Modifications in Ultrastructural Characteristics and Redox Status of Plants under Environmental Stress: A Review
Abstract
:1. Introduction
2. Abiotic Environmental Stress Factors
2.1. Drought (Water Stress)
2.2. Salinity (Salt Stress)
2.3. Extreme Temperature (Cold/Heat Stress)
2.4. Metal and Nanoparticle Toxicity Stress
3. Some Selected Plant Defense Responses and Their Activated Mechanisms against Abiotic Constraints, with Special Emphasis on Oxidative/Antioxidative Status and Cell Ultrastructure
3.1. Protein Quality Control Systems—Protein Folding Stability and Dynamics
3.2. Osmoregulation and Compatible Solutes
3.3. Unsaturated Fatty Acids as General Defenders
3.4. Oxidative/Antioxidative Stress Concept
3.4.1. Reactive Oxygen Species
3.4.2. Oxidative Stress
3.4.3. Antioxidant Defense System
3.5. Cell Ultrastructure (Subcellular Organelles) as a Reliable Abiotic Stress Marker and Its Adaptive Strategies
3.5.1. Cell Wall and Plasma Membrane
3.5.2. Nucleus
3.5.3. Plastids (Chloroplasts and Amyloplasts)
3.5.4. Mitochondria
3.5.5. Endoplasmic Reticulum, Golgi Apparatus (Dictyosomes), and Vacuoles
4. Root Cap as a Valuable Model System for Study of Ultrastructural Plant Responses to Abiotic Stress
Ultrastructure of Statocytes in Plant Root Tips
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Compound | Notations | Sources |
---|---|---|
Singlet oxygen | 1O2 | UV radiation, photoinhibition, photosystem II electron transfer reactions |
Superoxide anion | O2•− | Mehler reaction in photosynthetic electron transport, photorespiration, mitochondrial electron transport, plasmalemma, nitrogen fixation, O3 and OH− reactions in apoplast, pathogen defense responses |
Hydrogen peroxide | H2O2 | Photorespiration, β-oxidation, pathogen defense responses |
Hydroxyl radical | OH• | O3 reaction in apoplast, pathogens defense responses |
Perhydroxyl radical | O2H• | O3 and OH− reactions in apoplast |
Compartment/Structure | Abiotic Factor | Plants Species | Cell Effects | Reference |
---|---|---|---|---|
Cell wall | Salinity (25–200 mM NaCl) | Solanum tuberosum | Twisted and ruptured cell walls, cell wall disintegration | [153] |
Salinity (100 mM NaCl) | Arabidopsis thaliana | Detachment of plasmalemma from cell wall | [151] | |
Oxidative stress (20 mM H2O2) | Brachypodium distachyon | Broken cell walls | [66] | |
Osmotic stress (15% PEG6000) | Brachypodium distachyon | Broken cell walls | [65] | |
Metal stress (80–320 μM Na2SeO4) | Allium sativum | Local thickenings of cell walls | [154] | |
Heat stress (37 °C) | Coffea arabica | Modification of cell wall structure | [155] | |
Plasma membrane | Salinity (25–200 mM NaCl) | Solanum tuberosum | Membrane invagination | [153] |
Osmotic stress (15% PEG6000) | Brachypodium distachyon | Obscured cell membranes, plasmolysis | [65] | |
Plasmodesmata | Cold stress (12/10 °C day/night) | Miscanthus × giganteus | Marked constriction of the cytoplasmic sleeve of the plasmodesmata at the mesophyll–bundle sheath interface | [156] |
Chilling stress (14 °C) | Zea mays | Strong constriction and swelling of the sphincters in plasmodesmata | [157] | |
Nucleus | Alkaline stress (pH 8.0) | Triticum aestivum | Increase in the number of amoeboid nucleoli with protuberances, disturbances in chromatin compaction, and occurrence of nuclear bodies of unknown etiology | [158] |
Oxidative stress (20 mM H2O2) | Brachypodium distachyon | Damage to nuclear membrane | [66] | |
Osmotic stress (15% PEG6000) | Brachypodium distachyon | Deformation and spreading of nucleoli | [65] | |
Metal stress (0.1 mM CuSO4) | Allium sativum | Disruption of nuclear membranes and high condensation of chromatin | [159] | |
Salinity (0.1 M NaCl and 0.1 M Na2SO4) | Triticum aestivum | Lumps of condensed chromatin inside the nucleus and nucleolus, increased separation between condensed and decondensed chromatin, appearance of nucleus invagination, and complete change in the shape of the nuclei | [152] | |
Plastid | High light stress (1500 μmol m−2 s−1) Pathogen infection (Botrytis cinerea) Dark-induced senescence | Arabidopsis thaliana | Significant decrease in chloroplast number, chloroplast size reduction, thylakoid area reduction, increase in plastoglobules, changes in starch content | [121] |
Chilling stress (2.5–4 °C) | Arabidopsis thaliana | Undulated and distorted thylakoid membranes arranged in grana stacks, large accumulation of starch, increase in average area per chloroplast | [160] | |
Heat stress (37 °C) | Coffea arabica | Changes in thylakoid integration, loss of grana stacking | [155] | |
Oxidative stress (20 mM H2O2) | Brachypodium distachyon | Swollen and deformed chloroplasts with dissolved grana thylakoid lamellae | [66] | |
Salinity (25–200 mM NaCl) | Solanum tuberosum | Aggregation of chloroplasts accompanied by swelling of grana and fret compartments or by the complete distortion of chloroplast grana and thylakoid structures | [153] | |
Salinity (100 mM NaCl) | Arabidopsis thaliana | Dilated thylakoid membranes, plastoglobuli accumulation | [151] | |
Osmotic stress (100 mM mannitol) | Arabidopsis thaliana | Large starch grain accumulation | [151] | |
Oxidative stress (0.5 mM H2O2) | Arabidopsis thaliana | Destruction of the lamellar system, marked alterations in stroma and thylakoid organization | [151] | |
Metal stress (150 μM ZnSO4) | Arabidopsis thaliana | Disorganized and curved stroma and thylakoid membranes, occurrence of several plastoglobuli inclusions and large starch granules | [151] | |
Plastid | Metal stress (100 μM SbCl3) | Trapa natans | Damaged chloroplasts, disintegrated inner membrane, disturbances in the orientation of the grana, starch accumulation | [161] |
Metal stress (0.1 mM Fe(III)-EDTA) | Cucumis sativus | Swollen chloroplasts and impaired thylakoids | [162] | |
Amyloplast | Salinity (25–125 mM NaCl) | Arabidopsis thaliana | Rapid degradation of amyloplasts | [163] |
Salinity (120 mM NaCl) | Pisum sativum | Changes in amyloplast distribution | [164] | |
Salinity (77.5 mM Na2SO4) | Nicotiana tabacum | Decrease in the number of starch grains in amyloplasts of the columella, no amyloplasts in the peripheral zone of the root cap | [165] | |
Osmotic stress (sorbitol solution) | Arabidopsis thaliana and Raphanus sativus | Degradation of the starch amyloplasts in root columella cells | [166] | |
Metal stress (0.75 mM CrCl3) | Iris pseudacorus | Decrease in the size of amyloplasts in the rhizome parenchyma | [167] | |
Mitochondria | Metal stress (0.1 mM Fe(III)-EDTA) | Cucumis sativus | Mitochondria rearrangements, cristae remodeling | [162] |
Chilling stress (0.5–4 °C) | Ranunculus glacialis | Fusion and aggregation of mitochondria | [168] | |
Salt stress (86.2–258 mM NaCl) Oxidative stress (20 mM H2O2) Osmotic stress (15% PEG6000) Metal stress (80–320 μM Na2SeO4) | Nicotiana tabacum Brachypodium distachyon Allium sativum | Lower matrix density with reduced number of cristae, dilated cristae, disintegrated matrix with messy or absent cristae | [65,66,154,169] | |
Alkaline stress (pH 8.0) | Triticum aestivum | Formation of invaginations or even cup-shaped mitochondria | [152] | |
Metal stress (0.1 mM CuSO4) | Allium sativum | Modifications in mitochondrial shape in the root meristematic cells, loss of matrix density, and an extension of cisternae | [159] | |
Mitochondria | Alkaline stress (pH 8.0) | Triticum aestivum | Formation of invaginations or even cup-shaped mitochondria | [152] |
Metal stress (0.1 mM CuSO4) | Allium sativum | Modifications in mitochondrial shape in the root meristematic cells, loss of matrix density, and an extension of cisternae | [159] | |
Endoplasmic reticulum | Salinity (100 mM NaCl) | Arabidopsis thaliana | Endomembrane rearrangements | [151] |
Metal stress (80–320 μM Na2SeO4) | Allium sativum | Appearance of concentric or parallel arrangement of abundant ER cisternae | [154] | |
Metal stress (200–500 mg/L Na2WO4) | Pisum sativum | Ribosome-bearing cisternae of ER with concentric conformations frequently enclose cytoplasmic organelles | [170] | |
Metal stress (0.1 mM CuSO4) | Allium sativum | Dilation of flattened cisternae of ER and their disintegration into small closed vesicles | [159] | |
Oxidative stress (20 mM H2O2) | Brachypodium distachyon | Broken ER scattered close to the plasma membrane | [66] | |
Golgi apparatus | Oxidative stress (0.5 mM H2O2) | Arabidopsis thaliana | Hypertrophied Golgi, high degree of membrane remodeling | [151] |
Metal stress (80–320 μM Na2SeO4) | Allium sativum | Significant ultrastructural changes in GA | [154] | |
Metal stress (0.1 mM CuSO4) | Allium sativum | Increase in dictyosome vesicles | [159] | |
Vacuole | Metal stress (200–500 mg/L Na2WO4) | Pisum sativum | Deformation and variation in size and shape of vacuoles | [170] |
Metal stress (0.1 mM CuSO4) | Allium sativum | Formation of larger vacuoles | [159] | |
Salinity (NaCl, Na2SO4) and Osmotic stress (mannitol), | Medicago sativa | Modifications in the quantity and form of residual protein bodies within vacuoles | [171] | |
Metal stress (100 μM SbCl3) | Trapa natans | Accumulation of Sb in vacuoles | [161] | |
Metal stress (20–60 μμM CdCl2) | Oryza sativa | Cd compartmentation in vacuoles | [172] |
Compartment/Plant Organ | Abiotic Factor | Plant Species | Cell Effects | Reference |
---|---|---|---|---|
Leaf—mesophyll cells | Chilling (2.5–4 °C in the dark and 3.2–4 °C in the light for 72 h) | Arabidopsis thaliana (Col 0) | Increased average area per chloroplast in cell sections | [160] |
Reduced chloroplast size | ||||
Significantly higher abundance of ring-shaped and other morphologically aberrant mitochondria | ||||
Leaf—mesophyll cells | Drought (induced by slowly decreasing the amount of supplied water over a time period of 4 weeks) | Spinacia oleracea L. cv. Matador | Increased absolute total volume and surface area of chloroplasts | [188] |
Increased volume of stroma and thylakoids, and increased thylakoid surface area in chloroplasts | ||||
Lack of starch grains | ||||
Decreased mean volume and surface area of mitochondria | ||||
Leaf—mesophyll cells | Chilling (18 °C during day and 8 °C during night for four weeks) | Zea mays L. | Suppressed development of the system of thylakoids, and decreased volume and surface density of all thylakoids in the chloroplasts | [189] |
Decreased volume and surface density of intergranal thylakoids in chloroplasts | ||||
Leaf—mesophyll cells | Drought (induced by withholding watering for 7 days) | Triticum aestivum L. | Increased proportion of spherical and oval-shaped mitochondria | [190] |
Increased mean size of mitochondria | ||||
Decreased relative cell area occupied by mitochondria in the drought-sensitive varieties | ||||
Leaf—mesophyll cells | Drought (induced by withholding watering for 7 days) | Triticum aestivum L. (drought-sensitive variety) | Increased size of chloroplasts, mitochondria, and plastoglobules | [191] |
Increased number of chloroplasts and plastoglobules per 100 µm2 visible field | ||||
Decreased number of mitochondria per 100 µm2 visible field | ||||
High temperature (40 °C for 5 h) | Increased size of chloroplasts, mitochondria, and plastoglobules | |||
Increased number of chloroplasts and mitochondria per 100 µm2 visible field | ||||
Drought + high temperature | Increased size of chloroplasts, mitochondria, and plastoglobules | |||
Increased number of chloroplasts, mitochondria, and plastoglobules per 100 µm2 visible field | ||||
Apical layer of curds | Cold stress (8 °C for 10 days) and heat stress (40 °C for 4 h) | Brassica oleracea var. botrytis | No significant changes in mitochondrial number and mitochondrial area per field | [192] |
Decreased mitochondrial number per field after stress (heat and cold) recovery | ||||
Leaf—mesophyll cells | Drought (simulated by 20% polyethylene glycol 6000 (−0.6 MPa) for 2 days) | Zea mays L. | No significant changes in the cell area occupied by chloroplasts and in the size and length-to-width ratio of chloroplasts in the drought-resistant line | [193] |
Significant reduction in the length-to-width ratios of chloroplasts and the cell area occupied by chloroplasts in drought-sensitive lines | ||||
Needle—mesophyll cells | Air CO2 | Picea abies L. Karst. | Increased number of chloroplasts per mesophyll volume (sampled systematically, uniformly, and randomly from the whole needle cross-section area) | [194] |
Increased starch areal density and starch grain area in chloroplasts (sampled from both the whole needle cross-section area and from the first layer of mesophyll) | ||||
Irradiance | Increased starch areal density and starch grain area in chloroplasts (sampled from both the whole needle cross-section area and from the first layer of mesophyll) |
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Ďúranová, H.; Šimora, V.; Ďurišová, Ľ.; Olexiková, L.; Kovár, M.; Požgajová, M. Modifications in Ultrastructural Characteristics and Redox Status of Plants under Environmental Stress: A Review. Plants 2023, 12, 1666. https://doi.org/10.3390/plants12081666
Ďúranová H, Šimora V, Ďurišová Ľ, Olexiková L, Kovár M, Požgajová M. Modifications in Ultrastructural Characteristics and Redox Status of Plants under Environmental Stress: A Review. Plants. 2023; 12(8):1666. https://doi.org/10.3390/plants12081666
Chicago/Turabian StyleĎúranová, Hana, Veronika Šimora, Ľuba Ďurišová, Lucia Olexiková, Marek Kovár, and Miroslava Požgajová. 2023. "Modifications in Ultrastructural Characteristics and Redox Status of Plants under Environmental Stress: A Review" Plants 12, no. 8: 1666. https://doi.org/10.3390/plants12081666