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Zandalinas, S. I.

Publications and source records attributed to Zandalinas, S. I..

13 recordsLinked to original sources

Identification of a putative RBOHD-FERONIA-CRK10-PIP2;6 plasma membrane complex that interacts with phyB to regulate ROS production in Arabidopsis thaliana

O_LIReactive oxygen species (ROS) regulate plant growth, development, and responses to the environment. ROS production by the RESPIRATORY BURST OXIDASE PROTEIN D (RBOHD) protein was recently shown to be regulated by PHYTOCHROME B (phyB), and phyB was found to be phosphorylated by FERONIA, highlighting the possibility that these three proteins interact to regulate ROS levels during stress. C_LIO_LIImmunoprecipitation and proximity labelling, followed by split-luciferase and functional validation assays, were used to study the interactions between FERONIA, phyB, and RBOHD during excess light (EL) stress in Arabidopsis thaliana. C_LIO_LIWe reveal that phyB and FERONIA interact with RBOHD, that phosphorylation of phyB by FERONIA, as well as the kinase activity of FERONIA, are required for RBOHD-driven ROS production in response to EL stress, and that CYSTEINE-RICH RECEPTOR LIKE KINASE 10 (CRK10) and PLASMA MEMBRANE INTRINSIC PROTEIN 2;6 (PIP2;6) interact with RBOHD and phyB and are also required for EL-driven RBOHD ROS production. C_LIO_LIOur findings uncover the existence of a putative plasma membrane complex between FERONIA, RBOHD, CRK10, and PIP2;6 that interacts with phyB to regulate ROS production in Arabidopsis in response to stress. This complex could play a canonical role in the integration and regulation of multiple signaling pathways in plants. C_LI Plain Language SummaryWe identified a complex between several different proteins at the plasma membrane that interacts with the light and temperature receptor protein phytochrome B to regulate reactive oxygen species formation during stress in plants. This complex could be involved in the regulation and integration of multiple abiotic and biotic signals in plants. tenten

plant biology↗

Enhanced cell aggregation in the Chlamydomonas reinhardtii rbo1 mutant in response to multifactorial stress combination

Global change factors associated with climate change and increased pollution are subjecting plants, microbes, and different ecosystems to conditions of multifactorial stress combination (MFSC). While recent studies centered on the effects of MFSC on different plants and ecosystems, much less is known about how these conditions impact unicellular organisms. Here, we report on the physiological and proteomic responses of wild type and respiratory burst oxidase homolog 1 (rbo1) mutant cells of Chlamydomonas reinhardtii to a MFSC of 5 different abiotic stresses. While several similarities were found between plant and C. reinhardtii responses to MFSC, our work revealed that MFSC induces aggregation in the unicellular organism C. reinhardtii. We further show that MFSC induced aggregation is enhanced in the rbo1 mutant and can be triggered by H2O2. As aggregation typically leads to reduced growth, respiration and/or photosynthesis, enhanced aggregation of unicellular organisms in different ecosystems subjected to MFSC could explain part of the negative impacts of MFSC on the services they provide. Our findings shed new light on the response of unicellular organisms to MFSC and suggest that one of the main drivers leading to multicellularity during evolution was early conditions of MFSC under an oxygenated environment.

plant biology↗

bHLH35 mediates specificity in plant responses to multiple stress conditions

How biological systems respond to stress is a fundamental question in biology, primarily addressed using the reductionist approach of applying one stress condition at a time. In nature, however, organisms experience a multitude of stresses, simultaneously or sequentially, questioning the validity of the reductionist approach for predicting plant responses to stress under natural conditions. Here, we reveal that in the flowering plant Arabidopsis thaliana, the transcriptional regulator bHLH35 is required for plant survival under a specific set of stress conditions that includes a combination of salinity, excess light, and heat, occurring simultaneously (but not for each of these stresses applied individually or in any other combination). Under these conditions, bHLH35 interacts with NAC069 and binds the promoter of LBD31, also specifically required for survival under the 3-stress combination. Our findings uncover a high degree of specificity in the response of organisms to stress, a specificity that would not have been revealed using the reductionist approach, and one that should be taken into consideration when developing agronomically important crops with heightened resilience to climate change.

plant biology↗

Transcriptomic and physiological responses of soybean plants subjected to a combination of water deficit and heat stress under field conditions

Water deficit, heat stress, and a combination of water deficit and heat stress are highly disruptive to crop yield worldwide. Unfortunately, the frequency and intensity of these conditions is gradually increasing due to climate change. Previous studies of water deficit and heat stress combination were primarily conducted under controlled growth conditions, revealing that the combination of water deficit and heat stress resulted in the activation of unique stress responses and acclimation pathways. However, whether similar responses to stress combination occur in the field remained largely unknown. Here we report on a two-year field study in which the transcriptomic and physiological responses of vegetative and reproductive tissues of soybean (Glycine max) to water deficit, heat treatment and their combination were studied. Our findings reveal that the transcriptomic responses of soybeans grown in the field are different from those grown under controlled growth chamber conditions. These differences were especially noticeable in plants subjected to the heat or water deficit treatments, and less in plants subjected to the stress combination. In addition, we report that differential transpiration between leaves and pods, that was originally discovered in plants grown under controlled growth conditions, occurs in field grown soybeans in response to heat stress, as well as heat stress combined with water deficit. We hope that the transcriptomic datasets generated by our study will contribute to future studies of crop responses to different stresses in the field, as well as highlight the need for more omics studies of plants grown under field conditions.

plant biology↗

Integrative analysis of plant responses to a combination of water deficit, heat stress and eCO2 reveals a role for OST1 and SLAH3 in regulating stomatal responses

The frequency, intensity and duration of global change factors and/or environmental stressors, such as droughts, heat waves, floods, and pollution, are increasing due to anthropogenic activities, subjecting plants to compound conditions of Global Change Factor combination (GCFc), or stress combination. These can have contrasting or additive effects on plant physiological performance and impact different ecosystems and agro-ecosystems worldwide. Using an integrative physiological, genetic, hormonal, and transcriptomic analysis, we studied the response of Arabidopsis thaliana (L.) Heynh to a combination of water deficit (WD), heat stress (HS) and/or elevated levels of CO2 (eCO2). Our findings reveal high specificity in plant responses to GCFc. We further reveal that stomatal aperture regulation under conditions of GCFc is controlled by a blend of unique and shared regulators, that together determine the specific aperture size under each different set of GCFc conditions. Under a combination of WD, HS, and eCO2 (WD+HS+eCO2), for example, stomatal closure required the function of nitric oxide, OPEN STOMATA 1 and the S-type anion channel SLAH3, but not the S-type anion channel SLAC1, or many other regulators typically found to control stomatal aperture under less complex conditions, including HS+WD. Our findings highlight the complexity of plant physiological and molecular responses to conditions of stress combination and open the way for future studies of plant responses to stress combination, crucial to our understanding of how GCFc impacts different ecosystems and agro-ecosystems worldwide. In addition, our study provides an initial definition for a stomatal hierarchical stress code that could apply to future studies.

plant biology↗

Integrative phenotypic-transcriptomic analysis of soybean plants subjected to multifactorial stress combination

Global warming, climate change, and industrial pollution are altering our environment subjecting crops to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. Recent studies revealed that a combination of 3 or more stresses simultaneously impacting a plant (termed multifactorial stress combination; MFSC) can cause a drastic decline in plant growth and survival, even if the level of each stress involved in the MFSC has a negligible effect on plants. However, the impacts of MFSC on crops are largely unknown. We subjected soybean plants to a MFSC of up to five different stresses (water deficit, salinity, low phosphate, acidity, and cadmium), in an increasing level of complexity, and conducted integrative transcriptomic-phenotypic analysis of reproductive and vegetative tissues. We reveal that MFSC has a negative cumulative effect on soybean yield, that each set of MFSC condition elicits a unique transcriptomic response (that is different between flowers and leaves), and that selected genes expressed in leaves or flowers are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. We further reveal that the transcriptomic response of soybean and Arabidopsis to MFSC shares common features associated with reactive oxygen and iron/copper signaling/metabolism. Our study provides unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.

plant biology↗

The transcriptome of soybean reproductive tissues subjected to water deficit, heat stress, and a combination of water deficit and heat stress.

Global warming and climate change are driving an alarming increase in the frequency and intensity of extreme climate events, such as droughts, heat waves, and their combination, inflicting heavy losses to agricultural production. Recent studies revealed that the transcriptomic responses of different crops to water deficit (WD) or heat stress (HS) is very different from that to a combination of WD+HS. In addition, it was found that the effects of WD, HS, and WD+HS are significantly more devastating when these stresses occur during the reproductive growth phase of crops, compared to vegetative growth. As the molecular responses of different reproductive and vegetative tissues of plants to WD, HS, or WD+HS could be different from each other, and these differences could impact many current and future breeding and/or engineering attempts to enhance the resilience of crops to climate change, we conducted a transcriptomic analysis of different soybean (Glycine max) tissues to WD, HS, and WD+HS. Here we present a reference transcriptomic dataset that includes the response of soybean leaf, pod, anther, stigma, ovary, and sepal to WD, HS, and WD+HS conditions. Mining this data set for the expression pattern of different stress-response transcripts revealed that each tissue had a unique transcriptomic response to each of the different stress conditions. This finding is important as it suggests that attempting to enhance the overall resilience of crops to climate change could require a coordinated approach that simultaneously alters the expression of different groups of transcripts in different tissues in a stress-specific manner. SIGNIFICANCE STATEMENTA reference transcriptomic dataset of different reproductive tissues of soybean subjected to water deficit, heat stress, and their combination, generated by this study, reveals that different tissues display different responses to these stress conditions. Attempting to enhance the resilience of crops to different stress combinations, associated with climate change, might therefore require simultaneously altering the expression of different sets of transcripts in different tissues in a coordinated and stress-specific manner.

plant biology↗

The effects of multifactorial stress combination on rice and maize

The complexity of environmental factors affecting plants is gradually increasing due to global warming, an increase in the number and intensity of climate change-driven weather events, such as droughts, heat waves, and floods, and the accumulation of different pollutants. The impact of multiple stress conditions on plants was recently termed multifactorial stress combination (MFSC) and defined as the occurrence of three or more stressors that impact plants simultaneously or sequentially. We recently reported that with the increased number and complexity of different stressors, the growth and survival of Arabidopsis thaliana seedlings declines; even if the level of each individual stress is low enough to have no significant effect on plants. This finding is alarming since it reveals that MFSCs of different low-level stressors could impact crops and cause a dramatic reduction in overall growth. However, whether MFSC would impact commercial crop cultivars has not been studied. Here, we reveal that a MFSC of 5 different low level abiotic stresses (salinity, heat, the herbicide paraquat, phosphorus deficiency, and the heavy metal cadmium), applied in an increasing level of complexity, has a significant negative impact on the growth and biomass of a commercial rice (Oryza sativa) cultivar and a maize (Zea mays) hybrid. We further report on the first proteomics analysis of MFSC in plants that identified over 300 proteins common to all 4- and 5-MFSCs. Taken together our findings reveal that the impacts of MFSC on two different crop species are severe, and that MFSC may significantly affect agricultural productivity.

plant biology↗

Differential transpiration between pods and leaves during stress combination in soybean

Climate change is causing an increase in the frequency and intensity of droughts, heat waves, and their combinations, diminishing agricultural productivity and destabilizing societies worldwide. We recently reported that during a combination of water deficit (WD) and heat stress (HS) stomata on leaves of soybean plants are closed, while stomata on flowers are open. This unique stomatal response was accompanied by differential transpiration (higher in flowers, while lower in leaves) that cooled flowers during a combination of WD+HS. Here we reveal that developing pods of soybean plants subjected to a combination of WD+HS use a similar acclimation strategy of differential transpiration to reduce internal pod temperature by about 4{degrees}C. We further show that enhanced expression of transcripts involved in abscisic acid degradation accompanies this response, and that preventing pod transpiration by sealing stomata causes a significant increase in internal pod temperature. Using an RNA-Seq analysis of pods developing on plants subjected to WD+HS, we also show that the response of pods to WD, HS, or WD+HS is distinct from that of leaves or flowers. Interestingly, we report that although flower, pod and seed numbers per plant are decreased under conditions of WD+HS, seed mass of plants subjected to WD+HS is larger than that of plants subjected to HS, and number of seeds with suppressed/aborted development is lower in WD+HS compared to HS. Taken together our findings reveal that differential transpiration occurs in pods of soybean plants subjected to WD+HS and that this process limits heat-induced damage to seed production. One sentence summaryDifferential transpiration between pods and leaves of soybean plants subjected to a combination of water deficit and heat stress buffers internal pod temperature.

plant biology↗

The cluster transfer function of AtNEET supports the ferredoxin-thioredoxin network of plant cells

NEET proteins are conserved 2Fe-2S proteins that regulate the levels of iron and reactive oxygen species in plant and mammalian cells. Previous studies of seedlings with constitutive expression of AtNEET, or its dominant-negative variant H89C (impaired in 2Fe-2S cluster transfer), revealed that disrupting AtNEET function causes oxidative stress, chloroplast iron overload, activation of iron-deficiency responses, and cell death. Because disrupting AtNEET function is deleterious to plants, we developed an inducible expression system to study AtNEET function in mature plants using a time-course proteomics approach. Here, we report that suppression of AtNEET cluster transfer function results in drastic changes in the expression of different members of the ferredoxin (Fd), Fd-thioredoxin (TRX) reductase (FTR), and TRX network of Arabidopsis, as well as in cytosolic cluster assembly proteins. In addition, the expression of Yellow Stripe-Like 6 (YSL6), involved in iron export from chloroplasts was elevated. Taken together, our findings reveal new roles for AtNEET in supporting the Fd-TFR-TRX network of plants, iron mobilization from the chloroplast, and cytosolic 2Fe-2S cluster assembly. In addition, we show that AtNEET function is linked to the expression of glutathione peroxidases (GPXs) which play a key role in the regulation of ferroptosis and redox balance in different organisms. HighlightUsing proteomics analysis and an inducible expression system, the iron-sulfur cluster transfer function of AtNEET was found to support the ferredoxin-thioredoxin network of Arabidopsis.

plant biology↗

HPCA1 is required for systemic ROS and calcium cell-to-cell signaling and plant acclimation to stress

As multicellular organisms, plants constantly balance and coordinate many metabolic, physiological, and molecular responses between different cell types and tissues. This process is essential for plant development, growth, and response to different environmental cues. Because plants lack a nervous system, they transmit different signals over long distances via cell-to-cell signaling. Recent studies revealed that reactive oxygen species (ROS), produced by respiratory burst oxidase homologs (RBOHs) at the apoplast play a key role in cell-to-cell signaling. A state of enhanced ROS production by one cell is thereby sensed by a neighboring cell, causing it to produce ROS, creating a continuous chain of cell-to-cell ROS accumulation termed the ROS wave. This process was found to mediate systemic signals throughout the plant and is required for plant acclimation to different stresses. Although RBOHs were found to produce ROS essential for this process, the identity of the receptor(s) perceiving the apoplastic ROS signal is currently unknow. Here we reveal that the leucine-rich-repeat receptor-like kinase HPCA1 (H2O2-induced Ca2+ increases 1) acts as a central ROS receptor required for the propagation of cell-to-cell ROS signals, systemic signaling in response to different biotic and abiotic stresses, and plant acclimation to stress. We further report that HPCA1 is required for systemic calcium signals, but not systemic membrane depolarization responses, and identify key calcium-dependent signal transduction proteins involved in this process. Our findings reveal that HPCA1 plays a key role in mediating and coordinating systemic cell-to-cell ROS and calcium signals that are required for plant acclimation to stress.

plant biology↗

Differential regulation of flower transpiration during abiotic stress in plants

Heat waves, occurring during droughts, can have a devastating impact on yield, especially if they happen during the flowering and seed set stages of the crop cycle. Global warming and climate change are driving an alarming increase in the frequency and intensity of combined drought and heat stress episodes, critically threatening global food security. Previous studies revealed that during a combination of drought and heat stress stomata on leaves of many plants are closed, preventing cooling by transpiration. Because high temperature is detrimental to reproductive processes, essential for plant yield, we measured the inner temperature, transpiration, and sepal stomatal aperture of closed soybean flowers, developing on plants subjected to a combination of drought and heat stress. Here, we report that during a combination of drought and heat stress soybean plants prioritize transpiration through flowers over transpiration through leaves by opening their flower stomata, while keeping their leaf stomata closed. This acclimation strategy, termed differential transpiration, lowers flower inner temperature by about 2-3{degrees}C, protecting reproductive processes at the expense of vegetative tissues. Manipulating stomatal regulation, stomatal size and/or stomatal density of flowers could therefore serve as a viable strategy to enhance the yield of different crops and mitigate some of the current and future impacts of global warming and climate change on agriculture. One sentence summaryDuring stress conditions that result in higher flower inner temperature plants use a differential transpiration strategy to protect reproductive processes at the expense of vegetative tissues.

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↗