The Arabidopsis pentatricopeptide repeat protein LPE1 and its maize ortholog are required for translation of the chloroplast <i>psbJ</i> RNA

Williams‐Carrier, Rosalind; Brewster, Carolyn E.; Belcher, Susan; Rojas, Margarita; Chotewutmontri, Prakitchai; Ljungdahl, Sonja; Barkan, Alice

doi:10.1111/tpj.14308

Cited by 35 publications

(37 citation statements)

References 36 publications

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“…Moreover, regulated D1 synthesis for de novo biogenesis of PSII during cell growth requires additional regulatory levels of psbA mRNA translation. Consistently, a number of proteins have been co-purified with the psbA mRNA in Chlamydomonas, spinach, Arabidopsis and maize, and or have been identified by genetic analyses [27][28][29][30][31][32][33][34][35]. Among the proteins co-precipitating with the psbA mRNA was CP33B (AT2G35410) [9].…”

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confidence: 85%

The Chloroplast Ribonucleoprotein CP33B Quantitatively Binds the psbA mRNA

Teubner

Lenzen

Espenberger

et al. 2020

Plants

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Chloroplast RNAs are stabilized and processed by a multitude of nuclear-encoded RNA-binding proteins, often in response to external stimuli like light and temperature. A particularly interesting RNA-based regulation occurs with the psbA mRNA, which shows light-dependent translation. Recently, the chloroplast ribonucleoprotein CP33B was identified as a ligand of the psbA mRNA. We here characterized the interaction of CP33B with chloroplast RNAs in greater detail using a combination of RIP-chip, quantitative dot-blot, and RNA-Bind-n-Seq experiments. We demonstrate that CP33B prefers psbA over all other chloroplast RNAs and associates with the vast majority of the psbA transcript pool. The RNA sequence target motif, determined in vitro, does not fully explain CP33B's preference for psbA, suggesting that there are other determinants of specificity in vivo.Plants 2020, 9, 367 2 of 15 of target mRNAs for various cpRNPs [7][8][9]. rRNAs and intron-less tRNAs are not or only weakly bound [6,7,10]. Since the cpRNPs do not co-fractionate with polysomal RNAs [6,8,11], they are mainly attributed a function prior to translation within posttranscriptional processes.Prediction algorithms for subcellular localization and shotgun proteome analysis identified all ten cpRNPs of Arabidopsis in the chloroplast [summarized in 2]. Fluorescence microscopy of GFP fusion proteins confirmed the chloroplast localization [8,[12][13][14]. Within the chloroplasts, the stroma is the main destination of cpRNPs, with small amounts also being associated with thylakoids. This was proven by immunological analyses for the five cpRNPs from tobacco [6].The expression of cpRNPs is regulated by various external and internal signals. Light especially leads to an accumulation of cpRNPs [summarized in 2]. In general, cpRNPs are involved in a variety of posttranscriptional processes, including 3'-end processing of RNAs [15], RNA editing [16,17], RNA splicing [7], and RNA stabilization [7,8,10]. Some of these processes are modulated by cpRNPs in response to environmental cues and several cpRNPs have been implicated in different acclimation and stress responses [2,7,13,18]. Such a multi-level and far-reaching regulation by multiple external and internal stimuli is unknown for most other chloroplast RBPs, including PPR proteins. cpRNPs are thus considered as prime candidates for post-transcriptional regulators of plastid gene expression [19].A particularly interesting case of chloroplast gene regulation is the light-induced translation of psbA, which codes for the D1 protein, the core subunit of photosytem II [20][21][22][23]. D1 is constantly damaged, most pronouncedly by excess light and other unfavourable conditions, i.e., cold. As a consequence, D1 is constantly synthesized for the repair of PSII [24][25][26]. Moreover, regulated D1 synthesis for de novo biogenesis of PSII during cell growth requires additional regulatory levels of psbA mRNA translation. Consistently, a number of proteins have been co-purified with the psbA mRNA in Chlamydomonas, spinach, A...

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confidence: 85%

The Chloroplast Ribonucleoprotein CP33B Quantitatively Binds the psbA mRNA

Teubner

Lenzen

Espenberger

et al. 2020

Plants

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“…HCF173 is a protein of ~60 kDa that is required specifically for psbA translation in Arabidopsis, and that has been shown to bind psbA mRNA in Arabidopsis and maize (Schult et al , ; McDermott et al , ; Williams‐Carrier et al , ). An HCF173 ortholog exists in Chlamydomonas (Schult et al , ), but has not been characterized.…”

Section: Introductionmentioning

confidence: 99%

Exploring the proteome associated with the mRNA encoding the D1 reaction center protein of Photosystem II in plant chloroplasts

et al. 2020

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Synthesis of the D1 reaction center protein of Photosystem II is dynamically regulated in response to environmental and developmental cues. In chloroplasts, much of this regulation occurs at the post-transcriptional level, but the proteins responsible are largely unknown. To discover proteins that impact psbA expression, we identified proteins that associate with maize psbA mRNA by: (i) formaldehyde cross-linking of leaf tissue followed by antisense oligonucleotide affinity capture of psbA mRNA; and (ii) co-immunoprecipitation with HCF173, a psbA translational activator that is known to bind psbA mRNA. The S1 domain protein SRRP1 and two RNA Recognition Motif (RRM) domain proteins, CP33C and CP33B, were enriched with both approaches. Orthologous proteins were also among the enriched protein set in a previous study in Arabidopsis that employed a designer RNA-binding protein as a psbA RNA affinity tag. We show here that CP33B is bound to psbA mRNA in vivo, as was shown previously for CP33C and SRRP1. Immunoblot, pulse labeling, and ribosome profiling analyses of mutants lacking CP33B and/or CP33C detected some decreases in D1 protein levels under some conditions, but no change in psbA RNA abundance or translation. However, analogous experiments showed that SRRP1 represses psbA ribosome association in the dark, represses ycf1 ribosome association, and promotes accumulation of ndhC mRNA. As SRRP1 is known to harbor RNA chaperone activity, we postulate that SRRP1 mediates these effects by modulating RNA structures. The uncharacterized proteins that emerged from our analyses provide a resource for the discovery of proteins that impact the expression of psbA and other chloroplast genes.psbA mRNA-associated proteome 371 d Cutoff: >3-fold enrichment in the designer SCD11 pull-down data (McDermott et al., 2019). Proteins not found in the chloroplast were excluded. *Not detected in control (pre-immune serum for HCF173 co-immunoprecipitates, leaf proteome for PIRP, anti-FLAG pull-down of Col-0 for dPPR).

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“…We show the canonical RC47* complex (6,7) as the repair intermediate that accepts nascent D1, but the mechanism would be similar with the alternative repair intermediate detected recently in Synechocystis (77). We propose that the D1-less HCF244 complex communicates with HCF173 in the stroma, which is known to bind the psbA 5' UTR and to activate translation initiation (48,79,81). Two transposon insertion alleles were recovered from the Photosynthetic Mutant Library (5).…”

Section: Data Availability Statementmentioning

confidence: 64%

“…(B) Analysis of Zm-hcf107 and At-hcf107 mutants. The data show the known loss of psbH expression in these mutants (60,81). Two replicates were performed for Zm-hcf107.…”

Section: Data Availability Statementmentioning

confidence: 98%

Light-inducedpsbAtranslation in plants is triggered by photosystem II damage via an assembly-linked autoregulatory circuit

Chotewutmontri

Barkan

2020

Preprint

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The D1 reaction center protein of Photosystem II (PSII) is subject to light-induced damage.Degradation of damaged D1 and its replacement by nascent D1 are at the heart of a PSII repair cycle, without which photosynthesis is inhibited. In mature plant chloroplasts, light stimulates the recruitment of ribosomes specifically to psbA mRNA to provide nascent D1 for PSII repair, and also triggers a global increase in translation elongation rate. The light-induced signals that initiate these responses are unclear. We present action spectrum and genetic data indicating that the light-induced recruitment of ribosomes to psbA mRNA is triggered by D1 photodamage, whereas the global stimulation of translation elongation is triggered by photosynthetic electron transport. Furthermore, mutants lacking HCF136, which mediates an early step in D1 assembly, exhibit constitutively high psbA ribosome occupancy in the dark, and differ in this way from mutants lacking PSII for other reasons. These results, together with the recent elucidation of a thylakoid membrane complex that functions in PSII assembly, PSII repair and psbA translation, suggest an autoregulatory mechanism in which the light-induced degradation of D1 relieves repressive interactions between D1 and translational activators in the complex. We suggest that the presence of D1 in this complex coordinates D1 synthesis with the need for nascent D1 during both PSII biogenesis and PSII repair in plant chloroplasts. Significance StatementPhotosystem II (PSII) harbors the water-splitting activity underlying oxygenic photosynthesis.The PSII reaction center protein D1 is subject to photodamage and must be replaced with nascent D1 to maintain photosynthetic activity. How new D1 synthesis is coordinated with D1 damage has been a long-standing question. Our results clarify the nature of the light-induced signal that activates D1 synthesis for PSII repair in plants, and suggest an autoregulatory mechanism in which degradation of damaged D1 relieves a repressive interaction between D1 and translational activators in a complex that functions in PSII assembly and repair. This proposed mechanism comprises a responsive switch that couples D1 synthesis to need for D1 during PSII biogenesis and repair.

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The Arabidopsis pentatricopeptide repeat protein LPE1 and its maize ortholog are required for translation of the chloroplast psbJ RNA

Cited by 35 publications

References 36 publications

The Chloroplast Ribonucleoprotein CP33B Quantitatively Binds the psbA mRNA

The Chloroplast Ribonucleoprotein CP33B Quantitatively Binds the psbA mRNA

Exploring the proteome associated with the mRNA encoding the D1 reaction center protein of Photosystem II in plant chloroplasts

Light-inducedpsbAtranslation in plants is triggered by photosystem II damage via an assembly-linked autoregulatory circuit

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