Singlet oxygen initiates a plastid signal controlling photosynthetic gene expression

Abstract

Summary Retrograde signals from the plastid regulate photosynthesis‐associated nuclear genes and are essential to successful chloroplast biogenesis. One model is that a positive haem‐related signal promotes photosynthetic gene expression in a pathway that is abolished by the herbicide norflurazon. Far‐red light (FR) pretreatment and transfer to white light also results in plastid damage and loss of photosynthetic gene expression. Here, we investigated whether norflurazon and FR pretreatment affect the same retrograde signal.We used transcriptome analysis and real‐time reverse transcription−polymerase chain reaction (RT‐PCR) to analyse the effects of these treatments on nuclear gene expression in various Arabidopsis (Arabidopsis thaliana) retrograde signalling mutants.Results showed that the two treatments inhibited largely different nuclear gene sets, suggesting that they affected different retrograde signals. Moreover, FR pretreatment resulted in singlet oxygen (1O2) production and a rapid inhibition of photosynthetic gene expression. This inhibition was partially blocked in the executer1executer2 mutant, which is impaired in 1O2 signalling.Our data support a new model in which a 1O2 retrograde signal, generated by chlorophyll precursors, inhibits expression of key photosynthetic and chlorophyll synthesis genes to prevent photo‐oxidative damage during de‐etiolation. Such a signal would provide a counterbalance to the positive haem‐related signal to fine tune regulation of chloroplast biogenesis.

Light and Plastid Signals Regulate Different Sets of Genes in the Albino Mutant Pap7-1

“…The question of whether a weaker nuclear gene expression indicates the action of a negative signal or the missing action of a positive signal has been debated in the past (Pfannschmidt, 2010;Terry and Smith, 2013;Hills et al, 2015). A recent study (Page et al, 2017a(Page et al, , 2017b and our data presented here indicate that the action of both positive and negative signals needs to be considered in current models.…”

“…Proteins proposed to act as plastid signals include envelope-tethered eukaryotic transcription factors TFIIB-like and PTM, both being released from the outer plastid membrane by targeted proteolysis (Lagrange et al, 2003;Sun et al, 2011) and a plastid localized Whirly1 protein that is released from plastids upon stress (Isemer et al, 2012). A very recent study, however, puts this particular function of PTM in retrograde signaling into question (Page et al, 2017a(Page et al, , 2017b. Most of these retrograde signaling molecules are discussed as stress signals operating from fully developed chloroplasts.…”

Early physiological and biochemical responses of soyabean to neighbouring weeds under resource‐independent competition

“…Although the volatile compound ethylene has been shown to induce shade avoidance characteristics (Pierik et al ., ,b), our literature search failed to find a particular study that shows volatile compounds such as ethylene emanating from neighbouring weeds can increase 1 O 2 production in crop plants. In contrast, our ‘in planta’ demonstration of rapid 1 O 2 production in soyabean leaves in response to neighbouring weeds corresponds well with a recent study, where continuous FR pre‐treatment of Arabidopsis seedlings before transfer to continuous white light resulted in rapid 1 O 2 production in rosette leaves (Page et al ., ).…”

Seedlings Lacking the PTM Protein Do Not Show a genomes uncoupled (gun) Mutant Phenotype

“…Retrograde signaling from the developing chloroplast (plastid) to the nucleus, which is termed biogenic signaling (Pogson et al, 2008), can be revealed using either the bleaching herbicide Norflurazon (NF), an inhibitor of carotenoid synthesis, or the plastid translation inhibitor, lincomycin (Lin) to damage the plastid. Under these conditions there is a strong downregulation of hundreds of nuclear genes (Koussevitzky et al, 2007;Aluru et al, 2009;Page et al, 2017). Despite decades of research, the biogenic retrograde signaling pathway is still very poorly understood.…”