Genetic Architecture of Mitochondrial Editing in Arabidopsis Thaliana

By Bentolila, Stéphane; Elliott, Leah E. et al. | Genetics, March 2008 | Go to article overview

Genetic Architecture of Mitochondrial Editing in Arabidopsis Thaliana


Bentolila, Stéphane, Elliott, Leah E., Hanson, Maureen R., Genetics


ABSTRACT

We have analyzed the mitochondrial editing behavior of two Arabidopsis thaliana accessions, Landsberg erecta (Ler) and Columbia (Col). A survey of 362 C-to-U editing sites in 33 mitochondrial genes was conducted on RNA extracted from rosette leaves. We detected 67 new editing events in A. thaliana rosette leaves that had not been observed in a prior study of mitochondrial editing in suspension cultures. Furthermore, 37 of the 441 C-to-U editing events reported in A. thaliana suspension cultures were not observed in rosette leaves. Forty editing sites that are polymorphic in extent of editing were detected between Col and Ler. Silent editing sites, which do not change the encoded amino acid, were found in a large excess compared to nonsilent sites among the editing events that differed between accessions and between tissue types. Dominance relationships were assessed for 15 of the most polymorphic sites by evaluating the editing values of the reciprocal hybrids. Dominance is more common in nonsilent sites than in silent sites, while additivity was observed only in silent sites. A maternal effect was detected for 8 sites. QTL mapping with recombinant inbred lines detected 12 major QTL for 11 of the 13 editing traits analyzed, demonstrating that efficiency of editing of individual mitochondrial C targets is generally governed by a major factor.

IN vascular plants, organelle transcripts are modified by C-to-U editing. While ~30 C-to-U editing events are typically found in vascular plant chloroplast transcriptomes (Maier et al. 1995; Tillich et al. 2005), hundreds of cytosine residues are subject to editing in themitochondria of flowering plants; 427, 456, 491, and 357 sites have been reported, respectively, in rapeseed (Brassica napus), Arabidopsis (Arabidopsis thaliana), rice (Oryza sativa), and sugarbeet (Beta vulgaris) (Giege and Brennicke 1999;Notsu et al. 2002;Handa 2003;Mower and Palmer 2006)

Sequence requirements for recognition and editing of C's to U's in plant organelles have been probed in chloroplasts by analysis of editing of transcripts in chloroplast transgenic plants and in chloroplast extracts (Chaudhuri and Maliga 1996; Hirose and Sugiura 2001). In plant mitochondria, similar studies have been carried out by electroporation of transcripts into isolated mitochondria or by analysis of editing of exogenous RNAs in mitochondrial extracts (Staudinger and Kempken 2003; Takenaka and Brennicke 2003). Sequences within 20-40 nt 59 and 2-10 nt downstream of the C targets of editing in both organelles have been found to be critical for editing reactions (Choury et al. 2004; Hayes et al. 2006; Van Der Merwe et al. 2006; Verbitskiy et al. 2006; Hayes and Hanson 2007a). Another common feature of editing in both plant organelles is the bias toward having a U upstream and an A downstream of the edited C (Giege and Brennicke 1999; Tillich et al. 2006).

In neither system is there evidence for the involvement of "guide RNAs" in recognition of C targets or catalysis of the editing reaction. In contrast, biochemical and genetic analyses suggest that proteins may mediate recognition of chloroplast editing substrates. Proteins bound to particular chloroplast editing sites could be detected in chloroplast extracts capable of editing exogenously added transcripts (Miyamoto et al. 2002). Two different nuclear-encoded chloroplast proteins, CRR4 and CRR21, were found to be required for editing of two specific C targets in ndhD (Kotera et al. 2005; Okuda et al. 2007), after identification of nuclear genes needed to restore chloroplast NADH dehydrogenase activity to two different Arabidopsis mutants. Both CRR4 and CRR21 are pentatricopeptide repeat (PPR) motif proteins, encoded by members of a large gene family previously observed to be involved in RNA processing and splicing in plant organelles (e.g., Fisk et al. 1999; Meierhoff et al. 2003). Recombinant CRR4 expressed in Escherichia coli bound specifically to a sequence comprising the 25 nucleotides upstream and 10 nucleotides downstream of the ndhD-1 editing site (Okuda et al. …

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Genetic Architecture of Mitochondrial Editing in Arabidopsis Thaliana
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