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Mittler, R.

Publications and source records attributed to Mittler, R..

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GABA plays a key role in plant acclimation to a combination of high light and heat stress

Plants are frequently subjected to different combinations of abiotic stresses, such as high light intensity and elevated temperatures. These environmental conditions pose an important threat to agriculture production, affecting photosynthesis and decreasing yield. Metabolic responses of plants, such as alterations in carbohydrates and amino acid fluxes, play a key role in the successful acclimation of plants to different abiotic stresses, directing resources towards stress responses and suppressing growth. Here we show that the primary metabolic response of Arabidopsis thaliana plants to high light or heat stress is different than that of plants subjected to a combination of high light and heat stress. We further demonstrate that a combination of high light and heat stress results in a unique metabolic response that includes increased accumulation of sugars and amino acids, coupled with decreased levels of metabolites participating in the tricarboxylic acid (TCA) cycle. Among the amino acids exclusively accumulated during a combination of high light and heat stress, we identified the non-proteinogenic amino acid {gamma}-aminobutyric acid (GABA). Analysis of different mutants deficient in GABA biosynthesis, in particular two independent alleles of glutamate decarboxylase 3 (gad3), reveal that GABA plays a key role in the acclimation of plants to a combination of high light and heat stress. Taken together, our findings identify a new role for GABA in regulating plant responses to stress combination. One sentence summaryThe non-proteinogenic amino acid {gamma}-aminobutyric acid (GABA) is required for plant acclimation to a combination of high light and heat stress in Arabidopsis.

plant biology

Integration of electric, calcium, reactive oxygen species and hydraulic signals during rapid systemic signaling in plants

The sensing of abiotic stress, mechanical injury, or pathogen attack by a single plant tissue results in the activation of systemic signals that travel from the affected tissue to the entire plant, alerting it of an impending stress or pathogen attack. This process is essential for plant survival during stress and is termed systemic signaling. Among the different signals triggered during this process are calcium, electric, reactive oxygen species (ROS) and hydraulic signals. These are thought to propagate at rapid rates through the plant vascular bundles and to regulate many of the systemic processes essential for plant survival. Although the different signals activated during systemic signaling are thought to be interlinked, their coordination and hierarchy remain to be determined. Here, using a combination of advanced whole-plant imaging and hydraulic pressure measurements, we studied the activation of all four systemic signals in wild type and different Arabidopsis thaliana mutants subjected to a local high light (HL) stress or wounding. Our findings reveal that in response to wounding systemic changes in membrane potential, calcium, ROS, and hydraulic pressure are coordinated by glutamate receptor-like (GLR) proteins 3.3 and 3.6, while in response to HL the respiratory burst oxidase homolog D-driven systemic ROS signal could be separated from systemic changes in membrane potential and calcium levels. We further determine that plasmodesmata functions are required for systemic changes in membrane potential, calcium, and ROS during systemic signaling. Our findings shed new light on the different mechanisms that integrate different systemic signals in plants during stress. Significance statementThe ability of plants to transmit a signal from a stressed or wounded tissue to the entire plant, termed systemic signaling, is key to plant survival during conditions of environmental stress. At least four different systemic signals are thought to be involved in this process: electric, calcium, reactive oxygen and hydraulic. However, how are they coordinated and whether they can be stress-specific is mostly unknown. Here we report that different types of stimuli can induce different types of systemic signals that may or may not be linked with each other. We further reveal that hydraulic waves can be actively regulated in plants in response to wounding, and that proteins that regulate plasmodesmata pores play a key role in systemic signaling.

plant biology

Mesophyll cells mediate systemic reactive oxygen signaling during wounding or heat stress

Sensing of heat, high light (HL), or mechanical injury by a single leaf of a plant results in the activation of different systemic signals that reach systemic tissues within minutes and trigger systemic acquired acclimation (SAA) or systemic wound responses (SWRs), resulting in a heightened state of stress readiness of the entire plant. Among the different signals associated with rapid systemic responses to stress in plants are electric, calcium and reactive oxygen species (ROS) waves. These signals propagate from the stressed or injured leaf to the rest of the plant through the plant vascular bundles, and trigger SWRs and SAA in systemic tissues. However, whether they can propagate through other cell types, and whether or not they are interlinked, remain open questions. Here we report that in response to wounding or heat stress (HS), but not HL stress, the ROS wave can propagate through mesophyll cells of Arabidopsis thaliana. Moreover, we show that propagation of the ROS wave through mesophyll cells during these stresses is sufficient to restore SWR and SAA transcript accumulation in systemic leaves, as well as SAA to HS (but not HL). We further show that propagation of the ROS wave through mesophyll cells could contribute to systemic signal integration during HL&HS stress combination. Our findings reveal that the ROS wave can propagate through tissues other than the vascular bundles of plants, and that different stresses can trigger different types of systemic signals that propagate through different cell layers and induce stress-specific systemic responses. One-sentence summaryIn addition to vascular bundles, mesophyll cells can mediate the ROS wave during systemic responses to wounding or heat stress in Arabidopsis.

plant biology

The impact of multifactorial stress combination on plant growth and survival

O_LIClimate change-driven extreme weather events, combined with increasing temperatures, harsh soil conditions, low water availability and quality, and the introduction of many man-made pollutants, pose a unique challenge to plants. Although our knowledge of the response of plants to each of these individual conditions is vast, we know very little about how a combination of many of these factors, occurring simultaneously, i.e., multifactorial stress combination, impacts plants. C_LIO_LISeedlings of wild type and different mutants of Arabidopsis thaliana plants were subjected to a multifactorial stress combination of six different stresses, each applied at a low level, and their survival, physiological and molecular responses determined. C_LIO_LIOur findings reveal that while each of the different stresses, applied individually, had a negligible effect on plant growth and survival, the accumulated impact of multifactorial stress combination on plants was detrimental. We further show that the response of plants to multifactorial stress combination is unique and that specific pathways and processes play a critical role in the acclimation of plants to multifactorial stress combination. C_LIO_LITaken together our findings reveal that further polluting our environment could result in higher complexities of multifactorial stress combinations that in turn could drive a critical decline in plant growth and survival. C_LI Plain Language SummaryThe effects of multiple stress conditions occurring simultaneously, i.e., multifactorial stress combination, on plants is currently unknown. Here we show that different co-occurring stresses can interact to negatively impact plant growth and survival, even if the effect of each individual stress is negligible. We further identify several key pathways essential for plant acclimation to multifactorial stress combination.

plant biology

A systemic whole-plant change in redox levels accompanies the rapid systemic response of Arabidopsis to wounding

Reactive oxygen species (ROS) play a key role in regulating plant responses to different abiotic stresses, wounding and pathogen attack. In addition to triggering responses at the tissues directly subjected to stress, ROS were recently shown to mediate a rapid whole-plant systemic signal, termed the "ROS wave", required for inducing a state of systemic acquired acclimation, or systemic wound response. However, whether the ROS wave that spreads from the local tissues subjected to wounding to the rest of the plant triggers alterations in redox levels, is mostly unknown at present. Here, using a genetically-encoded reporter for cellular glutathione redox changes, roGFP1, we show that the wounding-induced systemic ROS wave in Arabidopsis thaliana is accompanied by a rapid systemic wave of cytosolic redox oxidation, termed a "redox wave". The ROS wave may therefore trigger changes in redox levels in systemic leaves that in turn can trigger transcriptional, metabolic and proteomic changes resulting in acclimation and/or systemic wound responses. One sentence summaryThe wounding-induced reactive oxygen species (ROS) wave is accompanied by a systemic whole-plant redox response.

plant biology

Plasmodesmata-localized proteins and reactive oxygen species orchestrate light-induced rapid systemic signaling in Arabidopsis

Systemic signaling and systemic acquired acclimation (SAA) are key to the survival of plants during episodes of abiotic stress. These processes depend on a continuous chain of cell-to-cell signaling events that extends from the initial tissue that senses the stress (local tissue) to the entire plant (systemic tissues). Among the different systemic signaling molecules and processes thought to be involved in this cell-to-cell signaling mechanism are reactive oxygen species (ROS), calcium, electric and hydraulic signals. How these different signals and processes are interlinked, and how they transmit the systemic signal all the way from the local tissue to the entire plant, remain however largely unknown. Here, studying the systemic response of Arabidopsis thaliana to a local treatment of excess light stress, we report that respiratory burst oxidase homolog D (RBOHD)-generated ROS enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of systemic signals during responses to light stress. We further identify aquaporins, and several different calcium-permeable channels, belonging to the glutamate receptor-like, mechanosensitive small conductance-like, and cyclic nucleotide-gated families, as involved in this process, but determine that their function is primarily required for the maintenance of the signal in each cell along the path of the systemic signal, as well as for the establishment of acclimation at the local and systemic tissues. PD and RBOHD-generated ROS orchestrate therefore light stress-induced rapid cell-to-cell spread of systemic signals in Arabidopsis. One-sentence summaryRespiratory burst oxidase homolog D-generated reactive oxygen species enhance cell-to-cell transport and plasmodesmata (PD) pore size in a process that depends on the function of the PD-localized proteins (PDLPs) 1 and 5, promoting the cell-to-cell transport of rapid systemic signals during the response of Arabidopsis to excess light stress.

plant biology

The impact of water deficit and heat stress combination on the molecular response, physiology and seed production of soybean

A combination of drought and heat stress, occurring at the vegetative or reproductive growth phase of many different crops, can have a devastating impact on yield. In soybean (Glycine max), a considerable effort has been made to develop genotypes with enhanced yield production under conditions of drought or heat stress. However, how these genotypes perform in terms of growth, physiological responses and most importantly seed production, under conditions of drought and heat combination is mostly unknown. Here, we studied the impact of water deficit and heat stress combination on the physiology, seed production and yield per plant of two soybean genotypes, Magellan and Plant Introduction (PI) 548313, that differ in their reproductive responses to heat stress. Our findings reveal that although PI 548313 produced more seeds than Magellan under conditions of heat stress, under conditions of water deficit and heat stress combination its seed production decreased. Because number of flowers and pollen germination of PI 548313 remained high under heat or water deficit and heat combination, the reduced seed production exhibited by PI 548313 under the stress combination could be a result of processes that occur at the stigma, ovaries and/or other parts of the flower following pollen germination. HighlightTolerance to heat stress was found not to confer tolerance to a combination of water deficit and heat stress in soybean, highlighting the need for breeding strategies targeting the stress combination.

plant biology

Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species

Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or oxidative stress. Cadmium (Cd) is a non-essential heavy metal that induces both Fe-deficiency and oxidative stress; however, the mechanisms underlying these Cd-induced responses are still elusive. Here we explored Cd-induced Fe-associated responses in wildtype Arabidopsis and opt3-2, a mutant that over-accumulates Fe. Gene expression profiling revealed a large overlap between transcripts induced by Fe-deficiency and Cd exposure in wildtype plants and the opt3 mutant. Interestingly, vascular-localized Fe-responsive genes were found to be highly induced by Cd even in the presence of high Fe and H2O2 levels, suggesting that Cd impairs Fe sensing. It was recently shown that Fe-S cluster-containing proteins AtNEET, play a role in Fe sensing. Our data shows that Cd negatively impacts both the stability and Fe-S transfer activity of AtNEET. Altogether, our data indicate that Fe-deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe-deficiency responses prevents the induction of specific gene networks when Fe and H2O2 levels are high. Other Cd/Fe-responsive genes however, are insensitive to this negative feedback regulation suggesting that their induction is the result of an impaired Fe sensing as opposed to the traditional view of Cd/Fe uptake competition at the root level.Highlight Cadmium induces an iron-deficiency response often explained by root uptake competition; here we show that Cd also impairs Fe sensing in leaves, even when Fe is in sufficient quantities.Competing Interest StatementThe authors have declared no competing interest.View Full Text

plant biology