Chloroplast Translation Elongation Factor EF-Tu/SVR11 Is Involved in var2-Mediated Leaf Variegation and Leaf Development in Arabidopsis

Liu, Siyu; Zheng, Lu; Jia, Jia; Guo, Jia; Zheng, Mengdi; Zhao, Jun; Shao, Jingxia; Liu, Xiayan; An, Lijun; Yu, Fei; Qi, Yafei

doi:10.3389/fpls.2019.00295

Cited by 27 publications

(27 citation statements)

References 60 publications

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“…Thylakoid FtsH complexes comprise four members of FtsH proteins, FtsH1 and FtsH5 (type A), and FtsH2 and FtsH8 (type B), in which VAR2/AtFtsH2 is one of the most abundant subunits. Biochemical analysis suggested that thylakoid FtsHs are required to degrade the photodamaged reaction center protein D1 during the Photosystem II repair cycle (Liu et al 2019). All normal green tissues and organs of var2, except for cotyledons, are variegated, and the green sectors arise from white sectors during early leaf expansion, and sector formation is irreversible in the mature leaves (Putarjunan et al 2013).…”

Section: Electronic Supplementary Materialsmentioning

confidence: 99%

Disruption of carotene biosynthesis leads to abnormal plastids and variegated leaves in Brassica napus

Zhao

Yan

et al. 2020

Mol Genet Genomics

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Leaf color is an important characteristic of normal chloroplast development. Variegated plants have green-and white-sectored leaves, which can be used to identify important pathways and molecular mechanisms of chloroplast development. We studied two Brassica napus variegation mutants from same one variegated ancestor, designated ZY-4 and ZY-8, which have different degrees of variegation. When grown in identical conditions, the ratio of white sectors in ZY-4 leaves is higher than in ZY-8. In both mutants, the cells in green sectors contain normal chloroplasts; while, the cells in white sectors contain abnormal plastids. Seedling chloroplasts ultrastructure of both mutants showed that the biogenesis of chloroplasts was blocked in early stages; delayed development and structual damage in ZY-4 were more serious than in ZY-8. Employing bulked segregant analysis(BSA), two bulks (BY142 and BY137) from BC 2 F 1 lines derived from ZY-4 and ZS11, and one bulk (BY56) from BC 2 F 1 lines derived from ZY-8 and ZS11, and screening by Brassica 60K SNP BeadChip Array, showed the candidate regions localized in chromosome A08 (BY142), C04 (BY137), and A08 (BY56), respectively. Transcriptome analysis of five seedling development stages of ZY-4, ZY-8, and ZS11 showed that photosynthesis, energy metabolism-related pathways and translation-related pathways were important for chloroplast biogenesis. The number of down-or up-regulated genes related to immune system process in ZY-4 was more than in ZY-8. The retrograde signaling pathway was mis-regulated in both mutants. DEG analysis indicated that both mutants showed photooxidative damages. By coupling transcriptome and BSA CHIP analyses, some candidate genes were identified. The gene expression pattern of carotene biosynthesis pathway was disrupted in both mutants. However, histochemical analysis of ROS revealed that there was no excessive accumulation of ROS in ZY-4 and ZY-8. Taken together, our data indicate that the disruption of carotene biosynthetic pathways leads to the variegation phenotypes of ZY-4 and ZY-8 and there are some functions that can compensate for the disruption of carotene biosynthesis in ZY-4 and ZY-8 to reduce ROS and prevent seedling mortality.

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Section: Electronic Supplementary Materialsmentioning

confidence: 99%

Disruption of carotene biosynthesis leads to abnormal plastids and variegated leaves in Brassica napus

Zhao

Yan

et al. 2020

Mol Genet Genomics

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“…Twelve proteins from the small and large ribosomal subunits were respectively enriched under both conditions along with six chloroplast rRNA processing and translation factors (Figure 7E and Supplementary Data Set 1 ). These include the following rRNA processing factors: RNA helicases, RH3 ( 47 , 48 ) and ISE2 ( 49 ), Ribonuclease J RNJ ( 50 ), RNA binding protein RHON1 ( 51 ) and the translation initiation and elongation factors FUG1 ( 52 ) and EF-Tu/SVR11 ( 53 ), respectively. Finally, ten TAC components co-immunoprecipitated with mTERF9 under both conditions.…”

Section: Resultsmentioning

confidence: 99%

Arabidopsis mTERF9 protein promotes chloroplast ribosomal assembly and translation by establishing ribonucleoprotein interactions in vivo

Méteignier

Ghandour

Zimmerman

et al. 2021

Nucleic Acids Research

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The mitochondrial transcription termination factor proteins are nuclear-encoded nucleic acid binders defined by degenerate tandem helical-repeats of ∼30 amino acids. They are found in metazoans and plants where they localize in organelles. In higher plants, the mTERF family comprises ∼30 members and several of these have been linked to plant development and response to abiotic stress. However, knowledge of the molecular basis underlying these physiological effects is scarce. We show that the Arabidopsis mTERF9 protein promotes the accumulation of the 16S and 23S rRNAs in chloroplasts, and interacts predominantly with the 16S rRNA in vivo and in vitro. Furthermore, mTERF9 is found in large complexes containing ribosomes and polysomes in chloroplasts. The comprehensive analysis of mTERF9 in vivo protein interactome identified many subunits of the 70S ribosome whose assembly is compromised in the null mterf9 mutant, putative ribosome biogenesis factors and CPN60 chaperonins. Protein interaction assays in yeast revealed that mTERF9 directly interact with these proteins. Our data demonstrate that mTERF9 integrates protein-protein and protein-RNA interactions to promote chloroplast ribosomal assembly and translation. Besides extending our knowledge of mTERF functional repertoire in plants, these findings provide an important insight into the chloroplast ribosome biogenesis.

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“…Twelve proteins from the small and large ribosomal subunits were respectively enriched under both conditions along with 6 chloroplast rRNA processing and translation factors (Figure 7E and Supplementary Data Set 1). These include the following rRNA processing factors: RNA helicases, RH3 (47,48) and ISE2 (49), Ribonuclease J RNJ (50), RNA binding protein RHON1 (51) and the translation initiation and elongation factors FUG1 (52) and EF-Tu/SVR11 (53), respectively. Finally, ten TAC components co-immunoprecipitated with mTERF9 under both conditions.…”

Section: Resultsmentioning

confidence: 99%

Arabidopsis mTERF9 protein promotes chloroplast ribosomal assembly and translation by establishing ribonucleoprotein interactionsin vivo

Méteignier

Ghandour

Zimmermann

et al. 2020

Preprint

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23The mitochondrial transcription termination factor proteins are nuclear-encoded nucleic 24 acid binders defined by degenerate tandem helical-repeats of 30 amino acids. They are 25 found in metazoans and plants where they localize in organelles. In higher plants, the 26 mTERF family comprises 30 members and several of these have been linked to plant 27 development and response to abiotic stress. However, knowledge of the molecular basis 28 underlying these physiological effects is scare. We show that the Arabidopsis mTERF9 29 protein, promotes the accumulation of the 16S rRNA and the formation of the 23S rRNA 30 first hidden break in chloroplasts, and co-immunoprecipitates with the 16S rRNA. 42organelles is scare. In fact, only five of the ~30 mTERF proteins found in angiosperms 63 have been connected to their gene targets and functions in organelles. In Arabidopsis, 64 mTERF5 (known as well as MDA1), mTERF6 and mTERF8 are chloroplast DNA binding 65 proteins involved in the regulation of chloroplast gene transcription (Zhang et al., 2018; 66 Ding et al., 2019; Xiong et al., 2020). mTERF5 stimulates the transcription initiation of 67 psbE and ndhA genes (Ding et al., 2019; Méteignier et al., 2020) whereas mTERF8 and 68 mTERF6 promote the transcription termination of psbJ and rpoA, respectively (Zhang et 69 al., 2018; Xiong et al., 2020). mTERF6 has additionally been reported to affect the 70 maturation of trnI.2 but the reason for this effect remained unclear (Romani et al., 2015). 71Finally, mTERF15 and mTERF4 assist in RNA splicing of the nad2-3 intron in Arabidopsis 72 mitochondria and group II introns in maize chloroplasts, respectively. Therefore, the 73 functional repertoire of mTERFs in plant organelles concerns the regulation of gene 74 transcription and intron splicing. In Arabidopsis, the mTERF9 gene (known as well as 75 TWIRT1) encodes a chloroplastic mTERF protein that has been involved in the 76 development of the shoot apical meristem (Mokry et al., 2011) and the plant acclimation 77 to high salinity (Robles et al., 2015; Nunez-Delegido et al., 2019). However, the function 78 of mTERF9 in chloroplasts was not further investigated and the molecular basis 79 underlying its physiological effects on plants is unknown. Understanding the connection 80 between mTERF genes and the plant response to abiotic stress would require the 81 elucidation of their molecular functions in organelles. To this end, we examined the 82 molecular defects in the mterf9 mutant and characterized the primary functions of 83 mTERF9 in Arabidopsis. We show that mTERF9 is required for chloroplast ribosomal 84 assembly and therefore, translation. Our findings further reveal that mTERF9 promotes 85 ribosomal assembly via ribonucleoprotein interactions in vivo. Finally, we demonstrate 86 that mTERF9 interacts physically with the CPN60 chaperonin complex in vivo suggesting 87 a functional cooperation between these proteins in chloroplast ribosome biogenesis and 88 translation. This study provides molecular evidence for a conn...

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Chloroplast Translation Elongation Factor EF-Tu/SVR11 Is Involved in var2-Mediated Leaf Variegation and Leaf Development in Arabidopsis

Cited by 27 publications

References 60 publications

Disruption of carotene biosynthesis leads to abnormal plastids and variegated leaves in Brassica napus

Disruption of carotene biosynthesis leads to abnormal plastids and variegated leaves in Brassica napus

Arabidopsis mTERF9 protein promotes chloroplast ribosomal assembly and translation by establishing ribonucleoprotein interactions in vivo

Arabidopsis mTERF9 protein promotes chloroplast ribosomal assembly and translation by establishing ribonucleoprotein interactionsin vivo

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