A model for tetrapyrrole synthesis as the primary mechanism for plastid-to-nucleus signaling during chloroplast biogenesis

Matthew J Terry,Alison G Smith

doi:10.3389/fpls.2013.00014

Abstract

Chloroplast biogenesis involves the co-ordinated expression of the chloroplast and nuclear genomes, requiring information to be sent from the developing chloroplasts to the nucleus. This is achieved through retrograde signaling pathways and can be demonstrated experimentally using the photobleaching herbicide, norflurazon, which in seedlings results in chloroplast damage and the reduced expression of many photosynthesis-related, nuclear genes. Genetic analysis of this pathway points to a major role for tetrapyrrole synthesis in retrograde signaling, as well as a strong interaction with light signaling pathways. Currently, the best model to explain the genetic data is that a specific heme pool generated by flux through ferrochelatase-1 functions as a positive signal to promote the expression of genes required for chloroplast development. We propose that this heme-related signal is the primary positive signal during chloroplast biogenesis, and that treatments and mutations affecting chloroplast transcription, RNA editing, translation, or protein import all impact on the synthesis and/or processing of this signal. A positive signal is consistent with the need to provide information on chloroplast status at all times. We further propose that GUN1 normally serves to restrict the production of the heme signal. In addition to a positive signal re-enforcing chloroplast development under normal conditions, aberrant chloroplast development may produce a negative signal due to accumulation of unbound chlorophyll biosynthesis intermediates, such as Mg-porphyrins. Under these conditions a rapid shut-down of tetrapyrrole synthesis is required. We propose that accumulation of these intermediates results in a rapid light-dependent inhibition of nuclear gene expression that is most likely mediated via singlet oxygen generated by photo-excitation of Mg-porphyrins. Thus, the tetrapyrrole pathway may provide both positive and inhibitory signals to control expression of nuclear genes.

Highlights

Chloroplasts are essential organelles in plant cells, responsible for harvesting the majority of the Earth’s energy obtained from the sun
There are two major groups of chloroplast-targeted proteins encoded by the nucleus: important components of the chloroplast genetic machinery, including one of the RNA polymerases and a large number of pentatricopeptide repeat (PPR) proteins involved in RNA processing; and the enzymes and other nucleusencoded chloroplast proteins that comprise the components of the photosynthetic machinery
In this article we have described a model for the role of chloroplastlocalized tetrapyrrole synthesis in regulating nuclear gene expression

Summary

INTRODUCTION

Chloroplasts are essential organelles in plant cells, responsible for harvesting the majority of the Earth’s energy obtained from the sun. There are two major groups of chloroplast-targeted proteins encoded by the nucleus: important components of the chloroplast genetic machinery, including one of the RNA polymerases and a large number of pentatricopeptide repeat (PPR) proteins involved in RNA processing; and the enzymes and other nucleusencoded chloroplast proteins that comprise the components of the photosynthetic machinery. This latter group, referred to as“photosynthetic genes” (Figure 1A) are expressed in response to light via anterograde signaling pathways, which include those mediated by the phytochrome and cryptochrome families of photoreceptors (Waters and Langdale, 2009). In any regulatory system information needs to travel in both directions, and chloroplasts are able to send information back to the nucleus to control expression of photosynthetic www.frontiersin.org

Terry and Smith

Findings

CONCLUSION