The discovery of plastid-to-nucleus retrograde signaling\u2014a personal perspective

Thomas Börner

doi:10.1007/s00709-017-1104-1

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.

Highlights

It was firmly established already in the early 1970s that plastids of algae like Euglena, Chlamydomonas, and Acetabularia and of higher plants contain their own genomes, RNA polymerase activity to transcribe their genes, as well as ribosomes, tRNAs, and aminoacyl tRNA synthetases for protein synthesis (Gibor and Granick 1964; Kirk 1971; Tewari 1971; Gillham 1974)
Woodson et al (2013) observed that in an Arabidopsis sig2 mutant the levels of tRNAGlu, non-covalently bound heme, and photosynthesis-associated nuclear genes (PhANGs) transcripts were low—a situation similar to what we found in white leaves of albostrians
Reviewing research on regulatory interactions between nuclear and plastid genomes from the first reports on albostrians barley until the end of the 1980s, William Taylor (1989) speculated BWhat sort of molecule might the chloroplast signal be?...It appears to be a positive regulator, given that Cab is transcriptionally inactive in cells with nongreen plastids or with photooxidatively destroyed chloroplasts. It could be a small molecule produced by chloroplast metabolic activity.^. This was a wise prediction since in the following 25 years several metabolic pathways in chloroplasts could be shown to be the origin of signals controlling the activities of nuclear genes

Summary

Introduction

It was firmly established already in the early 1970s that plastids of algae like Euglena, Chlamydomonas, and Acetabularia and of higher plants contain their own genomes, RNA polymerase activity to transcribe their genes, as well as ribosomes, tRNAs, and aminoacyl tRNA synthetases for protein synthesis (Gibor and Granick 1964; Kirk 1971; Tewari 1971; Gillham 1974). The results of this preliminary study suggested a marked reduction of this enzyme in white primary leaves of albostrians barley, a reduction being much more drastic than in the case of the ferredoxin reductase Since all these observations supported the hypothesis of a controlling influence of the plastid/ chloroplast on the expression of nuclear genes coding for chloroplast proteins, I was already in the mid 1970s convinced that such a regulatory mechanism really operates in leaves. The poster reported results of studies performed in Halle on the large and small subunits of Rubisco, phosphoribulokinase, and ferredoxin: NADP+ reductase together with the hypothesis of regulatory effects of the plastid/chloroplast on the expression of nuclear-encoded plastid proteins (Börner 1977). It could be a small molecule produced by chloroplast metabolic activity.^

Concluding remarks

Findings

Compliance with ethical standards