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Cyanobacteria evolution: Insight from the fossil record.
Demoulin, CF, Lara, YJ, Cornet, L, François, C, Baurain, D, Wilmotte, A, Javaux, EJ
Free radical biology & medicine. 2019;:206-223
Abstract
Cyanobacteria played an important role in the evolution of Early Earth and the biosphere. They are responsible for the oxygenation of the atmosphere and oceans since the Great Oxidation Event around 2.4 Ga, debatably earlier. They are also major primary producers in past and present oceans, and the ancestors of the chloroplast. Nevertheless, the identification of cyanobacteria in the early fossil record remains ambiguous because the morphological criteria commonly used are not always reliable for microfossil interpretation. Recently, new biosignatures specific to cyanobacteria were proposed. Here, we review the classic and new cyanobacterial biosignatures. We also assess the reliability of the previously described cyanobacteria fossil record and the challenges of molecular approaches on modern cyanobacteria. Finally, we suggest possible new calibration points for molecular clocks, and strategies to improve our understanding of the timing and pattern of the evolution of cyanobacteria and oxygenic photosynthesis.
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2.
Metabolic Innovations Underpinning the Origin and Diversification of the Diatom Chloroplast.
Nonoyama, T, Kazamia, E, Nawaly, H, Gao, X, Tsuji, Y, Matsuda, Y, Bowler, C, Tanaka, T, Dorrell, RG
Biomolecules. 2019;(8)
Abstract
: Of all the eukaryotic algal groups, diatoms make the most substantial contributions to photosynthesis in the contemporary ocean. Understanding the biological innovations that have occurred in the diatom chloroplast may provide us with explanations to the ecological success of this lineage and clues as to how best to exploit the biology of these organisms for biotechnology. In this paper, we use multi-species transcriptome datasets to compare chloroplast metabolism pathways in diatoms to other algal lineages. We identify possible diatom-specific innovations in chloroplast metabolism, including the completion of tocopherol synthesis via a chloroplast-targeted tocopherol cyclase, a complete chloroplast ornithine cycle, and chloroplast-targeted proteins involved in iron acquisition and CO2 concentration not shared between diatoms and their closest relatives in the stramenopiles. We additionally present a detailed investigation of the chloroplast metabolism of the oil-producing diatom Fistuliferasolaris, which is of industrial interest for biofuel production. These include modified amino acid and pyruvate hub metabolism that might enhance acetyl-coA production for chloroplast lipid biosynthesis and the presence of a chloroplast-localised squalene synthesis pathway unknown in other diatoms. Our data provides valuable insights into the biological adaptations underpinning an ecologically critical lineage, and how chloroplast metabolism can change even at a species level in extant algae.
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3.
Control of plastidial metabolism by the Clp protease complex.
Rodriguez-Concepcion, M, D'Andrea, L, Pulido, P
Journal of experimental botany. 2019;(7):2049-2058
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Abstract
Plant metabolism is strongly dependent on plastids. Besides hosting the photosynthetic machinery, these endosymbiotic organelles synthesize starch, fatty acids, amino acids, nucleotides, tetrapyrroles, and isoprenoids. Virtually all enzymes involved in plastid-localized metabolic pathways are encoded by the nuclear genome and imported into plastids. Once there, protein quality control systems ensure proper folding of the mature forms and remove irreversibly damaged proteins. The Clp protease is the main machinery for protein degradation in the plastid stroma. Recent work has unveiled an increasing number of client proteins of this proteolytic complex in plants. Notably, a substantial proportion of these substrates are required for normal chloroplast metabolism, including enzymes involved in the production of essential tetrapyrroles and isoprenoids such as chlorophylls and carotenoids. The Clp protease complex acts in coordination with nuclear-encoded plastidial chaperones for the control of both enzyme levels and proper folding (i.e. activity). This communication involves a retrograde signaling pathway, similarly to the unfolded protein response previously characterized in mitochondria and endoplasmic reticulum. Coordinated Clp protease and chaperone activities appear to further influence other plastid processes, such as the differentiation of chloroplasts into carotenoid-accumulating chromoplasts during fruit ripening.
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Toward an Integrated Understanding of Retrograde Control of Photosynthesis.
Dietz, KJ, Wesemann, C, Wegener, M, Seidel, T
Antioxidants & redox signaling. 2019;(9):1186-1205
Abstract
SIGNIFICANCE Photosynthesis takes place in the chloroplast of eukaryotes, which occupies a large portion of the photosynthetic cell. The chloroplast function and integrity depend on intensive material and signal exchange between all genetic compartments and conditionally secure efficient photosynthesis and high fitness. Recent Advances: During the last two decades, the concept of mutual control of plastid performance by extraplastidic anterograde signals acting on the chloroplast and the feedback from the chloroplast to the extraplastidic space by retrograde signals has been profoundly revised and expanded. It has become clear that a complex set of diverse signals is released from the chloroplast and exceeds the historically proposed small number of information signals. Thus, it is also recognized that redox compounds and reactive oxygen species play a decisive role in retrograde signaling. CRITICAL ISSUES The diversity of processes controlled or modulated by the retrograde network covers all molecular levels, including RNA fate and translation, and also includes subcellular heterogeneity, indirect gating of other organelles' metabolism, and specific signaling routes and pathways, previously not considered. All these processes must be integrated for optimal adjustment of the chloroplast processes. Thus, evidence is presented suggesting that retrograde signaling affects translation, stress granule, and processing body (P-body) dynamics. FUTURE DIRECTIONS Redundancy of signal transduction elements, parallelisms of pathways, and conditionally alternative mechanisms generate a robust network and system that only tentatively can be assessed by use of single-site mutants.
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Chloroplast ultrastructure in plants.
Kirchhoff, H
The New phytologist. 2019;(2):565-574
Abstract
The chloroplast organelle in mesophyll cells of higher plants represents a sunlight-driven metabolic factory that eventually fuels life on our planet. Knowledge of the ultrastructure and the dynamics of this unique organelle is essential to understanding its function in an ever-changing and challenging environment. Recent technological developments promise unprecedented insights into chloroplast architecture and its functionality. The review highlights these new methodical approaches and provides structural models based on recent findings about the plasticity of the thylakoid membrane system in response to different light regimes. Furthermore, the potential role of the lipid droplets plastoglobuli is discussed. It is emphasized that detailed structural insights are necessary on different levels ranging from molecules to entire membrane systems for a holistic understanding of chloroplast function.
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6.
Piecing the Puzzle Together: The Central Role of Reactive Oxygen Species and Redox Hubs in Chloroplast Retrograde Signaling.
Leister, D
Antioxidants & redox signaling. 2019;(9):1206-1219
Abstract
SIGNIFICANCE Reactive oxygen species (ROS) and redox regulation are established components of chloroplast-nucleus retrograde signaling. Recent Advances: In recent years, a complex array of putative retrograde signaling molecules and novel signaling pathways have emerged, including various metabolites, chloroplast translation, mobile transcription factors, calcium, and links to the unfolded protein response. This critical mass of information now permits us to fit individual pieces into a larger picture and outline a few important stimuli and pathways. CRITICAL ISSUES In this review, we summarize how ROS and redox hubs directly (e.g., via hydrogen peroxide [H2O2]) and indirectly (e.g., by triggering the production of signaling metabolites) regulate chloroplast retrograde signaling. Indeed, evidence is accumulating that most of the presumptive signaling metabolites so far identified are produced directly by ROS (such as β-cyclocitral) or indirectly by redox- or ROS-mediated regulation of key enzymes in metabolic pathways, ultimately leading to the accumulation of certain precursors (e.g., methylerythritol cyclodiphosphate and 3'-phosphoadenosine 5'-phosphate) with signal function. Of the ROS generated in the chloroplast, only H2O2 is likely to leave the organelle, and recent results suggest that efficient and specific transfer of information via H2O2 occurs through physical association of chloroplasts with the nucleus. FUTURE DIRECTIONS The impact of ROS and redox regulation on chloroplast-nucleus communication is even greater than previously thought, and it can be expected that further instances of control of retrograde signaling by ROS/redox regulation will be revealed in future, perhaps including the basis for the enigmatic GUN response and translation-dependent signals.
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Mg2+ homeostasis and transport in cyanobacteria - at the crossroads of bacterial and chloroplast Mg2+ import.
Pohland, AC, Schneider, D
Biological chemistry. 2019;(10):1289-1301
Abstract
Magnesium cation (Mg2+) is the most abundant divalent cation in living cells, where it is required for various intracellular functions. In chloroplasts and cyanobacteria, established photosynthetic model systems, Mg2+ is the central ion in chlorophylls, and Mg2+ flux across the thylakoid membrane is required for counterbalancing the light-induced generation of a ΔpH across the thylakoid membrane. Yet, not much is known about Mg2+ homoeostasis, transport and distribution within cyanobacteria. However, Mg2+ transport across membranes has been studied in non-photosynthetic bacteria, and first observations and findings are reported for chloroplasts. Cyanobacterial cytoplasmic membranes appear to contain the well-characterized Mg2+ channels CorA and/or MgtE, which both facilitate transmembrane Mg2+ flux down the electrochemical gradient. Both Mg2+ channels are typical for non-photosynthetic bacteria. Furthermore, Mg2+ transporters of the MgtA/B family are also present in the cytoplasmic membrane to mediate active Mg2+ import into the bacterial cell. While the cytoplasmic membrane of cyanobacteria resembles a 'classical' bacterial membrane, essentially nothing is known about Mg2+ channels and/or transporters in thylakoid membranes of cyanobacteria or chloroplasts. As discussed here, at least one Mg2+ channelling protein must be localized within thylakoid membranes. Thus, either one of the 'typical' bacterial Mg2+ channels has a dual localization in the cytoplasmic plus the thylakoid membrane, or another, yet unidentified channel is present in cyanobacterial thylakoid membranes.
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8.
The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants.
Trösch, R, Willmund, F
Biological chemistry. 2019;(7):879-893
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Abstract
Cells are highly adaptive systems that respond and adapt to changing environmental conditions such as temperature fluctuations or altered nutrient availability. Such acclimation processes involve reprogramming of the cellular gene expression profile, tuning of protein synthesis, remodeling of metabolic pathways and morphological changes of the cell shape. Nutrient starvation can lead to limited energy supply and consequently, remodeling of protein synthesis is one of the key steps of regulation since the translation of the genetic code into functional polypeptides may consume up to 40% of a cell's energy during proliferation. In eukaryotic cells, downregulation of protein synthesis during stress is mainly mediated by modification of the translation initiation factors. Prokaryotic cells suppress protein synthesis by the active formation of dimeric so-called 'hibernating' 100S ribosome complexes. Such a transition involves a number of proteins which are found in various forms in prokaryotes but also in chloroplasts of plants. Here, we review the current understanding of these hibernation factors and elaborate conserved principles which are shared between species.
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Singlet oxygen-triggered chloroplast-to-nucleus retrograde signalling pathways: An emerging perspective.
Dogra, V, Rochaix, JD, Kim, C
Plant, cell & environment. 2018;(8):1727-1738
Abstract
Singlet oxygen (1 O2 ) is a prime cause of photo-damage of the photosynthetic apparatus. The chlorophyll molecules in the photosystem II reaction center and in the light-harvesting antenna complex are major sources of 1 O2 generation. It has been thought that the generation of 1 O2 mainly takes place in the appressed regions of the thylakoid membranes, namely, the grana core, where most of the active photosystem II complexes are localized. Apart from being a toxic molecule, new evidence suggests that 1 O2 significantly contributes to chloroplast-to-nucleus retrograde signalling that primes acclimation and cell death responses. Interestingly, recent studies reveal that chloroplasts operate two distinct 1 O2 -triggered retrograde signalling pathways in which β-carotene and a nuclear-encoded chloroplast protein EXECUTER1 play essential roles as signalling mediators. The coexistence of these mediators raises several questions: their crosstalk, source(s) of 1 O2 , downstream signalling components, and the perception and reaction mechanism of these mediators towards 1 O2 . In this review, we mainly discuss the molecular genetic basis of the mode of action of these two putative 1 O2 sensors and their corresponding retrograde signalling pathways. In addition, we also propose the possible existence of an alternative source of 1 O2 , which is spatially and functionally separated from the grana core.
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10.
Chloroplast signaling and quality control.
Rochaix, JD, Ramundo, S
Essays in biochemistry. 2018;(1):13-20
Abstract
Although chloroplasts contain their own genetic system and are semi-autonomous cell organelles, plastid biogenesis and homeostasis are heavily dependent on the nucleo-cytosolic compartment. These two cellular compartments are closely co-ordinated through a complex signaling network comprising both anterograde and retrograde signaling chains. Developmental changes or any perturbation in the chloroplast system induced by a particular stress resulting from changes in environmental conditions such as excess light, elevated temperature, nutrient limitation, pathogen infection, give rise to specific signals. They migrate out of the chloroplast and are perceived by the nucleus where they elicit changes in expression of particular genes that allow for the maintenance of plastid homeostasis toward environmental cues. These genes mainly include those of photosynthesis-associated proteins, chaperones, proteases, nucleases and immune/defense proteins. Besides this transcriptional response, a chloroplast quality control system exists that is involved in the repair and turnover of damaged plastid proteins. This system degrades aggregated or damaged proteins and it can even remove entire chloroplasts when they have suffered heavy damage. This response comprises several processes such as plastid autophagy and ubiquitin-proteasome mediated proteolysis that occurs on the plastid envelope through the action of the ubiquitin-proteasome system.