PPR-SMR1 is required for the splicing of multiple mitochondrial introns, interacts with Zm-mCSF1, and is essential for seed development in maize

Chen, Zongliang; Wang, Hongchun; Shen, Jiayu; Sun, Feng; Wang, Miaodi; Xu, Chunhui; Tan, Bin

doi:10.1093/jxb/erz305

Cited by 42 publications

(59 citation statements)

References 61 publications

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“…In vivo, their splicing requires the assistance of many factors from several protein families other than the maturases. For mitochondrial intron splicing, these proteins include the pentatricopeptide repeat (PPR) proteins (de Longevialle et al, 2007;Koprivova et al, 2010;Hsieh et al, 2015;Haili et al, 2016;Xiu et al, 2016;Sun et al, 2018;Chen et al, 2019;Sun et al, 2019;Yang et al, 2019), CRM/CRS1-YhbY domain proteins (Zmudjak et al, 2013), plant organellar RNA recognition domain-containing family proteins (Francs-Small et al, 2012), mitochondrial transcription termination factors (Hsu et al, 2014) and DEAD-box RNA helicases (Kohler et al, 2010). As RNAbinding proteins, these are proposed to facilitate the intron's formation of the catalytic structure during intron splicing (Lambowitz and Perlman, 1990).…”

Section: Introductionmentioning

confidence: 99%

DEK46 performs C‐to‐U editing of a specific site in mitochondrial nad7 introns that is critical for intron splicing and seed development in maize

Song

Yang

et al. 2020

The Plant Journal

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SUMMARY The self‐splicing of group II introns during RNA processing depends on their catalytic structure and is influenced by numerous factors that promote the formation of that structure through direct binding. Here we report that C‐to‐U editing at a specific position in two nad7 introns is essential to splicing, which also implies that the catalytic activity of non‐functional group II introns could be restored by editing. We characterized a maize (Zea mays) mutant, dek46, with a defective kernel phenotype; Dek46 encodes a pentatricopeptide repeat DYW protein exclusively localized in mitochondria. Analyses of the coding regions of mitochondrial transcripts did not uncover differences in RNA editing between dek46 mutant and wild‐type maize, but showed that splicing of nad7 introns 3 and 4 is severely reduced in the mutant. Furthermore, editing at nucleotide 22 of domain 5 (D5‐C22) of both introns is abolished in dek46. We constructed chimeric introns by swapping D5 of P.li.LSUI2 with D5 of nad7 intron 3. In vitro splicing assays indicated that the chimeric intron containing D5‐U22 can be self‐spliced, but the one containing D5‐C22 cannot. These results indicate that DEK46 functions in the C‐to‐U editing of D5‐C22 of both introns, and the U base at this position is critical to intron splicing.

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Section: Introductionmentioning

confidence: 99%

DEK46 performs C‐to‐U editing of a specific site in mitochondrial nad7 introns that is critical for intron splicing and seed development in maize

Song

Yang

et al. 2020

The Plant Journal

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“…We noticed that the CRM family genes were also highly expressed in young spikelets, suggesting that they might function in spikelet development (Figure 4). It iss reported that ZmmCSF1 and AtmCSF1 were essential for seed development [4,31]. Therefore, Os08g0174900, which is homologous with AtmCSF1, may also play an important role in seed development in rice.…”

Section: Discussionmentioning

confidence: 99%

Characterization of the CRM Gene Family and Elucidating the Function of OsCFM2 in Rice

et al. 2020

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The chloroplast RNA splicing and ribosome maturation (CRM) domain-containing proteins regulate the expression of chloroplast or mitochondrial genes that influence plant growth and development. Although 14 CRM domain proteins have previously been identified in rice, there are few studies of these gene expression patterns in various tissues and under abiotic stress. In our study, we found that 14 CRM domain-containing proteins have a conservative motif1. Under salt stress, the expression levels of 14 CRM genes were downregulated. However, under drought and cold stress, the expression level of some CRM genes was increased. The analysis of gene expression patterns showed that 14 CRM genes were expressed in all tissues but especially highly expressed in leaves. In addition, we analyzed the functions of OsCFM2 and found that this protein influences chloroplast development by regulating the splicing of a group I and five group II introns. Our study provides information for the function analysis of CRM domain-containing proteins in rice.

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“…Recent studies have shown that most PPR proteins are required for the post-transcriptional processing events in plastids and mitochondria (Barkan and Small, 2014). PPR proteins involved in the splicing of specific mitochondrial transcripts include OTP43 (de Longevialle et al, 2007), ABO5 (Liu et al, 2010), BIR6 (Koprivova et al, 2010), SLO3 (Hsieh et al, 2015), MTL1 (Haïli et al, 2016), TANG2, andOTP439 (des Francs-Small et al, 2014) in Arabidopsis and EMP16 (Xiu et al, 2016), Dek35 (Chen et al, 2017), Dek2 (Qi et al, 2017), and PPR-SMR1 (Chen et al, 2019) in maize. All these splicing cofactors belong to the P-type PPR proteins.…”

Section: Introductionmentioning

confidence: 99%

PPR14 Interacts With PPR-SMR1 and CRM Protein Zm-mCSF1 to Facilitate Mitochondrial Intron Splicing in Maize

et al. 2020

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In plants, splicing of organellar group II introns involves numerous nucleus-encoded trans-factors. But, how these trans-factors function and interact is not well understood. Here we report the function of a pentatricopeptide repeat (PPR) protein PPR14 and its physical relationship with other splicing factors in mitochondria. Null mutations of PPR14 severely arrest the embryo and endosperm development, causing an empty pericarp phenotype. PPR14 is required for the splicing of NADH dehydrogenase 2 (nad2) intron 3 and nad7 introns 1 and 2 in mitochondria. The absence of nad2 and nad7 transcripts leads to disruption of the mitochondrial complex I assembly and abolishes its NADH dehydrogenase activity. This is accompanied with increased levels of other mitochondrial complexes and elevated expression of the alternative oxidase proteins. As the function of PPR14 overlaps with PPR-SMR1 and the CRM-domain containing protein Zm-mCSF1, we tested their interactions. Protein-protein interaction analysis indicated that PPR14 interacts with PPR-SMR1 and Zm-mCSF1, suggesting that these three proteins may form a complex. As PPR proteins and CRM-domain containing proteins have many members in mitochondria and chloroplasts, we propose that organellar group II intron splicing is probably mediated by a dynamic complex that includes different PPR and CRM proteins in plants.

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PPR-SMR1 is required for the splicing of multiple mitochondrial introns, interacts with Zm-mCSF1, and is essential for seed development in maize

Abstract: Two maize nucleus-encoded splicing factors, PPR-SMR1 and Zm-mCSF1, are required for the splicing of most mitochondrial group II introns and subsequent complex I biogenesis, and therefore play important roles in seed development.

Cited by 42 publications

References 61 publications

DEK46 performs C‐to‐U editing of a specific site in mitochondrial nad7 introns that is critical for intron splicing and seed development in maize

DEK46 performs C‐to‐U editing of a specific site in mitochondrial nad7 introns that is critical for intron splicing and seed development in maize

Characterization of the CRM Gene Family and Elucidating the Function of OsCFM2 in Rice

PPR14 Interacts With PPR-SMR1 and CRM Protein Zm-mCSF1 to Facilitate Mitochondrial Intron Splicing in Maize

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