Identification of Target Genes and Transcription Factors Implicated in Translation-Dependent Retrograde Signaling in Arabidopsis

Leister, Dario; Romani, Isidora; Mittermayr, Lukas; Paieri, Francesca; Fenino, Elena; Kleine, Tatjana

doi:10.1093/mp/ssu066

Cited by 25 publications

(13 citation statements)

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“…It has been noted before that light and chloroplast signaling pathways converge at some point (Ruckle et al, 2007;Leister et al, 2014;Martín et al, 2016). In agreement with this, we have identified PIF-related ciselements in the promoters of pp7l-deregulated genes (Fig.…”

Section: The Role Of Pp7l In Chloroplast Development Is Not Mediated supporting

confidence: 91%

Extrachloroplastic PP7L Functions in Chloroplast Development and Abiotic Stress Tolerance

Marino

Klingl

et al. 2019

Plant Physiol.

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Chloroplast biogenesis is indispensable for proper plant development and environmental acclimation. In a screen for mutants affected in photosynthesis, we identified the protein phosphatase7-like (pp7l) mutant, which displayed delayed chloroplast development in cotyledons and young leaves. PP7L, PP7, and PP7-long constitute a subfamily of phosphoprotein phosphatases. PP7 is thought to transduce a blue-light signal perceived by crys and phy a that induces expression of SIGMA FACTOR5 (SIG5). We observed that, like PP7, PP7L was predominantly localized to the nucleus in Arabidopsis (Arabidopsis thaliana), and the pp7l phenotype was similar to that of the sig6 mutant. However, SIG6 expression was unaltered in pp7l mutants. Instead, loss of PP7L compromised translation and ribosomal RNA (rRNA) maturation in chloroplasts, pointing to a distinct mechanism influencing chloroplast development. Promoters of genes deregulated in pp7l-1 were enriched in PHYTOCHROME-INTERACTING FACTOR (PIF)-binding motifs and the transcriptome of pp7l-1 resembled those of pif and CONSTITUTIVE PHOTOMORPHOGENESIS1 (COP1) signalosome complex (csn) mutants. However, pif and csn mutants, as well as cop1, cryptochromes (cry)1 cry2, and phytochromes (phy)A phyB mutants, do not share the pp7l photosynthesis phenotype. PhyB protein levels were elevated in pp7l mutants, but phyB overexpression plants did not resemble pp7l. These results indicate that PP7L operates through a different pathway and that the control of greening and photosystem biogenesis can be separated. The lack of PP7L increased susceptibility to salt and high-light stress, whereas PP7L overexpression conferred resistance to highlight stress. Strikingly, PP7L was specifically recruited to Brassicales for the regulation of chloroplast development. This study adds another player involved in chloroplast biogenesis.

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Section: The Role Of Pp7l In Chloroplast Development Is Not Mediated supporting

confidence: 91%

Extrachloroplastic PP7L Functions in Chloroplast Development and Abiotic Stress Tolerance

Marino

Klingl

et al. 2019

Plant Physiol.

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“…Interestingly, it was recently shown that phototropins are required to maintain robust circadian oscillations in photosystem II efficiency under constant blue light (Litthauer et al ). Furthermore, we previously suggested that early OGE‐dependent signaling (triggered by an impairment of PRORS1), and temperature‐acclimation and light‐signaling pathways might target the same transcription factors (Leister et al ). The mutants that are defective in mTERF proteins – namely mterf9 , mda1 , rug2‐1 and s oldat10 plants – also flower earlier than WT (reviewed in Kleine and Leister ) provides another link between mTERF/OGE‐ and light‐signaling pathways.…”

Section: Discussionmentioning

confidence: 99%

Definition of a core module for the nuclear retrograde response to altered organellar gene expression identifies GLK overexpressors as gun mutants

Leister¹,

Kleine²

2016

Physiologia Plantarum

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Retrograde signaling can be triggered by changes in organellar gene expression (OGE) induced by inhibitors such as lincomycin (LIN) or mutations that perturb OGE. Thus, an insufficiency of the organelle-targeted prolyl-tRNA synthetase PRORS1 in Arabidopsis thaliana activates retrograde signaling and reduces the expression of nuclear genes for photosynthetic proteins.Recently, we showed that mTERF6, a member of the so-called mitochondrial transcription termination factor (mTERF) family, is involved in the formation of chloroplast (cp) isoleucine-tRNA. To obtain further insights into its functions, co-expression analysis of MTERF6, PRORS1 and two other genes for organellar aminoacyl-tRNA synthetases was conducted. The results suggest a prominent role of mTERF6 in aminoacylation activity, light signaling and seed storage. Analysis of changes in whole-genome transcriptomes in the mterf6-1 mutant showed that levels of nuclear transcripts for cp OGE proteins were particularly affected. Comparison of the mterf6-1 transcriptome with that of prors1-2 showed that reduced aminoacylation of proline (prors1-2) and isoleucine (mterf6-1) tRNAs alters retrograde signaling in similar ways. Database analyses indicate that comparable gene expression changes are provoked by treatment with LIN, norflurazon or high light. A core OGE response module was defined by identifying genes that were differentially expressed under at least four of six conditions relevant to OGE signaling. Based on this module, overexpressors of the Golden2-like transcription factors GLK1 and GLK2 were identified as genomes uncoupled mutants.

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“…Affymetrix ATH1-121501 data were from the following sources: Gene Expression Omnibus https://www.ncbi.nlm.nih.gov/geo/, AA 3 hours (in figures labelled as experiment 1), GSE57140 (Ivanova et al, 2014); AA and H 2 O 2 , 3 hour treatments (in figures labelled as experiment 2), GSE41136 (Ng et al 2013); MV 3 hours, GSE41963 (Sharma et al, 2013); mterf6-1, GSE75824 (Leister and Kleine 2016); prors1-2, GSE54573 (Leister et al, 2014); H 2 O 2 30 min, GSE43551 (Gutiérrez et al, 2014); high light 1 hour (in figures labelled as experiment 1), GSE46107 (Van Aken et al, 2013); high light 30 min in cell culture, GSE22671 (González-Pérez et al, 2011); high light 3 hours (in figures labelled as experiment 2), GSE7743 (Kleine et al, 2007); oligomycin 1 and 4 hours, GSE38965 (Geisler et al, 2012); norflurazon – 5 day-old seedlings grown on plates with norflurazon, GSE12887 (Koussevitzky et al, 2007); msh1 recA3 double mutant, GSE19603 (Shedge et al, 2010). AtGenExpress oxidative time series, MV 12 and 24 hours, http://www.arabidopsis.org/servlets/TairObject?type=expressionset&id=1007966941.…”

Section: Methodsmentioning

confidence: 99%

RCD1 Coordinates Chloroplastic and Mitochondrial Electron Transfer through Interaction with ANAC Transcription Factors in Arabidopsis

Shapiguzov

Vainonen

Hunter

et al. 2018

Preprint

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43Signaling from chloroplasts and mitochondria, both dependent on reactive oxygen 44 species (ROS), merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 45 (RCD1). ROS produced in the chloroplasts affect the abundance, thiol redox state and 46 oligomerization of RCD1. RCD1 directly interacts in vivo with ANAC013 and ANAC017 47 transcription factors, which are the mediators of the ROS-related mitochondrial complex 48 III retrograde signa and suppresses activity of ANAC013 and ANAC017. Inactivation of 49 RCD1 leads to increased expression of ANAC013 and ANAC017-regulated genes 50 belonging to the mitochondrial dysfunction stimulon (MDS), including genes for 51 mitochondrial alternative oxidases (AOXs). Accumulating AOXs and other MDS gene 52 products alter electron transfer pathways in the chloroplasts, leading to diminished 53 production of chloroplastic ROS and increased protection of photosynthetic apparatus 54 from ROS damage. RCD1-dependent regulation affects chloroplastic and mitochondrial 55 retrograde signaling including chloroplast signaling by 3'-phosphoadenosine 5'-56 phosphate (PAP). Sensitivity of RCD1 to organellar ROS provides feedback control of 57 nuclear gene expression. 58 157 Nishiyama et al., 2011).To reveal the significance of RCD1 in responses to PSI-produced 158 chloroplastic ROS, rosettes of Arabidopsis were pre-treated overnight in darkness with 159 MV and exposed to light. After the dark period, the plants displayed unchanged PSII 160 photochemical yield (Fv/Fm). Subsequent exposure to three hours of light resulted in 161 decrease of Fv/Fm in wild type (Col-0) (Fig. 1A), but not in the rcd1 mutant. Moreover, 162 tolerance of rcd1 was evident under various concentrations of MV (Fig. 1B). The 163 superoxide anion is an unstable compound that is enzymatically reduced to the more 164 long-lived H2O2. Chloroplastic production of H2O2 in the presence of MV in the light was 165 assessed by staining plants with 3,3′-diaminobenzidine (DAB). After pre-treatment with 166 MV, higher H2O2 accumulation was evident in both Col-0 and rcd1 (Fig. S1A). Subsequent 167 incubation of these plants under light led to a time-dependent increase in the H2O2 168accumulation in Col-0, but not in rcd1. 169 In several MV-tolerant mutants the resistance is based on restricted access of MV to 170 chloroplasts (Hawkes 2014). However, in rcd1 pretreatment with MV led to initial increase 171 in H2O2 production similar to that in the wild type ( Fig. S1A), suggesting that resistance 172 of rcd1 was not due to restricted delivery of MV to PSI. In order to test this directly, 173 oxidation of PSI was assessed by in vivo spectroscopy using DUAL-PAM. Leaves were 174 adapted to far-red light, which is more efficiently used by PSI than PSII. Under these 175 conditions PSI is producing electrons at a faster rate than it is supplied by electrons 176 coming from PSII, and hence the PSI reaction center P700 becomes oxidized. Then a 177 flash of orange light was provided that is efficiently absorbed by PSII. Electrons generated...

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Identification of Target Genes and Transcription Factors Implicated in Translation-Dependent Retrograde Signaling in Arabidopsis

Cited by 25 publications

References 80 publications

Extrachloroplastic PP7L Functions in Chloroplast Development and Abiotic Stress Tolerance

Extrachloroplastic PP7L Functions in Chloroplast Development and Abiotic Stress Tolerance

Definition of a core module for the nuclear retrograde response to altered organellar gene expression identifies GLK overexpressors as gun mutants

RCD1 Coordinates Chloroplastic and Mitochondrial Electron Transfer through Interaction with ANAC Transcription Factors in Arabidopsis

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