, Volume 242, Issue 3, pp 305-312

Ribosome-deficient plastids affect transcription of light-induced nuclear genes: genetic evidence for a plastid-derived signal

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Abstract

Transcription of ten nuclear genes was analysed in the albostrians mutant of barley (Hordeum vulgare L.). The lack of plastid ribosomes in white seedlings of this mutant results in a complex alteration of nuclear gene expression at the transcriptional level. We found a strong reduction in the accumulation of mRNAs transcribed from nuclear genes encoding chloroplast enzymes involved in the Calvin cycle, the chlorophyll a/b binding protein, and the cytosolic enzyme nitrate reductase. In contrast, the levels of transcripts of the genes encoding the cytosolic glycolytic enzymes glyceraldehyde phosphate dehydrogenase and phosphoglycerate kinase were slightly enhanced. Accumulation of chalcone synthase mRNA even reaches much higher levels in white than in green leaves. Ribosome-deficient plastids were combined by crossing with a nuclear genotype heterozygous for the albostrians allele. Analysis of transcript levels in F 1 plants having the same nuclear genotype and differing only with respect to their content of normally developed chloroplasts versus undifferentiated mutant plastids, provided strong genetic evidence for the plastid being the origin of a signal (chain) involved in regulation of nuclear gene expression. Results of run-on transcription in isolated nuclei demonstrated that the plastid signal acts at the level of transcription; it does not interfere with gene regulation in general. Mechanisms triggering nuclear gene expression in response to light operate in white mutant leaves: the very low levels of mRNAs derived from nuclear genes encoding chloroplast proteins and the strongly enhanced level of chalcone synthase mRNA were both light inducible. Also the negative regulation of leaf thionin gene expression by light is observed in white albostrians seedlings. Furthermore, in spite of its low absolute level, the circadian rhythm in the abundance of the cab mRNA is still detectable in plastid ribosome-deficient seedlings. Thus, functional plastid protein biosynthesis and photosynthesis are not preconditions for the circadian oscillations in the level of mRNA transcribed from this gene (family).

Communicated by H. Böhme