Nuclear-Ecoded Plastid RNA Polymerases Are Components of Anterograde Control in Hormonal Regulation of Chloroplast Gene Expression

Phytohormones are known to play an important role in the regulation of chloroplast biogenesis. However, information on the pathways of hormonal signal perception by chloroplasts is limited. In order to analyze the possible mechanisms of hormone action, the response to abscisic acid (ABA) and cytokinin (CKs) treatment of Arabidopsis thaliana (L.) Heynh. scabra3-2 (sca3-2) and rpotmp mutants with defective genes for nuclear-encoded plastid RNA polymerases was studied. The reaction of the rpotmp mutant usually did not differ from the response of wild-type plants: trans-zeatin activated the accumulation of transcripts of genes encoding the transcription apparatus and genes encoded by the plastid genome, while ABA weakly suppressed their expression or had no significant effect. However, the steady-state levels of gene templates of the plastid-encoded RNA polymerase (PEP-A) enzyme complex in the rpotmp mutant were higher than in wild-type plants, probably due to a compensatory mechanism that allows the mutant to enhance PEP-dependent transcription in the absence of the RPOTmp enzyme. Dysfunction of the plastid RNA polymerase RPOTp enzyme in the sca3-2 mutant induced an altered hormonal response of the genes for plastid transcriptional complex and plastid-encoded genes in comparison with the response of wild-type plants. The absence of a significant up-regulating effect of CKs on the expression of genes encoding the transcription apparatus correlated with the retention of the steady-state levels of transcripts for chloroplast genes and plastid proteins. In addition, the sca3-2 mutant had an increased steady-state expression of genes for CK metabolism: IPT3, IPT5, and CKX5. However, the response to the inhibitory effect of ABA in this mutant, on the contrary, was more pronounced, which is possibly caused by the changes in the steady-state levels of the transcripts of a number of genes encoding of ABA signaling and metabolism proteins. Thus, changes in the expression of NEP (nuclear-encoded RNA polymerases) genes under the action of hormones can be transformed into activation or inhibition in the expression of chloroplast genes of nuclear or plastome coding, providing the regulation of chloroplast functions through the mechanisms of anterograde signaling.