and nonsense-mediated decay (NMD) associated ribosome in RS. Functional ribosomes of RS occupied 5’untranslated regions (5’UTR) of SP specific transcripts and correlated its’ RNA and protein downregulation. These findings suggested a branched NMD pathway was activated in RS to eliminate SP specific transcripts and keep them from being translated. Our discovery suggested the heterogeneity of ribosomal interactome may play an important role in spermatogenesis.