The discovery of plastid-to-nucleus retrograde signaling-a personal perspective

Abstract

DNA and machinery for gene expression have been discovered in chloroplasts during the 1960s. It was soon evident that the chloroplast genome is relatively small, that most genes for chloroplast-localized proteins reside in the nucleus and that chloroplast membranes, ribosomes, and protein complexes are composed of proteins encoded in both the chloroplast and the nuclear genome. This situation has made the existence of mechanisms highly probable that coordinate the gene expression in plastids and nucleus. In the 1970s, the first evidence for plastid signals controlling nuclear gene expression was provided by studies on plastid ribosome deficient mutants with reduced amounts and/or activities of nuclear-encoded chloroplast proteins including the small subunit of Rubisco, ferredoxin NADP+ reductase, and enzymes of the Calvin cycle. This review describes first models of plastid-to-nucleus signaling and their discovery. Today, many plastid signals are known. They do not only balance gene expression in chloroplasts and nucleus during developmental processes but are also generated in response to environmental changes sensed by the organelles.

Keywords: Chloroplast development; Chloroplast signal; Plastid signal; Regulation of gene expression; Retrograde signaling.

Fig. 1

RNA, protein, metabolites, or hormones might act as plastid signals and control the expression of nuclear genes at the level of transcription or translation. This model reflects the hypotheses developed on the basis of reduced amounts and activities of nuclear-encoded chloroplast proteins in barley mutants (Bradbeer and Börner ; Hagemann and Börner ; Bradbeer et al. 1979). That plastid signals affect nuclear gene expression already at the level of transcription was shown by studies on LHCP transcription and transcript levels in albinotic mutants and norflurazon-treated seedlings in the mid of the 1980s (Mayfield and Taylor ; Batschauer et al. ; Oelmüller and Mohr 1986)