The coordinated action of <scp>PPR</scp>4 and <scp>EMB</scp>2654 on each intron half mediates <i>trans</i>‐splicing of <i>rps12</i> transcripts in plant chloroplasts

Lee, Kwanuk; Park, Su Jung; Francs‐Small, Catherine Colas des; Whitby, Michael; Small, Ian; Kang, Hunseung

doi:10.1111/tpj.14509

Cited by 50 publications

(45 citation statements)

References 70 publications

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“…In contrast, defects in Rps8 translation due to loss of PGR3 in not4a likely explains why ribosome depletion is specific to the 30S subunit, since protein complex stoichiometries are highly regulated, with the inability to assemble complete complexes often leading to degradation of orphan subunits (Juszkiewicz and Hegde, 2018; Taggart et al, 2020). In addition, upregulation of PPR proteins SOT1, EMB2654, PPR4 and PPR2 (which all promote chloroplast rRNA maturation), and GUN1 (implicated in the production of chloroplast ribosomal subunits RPS1 and RPL11) present further evidence of compensatory responses to reduced ribosome abundance and protein synthesis within not4a chloroplasts (Figure S6B)(Aryamanesh et al, 2017; Lee et al, 2019; Lu et al, 2011; Tadini et al, 2016; Wu et al, 2016).…”

Section: Resultsmentioning

confidence: 96%

TheArabidopsisNOT4A E3 ligase coordinates PGR3 expression to regulate chloroplast protein translation

Bailey

Ivanauskaite

Grimmer

et al. 2020

Preprint

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31Chloroplast function requires the coordinated action of nuclear-and chloroplast-derived 32 proteins, including several hundred nuclear-encoded pentatricopeptide repeat (PPR) 33 proteins that regulate plastid mRNA metabolism. Despite their large number and importance, 34 regulatory mechanisms controlling PPR expression are poorly understood. Here we show 35 that the Arabidopsis NOT4A ubiquitin-ligase positively regulates PROTON GRADIENT 3 36 (PGR3), a PPR protein required for translating 30S ribosome subunits and several thylakoid-37 localised photosynthetic components within chloroplasts. Loss of NOT4A function leads to a 38 strong depletion of plastid ribosomes, which reduces mRNA translation and negatively 39 impacts photosynthetic capacity, causing pale-yellow and slow-growth phenotypes. 40Quantitative transcriptome and proteome analyses reveal that these defects are due to a 41 lack of PGR3 expression in not4a, and we show that normal plastid function is restored 42 through transgenic PGR3 expression. Our work identifies NOT4A as crucial for ensuring 43 robust photosynthetic function during development and stress-response, through modulating 44 PGR3 levels to coordinate chloroplast protein synthesis.The synthesis of energy from the sun, photosynthesis, supports organic life on earth. Light 68 harvesting in green plants takes place within the specialized chloroplast organelle, believed 69 to have arisen from engulfment of a photosynthetic prokaryote by an ancestral eukaryotic 70 cell (Archibald, 2015). Coevolution and merging of these organisms has resulted in nuclear 71 and chloroplast genomes separated within cellular compartments. In land plants, the 72 chloroplast genome comprises of ~130 genes, yet chloroplasts contain around 3000 different 73 proteins (Zoschke and Bock, 2018). Consequently, chloroplast function requires expression 74 not only of chloroplast encoded proteins, but a multitude of nuclear encoded genes, which 75 are imported into chloroplasts post-translationally. One such group of nuclear derived factors 76 is the pentatricopeptide repeat domain (PPR) containing proteins. The PPR protein family 77 has significantly expanded in plants (~450 in Arabidopsis, vs <10 in humans and yeast; 78 (Schmitz-Linneweber and Small, 2008)), and members are characterized by a 35-amino acid 79 repeat sequence that facilitates RNA binding and enables them to provide critical gene 80 expression control within chloroplasts and mitochondria (Barkan and Small, 2014). Through 81 binding to organellar RNAs, PPR proteins stabilize gene transcripts, facilitate post-82 transcriptional processing and promote translation of the encoded proteins (Barkan and 83 Small, 2014; Manna, 2015). Whilst their function in the regulation of gene expression control 84 within organelles has been described, including many of the RNA species to which they 85 bind, little is known about how their expression is regulated prior to import. 86Precise, selective removal of proteins is essential to cellular development and response. In 87...

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Section: Resultsmentioning

confidence: 96%

TheArabidopsisNOT4A E3 ligase coordinates PGR3 expression to regulate chloroplast protein translation

Bailey

Ivanauskaite

Grimmer

et al. 2020

Preprint

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“…Nearly all PPR proteins identified to be involved in splicing in chloroplasts so far are P-class PPR proteins that appear to be primarily required for the splicing of a single, specific intron (Schmitz-Linneweber et al 2006;de Longevialle et al 2008de Longevialle et al , 2010Khrouchtchova et al 2012;Goto et al 2016;Aryamanesh et al 2017;Wang et al 2017b;Huang et al 2018;Ito et al 2018;Lee et al 2019). However, the roles of these P-class PPR proteins involved in splicing in chloroplast RNAs remain largely unclear.…”

Section: Discussionmentioning

confidence: 99%

Pentatricopeptide repeat protein PHOTOSYSTEM I BIOGENESIS FACTOR2 is required for splicing of ycf3

Wang

Yang

Zhang

et al. 2020

JIPB

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To gain a better understanding of the molecular mechanisms of photosystem I (PSI) biogenesis, we characterized the Arabidopsis thaliana photosystem I biogenesis factor 2 (pbf2) mutant, which lacks PSI complex. PBF2 encodes a P-class pentatricopeptide repeat (PPR) protein. In the pbf2 mutants, we observed a striking decrease in the transcript level of only one gene, the chloroplast gene ycf3, which is essential for PSI assembly. Further analysis of ycf3 transcripts showed that PBF2 is specifically required for the splicing of ycf3 intron 1. Computational prediction of binding sequences and electrophoretic mobility shift assays reveal that PBF2 specifically binds to a sequence in ycf3 intron 1. Moreover, we found that PBF2 interacted with two general factors for group II intron splicing CHLOROPLAST RNA SPLICING2-ASSOCIATED FACTOR1 (CAF1) and CAF2, and facilitated the association of these two factors with ycf3 intron 1. Our results suggest that PBF2 is specifically required for the splicing of ycf3 intron 1 through cooperating with CAF1 and CAF2. Our results also suggest that additional proteins are required to contribute to the specificity of CAFdependent group II intron splicing.

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“…Previous analysis of PPR proteins has demonstrated that chloroplast-localized maize PPR4 [ 62 ] and THA8 [ 63 ], and Arabidopsis OTP51 [ 64 ] and OTP70 [ 65 ], are essential for the splicing of chloroplast specific introns. Interestingly, recent studies of PPR4 [ 25 ], EMB2654 [ 66 ], PBF2 [ 67 ], and SOT5 [ 68 ] in Arabidopsis showed that these proteins play a role in the splicing of chloroplast introns through their role in the recognition of the specific RNA sequences. Arabidopsis HCF152 [ 69 ], MRL1 [ 70 ], PGR3 [ 71 ], BFA2 [ 72 ], and maize PPR5 [ 73 ] and PPR10 [ 74 ] were shown to be essential for the stabilization of chloroplast transcripts.…”

Section: Functions Of Ncmrbps In Plant Growth and Developmentmentioning

confidence: 99%

“…Importantly, it is now known that the nCMRBPs function as either specific RNA-binding proteins or non-specific RNA-binding proteins (RNA chaperones), which facilitates the correct folding of the target RNA structure during plant growth and under environmental stress [ 15 , 23 ]. Chloroplast- or mitochondria-localized CRM, PPR, DBRH, and SDP proteins have been assessed in terms of their roles as RNA chaperones [ 21 , 24 , 25 , 26 , 27 ]. In this review, we will focus on the recent advances in research on the function and cellular mechanisms of CRM, PPR, DBRH, and SDP proteins in organellar RNA metabolism during plant growth, development, and abiotic stress responses.…”

Section: Introductionmentioning

confidence: 99%

Roles of Organellar RNA-Binding Proteins in Plant Growth, Development, and Abiotic Stress Responses

Lee

Kang

2020

IJMS

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Organellar gene expression (OGE) in chloroplasts and mitochondria is primarily modulated at post-transcriptional levels, including RNA processing, intron splicing, RNA stability, editing, and translational control. Nucleus-encoded Chloroplast or Mitochondrial RNA-Binding Proteins (nCMRBPs) are key regulatory factors that are crucial for the fine-tuned regulation of post-transcriptional RNA metabolism in organelles. Although the functional roles of nCMRBPs have been studied in plants, their cellular and physiological functions remain largely unknown. Nevertheless, existing studies that have characterized the functions of nCMRBP families, such as chloroplast ribosome maturation and splicing domain (CRM) proteins, pentatricopeptide repeat (PPR) proteins, DEAD-Box RNA helicase (DBRH) proteins, and S1-domain containing proteins (SDPs), have begun to shed light on the role of nCMRBPs in plant growth, development, and stress responses. Here, we review the latest research developments regarding the functional roles of organellar RBPs in RNA metabolism during growth, development, and abiotic stress responses in plants.

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The coordinated action of PPR4 and EMB2654 on each intron half mediates trans‐splicing of rps12 transcripts in plant chloroplasts

Cited by 50 publications

References 70 publications

TheArabidopsisNOT4A E3 ligase coordinates PGR3 expression to regulate chloroplast protein translation

TheArabidopsisNOT4A E3 ligase coordinates PGR3 expression to regulate chloroplast protein translation

Pentatricopeptide repeat protein PHOTOSYSTEM I BIOGENESIS FACTOR2 is required for splicing of ycf3

Roles of Organellar RNA-Binding Proteins in Plant Growth, Development, and Abiotic Stress Responses

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