Activation of the plastid-encoded RNA polymerase is tightly controlled
and involves a network of phosphorylation and, as yet unidentified,
thiol-mediated events. Here, we characterize PLASTID REDOX INSENSITIVE2,
a redox-regulated protein required for full PEP-driven transcription.
PRIN2 dimers can be reduced into the active monomeric form by
thioredoxins through reduction of a disulfide bond. Exposure to light
increases the ratio between the monomeric and dimeric forms of PRIN2.
Complementation of prin2-2 with different PRIN2 protein variants
demonstrates that the monomer is required for light-activated
PEP-dependent transcription and that expression of the nuclear-encoded
photosynthesis genes is linked to the activity of PEP. Activation of PEP
during chloroplast development likely is the source of a retrograde
signal that promotes nuclear LHCB expression. Thus, regulation of
PRIN2 is the thiol-mediated mechanism required for full PEP activity,
with PRIN2 monomerization via reduction by TRXs providing a mechanistic
link between photosynthetic electron transport and activation of
photosynthetic gene expression.