Genetic architecture of mitochondrial editing in Arabidopsis thaliana

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.

Figure 1.—

Editing values of parental accessions and reciprocal hybrids for polymorphic sites between Col and Ler. Col, Ler, and Col × Ler were grown at the same time as the recombinant inbred lines. Ler2 and Ler × Col were grown in the same greenhouse conditions as the previous lines but not at the same time. Error bars are calculated as 1 SD from the mean. The nature of the site, silent (S) or nonsilent (NS), is given after the name of the site. A minus sign following dominant and the F₁ indicates dominance of the less edited phenotype in the F₁, whereas a plus sign indicates dominance of the most edited phenotype.

Figure 2.—

Localization of the editing QTL on the Col × Ler linkage map. The linkage map is shown on the left, with distance between markers in centimorgans on the left of each chromosome and the name of the markers on the right of each chromosome. Editing QTL (P < 0.05) are represented by arrows whose lengths indicate the LOD2 support intervals. The direction of the arrows indicates the allelic effect: upward, Ler increasing and Col decreasing; downward, Col increasing and Ler decreasing. The shading of the arrow refers to the percentage of variance explained by each QTL. Five colocalization groups of QTL are represented by boxes and are numbered from 1 to 5. The QTL obtained with interval mapping (IM) and composite interval mapping (CIM) are given for each editing trait.

Figure 3.—

Alignment of the sequences around the editable C in sites for which the editing extent shows a strong phenotypic correlation (P < 0.001) and a colocalization of the mapped QTL. Thirty nucleotides upstream and 15 nucleotides downstream of the target C are shown. The target C is capitalized and the edited C's are underlined. Gaps were introduced in the alignments to show similar sequences. Letters in boldface type represent conserved nucleotides, and blocks of conserved nucleotides are shaded. The arrows on the right of the sequences indicate both the allelic effect of the corresponding QTL (upward, Ler increasing and Col decreasing; downward, Col increasing and Ler decreasing) and the sense of the correlation of the corresponding traits (same sense, positive correlation; opposite sense, negative correlation). As a comparison, putative cis-elements found in the upstream sequence of chloroplast sites, rpoB-2, psbL-1, and rps14-1, are shown at the bottom. Overexpression of rpoB-2 in transplastomic plants results in reduction of the editing efficiency of psbL-1 and rps14-1 but does not affect editing efficiency of sites lacking the putative elements (Chateigner-Boutin and Hanson 2002).