The dual-targeted transcription factor BAI1 orchestrates nuclear and plastid gene transcription in land plants

Coordinated gene transcription in plastids and nuclei is necessary for the photosynthetic apparatus assembly during chloroplast biogenesis. Despite the identification of several transcription factors regulating nuclear-encoded photosynthetic gene transcription, transcription factors regulating plastid gene transcription are barely reported. Here, we report that BAI1 ("albino" in Chinese), a nucleus-plastid dual-targeted C2H2-type zinc-finger transcription factor in Arabidopsis, positively regulates and tunes the transcription of both nuclear and plastid genes. Knockout of BAI1 blocks chloroplast formation, producing albino seedlings and lethality. In plastids, BAI1 is a newly identified functional component of the pTAC (transcriptionally active chromosome complex), which interacts with another pTAC component, pTAC12/PAP5/HMR, to allow the effective assembly of plastid-encoded RNA polymerase (PEP) complexes. The transcript levels of PEP-dependent genes were reduced in the bai1 mutant. In contrast, the accumulation of nuclear-encoded RNA polymerase (NEP)-dependent transcripts was increased, suggesting that BAI1 is critical in maintaining PEP activity. BAI1 directly binds to the promoter regions of nuclear genes RbcSs and a plastid gene RbcL to activate their expression for RubisCO assembly. AtBAI1 homologs TaBAI1, GmBAI1a, and GmBAI1b from monocots and dicots can fully complement the defects of the Arabidopsis bai1 mutant. In contrast, Physcomitrium patens BAI1 (PpBAI1) only partially complements the bai1 mutant. Phylogenetic analysis of BAI1 and HMR uncovered that both components arose from late-diverging streptophyte algae, following a conserved evolutionary path during terrestrialization. In summary, this work unveils a BAI1-mediated transcription regulatory mechanism synchronizing the transcription of nuclear and plastid genes, necessary for hybrid photosynthetic complex assembly. This could be an intrinsic feature facilitating plant terrestrialization.