The Mitochondrial Pentatricopeptide Repeat Protein PPR18 Is Required for the cis-Splicing of nad4 Intron 1 and Essential to Seed Development in Maize.

Rui Liu,Shi-Kai Cao,Chunhui Xu,Feng Sun,Bao-Cai Tan,Aqib Sayyed,Xiaomin Wang

doi:10.3390/ijms21114047

Rui Liu, Shi-Kai Cao + Show 5 more

Open Access

https://doi.org/10.3390/ijms21114047

Copy DOI

Abstract

Pentatricopeptide repeat (PPR) protein comprises a large family, participating in various aspects of organellar RNA metabolism in land plants. There are approximately 600 PPR proteins in maize, but the functions of many PPR proteins remain unknown. In this study, we defined the function of PPR18 in the cis-splicing of nad4 intron 1 in mitochondria and seed development in maize. Loss function of PPR18 seriously impairs embryo and endosperm development, resulting in the empty pericarp (emp) phenotype in maize. PPR18 encodes a mitochondrion-targeted P-type PPR protein with 18 PPR motifs. Transcripts analysis indicated that the splicing of nad4 intron 1 is impaired in the ppr18 mutant, resulting in the absence of nad4 transcript, leading to severely reduced assembly and activity of mitochondrial complex I and dramatically reduced respiration rate. These results demonstrate that PPR18 is required for the cis-splicing of nad4 intron 1 in mitochondria, and critical to complex I assembly and seed development in maize.

Highlights

Mitochondria are originated from α-proteobacteria ancestors via endosymbiosis
Numerous additional nucleus-encoded splicing co-factors have been reported to be involved in the splicing of organellar introns, such as the chloroplast RNA splicing and ribosome maturation (CRM) domain-containing proteins [16,17], RNA helicase [18,19], mitochondrial transcription termination factors [20,21], plant organellar RNA recognition (PORR) domain proteins [22,23], regulator of chromosome condensation (RCC1) domain proteins [24], and the pentatricopeptide repeat (PPR) proteins [5,25,26]
A phylogenetic analysis based on the maize PPR18 and its homologous proteins revealed extensive conservation in the sequences in both monocots and dicots (Figure S1)

Summary

Introduction

Mitochondria are originated from α-proteobacteria ancestors via endosymbiosis. During evolution, the majority of the bacterial ancestral genes from mitochondrial genome have been lost or transferred to host nucleus [1]. RNA editing usually alters cytidine to uridine through a deamination reaction in mitochondria and plastids and RNA splicing is a processing event in which noncoding segments (intron) of precursor RNA are removed and coding sequences are joined. Numerous additional nucleus-encoded splicing co-factors have been reported to be involved in the splicing of organellar introns, such as the chloroplast RNA splicing and ribosome maturation (CRM) domain-containing proteins [16,17], RNA helicase [18,19], mitochondrial transcription termination factors (mTERF) [20,21], plant organellar RNA recognition (PORR) domain proteins [22,23], regulator of chromosome condensation (RCC1) domain proteins [24], and the pentatricopeptide repeat (PPR) proteins [5,25,26]

Methods

Results

Discussion

Conclusion