The Complexity of Mitochondrial Complex IV: An Update of Cytochrome c Oxidase Biogenesis in Plants

Abstract

Mitochondrial respiration is an energy producing process that involves the coordinated action of several protein complexes embedded in the inner membrane to finally produce ATP. Complex IV or Cytochrome c Oxidase (COX) is the last electron acceptor of the respiratory chain, involved in the reduction of O₂ to H₂O. COX is a multimeric complex formed by multiple structural subunits encoded in two different genomes, prosthetic groups (heme a and heme a₃), and metallic centers (Cu_A and Cu_B). Tens of accessory proteins are required for mitochondrial RNA processing, synthesis and delivery of prosthetic groups and metallic centers, and for the final assembly of subunits to build a functional complex. In this review, we perform a comparative analysis of COX composition and biogenesis factors in yeast, mammals and plants. We also describe possible external and internal factors controlling the expression of structural proteins and assembly factors at the transcriptional and post-translational levels, and the effect of deficiencies in different steps of COX biogenesis to infer the role of COX in different aspects of plant development. We conclude that COX assembly in plants has conserved and specific features, probably due to the incorporation of a different set of subunits during evolution.

Keywords: COX; OXPHOS; biogenesis; mETC; plant growth.

Figure 1

Hierarchical clustering of expression data across different tissues, cell types and developmental stages. Meta-analysis of the expression of genes encoding 68 COX-related proteins according to tissue- and cell-type, and in different developmental stages. Candidate proteins were classified into five different categories according to their putative or demonstrated role in COX biogenesis. Hierarchical clustering was performed within each category. Transcriptional data were collected and analyzed using publicly available microarray data included in the Genevestigator database (https://genevestigator.com/gv/doc/intro_plant.jsp, [100]). The expression level is represented as percent of maximal expression in the dataset analyzed.

Figure 2

Meta-analysis of transcriptional data for genes encoding COX-related proteins in response to different perturbations or in several mutant backgrounds. (A) Complete hierarchical clustering of the expression data. A larger image is available in Figure S3. (B–H) Detail of specific parts of the clustering for transcriptional responses to nutrients and light (B); in mutants in members of the COP9 signalosome and the cop1-4 mutant (C); in response to hormones (D); abiotic stress (E); biotic stress (F); during oxygen deprivation (G); and during germination (H). Expression level is represented as log2-ratio of differential expression, in red for up-regulation and in green for down-regulation.