Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in Arabidopsis

Zhang, Junxiang; Yuan, Hui; Yang, Yong; Fish, Tara; Lyi, Sangbom M.; Thannhauser, Theodore W.; Zhang, Lugang; Li, Li

doi:10.1093/jxb/erw106

Cited by 87 publications

(63 citation statements)

References 54 publications

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“…Furthermore, a relationship between photosynthesis and ribosomal machinery has been previously reported in Arabidopsis [61]. Thus, the decreased abundance of chloroplast 16S rRNA promoted by the lack of ribosomal protein S5 leads to the suppression of a great number of core components of PSI and PSII [61]. In summary, according to this study's findings, the pod maturation process in common bean leads to specific transcriptome changes that accelerate the breakdown of photosynthetic and ribosomal machinery.…”

Section: Pod Maturation Is Regulated At Translational Level and Involsupporting

confidence: 69%

“…All these results corroborate that the significant reduction of photosynthesis, as part of the senescence developmental program, is a key step for pod maturation in common bean. Furthermore, a relationship between photosynthesis and ribosomal machinery has been previously reported in Arabidopsis [61]. Thus, the decreased abundance of chloroplast 16S rRNA promoted by the lack of ribosomal protein S5 leads to the suppression of a great number of core components of PSI and PSII [61].…”

Section: Pod Maturation Is Regulated At Translational Level and Involmentioning

confidence: 92%

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Transcriptional Dynamics and Candidate Genes Involved in Pod Maturation of Common Bean (Phaseolus vulgaris L.)

Gómez-Martín

Capel

González

et al. 2020

Plants

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Pod maturation of common bean relies upon complex gene expression changes, which in turn are crucial for seed formation and dispersal. Hence, dissecting the transcriptional regulation of pod maturation would be of great significance for breeding programs. In this study, a comprehensive characterization of expression changes has been performed in two common bean cultivars (ancient and modern) by analyzing the transcriptomes of five developmental pod stages, from fruit setting to maturation. RNA-seq analysis allowed for the identification of key genes shared by both accessions, which in turn were homologous to known Arabidopsis maturation genes and furthermore showed a similar expression pattern along the maturation process. Gene-expression changes suggested a role in promoting an accelerated breakdown of photosynthetic and ribosomal machinery associated with chlorophyll degradation and early activation of alpha-linolenic acid metabolism. A further study of transcription factors and their DNA binding sites revealed three candidate genes whose functions may play a dominant role in regulating pod maturation. Altogether, this research identifies the first maturation gene set reported in common bean so far and contributes to a better understanding of the dynamic mechanisms of pod maturation, providing potentially useful information for genomic-assisted breeding of common bean yield and pod quality attributes.Plants 2020, 9, 545 2 of 20 metabolites such as carotenoids and anthocyanins [7][8][9][10][11]. Likewise, jasmonate promotes senescence and plays an important role in chlorophyll degradation [12,13], which is synthesized from alpha-linolenic acid [14,15], suggesting that the accumulation of this acid during maturation is responsible for stimulating chlorophyll loss [16]. In addition, the increased accumulation of antioxidant and monoterpene is also an important feature of the fruit maturation process [17][18][19].Like most species of the Fabaceae (also named as Leguminosae) family, common bean (Phaseolus vulgaris L.) produces dry fruits in the form of a pod, which is a photosynthetically active organ that encloses the developing seeds and protects them from pests and pathogens. Indeed, photosynthetically active pod tissue contributes to fuel seed growth with assimilates and nutrients [20]. As in most angiosperms, significant genetic, biochemical, and physiological changes take place during fruit maturation, which confers the functional and morphological properties of this plant organ. Unlike members of the Brassicaceae family that produce pods (siliques) derived from two fused carpels, legume pods are developed from a single carpel that emerges from the gynoecium after ovule fertilization. Subsequently, pods attain their maximum size through a growth phase caused by an active cell division and later cell expansion [21]. During the maturation phase, carbohydrate metabolism and amino acid biosynthesis are increased in pods, leading to the accumulation of storage compounds, mainly starch, total soluble amino acids, an...

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Section: Pod Maturation Is Regulated At Translational Level and Involsupporting

confidence: 69%

Section: Pod Maturation Is Regulated At Translational Level and Involmentioning

confidence: 92%

Transcriptional Dynamics and Candidate Genes Involved in Pod Maturation of Common Bean (Phaseolus vulgaris L.)

Gómez-Martín

Capel

González

et al. 2020

Plants

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“…Defects in plastid translational capacity are often associated with impaired acclimation to cold, as reported previously in mutants defective for PRPL33, PRPS5, or RDB1 (Rogalski et al, 2008;Wang et al, 2016;Zhang et al, 2016). Therefore, we quantified cold acclimation in both rh50-1 mutants and wild-type plants.…”

Section: Rh50 and Gun1: Coexpression And Colocalizationmentioning

confidence: 85%

The DEAD-box RNA Helicase RH50 Is a 23S-4.5S rRNA Maturation Factor that Functionally Overlaps with the Plastid Signaling Factor GUN1

Paieri

Tadini

Manavski³

et al. 2017

Plant Physiol.

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DEAD-box RNA helicases (DBRHs) modulate RNA secondary structure, allowing RNA molecules to adopt the conformations required for interaction with their target proteins. RH50 is a chloroplast-located DBRH that colocalizes and is coexpressed with GUN1, a central factor in chloroplast-to-nucleus signaling. When combined with mutations that impair plastid gene expression (prors1-1, prpl11-1, prps1-1, prps21-1, prps17-1, and prpl24-1), rh50 and gun1 mutations evoke similar patterns of epistatic effects. These observations, together with the synergistic growth phenotype of the double mutant rh50-1 gun1-102, suggest that RH50 and GUN1 are functionally related and that this function is associated with plastid gene expression, in particular ribosome functioning. However, rh50-1 itself is not a gun mutant, although-like gun1-102-the rh50-1 mutation suppresses the downregulation of nuclear genes for photosynthesis induced by the prors1-1 mutation. The RH50 protein comigrates with ribosomal particles, and is required for efficient translation of plastid proteins. RH50 binds to transcripts of the 23S-4.5S intergenic region and, in its absence, levels of the corresponding rRNA processing intermediate are strongly increased, implying that RH50 is required for the maturation of the 23S and 4.5S rRNAs. This inference is supported by the finding that loss of RH50 renders chloroplast protein synthesis sensitive to erythromycin and exposure to cold. Based on these results, we conclude that RH50 is a plastid rRNA maturation factor.

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“…Many mutants affected in plastid ribosomal activity are more sensitive to cold treatments than wildtype plants (Rogalski et al, 2008;Fleischmann et al, 2011;Wang et al, 2016;Zhang et al, 2016;Paieri et al, 2018). Experiments with plants grown for 2 weeks at 22°C and then transferred for 5 weeks to 4°C showed that both crass mutants were more susceptible to this treatment than wild-type plants or overexpressors of CRASS1:YFP in the crass-1 background (oeCRASS: YFP#1 crass-1; Fig.…”

Section: Crass Is Necessary For Tolerance To Cold Stressmentioning

confidence: 99%

“…For instance, loss of the 23S-4.5S maturation factor RH50 leads to erythromycin sensitivity and reduced chloroplast protein synthesis upon cold exposure (Paieri et al, 2018). Moreover, mutants for plastid ribosomal subunits (like PRPS5, PRPS6, and PRPL33) or the elongation factor SVR3 display reduced tolerance to cold stress (Rogalski et al, 2008;Liu et al, 2010;Zhang et al, 2016;Wang et al, 2017). Furthermore, the cytosolic pre-18S rRNA processing factor RH7 is involved in cold tolerance (Huang et al, 2016), providing a general link between temperature on the one hand and translation or ribosome biogenesis on the other.…”

Section: Crass Becomes Critical For Translation Only Under Certain Comentioning

confidence: 99%

CHLOROPLAST RIBOSOME ASSOCIATED Supports Translation under Stress and Interacts with the Ribosomal 30S Subunit

et al. 2018

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Chloroplast ribosomes, which originated from cyanobacteria, comprise a large subunit (50S) and a small subunit (30S) containing ribosomal RNAs (rRNAs) and various ribosomal proteins. Genes for many chloroplast ribosomal proteins, as well as proteins with auxiliary roles in ribosome biogenesis or functioning, reside in the nucleus. Here, we identified Arabidopsis () CHLOROPLAST RIBOSOME ASSOCIATED (CRASS), a member of the latter class of proteins, based on the tight coexpression of its mRNA with transcripts for nucleus-encoded chloroplast ribosomal proteins. CRASS was acquired during the evolution of embryophytes and is localized to the chloroplast stroma. Loss of CRASS results in minor defects in development, photosynthetic efficiency, and chloroplast translation activity under controlled growth conditions, but these phenotypes are greatly exacerbated under stress conditions induced by the translational inhibitors lincomycin and chloramphenicol or by cold treatment. The CRASS protein comigrates with chloroplast ribosomal particles and coimmunoprecipitates with the 16S rRNA and several chloroplast ribosomal proteins, particularly the plastid ribosomal proteins of the 30S subunit (PRPS1 and PRPS5). The association of CRASS with PRPS1 and PRPS5 is independent of rRNA and is not detectable in yeast two-hybrid experiments, implying that either CRASS interacts indirectly with PRPS1 and PRPS5 via another component of the small ribosomal subunit or that it recognizes structural features of the multiprotein/rRNA particle. CRASS plays a role in the biogenesis and/or stability of the chloroplast ribosome that becomes critical under certain stressful conditions when ribosomal activity is compromised.

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Plastid ribosomal protein S5 is involved in photosynthesis, plant development, and cold stress tolerance in Arabidopsis

Abstract: HighlightPlastid RPS5 affects proteins involved in photosynthesis and translation machinery and mediates cold stress tolerance in Arabidopsis.

Cited by 87 publications

References 54 publications

Transcriptional Dynamics and Candidate Genes Involved in Pod Maturation of Common Bean (Phaseolus vulgaris L.)

Transcriptional Dynamics and Candidate Genes Involved in Pod Maturation of Common Bean (Phaseolus vulgaris L.)

The DEAD-box RNA Helicase RH50 Is a 23S-4.5S rRNA Maturation Factor that Functionally Overlaps with the Plastid Signaling Factor GUN1

CHLOROPLAST RIBOSOME ASSOCIATED Supports Translation under Stress and Interacts with the Ribosomal 30S Subunit

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