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WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress.

ABSTRACT: Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, many other components affecting chloroplast biogenesis under cold conditions have not been characterized. Here, we report the functional characterization of a white stripe leaf 5 (wsl5) mutant in rice. The mutant develops white-striped leaves during early leaf development and is albinic when planted under cold stress. Genetic and molecular analysis revealed that WSL5 encodes a novel chloroplast-targeted pentatricopeptide repeat protein. RNA sequencing analysis showed that expression of nuclear-encoded photosynthetic genes in the mutant was significantly repressed, and expression of many chloroplast-encoded genes was also significantly changed. Notably, the wsl5 mutation causes defects in editing of rpl2 and atpA, and splicing of rpl2 and rps12. wsl5 was impaired in chloroplast ribosome biogenesis under cold stress. We propose that the WSL5 allele is required for normal chloroplast development in maintaining retrograde signaling from plastids to the nucleus under cold stress.

SUBMITTER: Liu X

PROVIDER: S-EPMC6054151 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress.

Liu Xi X Lan Jie J Huang Yunshuai Y Cao Penghui P Zhou Chunlei C Ren Yaken Y He Niqing N Liu Shijia S Tian Yunlu Y Nguyen Thanhliem T Jiang Ling L Wan Jianmin J

Journal of experimental botany 20180701 16

Chloroplasts play an essential role in plant growth and development, and cold conditions affect chloroplast development. Although many genes or regulators involved in chloroplast biogenesis and development have been isolated and characterized, many other components affecting chloroplast biogenesis under cold conditions have not been characterized. Here, we report the functional characterization of a white stripe leaf 5 (wsl5) mutant in rice. The mutant develops white-striped leaves during early ...[more]

PMID: 29893948

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Project description:BackgroundThe chloroplast is the organelle responsible for photosynthesis in higher plants. The generation of functional chloroplasts depends on the precise coordination of gene expression in the nucleus and chloroplasts and is essential for the development of plants. However, little is known about nuclear-plastid regulatory mechanisms at the early stage of chloroplast generation in rice.ResultsIn this study, we identified a rice (Oryza sativa) mutant that exhibited albino and seedling-lethal phenotypes and named it ssa1(seedling stage albino1). Transmission electron microscopy (TEM) analysis indicated that the chloroplasts of ssa1 did not have organized thylakoid lamellae and that the chloroplast structure was destroyed. Genetic analysis revealed that the albino phenotypes of ssa1 were controlled by a pair of recessive nuclear genes. Map-based cloning experiments found that SSA1 encoded a pentapeptide repeat (PPR) protein that was allelic to OSOTP51,which was previously reported to participate in Photosystem I (PSI) assembly. The albino phenotype was reversed to the wild type (WT) phenotype when the normal SSA1 sequence was expressed in ssa1 under the drive of the actin promoter. Knockout experiments further created mutants ssa1-2/1-9, which had a phenotype similar to that of ssa1. SSA1 consisted of 7 pentatricopeptide repeat domains and two C-terminal LAGLIDADG tandem sequence motifs and was located in the chloroplast. GUS staining and qRT-PCR analysis showed that SSA1 was mainly expressed in young leaves and stems. In the ssa1 mutants, plastid genes transcribed by plastid-encoded RNA polymerase decreased, while those transcribed by nuclear-encoded RNA polymerase increased at the mRNA level. Loss-of-function SSA1 destroys RNA editing of ndhB-737 and intron splicing of atpF and ycf3-2 in the plastid genome. Yeast two-hybrid and BiFC assays revealed that SSA1 physically interacted with two new RNA editing partners, OsMORF8 and OsTRXz, which have potential functions in RNA editing and chloroplast biogenesis.ConclusionsRice SSA1 encodes a pentatricopeptide repeat protein, which is targeted to the chloroplast. SSA1 regulates early chloroplast development and plays a critical role in RNA editing and intron splicing in rice. These data will facilitate efforts to further elucidate the molecular mechanism of chloroplast biogenesis.

Dataset Information

WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress.

Publications

WSL5, a pentatricopeptide repeat protein, is essential for chloroplast biogenesis in rice under cold stress.

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