scholarly journals Nucleo-plastidic PAP8/pTAC6 couples chloroplast formation with photomorphogenesis

2020 ◽  
Author(s):  
Monique Liebers ◽  
François-Xavier Gillet ◽  
Abir Israel ◽  
Kevin Pounot ◽  
Louise Chambon ◽  
...  

AbstractThe initial greening of angiosperm occurs upon light-activation of photoreceptors that trigger photomorphogenesis followed with the development of chloroplasts. In these semi-autonomous organelles, the construction of the photosynthetic apparatus depends on the coordination of nuclear and plastid gene expression. Here we show that PAP8, as an essential subunit of the plastid-encoded RNA polymerase, is under the control of a regulatory element recognized by the photomorphogenic factor HY5. PAP8 is localized and active in both plastids and the nucleus and particularly essential for the formation of late photobodies. In the albino pap8 mutant, phytochrome-mediated signalling is altered, PIFs are maintained, HY5 is not stabilized, and GLK1 expression is impaired. PAP8 translocates into plastids losing its pre-sequence, interacts with the PEP, and using an unknown route or a retrograde transport, reaches the nucleus where it has the ability to interact with pTAC12/HMR/PAP5. Since PAP8 is required for the phytochrome-B-mediated signalling cascade and the reshaping of the PEP, it may coordinate nuclear gene expression with the PEP-driven chloroplastic gene expression during chloroplast biogenesis.

During light-induced chloroplast formation in higher plants the synthesis of several nuclear encoded plastid proteins is under the control of phytochrome. Light acting through the phytochrome system is able both to increase the transcription of certain nuclear genes and to decrease the transcription of others. It has been generally assumed that regulation by phytochrome alone would be sufficient to account for the observed light-dependent changes in nuclear gene expression during chloroplast formation. However, it has recently become evident that the light-dependent control of nuclear gene expression may be far more complex than originally expected. There are at least two other factors that in addition to phytochrome may affect nuclear gene expression: (1) changes in chromatin organization from an inactive to a transcriptionally active state, and (2) a plastid-derived factor that seems to be involved in the transcriptional control of some nuclear genes encoding plastid-specific proteins. Although the light-dependent control of transcription has been studied intensively for nuclear genes, much less is known about the light-dependent control of plastid gene expression. The P700 chlorophyll a protein of photosystem I is a major membrane protein whose massive accumulation is induced by light and whose genes have been located on the plastid DNA. In barley a high concentration of mRNA for the P700 chlorophyll a protein was detected within the total RNA as well as within the polysomal fraction of etioplasts and remained almost constant during greening. Based on these results it can be inferred that the accumulation of the P700 chlorophyll a protein during light-dependent chloroplast development in barley is not coupled to its transcript concentration but is controlled at a translational — or post-translational - level. The possible function of protochlorophyllide as photoreceptor in this light-dependent control of plastid gene expression is discussed.


2020 ◽  
Author(s):  
Kamran Alamdari ◽  
Karen E. Fisher ◽  
Andrew B. Sinson ◽  
Joanne Chory ◽  
Jesse D. Woodson

SummaryChloroplasts constantly experience photo-oxidative stress while performing photosynthesis. This is particularly true under abiotic stresses that lead to the accumulation of reactive oxygen species (ROS). While ROS leads to the oxidation of DNA, proteins, and lipids, it can also act as a signal to induce acclimation through chloroplast degradation, cell death, and nuclear gene expression. Although the mechanisms behind ROS signaling from chloroplasts remain mostly unknown, several genetic systems have been devised in the model plant Arabidopsis to understand their signaling properties. One system uses the plastid ferrochelatase two (fc2) mutant that conditionally accumulates the ROS singlet oxygen (1O2) leading to chloroplast degradation and eventually cell death. Here we have mapped three mutations that suppress chloroplast degradation in the fc2 mutant and demonstrate that they affect two independent loci (PPR30 and mTERF9) encoding chloroplast proteins predicted to be involved in post-transcriptional gene expression. Mutations in either gene were shown to lead to broadly reduced chloroplast gene expression, impaired chloroplast development, and reduced chloroplast stress signaling. In these mutants, however, 1O2 levels were uncoupled to chloroplast degradation suggesting that PPR30 and mTERF9 are involved in ROS signaling pathways. In the wild type background, ppr30 and mTERF9 mutants were also observed to be less susceptible to cell death induced by excess light stress. Together these results suggest that plastid gene expression (or the expression of specific plastid genes) is a necessary prerequisite for chloroplasts to activate 1O2 signaling pathways to induce chloroplast degradation and/or cell death.Significance summaryReactive oxygen species accumulate in the chloroplast (photosynthetic plastids) and signal for stress acclimation by inducing chloroplast degradation, cell death, and changes in nuclear gene expression. We have identified two chloroplast-localized proteins involved in gene regulation that are required to transmit these signals, suggesting that proper plastid gene expression and chloroplast development is necessary to activate chloroplast controlled cellular degradation and nuclear gene expression pathways.


2003 ◽  
Vol 5 (1) ◽  
pp. 95-101 ◽  
Author(s):  
Thomas Pfannschmidt ◽  
Katia Schütze ◽  
Vidal Fey ◽  
Irena Sherameti ◽  
Ralf Oelmüller

PLoS Genetics ◽  
2020 ◽  
Vol 16 (7) ◽  
pp. e1008944 ◽  
Author(s):  
Thomas Baier ◽  
Nick Jacobebbinghaus ◽  
Alexander Einhaus ◽  
Kyle J. Lauersen ◽  
Olaf Kruse

2020 ◽  
Vol 11 ◽  
Author(s):  
Ehsan Kayal ◽  
Catharina Alves-de-Souza ◽  
Sarah Farhat ◽  
Lourdes Velo-Suarez ◽  
Joanne Monjol ◽  
...  

Dinoflagellates are major components of phytoplankton that play critical roles in many microbial food webs, many of them being hosts of countless intracellular parasites. The phototrophic dinoflagellate Scrippsiella acuminata (Dinophyceae) can be infected by the microeukaryotic parasitoids Amoebophrya spp. (Syndiniales), some of which primarily target and digest the host nucleus. Early digestion of the nucleus at the beginning of the infection is expected to greatly impact the host metabolism, inducing the knockout of the organellar machineries that highly depend upon nuclear gene expression, such as the mitochondrial OXPHOS pathway and the plastid photosynthetic carbon fixation. However, previous studies have reported that chloroplasts remain functional in swimming host cells infected by Amoebophrya. We report here a multi-approach monitoring study of S. acuminata organelles over a complete infection cycle by nucleus-targeting Amoebophrya sp. strain A120. Our results show sustained and efficient photosystem II activity as a hallmark of functional chloroplast throughout the infection period despite the complete digestion of the host nucleus. We also report the importance played by light on parasite production, i.e., the amount of host biomass converted to parasite infective propagules. Using a differential gene expression analysis, we observed an apparent increase of all 3 mitochondrial and 9 out of the 11 plastidial genes involved in the electron transport chains (ETC) of the respiration pathways during the first stages of the infection. The longer resilience of organellar genes compared to those encoded by the nucleus suggests that both mitochondria and chloroplasts remain functional throughout most of the infection. This extended organelle functionality, along with higher parasite production under light conditions, suggests that host bioenergetic organelles likely benefit the parasite Amoebophrya sp. A120 and improve its fitness during the intracellular infective stage.


2020 ◽  
Vol 375 (1801) ◽  
pp. 20190401 ◽  
Author(s):  
Mike T. Page ◽  
Tania Garcia-Becerra ◽  
Alison G. Smith ◽  
Matthew J. Terry

Chloroplast development requires communication between the progenitor plastids and the nucleus, where most of the genes encoding chloroplast proteins reside. Retrograde signals from the chloroplast to the nucleus control the expression of many of these genes, but the signalling pathway is poorly understood. Tetrapyrroles have been strongly implicated as mediators of this signal with the current hypothesis being that haem produced by the activity of ferrochelatase 1 (FC1) is required to promote nuclear gene expression. We have tested this hypothesis by overexpressing FC1 and specifically targeting it to either chloroplasts or mitochondria, two possible locations for this enzyme. Our results show that targeting of FC1 to chloroplasts results in increased expression of the nuclear-encoded chloroplast genes GUN4 , CA1 , HEMA1 , LHCB2.1, CHLH after treatment with Norflurazon (NF) and that this increase correlates to FC1 gene expression and haem production measured by feedback inhibition of protochlorophyllide synthesis. Targeting FC1 to mitochondria did not enhance the expression of nuclear-encoded chloroplast genes after NF treatment. The overexpression of FC1 also increased nuclear gene expression in the absence of NF treatment, demonstrating that this pathway is operational in the absence of a stress treatment. Our results therefore support the hypothesis that haem synthesis is a promotive chloroplast-to-nucleus retrograde signal. However, not all FC1 overexpression lines enhanced nuclear gene expression, suggesting there is still a lot we do not understand about the role of FC1 in this signalling pathway. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.


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