Retrograde Signals Navigate the Path to Chloroplast Development

Hernández‐Verdeja, Tamara; Strand, Åsa

doi:10.1104/pp.17.01299

Cited by 102 publications

(83 citation statements)

References 85 publications

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“…To our knowledge, no evidence has yet been reported for any interaction of CMF proteins with kinases or phosphatases involved in phosphorylation/dephosphorylation of thylakoid components, such as LHCII-specific phosphatase PPH1, PSII-specific phosphatase PBCP, protein kinases STN7 and STN8 (Fristedt et al, 2009; Pribil et al, 2010; Samol et al, 2012), or thylakoid curvator proteins (Armbruster et al, 2013). Also nuclear genes coding for proteins with roles in photosynthesis, thylakoid formation, and pigment synthesis are likely affected in their expression in chloroplast ribosome deficient mutants, due to plastid-to-nucleus retrograde signaling (Kleine and Leister, 2016; Borner, 2017; de Souza et al, 2017; Hernandez-Verdeja and Strand, 2018). Chloroplast ribosome deficiency as the reason of our phenotypic observations Hvcmf3 plants is also supported by the fact that severity of ribosome deficiency is correlated with increasingly drastic effects on chlorophyll content, PSII efficiency, and grana morphology.…”

Section: Discussionmentioning

confidence: 99%

Mutation of theALBOSTRIANSOhnologous GeneHvCMF3Impairs Chloroplast Development and Thylakoid Architecture in Barley due to Reduced Plastid Translation

Hensel²,

Melzer³

et al. 2019

Preprint

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Gene pairs resulting from whole genome duplication (WGD), so-called ohnologous genes, are retained only if at least one gene of the pair undergoes neo- or subfunctionalization. Sequence-based phylogenetic analyses of the ohnologous genes ALBOSTRIANS (HvAST/HvCMF7) and ALBOSTRIANS-LIKE (HvASL/HvCMF3) of barley (Hordeum vulgare) revealed that they belong to a newly identified subfamily of genes encoding CCT domain proteins with putative N-terminal chloroplast transit peptides. Recently, we showed that HvCMF7 is needed for chloroplast ribosome biogenesis. Here we demonstrate that mutations in HvCMF3 lead to seedlings delayed in development. They exhibit a xantha phenotype and successively develop pale green leaves. Compared to the wild type, plastids of the mutant seedlings show decreased PSII efficiency and lower amounts of ribosomal RNAs; they contain less thylakoids and grana with a higher number of more loosely stacked thylakoid membranes. Site-directed mutagenesis of HvCMF3 identified a previously unknown functional region, which is highly conserved within this subfamily of CCT domain containing proteins. HvCMF3:GFP fusion constructs localized to plastids. Hvcmf3Hvcmf7 double mutants indicated epistatic activity of HvCMF7 over HvCMF3. The chloroplast ribosome deficiency is discussed as the primary defect of the Hvcmf3 mutants. Our data suggests that HvCMF3 and HvCMF7 have similar but not identical functions.One-sentence summaryPhylogenetic and mutant analyses of the barley protein HvCMF3 (ALBOSTRIANS-LIKE) identified, in higher plants, a subfamily of CCT domain proteins with essential function in chloroplast development.

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Section: Discussionmentioning

confidence: 99%

Mutation of theALBOSTRIANSOhnologous GeneHvCMF3Impairs Chloroplast Development and Thylakoid Architecture in Barley due to Reduced Plastid Translation

Hensel²,

Melzer³

et al. 2019

Preprint

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“…Also, using this experimental setup, enough material for proteomic analyses could be obtained. We included the gun5 mutant as a control, since GUN5 only derepresses PhANG expression under NF treatment but not under Lin treatment (Mochizuki et al, 2001;Hernández-Verdeja and Strand, 2018).…”

Section: Gun1 Regulates Plastid Proteostasis Upon Interference With Rmentioning

confidence: 99%

Extensive Posttranscriptional Regulation of Nuclear Gene Expression by Plastid Retrograde Signals

Meyer

Bock

2019

Plant Physiol.

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Retrograde signals emanate from the DNA-containing cell organelles (plastids and mitochondria) and control the expression of a large number of nuclear genes in response to environmental and developmental cues. Previous studies on retrograde signaling have mainly analyzed the regulation of nuclear gene expression at the transcript level. To determine the contribution of translational and posttranslational regulation to plastid retrograde signaling, we combined label-free proteomics with transcriptomic analysis of Arabidopsis (Arabidopsis thaliana) seedlings and studied their response to interference with the plastid gene expression pathway of retrograde signaling. By comparing the proteomes of the genomes uncoupled1 (gun1) and gun5 mutants with the wild type, we show that GUN1 is critical in the maintenance of plastid protein homeostasis (proteostasis) when plastid translation is blocked. Combining transcriptomic and proteomic analyses of the wild type and gun1, we identified 181 highly translationally or posttranslationally regulated (HiToP) genes. We demonstrate that HiToP photosynthesis-associated nuclear genes (PhANGs) are largely regulated by translational repression, while HiToP ribosomal protein genes are regulated posttranslationally, likely at the level of protein stability without the involvement of GUN1. Our findings suggest distinct posttranscriptional control mechanisms of nuclear gene expression in response to plastid-derived retrograde signals. They also reveal a role for GUN1 in the translational regulation of several PhANGs and highlight extensive posttranslational regulation that does not necessitate GUN1. This study advances our understanding of the molecular mechanisms underlying intracellular communication and provides new insight into cellular responses to impaired plastid protein biosynthesis.

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“…Chloroplasts play an essential role in plant development by housing the photosynthesis machinery as well as in production of additional vital components of plant metabolism such as hormones, vitamins, carotenoids, amino acids and fatty acids. The genetic control of chloroplast development involves the action of chloroplast and nuclear genes in a coordinated manner that requires transmission of signals between the nucleus and the chloroplast (Hernández‐Verdeja and Strand, ). To date, most studies on physiological and genetic control of chloroplast development have been conducted in leaf tissues (Pogson et al ., ) and the factors that regulate chloroplast development in the fruit have been little studied.…”

Section: Introductionmentioning

confidence: 99%

“…GOLDEN LIKE 2 (GLK2) is a nuclear-encoded transcription factor that belongs to the GARP family and acts as a positive regulator of chloroplast development in leaf and fruit tissues (Powell et al, 2012;Chen et al, 2016;Safi et al, 2017). GLK2 promotes chloroplast development by activating the expression of genes coding for proteins associated with photosynthesis processes such as chlorophyll biosynthesis, light harvesting, and electron transport (Waters et al, 2009;Nguyen et al, 2014;Hern andez-Verdeja and Strand, 2018).…”

Section: Introductionmentioning

confidence: 99%

The zinc‐finger transcription factor CcLOL1 controls chloroplast development and immature pepper fruit color in Capsicum chinense and its function is conserved in tomato

et al. 2019

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Summary Chloroplast development and chlorophyll content in the immature fruit has a major impact on the morphology and quality in pepper (Capsicum spp.) fruit. Two major quantitative trait loci (QTLs), pc1 and pc10 that affect chlorophyll content in the pepper fruit by modulation of chloroplast compartment size were previously identified in chromosomes 1 and 10, respectively. The pepper homolog of GOLDEN2‐LIKE transcription factor (CaGLK2) has been found as underlying pc10, similar to its effect on tomato chloroplast development. In the present study, we identified the pepper homolog of the zinc‐finger transcription factor LOL1 (LSD ONE LIKE1; CcLOL1) as the gene underlying pc1. LOL1 has been identified in Arabidopsis as a positive regulator of programmed cell death and we report here on its role in controlling fruit development in the Solanaceae in a fruit‐specific manner. The light‐green C. chinense parent used for QTL mapping was found to carry a null mutation in CcLOL1. Verification of the function of the gene was done by generating CRISPR/Cas9 knockout mutants of the orthologous tomato gene resulting in light‐green tomato fruits, indicating functional conservation of the orthologous genes in controlling chlorophyll content in the Solanaceae. Transcriptome profiling of light and dark‐green bulks differing for pc1, showed that the QTL affects multiple photosynthesis and oxidation‐reduction associated genes in the immature green fruit. Allelic diversity of three known genes CcLOL1, CaGLK2, and CcAPRR2 that influence pepper immature fruit color, was found to be associated with variation in chlorophyll content primarily in C. chinense.

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Retrograde Signals Navigate the Path to Chloroplast Development

Cited by 102 publications

References 85 publications

Mutation of theALBOSTRIANSOhnologous GeneHvCMF3Impairs Chloroplast Development and Thylakoid Architecture in Barley due to Reduced Plastid Translation

Mutation of theALBOSTRIANSOhnologous GeneHvCMF3Impairs Chloroplast Development and Thylakoid Architecture in Barley due to Reduced Plastid Translation

Extensive Posttranscriptional Regulation of Nuclear Gene Expression by Plastid Retrograde Signals

The zinc‐finger transcription factor CcLOL1 controls chloroplast development and immature pepper fruit color in Capsicum chinense and its function is conserved in tomato

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