RNA C-to-U editing in organelles is essential for plant growth and development; however, the underlying mechanism is not fully understood. Here, we report that pentatricopeptide repeat (PPR)-E subclass proteins carry out RNA C-to-U editing by recruiting the trans deaminase PCW1 (PPR motifs, coiled-coil, and DYW domain-containing protein 1) in maize (Zea mays) mitochondria. Loss-of-function of bCCP1 (bZIP and coiled-coil domain-containing PPR 1) or PCW1 arrests seed development in maize. bCCP1 encodes a bZIP and coiled-coil domain-containing PPR protein, and PCW1 encodes an atypical PPR-DYW protein. bCCP1 is required for editing at 66 sites in mitochondria and PCW1 is required for editing at 102 sites, including the 66 sites that require bCCP1. The PCW1-mediated editing sites are exclusively associated with PPR-E proteins. bCCP1 interacts with PCW1 and the PPR-E protein EMP7 (Empty pericarp7). Two multiple organellar RNA editing factor (MORF) proteins, ZmMORF1 and ZmMORF8, interact with PCW1, EMP7, and bCCP1. ZmMORF8 enhanced the EMP7-PCW1 interaction in a yeast three-hybrid assay. C-to-U editing at the ccmFN-1553 site in maize required EMP7, bCCP1, and PCW1. These results suggest that PPR-E proteins function in RNA editing by recruiting the trans deaminase PCW1 and bCCP1 and MORF1/8 assist this recruitment through protein-protein interactions.

Maize PPR-E proteins mediate RNA C-to-U editing in mitochondria by recruiting the trans deaminase PCW1.

The genomes in the two energy-converting organelles of plant cells, chloroplasts and mitochondria, contain numerous "errors" that are corrected at the level of RNA transcript copies. The genes encoded in the two endosymbiotic organelles would not function properly if their transcripts would not be altered by site-specific cytidine-to-uridine exchanges and by additional reverse U-to-C exchanges in hornworts, lycophytes and ferns. These peculiar processes of plant RNA editing, re-establishing genetic information that could alternatively be present at the organelle genome level, has spurred much research over more than 30 years. Lately this has revealed numerous interesting insights, notably on the biochemical machinery identifying specific pyrimidine nucleobases for conversion from C to U and vice versa. Here, I will summarize prominent research findings that have lately contributed to our better understanding of these phenomena introducing an added layer of information processing in plant cells. Some of this recent progress is based on the successful functional expression of plant RNA editing factors in bacteria and mammalian cells. These research approaches have recapitulated natural processes of horizontal gene transfer through which some protist lineages seem to have acquired plant RNA editing factors and adapted them functionally for their own purposes.

C-to-U and U-to-C: RNA editing in plant organelles and beyond.

RNA editing is a post-transcriptional modification process that alters the RNA sequence relative to the genomic blueprint. In plant organelles (namely, mitochondria and chloroplasts), the most common type is C-to-U, and the absence of C-to-U RNA editing results in abnormal plant development, such as etiolation and albino leaves, aborted embryonic development and retarded seedling growth. Here, through PREP, RES-Scanner, PCR and RT-PCR analyses, 38 and 139 RNA editing sites were identified from the chloroplast and mitochondrial genomes of Camellia sinensis, respectively. Analysis of the base preference around the RNA editing sites showed that in the −1 position of the edited C had more frequent occurrences of T whereas rare occurrences of G. Three conserved motifs were identified at 25 bases upstream of the RNA editing site. Structural analyses indicated that the RNA secondary structure of 32 genes, protein secondary structure of 37 genes and the three-dimensional structure of 5 proteins were altered due to RNA editing. The editing level analysis of matK and ndhD in six tea cultivars indicated that matK-701 might be involved in the color change of tea leaves. Furthermore, 218 PLS-CsPPR proteins were predicted to interact with the identified RNA editing sites. In conclusion, this study provides comprehensive insight into RNA editing events, which will facilitate further study of the RNA editing phenomenon of the tea plant.

https://www.mdpi.com/1422-0067/23/21/13640/pdf?version=1667874242

Exploring the RNA Editing Events and Their Potential Regulatory Roles in Tea Plant (Camellia sinensis L.)

RNA cytidine-to-uridine editing is essential for plant organellar gene expression. Pentatricopeptide repeat (PPR)-E+ proteins have been proposed to bind to target sites and recruit the cytidine deaminase AtDYW2, facilitated by AtNUWA. Here we analyze the function of ZmNUWA, ZmDYW2A, and ZmDYW2B and their relationships with other editing factors in maize. The zmdyw2a and zmdyw2b single mutants are normal, but the zmdyw2a::zmdyw2b and zmnuwa mutants are severely arrested in seed development. ZmNUWA, ZmDYW2A, and ZmDYW2B are dual localized in mitochondria and plastids. Loss of ZmNUWA decreases the editing at 99 mitochondrial sites and 8 plastid sites. Surprisingly, loss of ZmDYW2A:ZmDYW2B affects almost the same set of sites targeted by PPR-E+ proteins. ZmNUWA interacts with ZmDYW2A and ZmDYW2B, suggesting that ZmNUWA recruits ZmDYW2A/2B in the editing of PPR-E+-targeted sites in maize. Further protein interaction analyses show that ZmNUWA and ZmDYW2A/2B interact with ZmMORF1, ZmMORF8, ZmMORF2, and ZmMORF9 and that ZmOZ1 interacts with ZmORRM1, ZmDYW2A, ZmDYW2B, ZmMORF8, and ZmMORF9. These results suggest that the maize mitochondrial PPR-E+ editosome contains PPR-E+, ZmDYW2A/2B, ZmNUWA, and ZmMORF1/8, whereas the plastid PPR-E+ editosome is composed of PPR-E+, ZmDYW2A/2B, ZmNUWA, ZmMORF2/8/9, ZmORRM1, and ZmOZ1. 

Multiple factors interact in the editing of the PPR-E+ targeted sites in maize mitochondria and plastids.

Grain yield is the most critical and complex quantitative trait in maize. Kernel length (KL), kernel width (KW), kernel thickness (KT) and hundred-kernel weight (HKW) associated with kernel size are essential components of yield-related traits in maize. With the extensive use of quantitative trait locus (QTL) mapping and genome-wide association study (GWAS) analyses, thousands of QTLs and quantitative trait nucleotides (QTNs) have been discovered for controlling these traits. However, only some of them have been cloned and successfully utilized in breeding programs. In this study, we exhaustively collected reported genes, QTLs and QTNs associated with the four traits, performed cluster identification of QTLs and QTNs, then combined QTL and QTN clusters to detect consensus hotspot regions. In total, 31 hotspots were identified for kernel size-related traits. Their candidate genes were predicted to be related to well-known pathways regulating the kernel developmental process. The identified hotspots can be further explored for fine mapping and candidate gene validation. Finally, we provided a strategy for high yield and quality maize. This study will not only facilitate causal genes cloning, but also guide the breeding practice for maize.

/pdf/a-systemic-investigation-of-genetic-architecture-and-gene-1u2rx5dd.pdf

A Systemic Investigation of Genetic Architecture and Gene Resources Controlling Kernel Size-Related Traits in Maize

In flowering plants, RNA editing is a post-transcriptional process that selectively deaminates cytidines (C) to uridines (U) in organellar transcripts. Pentatricopeptide repeat (PPR) proteins have been identified as site-specific recognition factors for RNA editing. Here, we report the map-based cloning and molecular characterization of the defective kernel mutant dek504 in maize. Loss of Dek504 function leads to delayed embryogenesis and endosperm development, which produce small and collapsed kernels. Dek504 encodes an E+-type PPR protein targeted to the mitochondria, which is required for RNA editing of mitochondrial NADH dehydrogenase 3 at the nad3-317 and nad3-44 sites. Biochemical analysis of mitochondrial protein complexes revealed a significant reduction in the mitochondrial NADH dehydrogenase complex I activity, indicating that the alteration of the amino acid sequence at nad3-44 and nad3-317 through RNA editing is essential for NAD3 function. Moreover, the amino acids are highly conserved in monocots and eudicots, whereas the events of C-to-U editing are not conserved in flowering plants. Thus, our results indicate that Dek504 is essential for RNA editing of nad3, which is critical for NAD3 function, mitochondrial complex I stability, and seed development in maize.

/pdf/dek504-encodes-a-mitochondrion-targeted-e-type-3k6j6ldo.pdf

Dek504 Encodes a Mitochondrion-Targeted E+-Type Pentatricopeptide Repeat Protein Essential for RNA Editing and Seed Development in Maize

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Dek504 Encodes a Mitochondrion-Targeted E+-Type Pentatricopeptide Repeat Protein Essential for RNA Editing and Seed Development in Maize