The Pentatricopeptide Repeat Proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 Are Involved in the Splicing of the Multipartite <i>nad5</i> Transcript Encoding a Subunit of Mitochondrial Complex I

Francs‐Small, Catherine Colas des; Longevialle, Andéol Falcon de; Li, Yunhai; Lowe, E. Cronin; Tanz, Sandra K.; Smith, Caroline; Bevan, Michael W.; Small, Ian

doi:10.1104/pp.114.244616

Cited by 75 publications

(55 citation statements)

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“…This conclusion is further supported by the recent study of the slow growth3 (slo3) mutant, which displays a similar reduction in nad7 intron 2 splicing but still accumulates detectable respiratory complex I (Hsieh et al, 2015). A comparison of published Arabidopsis mitochondrial splicing mutants indicates that splicing reductions of at least 5003 compared with the wild type seems necessary to result in a nearly complete loss of complex I on Blue Native gels (Koprivova et al, 2010;Kühn et al, 2011;Cohen et al, 2014;Colas des Francs-Small et al, 2014;Hsieh et al, 2015). The decrease in splicing efficiency can be much milder, though, when several complex I introns are concomitantly affected in a same mutant (Keren et al, 2012;Zmudjak et al, 2013).…”

Section: The Mtl1 Protein Is Also Essential For Optimal Splicing Of Nmentioning

confidence: 75%

“…S4). These very mild alterations could simply represent pleiotropic effects of the loss of complex I, as observed in several other complex I mutants (Haïli et al, 2013;Colas des Francs-Small et al, 2014;Hsieh et al, 2015), and do not support a direct role of MTL1 in the splicing of these introns. Oppositely, the 16-fold decrease of nad7 intron 2 splicing efficiency resulted in a measured 43 reduction in the accumulation level of nad7 mature mRNA ( Fig.…”

Section: The Mtl1 Protein Is Also Essential For Optimal Splicing Of Nmentioning

confidence: 75%

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The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis

et al. 2015

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Mitochondrial translation involves a complex interplay of ancient bacteria-like features and host-derived functionalities. Although the basic components of the mitochondrial translation apparatus have been recognized, very few protein factors aiding in recruiting ribosomes on mitochondria-encoded messenger RNA (mRNAs) have been identified in higher plants. In this study, we describe the identification of the Arabidopsis (Arabidopsis thaliana) MITOCHONDRIAL TRANSLATION FACTOR1 (MTL1) protein, a new member of the Pentatricopeptide Repeat family, and show that it is essential for the translation of the mitochondrial NADH dehydrogenase subunit7 (nad7) mRNA. We demonstrate that mtl1 mutant plants fail to accumulate the Nad7 protein, even though the nad7 mature mRNA is produced and bears the same 59 and 39 extremities as in wild-type plants. We next observed that polysome association of nad7 mature mRNA is specifically disrupted in mtl1 mutants, indicating that the absence of Nad7 results from a lack of translation of nad7 mRNA. These findings illustrate that mitochondrial translation requires the intervention of gene-specific nucleus-encoded PPR trans-factors and that their action does not necessarily involve the 59 processing of their target mRNA, as observed previously. Interestingly, a partial decrease in nad7 intron 2 splicing was also detected in mtl1 mutants, suggesting that MTL1 is also involved in group II intron splicing. However, this second function appears to be less essential for nad7 expression than its role in translation. MTL1 will be instrumental to understand the multifunctionality of PPR proteins and the mechanisms governing mRNA translation and intron splicing in plant mitochondria.

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Section: The Mtl1 Protein Is Also Essential For Optimal Splicing Of Nmentioning

confidence: 75%

Section: The Mtl1 Protein Is Also Essential For Optimal Splicing Of Nmentioning

confidence: 75%

The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis

et al. 2015

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“…Most complex I mutants show some form of growth retardation (de Longevialle et al, 2007;Keren et al, 2009Keren et al, , 2012Liu et al, 2010;Kühn et al, 2011;Haïli et al, 2013;Wydro et al, 2013;Zmudjak et al, 2013;Cohen et al, 2014;Colas des Francs-Small et al, 2014;Hsu et al, 2014). We used EdU staining to demonstrate that a smaller cell proliferation zone in the slo3 mutant root may be accountable for the short root phenotype of the mutant.…”

Section: Discussionmentioning

confidence: 99%

The SLOW GROWTH3 Pentatricopeptide Repeat Protein Is Required for the Splicing of Mitochondrial NADH Dehydrogenase Subunit7 Intron 2 in Arabidopsis

et al. 2015

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Mitochondria play an important role in maintaining metabolic and energy homeostasis in the cell. In plants, impairment in mitochondrial functions usually has detrimental effects on growth and development. To study genes that are important for plant growth, we have isolated a collection of slow growth (slo) mutants in Arabidopsis (Arabidopsis thaliana). One of the slo mutants, slo3, has a significant reduction in mitochondrial complex I activity. The slo3 mutant has a four-nucleotide deletion in At3g61360 that encodes a pentatricopeptide repeat (PPR) protein. The SLO3 protein contains nine classic PPR domains belonging to the P subfamily. The small deletion in the slo3 mutant changes the reading frame and creates a premature stop codon in the first PPR domain. We demonstrated that the SLO3-GFP is localized to the mitochondrion. Further analysis of mitochondrial RNA metabolism revealed that the slo3 mutant was defective in splicing of NADH dehydrogenase subunit7 (nad7) intron 2. This specific splicing defect led to a dramatic reduction in complex I activity in the mutant as revealed by blue native gel analysis. Complementation of slo3 by 35S:SLO3 or 35S:SLO3-GFP restored the splicing of nad7 intron 2, the complex I activity, and the growth defects of the mutant. Together, these results indicate that the SLO3 PPR protein is a splicing factor of nad7 intron 2 in Arabidopsis mitochondria.

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“…Interesting, many Arabidopsis mitochondrial mutants also have irregular leaf shapes, which are often described as "curly leaves" in the literature. [29][30][31][32][33][34][35][36][37] Nevertheless, the relationship between dysfunctional mitochondria and curly rosette leaves is rarely discussed or explored. One of the common themes for root and leaf growth is the regulation of cell proliferation, which includes setting the boundaries for meristem and elongation zone in the root, and control of the cell division arrest front in the leaf.…”

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Dysfunctional mitochondria regulate the size of root apical meristem and leaf development in Arabidopsis

Hsieh

Liao

Hsieh³

2015

Plant Signaling & Behavior

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The Pentatricopeptide Repeat Proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 Are Involved in the Splicing of the Multipartite nad5 Transcript Encoding a Subunit of Mitochondrial Complex I

Cited by 75 publications

References 51 publications

The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis

The MTL1 Pentatricopeptide Repeat Protein Is Required for Both Translation and Splicing of the Mitochondrial NADH DEHYDROGENASE SUBUNIT7 mRNA in Arabidopsis

The SLOW GROWTH3 Pentatricopeptide Repeat Protein Is Required for the Splicing of Mitochondrial NADH Dehydrogenase Subunit7 Intron 2 in Arabidopsis

Dysfunctional mitochondria regulate the size of root apical meristem and leaf development in Arabidopsis

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