OsSLC1 Encodes a Pentatricopeptide Repeat Protein Essential for Early Chloroplast Development and Seedling Survival

Abstract

Background: The large family of pentatricopeptide repeat (PPR) proteins is widely distributed among land plants. Such proteins play vital roles in intron splicing, RNA editing, RNA processing, RNA stability and RNA translation. However, only a small number of PPR genes have been identified in rice. Results: In this study, we raised a mutant from tissue-culture-derived plants of Oryza sativa subsp. japonica 'Zhonghua 11', which exhibited a lethal chlorosis phenotype from germination to the third-leaf stage. The mutant was designated seedling-lethal chlorosis 1 (slc1). The slc1 mutant leaves showed extremely low contents of photosynthetic pigments and abnormal chloroplast development, and were severely defective in photosynthesis. Map-based cloning of OsSLC1 revealed that a single base (G) deletion was detected in the first exon of Os06g0710800 in the slc1 mutant, which caused a premature stop codon. Knockout and complementation experiments further confirmed that OsSLC1 is responsible for the seedling-lethal chlorosis phenotype in the slc1 mutant. OsSLC1 was preferentially expressed in green leaves, and encoded a chloroplast-localized PPR protein harboring 12 PPR motifs. Loss-of-function of OsSLC1 affected the intron splicing of multiple group II introns, and especially precluded the intron splicing of rps16, and resulted in significant increase in the transcript levels of 3 chloroplast ribosomal RNAs and 16 chloroplast development-related and photosynthesis-related genes, and in significant reduction in the transcript levels of 1 chloroplast ribosomal RNAs and 2 chloroplast development-related and photosynthesis-related genes. Conclusion: We characterized a novel chloroplast-localized PPR protein, OsSLC1, which plays a vital role in the intron splicing of multiple group II introns, especially the rps16 intron, and is essential for early chloroplast development and seedling survival in rice.

A PPR Protein ACM1 Is Involved in Chloroplast Gene Expression and Early Plastid Development in Arabidopsis

“…Defective or damaged PPR proteins, therefore, usually lead to very severe phenotypes, such as embryo development delay, pigmentation defect, and abnormal chloroplast biogenesis [ 23 , 24 , 25 ]. Focusing on only chloroplasts, defective and damaged PPR proteins lead to several phenotypes: pale-yellowish, grana thylakoid formation altered, chlorophyll synthesis hindered, and even severe defects in photosynthesis [ 26 , 27 ]. In conclusion, PPR proteins can influence chloroplast biogenesis or development by diverse action modes and functional types.…”

GmPGL2, Encoding a Pentatricopeptide Repeat Protein, Is Essential for Chloroplast RNA Editing and Biogenesis in Soybean

“…However, in the Gmpgl2 mutant, the expression of NEP and PEP increased in developmental stages S1 and S2. Recently, this kind of changes has been observed in the knockout of SLC1 gene, which encodes a P subgroup of PPR protein in rice ( Lv et al, 2020 ). In slc1 mutant, the transcript levels of 3 chloroplast ribosomal RNAs and 16 chloroplast development-related and photosynthesis-related genes were also significant increased.…”

“…In slc1 mutant, the transcript levels of 3 chloroplast ribosomal RNAs and 16 chloroplast development-related and photosynthesis-related genes were also significant increased. This phenomenon was attributed to preclude the intron splicing of rps16 in the slc1 mutant, which blocked the post-transcriptional processing and translation of rps16 , and failed to assemble the normal 70S ribosomes ( Lv et al, 2020 ). In our study, the rps16 -56313 was the unique editing site, which was completely abolished in the Gmpgl2 mutant.…”

“…RNA editing converts hundreds of Cs to Us at specific positions in the plastid and mitochondrial transcripts; moreover, editing often creates start or stop codons ( Stern et al, 2010 ; Small et al, 2020 ). Meanwhile, a lack of RNA editing may have severe consequences, such as impaired chloroplast biogenesis ( Yu et al, 2009 ; Ma et al, 2017 ; Jiang et al, 2018 ; Lv et al, 2020 ) and embryo lethality ( Li et al, 2014 , 2019 ; Sun et al, 2015a ).…”

Fine Mapping of a Novel Major Quantitative Trait Locus, qPAA7, That Controls Panicle Apical Abortion in Rice

“…We analyzed the nine gene annotations in the qPAA7 interval. According to the results of the previous studies, LOC_Os07g41220,LOC_Os07g41230, and LOC_Os07g41280 showed the PCD or accumulation of ROS functions, and the other six candidate genes did not show similar functions (Zhang L. et al, 2015;Xiao et al, 2018;Lv et al, 2020). LOC_Os07g41220 was annotated as a peptidase aspartic family protein, and studies have found that aspartic proteases are related to plant development and cell death (Niu et al, 2013).…”