Plant mitochondria – past, present and future Møller, Ian Max; Rasmusson, Allan G.; Van Aken, Olivier
The Plant journal : for cell and molecular biology,
November 2021, Letnik:
108, Številka:
4
Journal Article
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SUMMARY
The study of plant mitochondria started in earnest around 1950 with the first isolations of mitochondria from animal and plant tissues. The first 35 years were spent establishing the basic ...properties of plant mitochondria and plant respiration using biochemical and physiological approaches. A number of unique properties (compared to mammalian mitochondria) were observed: (i) the ability to oxidize malate, glycine and cytosolic NAD(P)H at high rates; (ii) the partial insensitivity to rotenone, which turned out to be due to the presence of a second NADH dehydrogenase on the inner surface of the inner mitochondrial membrane in addition to the classical Complex I NADH dehydrogenase; and (iii) the partial insensitivity to cyanide, which turned out to be due to an alternative oxidase, which is also located on the inner surface of the inner mitochondrial membrane, in addition to the classical Complex IV, cytochrome oxidase. With the appearance of molecular biology methods around 1985, followed by genomics, further unique properties were discovered: (iv) plant mitochondrial DNA (mtDNA) is 10–600 times larger than the mammalian mtDNA, yet it only contains approximately 50% more genes; (v) plant mtDNA has kept the standard genetic code, and it has a low divergence rate with respect to point mutations, but a high recombinatorial activity; (vi) mitochondrial mRNA maturation includes a uniquely complex set of activities for processing, splicing and editing (at hundreds of sites); (vii) recombination in mtDNA creates novel reading frames that can produce male sterility; and (viii) plant mitochondria have a large proteome with 2000–3000 different proteins containing many unique proteins such as 200–300 pentatricopeptide repeat proteins. We describe the present and fairly detailed picture of the structure and function of plant mitochondria and how the unique properties make their metabolism more flexible allowing them to be involved in many diverse processes in the plant cell, such as photosynthesis, photorespiration, CAM and C4 metabolism, heat production, temperature control, stress resistance mechanisms, programmed cell death and genomic evolution. However, it is still a challenge to understand how the regulation of metabolism and mtDNA expression works at the cellular level and how retrograde signaling from the mitochondria coordinates all those processes.
Significance Statement
The history of plant mitochondria is briefly outlined. The present view of their unique properties and functions in cellular metabolism is described in detail both under standard conditions and in response to environmental stimuli.
In this overview of recent trends in plant mitochondrial research, four questions are considered: (1) How large is the mitochondrial proteome? It appears to be in excess of 1500 proteins in a tissue ...at any given time. It is proposed that the fusion–fission frequently observed for plant mitochondria provides a vital mixing function ensuring that all low‐abundance proteins are present in each mitochondrion at least some of the time. (2) What is the significance of posttranslational modifications (PTM) of proteins? As a result of PTM, many proteins are present in a very large number of slightly different forms. The most well‐studied PTMs, such as protein phosphorylation, acetylation and reversible cysteine oxidation, are known to regulate mitochondrial function. Recent studies have provided examples of the importance of this regulation, but it remains a research area with a massive growth potential. (3) What is the role(s) of pentatricopeptide repeat (PPR) proteins in plant mitochondria? There is general agreement that PPR proteins are involved in RNA metabolism such as RNA editing. Recent comprehensive proteomic studies raise the question of how many of the potential 250–300 mitochondrial PPR proteins encoded in the nuclear DNA are required to be present for a mitochondrion to be able to grow and divide. (4) What is the mechanism(s) of retrograde signal transduction from the mitochondria to the nucleus? The nature of the signal transduction molecule is still unknown, but calcium ions, hydrogen peroxide and/or oxidized peptides are potential candidates. Recent results place a receptor for the activation of a group of nuclear genes on the endoplasmic reticulum, possibly close to ER–mitochondrial contact points.
Proteomics, the large-scale study of the total complement of proteins in a given sample, has been applied to all aspects of seed biology mainly using model species such as Arabidopsis or important ...agricultural crops such as corn and rice. Proteins extracted from the sample have typically been separated and quantified by 2-dimensional polyacrylamide gel electrophoresis followed by liquid chromatography and mass spectrometry to identify the proteins in the gel spots. In this way, qualitative and quantitative changes in the proteome during seed development, desiccation tolerance, germination, dormancy release, vigor alteration and responses to environmental factors have all been studied. Many proteins or biological processes potentially important for each seed process have been highlighted by these studies, which greatly expands our knowledge of seed biology. Proteins that have been identified to be particularly important for at least two of the seed processes are involved in detoxification of reactive oxygen species, the cytoskeleton, glycolysis, protein biosynthesis, post-translational modifications, methionine metabolism, and late embryogenesis-abundant (LEA) proteins. It will be useful for molecular biologists and molecular plant breeders to identify and study genes encoding particularly interesting target proteins with the aim to improve the yield, stress tolerance or other critical properties of our crop species.
•Changes in the seed proteome have been studied mainly using 2D-PAGE.•In general, it is not possible to identify a single most important protein.•Proteins involved in defense against ROS are important for all seed processes.•Proteins of the cytoskeleton and glycolysis are also important.•The next omics frontier will be post-translational modifications of proteins.
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Prediction of protein localization plays an important role in understanding protein function and mechanisms. In this paper, we propose a general deep learning-based localization ...prediction framework, MULocDeep, which can predict multiple localizations of a protein at both subcellular and suborganellar levels. We collected a dataset with 44 suborganellar localization annotations in 10 major subcellular compartments—the most comprehensive suborganelle localization dataset to date. We also experimentally generated an independent dataset of mitochondrial proteins in Arabidopsis thaliana cell cultures, Solanum tuberosum tubers, and Vicia faba roots and made this dataset publicly available. Evaluations using the above datasets show that overall, MULocDeep outperforms other major methods at both subcellular and suborganellar levels. Furthermore, MULocDeep assesses each amino acid’s contribution to localization, which provides insights into the mechanism of protein sorting and localization motifs. A web server can be accessed at http://mu-loc.org.
Mitochondria function as hubs of plant metabolism. Oxidative phosphorylation produces ATP, but it is also a central high-capacity electron sink required by many metabolic pathways that must be ...flexibly coordinated and integrated. Here, we review the crucial roles of redox-associated posttranslational protein modifications (PTMs) in mitochondrial metabolic regulation. We discuss several major concepts. First, the major redox couples in the mitochondrial matrix (NAD, NADP, thioredoxin, glutathione, and ascorbate) are in kinetic steady state rather than thermodynamic equilibrium. Second, targeted proteomics have produced long lists of proteins potentially regulated by Cys oxidation/thioredoxin, Met-SO formation, phosphorylation, or Lys acetylation, but we currently only understand the functional importance of a few of these PTMs. Some site modifications may represent molecular noise caused by spurious reactions. Third, different PTMs on the same protein or on different proteins in the same metabolic pathway can interact to fine-tune metabolic regulation. Fourth, PTMs take part in the repair of stress-induced damage (e.g., by reducing Met and Cys oxidation products) as well as adjusting metabolic functions in response to environmental variation, such as changes in light irradiance or oxygen availability. Finally, PTMs form a multidimensional regulatory system that provides the speed and flexibility needed for mitochondrial coordination far beyond that provided by changes in nuclear gene expression alone.
Abstract
Plant mitogenomes can be difficult to assemble because they are structurally dynamic and prone to intergenomic DNA transfers, leading to the unusual situation where an organelle genome is ...far outnumbered by its nuclear counterparts. As a result, comparative mitogenome studies are in their infancy and some key aspects of genome evolution are still known mainly from pregenomic, qualitative methods. To help address these limitations, we combined machine learning and in silico enrichment of mitochondrial-like long reads to assemble the bacterial-sized mitogenome of Norway spruce (Pinaceae: Picea abies). We conducted comparative analyses of repeat abundance, intergenomic transfers, substitution and rearrangement rates, and estimated repeat-by-repeat homologous recombination rates. Prompted by our discovery of highly recombinogenic small repeats in P. abies, we assessed the genomic support for the prevailing hypothesis that intramolecular recombination is predominantly driven by repeat length, with larger repeats facilitating DNA exchange more readily. Overall, we found mixed support for this view: Recombination dynamics were heterogeneous across vascular plants and highly active small repeats (ca. 200 bp) were present in about one-third of studied mitogenomes. As in previous studies, we did not observe any robust relationships among commonly studied genome attributes, but we identify variation in recombination rates as a underinvestigated source of plant mitogenome diversity.
Nitric oxide (NO) has emerged as an important signal molecule in plants, having myriad roles in plant development. In addition, NO also orchestrates both biotic and abiotic stress responses, during ...which intensive cellular metabolic reprogramming occurs. Integral to these responses is the location of NO biosynthetic and scavenging pathways in diverse cellular compartments, enabling plants to effectively organize signal transduction pathways. NO regulates plant metabolism and, in turn, metabolic pathways reciprocally regulate NO accumulation and function. Thus, these diverse cellular processes are inextricably linked. This review addresses the numerous redox pathways, located in the various subcellular compartments that produce NO, in addition to the mechanisms underpinning NO scavenging. We focus on how this molecular dance is integrated into the metabolic state of the cell. Within this context, a reciprocal relationship between NO accumulation and metabolite production is often apparent. We also showcase cellular pathways, including those associated with nitrate reduction, that provide evidence for this integration of NO function and metabolism. Finally, we discuss the potential importance of the biochemical reactions governing NO levels in determining plant responses to a changing environment.
Nitric oxide (NO) has emerged as an important signal molecule in plants, having myriad roles in plant biotic and abiotic stress responses, during which intensive cellular metabolic reprogramming occurs. Numerous redox pathways, located in the various subcellular compartments produce NO, in addition to the mechanisms that underpin NO scavenging. Here, we focus on how this molecular dance is integrated into the metabolic state of the cell.In addition, we discuss the potential importance of the biochemical reactions governing NO levels in determining plant responses to a changing environment.
Cardiolipin is a mitochondrion-specific phospholipid that stabilizes the assembly of respiratory chain complexes, favoring full-yield operation. It also mediates key steps in apoptosis. In Barth ...syndrome, an X chromosome-linked cardiomyopathy caused by tafazzin mutations, cardiolipins display acyl chain modifications and are present at abnormally low concentrations, whereas monolysocardiolipin accumulates. Using immortalized lymphoblasts from Barth syndrome patients, we showed that the production of abnormal cardiolipin led to mitochondrial alterations. Indeed, the lack of normal cardiolipin led to changes in electron transport chain stability, resulting in cellular defects. We found a destabilization of the supercomplex (respirasome) I+III2+IVn but also decreased amounts of individual complexes I and IV and supercomplexes I+III and III+IV. No changes were observed in the amounts of individual complex III and complex II. We also found decreased levels of complex V. This complex is not part of the supercomplex suggesting that cardiolipin is required not only for the association/stabilization of the complexes into supercomplexes but also for the modulation of the amount of individual respiratory chain complexes. However, these alterations were compensated by an increase in mitochondrial mass, as demonstrated by electron microscopy and measurements of citrate synthase activity. We suggest that this compensatory increase in mitochondrial content prevents a decrease in mitochondrial respiration and ATP synthesis in the cells. We also show, by extensive flow cytometry analysis, that the type II apoptosis pathway was blocked at the mitochondrial level and that the mitochondria of patients with Barth syndrome cannot bind active caspase-8. Signal transduction is thus blocked before any mitochondrial event can occur. Remarkably, basal levels of superoxide anion production were slightly higher in patients' cells than in control cells as previously evidenced via an increased protein carbonylation in the taz1Δ mutant in the yeast. This may be deleterious to cells in the long term. The consequences of mitochondrial dysfunction and alterations to apoptosis signal transduction are considered in light of the potential for the development of future treatments.
•Barth syndrome lymphoblasts have impaired mitochondrial functions.•The lack of mature cardiolipin led to changes in electron transport chain stability.•A compensatory increase in mitochondrial content prevents a decrease ATP synthesis.•Apoptotic signal transduction for type II apoptosis is blocked before mitochondrial events can occur.•The basal levels of superoxide anion were slightly higher in patient's cells than in normal cells.
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