This review explores ROS production mechanisms and their signalling roles in the ER, and it discusses the roles of the unfolded protein response during plant hormone signalling and environmental ...stress
Abstract
Secretory proteins undergo modifications such as glycosylation and disulphide bond formation before proper folding, and move to their final destination via the endomembrane system. Accumulation of unfolded proteins in the endoplasmic reticulum (ER) due to suboptimal environmental conditions triggers a response called the unfolded protein response (UPR), which induces a set of genes that elevate protein folding capacity in the ER. This review aims to establish a connection among ER stress, UPR, and reactive oxygen species (ROS), which remains an unexplored topic in plants. For this, we focused on mechanisms of ROS production originating from ER stress, the interaction between ER stress and overall ROS signalling process in the cell, and the interaction of ER stress with other organellar ROS signalling pathways such as of the mitochondria and chloroplasts. The roles of the UPR during plant hormone signalling and abiotic and biotic stress responses are also discussed in connection with redox and ROS signalling.
•Combined stress greatly enhanced lipid peroxidation in 84-S in contrast to M-503.•Heat stress did not have any additional effect on that of only drought in both cultivars.•Tolerant M-503 showed a ...higher increase in proline content under combined stress.•The sensitivity of 84-S may be related with a decreased activity of CAT and POX.
Crop losses due to combined drought and heat is predicted be greater in the future especially due to climate change. Understanding underlying mechanisms under drought and heat combination will be crucial for the selection and breeding of tolerant varieties. The objective of this study was to assess the physiological and biochemical responses of two cotton cultivars (84-S and M-503) differing in drought tolerance to the combined effects of drought and heat. The relative growth rate (RGR) of the cultivars was decreased by 62.9% in drought sensitive 84-S and reduced by 34.58% in drought tolerant M-503 due to the combined drought and heat stresses. Combined stress also enhanced lipid peroxidation (TBARS) by 170.24% and 21.9% in 84-S and M-503, respectively which suggest that drought sensitive 84-S is more sensitive to combined stress than M-503. This sensitivity to combined stress of 84-S was associated with decreased activities of catalase (CAT) and peroxidase (POX) as compared to its control, resulting in higher H2O2 accumulation and oxidative stress induced lipid peroxidation. On the other hand, a higher combined stress tolerance of M-503 was associated with its ability to maintain constitutive activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX) and induced CAT and POX. The proline content of drought resistant M-503 was greatly enhanced under drought and the combination of drought and heat treatments as compared to 84-S. To the best of our knowledge, this is the first study conducted on the activities of antioxidant enzymes of cotton under drought and heat combination.
Accumulation of unfolded proteins caused by inefficient chaperone activity in the endoplasmic reticulum (ER) is termed 'ER stress', and it is perceived by a complex gene network. Induction of these ...genes triggers a response termed the 'unfolded protein response' (UPR). If a cell cannot overcome the accumulation of unfolded proteins, the ER-associated degradation (ERAD) system is induced to degrade those proteins. In addition to other factors, reactive oxygen species (ROS) are also produced during oxidative protein-folding in the ER. It has been shown in animal systems that there is a tight association between mitochondrial ROS and ER stress. However, in plants there are no reports concerning how induced ROS production in mitochondria and chloroplasts affects ER stress and if there is a possible role of organelle-originated ROS as a messenger molecule in the unfolded protein response. To address this issue, electron transport in chloroplasts and mitochondria and carnitine acetyl transferase (CAT) activity in peroxisomes were inhibited in wild-type Arabidopsis thaliana to induce ROS production. Expression of UPR genes was then investigated.
Plants of A. thaliana ecotype Col-0 were treated with various H2O2- and ROS-producing agents specific to different organelles, including the mitochondria, chloroplasts and peroxisomes. The expression of ER stress sensor/transducer genes (bZIP28, bZIP17, IRE1A, IRE1B, BiP1, BiP3), genes related to protein folding (CNX, ERO1) and ERAD genes (HRD1, SEL1, DER1, UBC32) were evaluated by qRT-PCR analysis.
Relatively low concentrations of ROS were more effective for induction of the ER stress response. Mitochondrial and chloroplastic ROS production had different induction mechanisms for the UPR and ER stress responses.
Chloroplast- and mitochondria-originated ROS have distinct roles in triggering the ER stress response. In general, low concentrations of ROS induced the transcription of ER stress-related genes, which can be attributed to the roles of ROS as secondary messengers. This is the first time that ROS production in organelles has been shown to affect the ER stress response in a plant system.
The element arsenic (As) is a non-essential metalloid that is found naturally in all soils and at high concentrations it is toxic to plant cells. As (V) can act as a chemical analogue of phosphate, ...it can disrupt phosphate-related energy metabolism and lipid structure. In this study, the contribution of mitochondrial alternative oxidase (AOX) and chloroplastic plastid terminal oxidase (PTOX) to As (V) stress tolerance was investigated. Our data indicate that As (V) stress (100, 200 and 300 µM) induces
AOX
gene expression by 3.3- to 10.5-fold depending on
AOX
gene, but not
PTOX
expression in wild-type
A. thaliana
plants. To further elucidate the role of AOX in As (V) stress tolerance, we utilized
aox1a
mutants and observed that
aox1a
mutants had decreased growth and higher oxidative stress damage under stress conditions, while there were no differences under control conditions. Moreover, acclimation of
aox1a
plants to new cellular redox environment was investigated by measuring the activities of reactive oxygen species (ROS)-scavenging enzymes. Induction of mitochondrial MnSOD activity at 300 µM As (V) was higher in
aox1a
plants (70%), when compared to wild type (43%). However, total ascorbate peroxidase and dehydroascorbate reductase activities were lower in
aox1a
plants when compared to wild type, which might explain higher oxidative damage observed in this genotype. On the other hand, NADPH oxidase activity, which is involved in ROS signaling, was lower in
aox1a
plants under normal conditions but a higher induction was observed with As (V) stress. Overall, our data indicate that
AOX1a
is involved in adaptation to As (V)-induced oxidative stress.
•Hormesis explains the biphasic dose-response of antioxidants in plants.•Allostasis explains the biphasic time-response antioxidants in plants.•Allostasis is complementary to hormesis.•Continued ...dose-eustress can manifest as time-distress as part of allostasis.•Allostasis and hormesis for oxidative stress follow the same mechanisms.
Hormesis, priming, and allostasis, three fields related to stress tolerance and toxicity, have much to say about reactive oxygen species (ROS), oxidative stress, and antioxidants. Among them, hormesis is a phenomenon that received much attention in the last two decades, and is about how toxic substances and stressful conditions often have a biphasic dose-response curve, showing that these substances and conditions have a beneficial effect at low doses. Another field, priming studies, has also been popular lately. H2O2 priming studies show that H2O2, a ROS, confers cross-tolerance to plants when applied at low doses, a classic example of eustress, as argued here. Last of the three is allostasis. A concept arising from human and mammalian studies, it shows that the stress response of the organism is beneficial in the short term and damaging in the long term. The existence of allostasis in plants has not been explored so far. In this article, it is proposed that hormesis, eustress (and H2O2 priming as eustress), and allostasis are all connected via ROS and oxidative stress in plants. These connections are elaborated and a workable approach for antioxidant activity is presented, with allostasis complementing hormesis in the temporal dimension. This approach can be used to explain the observed antioxidant activity decrease under prolonged or heavy stress in some studies. Evidence for the debated existence of eustress is also presented, and it is argued as an example of allostasis.
Single cell C
4
(SCC
4
) plants, discovered around two decades ago, are promising materials for efforts for genetic engineering of C
4
photosynthesis into C
3
crops. Unlike C
4
plants with Kranz ...anatomy, they exhibit a fully functional C
4
photosynthesis in just a single cell and do not require mesophyll and bundle sheath cell spatial separation.
Bienertia sinuspersici
is one such SCC
4
plant, with NAD-malic enzyme (NAD-ME) subtype C
4
photosynthesis. Its chlorenchyma cell consist of two compartments, peripheral compartment (PC), analogous to mesophyll cell, and central compartment (CC), analogous to bundle sheath cell. Since oxidative stress creates an important constraint for plants under salinity and drought, we comparatively examined the response of enzymatic antioxidant system, H
2
O
2
and TBARS contents, peroxiredoxin Q, NADPH thioredoxin reductase C, and plastid terminal oxidase protein levels of PC chloroplasts (PCC) and CC chloroplasts (CCC). Except for protein levels, these parameters were also examined on the whole leaf level, as well as catalase and NADPH oxidase activities, water status and growth parameters, and levels of C
4
photosynthesis related transcripts. Many C
4
photosynthesis related transcript levels were elevated, especially under drought. Activities of dehydroascorbate reductase and especially peroxidase were elevated under drought in both compartments (CCC and PCC). Even though decreases of antioxidant enzyme activities were more prevalent in PCC, and the examined redox regulating protein levels, especially of peroxiredoxin Q, were elevated in CCC under both stresses, PCC was less damaged by either stress. These suggest PCC is more tolerant and has other means of preventing or alleviating oxidative damage.
The Mediterranean climate is characterized by hot dry summers and frequent droughts. Mediterranean crops are frequently subjected to high evapotranspiration demands, soil water deficits, high ...temperatures, and photo-oxidative stress. These conditions will become more severe due to global warming which poses major challenges to the sustainability of the agricultural sector in Mediterranean countries. Selection of crop varieties adapted to future climatic conditions and more tolerant to extreme climatic events is urgently required. Plant phenotyping is a crucial approach to address these challenges. High-throughput plant phenotyping (HTPP) helps to monitor the performance of improved genotypes and is one of the most effective strategies to improve the sustainability of agricultural production. In spite of the remarkable progress in basic knowledge and technology of plant phenotyping, there are still several practical, financial, and political constraints to implement HTPP approaches in field and controlled conditions across the Mediterranean. The European panorama of phenotyping is heterogeneous and integration of phenotyping data across different scales and translation of “phytotron research” to the field, and from model species to crops, remain major challenges. Moreover, solutions specifically tailored to Mediterranean agriculture (e.g., crops and environmental stresses) are in high demand, as the region is vulnerable to climate change and to desertification processes. The specific phenotyping requirements of Mediterranean crops have not yet been fully identified. The high cost of HTPP infrastructures is a major limiting factor, though the limited availability of skilled personnel may also impair its implementation in Mediterranean countries. We propose that the lack of suitable phenotyping infrastructures is hindering the development of new Mediterranean agricultural varieties and will negatively affect future competitiveness of the agricultural sector. We provide an overview of the heterogeneous panorama of phenotyping within Mediterranean countries, describing the state of the art of agricultural production, breeding initiatives, and phenotyping capabilities in five countries: Italy, Greece, Portugal, Spain, and Turkey. We characterize some of the main impediments for development of plant phenotyping in those countries and identify strategies to overcome barriers and maximize the benefits of phenotyping and modeling approaches to Mediterranean agriculture and related sustainability.
Plant roots exert hydrotropism in response to moisture gradients to avoid drought stress. The regulatory mechanism underlying hydrotropism involves novel regulators such as MIZ1 and GNOM/MIZ2 as well ...as abscisic acid (ABA), reactive oxygen species (ROS), and Ca2+ signaling. ABA, ROS, and Ca2+ signaling are also involved in plant responses to drought stress. Although the mechanism of moisture gradient perception remains largely unknown, the sensory apparatus has been reported to reside in the root elongation zone rather than in the root cap. In Arabidopsis roots, hydrotropism is mediated by the action of MIZ1 and ABA in the cortex of the elongation zone, the accumulation of ROS at the root curvature, and the variation in the cytosolic Ca2+ concentration in the entire root tip including the root cap and stele of the elongation zone. Moreover, root exposure to moisture gradients has been proposed to cause asymmetric ABA distribution or Ca2+ signaling, leading to the induction of the hydrotropic response. A comprehensive and detailed analysis of hydrotropism regulators and their signaling network in relation to the tissues required for their function is apparently crucial for understanding the mechanisms unique to root hydrotropism. Here, referring to studies on plant responses to drought stress, we summarize the recent findings relating to the role of ABA, ROS, and Ca2+ signaling in hydrotropism, discuss their functional sites and plausible networks, and raise some questions that need to be answered in future studies.
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