Atomic structure of a mitochondrial complex I intermediate from vascular plants.

Maria Maldonado,Long Zhou,Fei Guo,Abhilash Padavannil,James A Letts

doi:10.7554/elife.56664

Maria Maldonado, Long Zhou + Show 3 more

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https://doi.org/10.7554/elife.56664

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Journal: eLife	Publication Date: Aug 25, 2020
Citations: 45	License type: CC BY 4.0

Affiliation: University of California, Davis

Abstract

Respiration, an essential metabolic process, provides cells with chemical energy. In eukaryotes, respiration occurs via the mitochondrial electron transport chain (mETC) composed of several large membrane-protein complexes. Complex I (CI) is the main entry point for electrons into the mETC. For plants, limited availability of mitochondrial material has curbed detailed biochemical and structural studies of their mETC. Here, we present the cryoEM structure of the known CI assembly intermediate CI* from Vigna radiata at 3.9 Å resolution. CI* contains CI's NADH-binding and CoQ-binding modules, the proximal-pumping module and the plant-specific γ-carbonic-anhydrase domain (γCA). Our structure reveals significant differences in core and accessory subunits of the plant complex compared to yeast, mammals and bacteria, as well as the details of the γCA domain subunit composition and membrane anchoring. The structure sheds light on differences in CI assembly across lineages and suggests potential physiological roles for CI* beyond assembly.

Highlights

Respiration is an essential metabolic process that provides the energy and intermediate metabolites needed for growth and maintenance of all eukaryotes
In order to investigate the plant mitochondrial electron transport chain, we identified V. radiata as an optimal model system
As expected from previously reported plant mitochondrial extractions (Bultema et al, 2009; Dudkina et al, 2005; Eubel et al, 2004a; Eubel et al, 2004b; Eubel et al, 2003; Krause et al, 2004), we observed a number of bands with NADH-dehydrogenase activity, representing Complex I (CI) in different assembly states, such as in mitochondrial supercomplexes (Bultema et al, 2009; Dudkina et al, 2005; Eubel et al, 2004a; Eubel et al, 2004b; Eubel et al, 2003; Krause et al, 2004; Dudkina et al, 2010; Figure 1—figure supplement 2A)

Summary

Introduction

Respiration is an essential metabolic process that provides the energy and intermediate metabolites needed for growth and maintenance of all eukaryotes. Despite the importance of respiratory processes to plants’ biomass accumulation, carbon flux and acclimation (O’Leary et al, 2019; Amthor et al, 2019; Heskel et al, 2016), the fundamental mechanisms by which the plant mitochondrial electron transport chain (mETC) produces proton (H+) gradients that are converted into chemical energy remain poorly understood. Energy is provided to the cytoplasm and peroxisome in the form of ATP and/or reduction equivalents (NAD(P)H), from the chloroplasts and mitochondria through many pathways. Pathways that export ATP or reduction equivalents from the chloroplast to the cytoplasm include: 1) the chloroplast malate valve; 2) the triose phosphate-3-phosphglycerate (TP-2PGA) shuttle and 3) the phosphoenolpyruvate (PEP)-pyruvate shuttle. Pathways that export ATP or reduction equivalents directly from the mitochondria to the cytoplasm include: 1) the mitochondrial malate valve; 2) the mitochondrial adenylate nucleotide translocase

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