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

Coordinated gene transcription in plastid and nucleus is essential for the photosynthetic apparatus assembly during chloroplast biogenesis. Despite identification of several transcription factors regulating the transcription of nuclear-encoded photosynthetic genes,no transcription factor regulating plastid gene transcription has been discovered. Here we report that BAI1 ("albino" in Chinese), a nucleus-plastid dual-targeted C2H2-type zinc finger transcription factor in Arabidopsis, positively regulates and orchestrates the transcription of nuclear and plastid genes. The knockout of BAI1 leads to the blockage of chloroplast formation, albino seedling, and lethality. In plastid, BAI1 is a newly identified functional component of the pTAC (transcriptionally active chromosome complex), which physically interacts with another pTAC component, pTAC12/PAP5/HMR to enable the effective assembly of PEP (plastid-encoded RNA polymerase) complex. The transcript levels of investigated PEP-dependent genes were reduced in the bai1 mutant, while the accumulation of NEP (nuclear-encoded RNA polymerase)-dependent transcripts was increased, indicating that BAI1 plays a vital role in maintaining PEP activity. BAI1 directly binds to the promoter regions of RbcSs, a nuclear gene, and RbcL, a plastid gene, to activate their expression for efficient RubisCO assembly. AtBAI1 homologs TaBAI1, GmBAI1a and GmBAI1b from both monocot and dicot can fully complement the defects of Arabidopsis bai1 mutant. In contrast, PpBAI1, from Physcomitrium patens, only partially complements the bai1 mutant. The phylogenetic analysis of BAI1 and HMR elucidated that both components originated from late-diverging streptophyte algae, following the conservative evolutionary path during plant terrestrialization. In summary, this work unveils a BAI1-mediated transcription regulatory mechanism synchronizing transcription of nuclear and plastid genes, which is required for hybrid photosynthetic complex assembly and could be an intrinsic feature facilitating plant terrestrialization.