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1.
Plant Chloroplast Stress Response: Insights from Thiol Redox Proteomics.
Yu, J, Li, Y, Qin, Z, Guo, S, Li, Y, Miao, Y, Song, C, Chen, S, Dai, S
Antioxidants & redox signaling. 2020;(1):35-57
Abstract
Significance: Plant chloroplasts generate reactive oxygen species (ROS) during photosynthesis, especially under stresses. The sulfhydryl groups of protein cysteine residues are susceptible to redox modifications, which regulate protein structure and function, and thus different signaling and metabolic processes. The ROS-governed protein thiol redox switches play important roles in chloroplasts. Recent Advances: Various high-throughput thiol redox proteomic approaches have been developed, and they have enabled the improved understanding of redox regulatory mechanisms in chloroplasts. For example, the thioredoxin-modulated antioxidant enzymes help to maintain cellular ROS homeostasis. The light- and dark-dependent redox regulation of photosynthetic electron transport, the Calvin/Benson cycle, and starch biosynthesis ensures metabolic coordination and efficient energy utilization. In addition, redox cascades link the light with the dynamic changes of metabolites in nitrate and sulfur assimilation, shikimate pathway, and biosynthesis of fatty acid hormone as well as purine, pyrimidine, and thiamine. Importantly, redox regulation of tetrapyrrole and chlorophyll biosynthesis is critical to balance the photodynamic tetrapyrrole intermediates and prevent oxidative damage. Moreover, redox regulation of diverse elongation factors, chaperones, and kinases plays an important role in the modulation of gene expression, protein conformation, and posttranslational modification that contribute to photosystem II (PSII) repair, state transition, and signaling in chloroplasts. Critical Issues: This review focuses on recent advances in plant thiol redox proteomics and redox protein networks toward understanding plant chloroplast signaling, metabolism, and stress responses. Future Directions: Using redox proteomics integrated with biochemical and molecular genetic approaches, detailed studies of cysteine residues, their redox states, cross talk with other modifications, and the functional implications will yield a holistic understanding of chloroplast stress responses.
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2.
Chloroplast avoidance movement: a novel paradigm of ROS signalling.
Majumdar, A, Kar, RK
Photosynthesis research. 2020;(1):109-121
Abstract
The damaging effects of supra-optimal irradiance on plants, often turning to be lethal, may be circumvented by chloroplast avoidance movement which realigns chloroplasts to the anticlinal surfaces of cells (parallel to the incident light), essentially minimizing photon absorption. In angiosperms and many other groups of plants, chloroplast avoidance movement has been identified to be a strong blue light (BL)-dependent process being mediated by actin filaments wherein phototropins are identified as the photoreceptor involved. Studies through the last few decades have identified key molecular mechanisms involving Chloroplast Unusual Positioning 1 (CHUP1) protein and specific chloroplast-actin (cp-actin) filaments. However, the signal transduction pathway from strong BL absorption down to directional re-localization of chloroplasts by actin filaments is complex and ambiguous. Being the immediate cellular products of high irradiance absorption and having properties of remodelling actin as well as phototropin, reactive oxygen species (ROS) deemed to be more able and prompt than any other signalling agent in mediating chloroplast avoidance movement. Although ROS are presently being identified as fundamental component for regulating different plant processes ranging from growth, development and immunity, its role in avoidance movement have hardly been explored in depth. However, few recent reports have demonstrated the direct stimulatory involvement of ROS, especially H2O2, in chloroplast avoidance movement with Ca2+ playing a pivotal role. With this perspective, the present review discusses the mechanisms of ROS-mediated chloroplast avoidance movement involving ROS-Ca2+-actin communication system and NADPH oxidase (NOX)-plasma membrane (PM) H+-ATPase positive feed-forward loop. A possible working model is proposed.
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3.
Mesophyll conductance: the leaf corridors for photosynthesis.
Gago, J, Daloso, DM, Carriquí, M, Nadal, M, Morales, M, Araújo, WL, Nunes-Nesi, A, Flexas, J
Biochemical Society transactions. 2020;(2):429-439
Abstract
Besides stomata, the photosynthetic CO2 pathway also involves the transport of CO2 from the sub-stomatal air spaces inside to the carboxylation sites in the chloroplast stroma, where Rubisco is located. This pathway is far to be a simple and direct way, formed by series of consecutive barriers that the CO2 should cross to be finally assimilated in photosynthesis, known as the mesophyll conductance (gm). Therefore, the gm reflects the pathway through different air, water and biophysical barriers within the leaf tissues and cell structures. Currently, it is known that gm can impose the same level of limitation (or even higher depending of the conditions) to photosynthesis than the wider known stomata or biochemistry. In this mini-review, we are focused on each of the gm determinants to summarize the current knowledge on the mechanisms driving gm from anatomical to metabolic and biochemical perspectives. Special attention deserve the latest studies demonstrating the importance of the molecular mechanisms driving anatomical traits as cell wall and the chloroplast surface exposed to the mesophyll airspaces (Sc/S) that significantly constrain gm. However, even considering these recent discoveries, still is poorly understood the mechanisms about signaling pathways linking the environment a/biotic stressors with gm responses. Thus, considering the main role of gm as a major driver of the CO2 availability at the carboxylation sites, future studies into these aspects will help us to understand photosynthesis responses in a global change framework.
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4.
Progress on Understanding Transcriptional Regulation of Chloroplast Development in Fleshy Fruit.
Jia, T, Cheng, Y, Khan, I, Zhao, X, Gu, T, Hu, X
International journal of molecular sciences. 2020;(18)
Abstract
Edible fleshy fruits are important food sources in the human diet. Their yield and nutritional quality have long been considered as breeding targets for improvement. Various developing fleshy fruits with functional chloroplasts are capable of photosynthesis and contribute to fruit photosynthate, leading to the accumulation of metabolites associated with nutritional quality in ripe fruit. Although tomato high-pigment mutants with dark-green fruits have been isolated for more than 100 years, our understanding of the mechanism of chloroplast development in fleshy fruit remain poor. During the past few years, several transcription factors that regulate chloroplast development in fleshy fruit were identified through map-based cloning. In addition, substantial progress has been made in elucidating the mechanisms that how these transcription factors regulate chloroplast development. This review provides a summary and update on this progress, with a framework for further investigations of the multifaceted and hierarchical regulation of chloroplast development in fleshy fruit.
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5.
Regulation of Iron Homeostasis and Use in Chloroplasts.
Kroh, GE, Pilon, M
International journal of molecular sciences. 2020;(9)
Abstract
Iron (Fe) is essential for life because of its role in protein cofactors. Photosynthesis, in particular photosynthetic electron transport, has a very high demand for Fe cofactors. Fe is commonly limiting in the environment, and therefore photosynthetic organisms must acclimate to Fe availability and avoid stress associated with Fe deficiency. In plants, adjustment of metabolism, of Fe utilization, and gene expression, is especially important in the chloroplasts during Fe limitation. In this review, we discuss Fe use, Fe transport, and mechanisms of acclimation to Fe limitation in photosynthetic lineages with a focus on the photosynthetic electron transport chain. We compare Fe homeostasis in Cyanobacteria, the evolutionary ancestors of chloroplasts, with Fe homeostasis in green algae and in land plants in order to provide a deeper understanding of how chloroplasts and photosynthesis may cope with Fe limitation.
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6.
Chloroplast-associated molecular patterns as concept for fine-tuned operational retrograde signalling.
Unal, D, García-Caparrós, P, Kumar, V, Dietz, KJ
Philosophical transactions of the Royal Society of London. Series B, Biological sciences. 2020;(1801):20190443
Abstract
Chloroplasts compose about one-quarter of the mesophyll cell volume and contain about 60% of the cell protein. Photosynthetic carbon assimilation is the dominating metabolism in illuminated leaves. To optimize the resource expenditure in these costly organelles and to control and adjust chloroplast metabolism, an intensive transfer of information between nucleus-cytoplasm and chloroplasts occurs in both directions as anterograde and retrograde signalling. Recent research identified multiple retrograde pathways that use metabolite transfer and include reaction products of lipids and carotenoids with reactive oxygen species (ROS). Other pathways use metabolites of carbon, sulfur and nitrogen metabolism, low molecular weight antioxidants and hormone precursors to carry information between the cell compartments. This review focuses on redox- and ROS-related retrograde signalling pathways. In analogy to the microbe-associated molecular pattern, we propose the term 'chloroplast-associated molecular pattern' which connects chloroplast performance to extrachloroplast processes such as nuclear gene transcription, posttranscriptional processing, including translation, and RNA and protein fate. This article is part of the theme issue 'Retrograde signalling from endosymbiotic organelles'.
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7.
Regulatory thiol oxidation in chloroplast metabolism, oxidative stress response and environmental signaling in plants.
Vogelsang, L, Dietz, KJ
The Biochemical journal. 2020;(10):1865-1878
Abstract
The antagonism between thiol oxidation and reduction enables efficient control of protein function and is used as central mechanism in cellular regulation. The best-studied mechanism is the dithiol-disulfide transition in the Calvin Benson Cycle in photosynthesis, including mixed disulfide formation by glutathionylation. The adjustment of the proper thiol redox state is a fundamental property of all cellular compartments. The glutathione redox potential of the cytosol, stroma, matrix and nucleoplasm usually ranges between -300 and -320 mV. Thiol reduction proceeds by short electron transfer cascades consisting of redox input elements and redox transmitters such as thioredoxins. Thiol oxidation ultimately is linked to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Enhanced ROS production under stress shifts the redox network to more positive redox potentials. ROS do not react randomly but primarily with few specific redox sensors in the cell. The most commonly encountered reaction within the redox regulatory network however is the disulfide swapping. The thiol oxidation dynamics also involves transnitrosylation. This review compiles present knowledge on this network and its central role in sensing environmental cues with focus on chloroplast metabolism.
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8.
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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9.
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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10.
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.