Showing papers by "Christine H. Foyer published in 2015"

Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance

Abstract: As a consequence of a sessile lifestyle, plants are continuously exposed to changing environmental conditions and often life-threatening stresses caused by exposure to excessive light, extremes of temperature, limiting nutrient or water availability, and pathogen/insect attack. The flexible coordination of plant growth and development is necessary to optimize vigour and fitness in a changing environment through rapid and appropriate responses to such stresses. The concept that reactive oxygen species (ROS) are versatile signalling molecules in plants that contribute to stress acclimation is well established. This review provides an overview of our current knowledge of how ROS production and signalling are integrated with the action of auxin, brassinosteroids, gibberellins, abscisic acid, ethylene, strigolactones, salicylic acid, and jasmonic acid in the coordinate regulation of plant growth and stress tolerance. We consider the local and systemic crosstalk between ROS and hormonal signalling pathways and identify multiple points of reciprocal control, as well as providing insights into the integration nodes that involve Ca(2+)-dependent processes and mitogen-activated protein kinase phosphorylation cascades.

Low glutathione regulates gene expression and the redox potentials of the nucleus and cytosol in Arabidopsis thaliana.

Abstract: Reduced glutathione (GSH) is considered to exert a strong influence on cellular redox homeostasis and to regulate gene expression, but these processes remain poorly characterized. Severe GSH depletion specifically inhibited root meristem development, while low root GSH levels decreased lateral root densities. The redox potential of the nucleus and cytosol of Arabidopsis thaliana roots determined using roGFP probes was between -300 and -320 mV. Growth in the presence of the GSH-synthesis inhibitor buthionine sulfoximine (BSO) increased the nuclear and cytosolic redox potentials to approximately -260 mV. GSH-responsive genes including transcription factors (SPATULA, MYB15, MYB75), proteins involved in cell division, redox regulation (glutaredoxinS17, thioredoxins, ACHT5 and TH8) and auxin signalling (HECATE), were identified in the GSH-deficient root meristemless 1-1 (rml1-1) mutant, and in other GSH-synthesis mutants (rax1-1, cad2-1, pad2-1) as well as in the wild type following the addition of BSO. Inhibition of auxin transport had no effect on organ GSH levels, but exogenous auxin decreased the root GSH pool. We conclude that GSH depletion significantly increases the redox potentials of the nucleus and cytosol, and causes arrest of the cell cycle in roots but not shoots, with accompanying transcript changes linked to altered hormone responses, but not oxidative stress.

Systematic analysis of phloem-feeding insect-induced transcriptional reprogramming in Arabidopsis highlights common features and reveals distinct responses to specialist and generalist insects

Abstract: Phloem-feeding insects (PFIs), of which aphids are the largest group, are major agricultural pests causing extensive damage to crop plants. In contrast to chewing insects, the nature of the plant response to PFIs remains poorly characterized. Scrutiny of the literature concerning transcriptional responses of model and crop plant species to PFIs reveals surprisingly little consensus with respect to the transcripts showing altered abundance following infestation. Nevertheless, core features of the transcriptional response to PFIs can be defined in Arabidopsis thaliana. This comparison of the PFI-associated transcriptional response observed in A. thaliana infested by the generalists Myzus persicae and Bemisia tabaci with the specialist Brevicoryne brassicae highlights the importance of calcium-dependent and receptor kinase-associated signalling. We discuss these findings within the context of the complex cross-talk between the different hormones regulating basal immune response mechanisms in plants. We identify PFI-responsive genes, highlighting the importance of cell wall-associated kinases in plant-PFI interactions, as well as the significant role of kinases containing the domain of unknown function 26. A common feature of plant-PFI interaction is enhanced abundance of transcripts encoding WRKY transcription factors. However, significant divergence was observed with respect to secondary metabolism dependent upon the insect attacker. Transcripts encoding enzymes and proteins associated with glucosinolate metabolism were decreased following attack by the generalist M. persicae but not by the specialist B. brassicae. This analysis provides a comprehensive overview of the molecular patterns associated with the plant response to PFIs and suggests that plants recognize and respond to perturbations in the cell wall occurring during PFI infestation.

Nitrogen deficiency in barley (Hordeum vulgare) seedlings induces molecular and metabolic adjustments that trigger aphid resistance.

Abstract: Agricultural nitrous oxide (N2O) pollution resulting from the use of synthetic fertilizers represents a significant contribution to anthropogenic greenhouse gas emissions, providing a rationale for reduced use of nitrogen (N) fertilizers. Nitrogen limitation results in extensive systems rebalancing that remodels metabolism and defence processes. To analyse the regulation underpinning these responses, barley (Horedeum vulgare) seedlings were grown for 7 d under N-deficient conditions until net photosynthesis was 50% lower than in N-replete controls. Although shoot growth was decreased there was no evidence for the induction of oxidative stress despite lower total concentrations of N-containing antioxidants. Nitrogen-deficient barley leaves were rich in amino acids, sugars and tricarboxylic acid cycle intermediates. In contrast to N-replete leaves one-day-old nymphs of the green peach aphid (Myzus persicae) failed to reach adulthood when transferred to N-deficient barley leaves. Transcripts encoding cell, sugar and nutrient signalling, protein degradation and secondary metabolism were over-represented in N-deficient leaves while those associated with hormone metabolism were similar under both nutrient regimes with the exception of mRNAs encoding proteins involved in auxin metabolism and responses. Significant similarities were observed between the N-limited barley leaf transcriptome and that of aphid-infested Arabidopsis leaves. These findings not only highlight significant similarities between biotic and abiotic stress signalling cascades but also identify potential targets for increasing aphid resistance with implications for the development of sustainable agriculture.

Potential use of phytocystatins in crop improvement, with a particular focus on legumes

Abstract: This work was funded by FP7-PIRSES-GA-2008-230830 (LEGIM) and PIIF-GA-2011- 299347 (Soylife; K.K.). This work was further funded by the International Foundation of Science (IFS grant C/5151-1), the NRF Thuthuka program (B.J.V.) and the NRF Incentive Funding program for rated researchers (K.K.). The funding received from the Genomic Research Institute, University of Pretoria, is hereby also acknowledged. S.G.V.W. thank the NRF/DST in South Africa for bursaries.

High atmospheric carbon dioxide-dependent alleviation of salt stress is linked to RESPIRATORY BURST OXIDASE 1 (RBOH1)-dependent H2O2 production in tomato (Solanum lycopersicum)

Abstract: Plants acclimate rapidly to stressful environmental conditions. Increasing atmospheric CO2 levels are predicted to influence tolerance to stresses such as soil salinity but the mechanisms are poorly understood. To resolve this issue, tomato (Solanum lycopersicum) plants were grown under ambient (380 μmol mol(-1)) or high (760 μmol mol(-1)) CO2 in the absence or presence of sodium chloride (100mM). The higher atmospheric CO2 level induced the expression of RESPIRATORY BURST OXIDASE 1 (SlRBOH1) and enhanced H2O2 accumulation in the vascular cells of roots, stems, leaf petioles, and the leaf apoplast. Plants grown with higher CO2 levels showed improved salt tolerance, together with decreased leaf transpiration rates and lower sodium concentrations in the xylem sap, vascular tissues, and leaves. Silencing SlRBOH1 abolished high CO2 -induced salt tolerance and increased leaf transpiration rates, as well as enhancing Na(+) accumulation in the plants. The higher atmospheric CO2 level increased the abundance of a subset of transcripts involved in Na(+) homeostasis in the controls but not in the SlRBOH1-silenced plants. It is concluded that high atmospheric CO2 concentrations increase salt stress tolerance in an apoplastic H2O2 dependent manner, by suppressing transpiration and hence Na(+) delivery from the roots to the shoots, leading to decreased leaf Na(+) accumulation.

PART OF A SPECIAL ISSUE ON REACTIVE OXYGEN AND NITROGEN SPECIES Spatio-temporal relief from hypoxia and production of reactive oxygen species during bud burst in grapevine (Vitis vinifera)

Abstract: Karlia Meitha, Dennis Konnerup, Timothy D. Colmer, John A. Considine, Christine H. Foyer and Michael J. Considine* School of Plant Biology, and The Institute of Agriculture, The University of Western Australia, Crawley, WA, 6009 Australia, Freshwater Biological Laboratory, Department of Biology, University of Copenhagen, Universitetsparken 4, 2100 Copenhagen, Denmark, Centre for Plant Sciences, University of Leeds, Leeds, Yorkshire LS29JT, UK and Department of Agriculture and Food Western Australia, South Perth, WA, 6151 Australia *For correspondence. E-mail michael.considine@uwa.edu.au

Redox homeostasis: Opening up ascorbate transport.

Abstract: Ascorbate is synthesized in mitochondria but needed in chloroplasts. Identification of a transporter bridging the chloroplast envelope membranes that separate cell cytoplasm from chloroplast stroma reveals a connection between ascorbate transport and cellular redox homeostasis.

Low concentrations of the toxin ophiobolin A lead to an arrest of the cell cycle and alter the intracellular partitioning of glutathione between the nuclei and cytoplasm

Abstract: Ophiobolin A, a tetracyclic sesterpenoid produced by phytopathogenic fungi, is responsible for catastrophic losses in crop yield but its mechanism of action is not understood. The effects of ophiobolin A were therefore investigated on the growth and redox metabolism of Tobacco Bright Yellow-2 (TBY-2) cell cultures by applying concentrations of the toxin that did not promote cell death. At concentrations between 2 and 5 μM, ophiobolin A inhibited growth and proliferation of the TBY-2 cells, which remained viable. Microscopic and cytofluorimetric analyses showed that ophiobolin A treatment caused a rapid decrease in mitotic index, with a lower percentage of the cells at G1 and increased numbers of cells at the S/G2 phases. Cell size was not changed following treatment suggesting that the arrest of cell cycle progression was not the result of a block on cell growth. The characteristic glutathione redox state and the localization of glutathione in the nucleus during cell proliferation were not changed by ophiobolin A. However, subsequent decreases in glutathione and the re-distribution of glutathione between the cytoplasm and nuclei after mitosis occurring in control cells, as well as the profile of glutathionylated proteins, were changed in the presence of the toxin. The profile of poly ADP-ribosylated proteins were also modified by ophiobolin A. Taken together, these data provide evidence of the mechanism of ophiobolin A action as a cell cycle inhibitor and further demonstrate the link between nuclear glutathione and the cell cycle regulation, suggesting that glutathione-dependent redox controls in the nuclei prior to cell division are of pivotal importance.

WHIRLY1 Functions in the Control of Responses to Nitrogen Deficiency But Not Aphid Infestation in Barley

Abstract: WHIRLY1 is largely targeted to plastids, where it is a major constituent of the nucleoids. To explore WHIRLY1 functions in barley, RNAi-knockdown lines (W1-1, W1-7 and W1-9) that have very low levels of HvWHIRLY1 transcripts were characterized in plants grown under optimal and stress conditions. The W1-1, W1-7 and W1-9 plants were phenotypically similar to the wild type but produced fewer tillers and seeds. Photosynthesis rates were similar in all lines but W1-1, W1-7 and W1-9 leaves had significantly more chlorophyll and less sucrose than the wild type. Transcripts encoding specific sub-sets of chloroplast-localised proteins such as ribosomal proteins, subunits of the RNA polymerase and the thylakoid NADH and cytochrome b6/f complexes were much more abundant in the W1-7 leaves than the wild type. While susceptibility of aphid infestation was similar in all lines, the WHIRLY1-deficient plants showed altered responses to nitrogen deficiency maintaining higher photosynthetic CO2 assimilation rates than the wild type under limiting nitrogen. While all lines showed globally similar low nitrogen-dependent changes in transcripts and metabolites, the increased abundance of FAR-RED IMPAIRED RESPONSE1-like transcripts in nitrogen-deficient W1-7 leaves infers that WHIRLY1 has a role in communication between plastid and nuclear genes encoding photosynthetic proteins during abiotic stress.

Mechanisms of plant–insect interaction

Abstract: The study of plant–insect interactions continues to be an exciting and fast-moving field that builds upon the more extensive literature available in plant–microbe interactions and offers new and significant insights into both the unique molecular determinants of plant–insect interactions and the wider ecological context. This special issue of the Journal of Experimental Botany brings together a collection of reviews and original research papers that reflect the breadth and quality of work undertaken in contemporary research into plant–insect interactions.

Metabolic responses to sulfur dioxide in grapevine (Vitis vinifera L.): photosynthetic tissues and berries

Abstract: Research on sulfur metabolism in plants has historically been undertaken within the context of industrial pollution. Resolution of the problem of sulfur pollution has led to sulfur deficiency in many soils. Key questions remain concerning how different plant organs deal with reactive and potentially toxic sulfur metabolites. In this review, we discuss sulfur dioxide/sulfite assimilation in grape berries in relation to gene expression and quality traits, features that remain significant to the food industry. We consider the intrinsic metabolism of sulfite and its consequences for fruit biology and postharvest physiology, comparing the different responses in fruit and leaves. We also highlight inconsistencies in what is considered the “ambient” environmental or industrial exposures to SO2. We discuss these findings in relation to the persistent threat to the table grape industry that intergovernmental agencies will revoke the industry’s exemption to the worldwide ban on the use of SO2 for preservation of fresh foods. Transcriptome profiling studies on fruit suggest that added value may accrue from effects of SO2 fumigation on the expression of genes encoding components involved in processes that underpin traits related to customer satisfaction, particularly in table grapes, where SO2 fumigation may extend for several months.

Unravelling the reactive oxygen and reactive nitrogen signalling networks in plants

Abstract: Plants are the basis of life on earth, generating oxygen from water to replenish the atmospheric oxygen required for aerobic respiration, as well as fixing atmospheric carbon to provide food and fuel that animals and humans need to survive. Photosynthesis is recognized as a key process in the evolution of aerobic life forms that not only allows carbon, oxygen, nitrogen, and other nutrients to move through ecosystems in a predictable manner but also serves as a paradigm for reduction–oxidation (redox) control and the regulated generation of reactive oxygen species (ROS). This type of control is particularly important in plant responses to stressful environmental conditions. Plants are continuously exposed to changing environmental conditions, many of which such as drought, salinity, high and low temperatures, heavy metals, and insect and pathogen attack cause ‘stress’ to the plant, limiting vigour and crop yields, with negative impacts on agronomy, human health and well-being. It is perhaps not surprising, therefore, that they have evolved a complex network of physical, metabolic, and genetic mechanisms that enable them to cope with external threats and challenges, including those imposed by the actions of humans, such as climate change and pollution. Most, if not all, biotic and abiotic stress conditions lead to changes in cellular redox homeostasis with increased ROS production and accumulation, and altered nitric oxide (NO) production and metabolism. ROS are produced by many other metabolic processes in addition to photosynthesis, particularly enzymes that are activated in times of stress to produce superoxide and hydrogen peroxide in a characteristic ‘oxidative burst’. ROS accumulation in such circumstances is often considered to underpin the phenomenon called oxidative stress. Like the gaseous signalling molecule NO, ROS are common intracellular and intercellular messengers with a broad spectrum of regulatory functions in many physiological processes. In his review, Luis A del Rio, a pioneer of ROS chemistry in plants has provided a comprehensive description of the history of research and advances that underpin our current knowledge and understanding of ROS and NO in plants, highlighting the major contributions made by different researchers and scientific groups. ROS and NO play important roles in the toxicity caused by heavy metals and in the metabolic disturbances caused by perturbations in nutritional status. The low-molecular-weight thiol antioxidant, reduced glutathione (GSH), has multiple functions in plants and it is particularly important in plant defences against xenobiotic and heavy metals, as discussed in detail by Hernandez et al. In addition, new evidence supports a role for the respiratory ALTERNATIVE OXIDASE1a in modulating oxidative stress in plants exposed to cadmium (Keunen et al.) and this paper provides new evidence for the crucial role of mitochondria in plant responses to metals. Like mitochondria, chloroplast processes are important in many plant stress responses. The timely review by Hernandez and Munne-Bosch provides novel insights into the role of photo-oxidative stress in the chloroplasts that is associated with phosphorous deficiency. NO and its derivatives, particularly reactive nitrogen species (RNS), interact with ROS and participate in plant responses to biotic and abiotic stresses. Although gene encoding classic nitric oxide synthase (NOS) enzymes exist in plant genomes, NO is produced by both enzymatic and non-enzymatic sources in plants. NO and RNS act together with ROS to regulate a wide range of physiological and developmental processes such as stomatal closure, germination, root development, gravitropism, and programmed cell death (PCD). An interesting example of ROS/NO/RNS that prevents self-fertilization and promotes genetic variability is described in the review by Serrano et al. A timely and up-to-the-minute description of our current knowledge concerning the pathways of ROS signalling, particularly through MAP kinase cascades, and the interplay between ROS and plant hormone signalling pathways is provided in the review by Xia et al. Similarly, a comprehensive account of the extensive network of ROS, NO, and phytohormone interactions in the control of plant development and stress tolerance is provided by Sanz et al. Considerable progress has also been made in our knowledge of the ROS/NO communication that underpins symbiotic interactions between leguminous plants and nitrogen-fixing Rhizobia. The paper by Hichri et al. provides new information on NO signalling during the establishment of this symbiosis, together with the multi-faceted functions of NO in the regulation of symbiotic nitrogen-fixation. In addition, the paper by Matamoros et al. provides exciting new information on the roles of glutathione peroxidases in nodule establishment and function. GSH plays important functions in the nucleus and cytosol during the cell division that underpins the formation of new organs such as nodules. The role of the nuclear GSH pool is described in relation to the action of the cell cycle inhibitor, ophiobolin A, in the paper by Locato et al. In this study, the addition of ophiobolin A, which is a sesterpenoid toxin produced by pathogenic fungi, is shown to cause arrest of the cell cycle at the G2/S phase and to alter the profile of glutathionylated and ADP-ribosylated proteins even though glutathione is retained in the nucleus. The regulated changes in ROS and NO/NRS production and accumulation are associated with wide range of post-translational modifications to proteins including carbonylation, glutathionylation, cysteine oxidation to sulphenic, sulphinic, and sulphonic acids, nitration, and S-nitrosylation, which act as metabolic switches regulating plant responses to environmental changes. These post-translational modifications function as metabolic switches in the cell signalling pathways that underpin plant stress responses. However, excessive cellular oxidation and/or NO accumulation lead to high levels of irreversible protein oxidation, nitration or S-nitrosylation. Correa-Aragunde et al. have provided a comprehensive description of NO-dependent post-transcriptional modifications and their roles in cellular redox homeostasis, with particular focus on the regulation of S-nitrosylation of the enzyme ascorbate oxidase. The importance of cysteine residues in such post-translational modifications is reviewed by Akter et al. and Waszczak et al. They discuss the different oxidized forms of cysteine found in proteins, together with the proteomic approaches that are currently being used to study these modifications. The accumulation of ROS and/or NO in a particular cellular location or at a given time is regulated by a subtle balance between the rates of production and scavenging/processing by antioxidant defences/NO metabolism. The tempo-spatial accumulation of NO and ROS are considered to be important in conferring specificity to the signals underpinning plant responses to a given stimulus. However, the mechanisms by which cellular stress-perception systems regulate the signalling microenvironments and form discrete niches for specific ROS and NO production remain largely unresolved. The review by Sevilla et al. provides a concise overview of our current knowledge of the thioredoxin/peroxiredoxin/sulphiredoxin systems in different cellular compartments and their respective roles in regulating different protein targets, processes that might also underpin cell signalling. Moreover, the paper by Puerto-Galan et al. provides new information on the contribution of NADPH thioredoxin reductase C and the sulphiredoxin to 2-Cys peroxiredoxin overoxidation to chloroplast regulation. The last five years have seen progress that has increased our understanding of the extensive cross-talk between ROS, NO, cellular redox changes, and hormone-mediated pathways. However, many questions remain. For example, even though the level of NO appears to be efficiently regulated in plant cells, little information is available concerning how the different mechanisms of NO production are integrated or how NO is scavenged or processed. Our incomplete knowledge of these systems and their regulation constitute significant bottlenecks to progress. One of the major challenges over the next ten years is to decipher the complexity of ROS and NO functions of biotic and abiotic stress signalling pathways particularly in terms of spatio-temporal regulation. The explosion of research interest and publications observed over the last 25 years in the multifaceted area of redox biology shows no signs of slowing down. Moreover, new avenues of research in this field continue to open, particularly, for example, in topics such as the redox-dependent genetic and epigenetic controls of target genes and the interplay between different post-translational mechanisms of protein regulation.

GSH Partitioning Between the Nucleus and Cytosol in Arabidopsis thaliana

Abstract: The thiol tripeptide, glutathione (GSH) is an essential redox metabolite in plant cells but little information is available concerning GSH partitioning between the cytosol and nucleus. In this article we discuss the evidence concerning the distribution of GSH between the nucleus and the cytosol. The glutathione redox potential was similar in the nucleus and cytosol of developing radicles of Arabidopsis thaliana seeds after germination. However, in the arrested embryonic root meristem of the root meristemless 1 (rml1) mutant that have less than 5 % GSH of the wild type, GSH was predominantly localised in the nuclei. This was also the case in wild type roots treated with the auxin transport inhibitor, N-1-napthylphthalamic acid (NPA), which have decreased root glutathione levels. GSH was co-localised with nuclear DNA at G1 and G2 in A. thaliana cultures in which the cell cycle was synchronised. The functions of GSH are considered in terms of cell cycle regulation and the regulation of gene expression.

PREFACE: PART OF A SPECIAL ISSUE ON REACTIVE OXYGEN AND NITROGEN SPECIES Unravelling how plants benefit from ROS and NO reactions, while resisting oxidative stress

Abstract: � Background and Aims Reactive oxygen species (ROS) and reactive nitrogen species (RNS), such as nitric oxide (NO), play crucial roles in the signal transduction pathways that regulate plant growth, development and defence responses, providing a nexus of reduction/oxidation (redox) control that impacts on nearly every aspect of plant biology. Here we summarize current knowledge and concepts that lay the foundations of a new vision for ROS/RNS functions – particularly through signalling hubs – for the next decade. � Scope Plants have mastered the art of redox control using ROS and RNS as secondary messengers to regulate a diverse range of protein functions through redox-based, post-translational modifications that act as regulators of molecular master-switches. Much current focus concerns the impact of this regulation on local and systemic signalling pathways, as well as understanding how such reactive molecules can be effectively used in the control of plant growth and stress responses. � Conclusions The spectre of oxidative stress still overshadows much of our current philosophy and understanding of ROS and RNS functions. While many questions remain to be addressed – for example regarding inter-organellar regulation and communication, the control of hypoxia and how ROS/RNS signalling is used in plant cells, not only to trigger acclimation responses but also to create molecular memories of stress – it is clear that ROS and RNS function as vital signals of living cells.