Abstract
Chloroplasts communicate information by signalling to nuclei during acclimation to fluctuating light. Several potential operating signals originating from chloroplasts have been proposed, but none have been shown to move to nuclei to modulate gene expression. One proposed signal is hydrogen peroxide (H2O2) produced by chloroplasts in a light-dependent manner. Using HyPer2, a genetically encoded fluorescent H2O2 sensor, we show that in photosynthetic Nicotiana benthamiana epidermal cells, exposure to high light increases H2O2 production in chloroplast stroma, cytosol and nuclei. Critically, over-expression of stromal ascorbate peroxidase (H2O2 scavenger) or treatment with DCMU (photosynthesis inhibitor) attenuates nuclear H2O2 accumulation and high light-responsive gene expression. Cytosolic ascorbate peroxidase over-expression has little effect on nuclear H2O2 accumulation and high light-responsive gene expression. This is because the H2O2 derives from a sub-population of chloroplasts closely associated with nuclei. Therefore, direct H2O2 transfer from chloroplasts to nuclei, avoiding the cytosol, enables photosynthetic control over gene expression.
Highlights
Chloroplasts communicate information by signalling to nuclei during acclimation to fluctuating light
We have found that the expression of HyPer[2] is strongly susceptible to silencing in stably transformed Arabidopsis thaliana (A. thaliana) but is well expressed in Nicotiana benthamiana abaxial epidermal cells following Agro-infiltration[25]
Since DCMU and stromal ascorbate peroxidase (sAPX) over-expression both attenuated the nuclear H2O2 increase in high light (HL) (Figs. 3c, d), we investigated their effect on the expression of NbAPXa (Fig. 4c)
Summary
Chloroplasts communicate information by signalling to nuclei during acclimation to fluctuating light. Exposure to high light (HL) causes rapid changes in nuclear gene expression in a photosynthesis-dependent manner[5,6,7] and is associated with chloroplast-to-nucleus (retrograde) signalling[1, 7, 8]. The involvement of H2O2 in signalling raises questions about its specificity and site of action in the face of multiple origins in chloroplasts, mitochondria and peroxisomes as well extracellularly via plasma membrane localised NADPH oxidases[19] Another problem for any retrograde signalling pathway is that plant cells harbour multiple chloroplasts, which may not respond to external stimuli in a uniform manner[5] and can move away from incident HL to increase self-shading[5, 21]. This raises the question of how a nucleus can integrate signalling from chloroplasts in different physiological states
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