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1. Systemic signaling during abiotic stress combination in plants

   https://doi.org/10.1073/pnas.2005077117  

   Zandalinas, Sara I.; Fichman, Yosef; Devireddy, Amith R.; Sengupta, Soham; Azad, Rajeev K.; Mittler, Ron (June 2020, Proceedings of the National Academy of Sciences)

   null (Ed.)

   Extreme environmental conditions, such as heat, salinity, and decreased water availability, can have a devastating impact on plant growth and productivity, potentially resulting in the collapse of entire ecosystems. Stress-induced systemic signaling and systemic acquired acclimation play canonical roles in plant survival during episodes of environmental stress. Recent studies revealed that in response to a single abiotic stress, applied to a single leaf, plants mount a comprehensive stress-specific systemic response that includes the accumulation of many different stress-specific transcripts and metabolites, as well as a coordinated stress-specific whole-plant stomatal response. However, in nature plants are routinely subjected to a combination of two or more different abiotic stresses, each potentially triggering its own stress-specific systemic response, highlighting a new fundamental question in plant biology: are plants capable of integrating two different systemic signals simultaneously generated during conditions of stress combination? Here we show that plants can integrate two different systemic signals simultaneously generated during stress combination, and that the manner in which plants sense the different stresses that trigger these signals (i.e., at the same or different parts of the plant) makes a significant difference in how fast and efficient they induce systemic reactive oxygen species (ROS) signals; transcriptomic, hormonal, and stomatal responses; as well as plant acclimation. Our results shed light on how plants acclimate to their environment and survive a combination of different abiotic stresses. In addition, they highlight a key role for systemic ROS signals in coordinating the response of different leaves to stress. 

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2. Leaf isoprene emission as a trait that mediates the growth-defense tradeoff in the face of climate stress

   https://doi.org/10.1007/s00442-020-04813-7  

   Monson, Russell K.; Weraduwage, Sarathi M.; Rosenkranz, Maaria; Schnitzler, Jörg-Peter; Sharkey, Thomas D. (November 2020, Oecologia)

   null (Ed.)

   Plant isoprene emissions are known to contribute to abiotic stress tolerance, especially during episodes of high temperature and drought, and during cellular oxidative stress. Recent studies have shown that genetic transformations to add or remove isoprene emissions cause a cascade of cellular modifications that include known signaling pathways, and interact to remodel adaptive growth-defense tradeoffs. The most compelling evidence for isoprene signaling is found in the shikimate and phenylpropanoid pathways, which produce salicylic acid, alkaloids, tannins, anthocyanins, flavonols and other flavonoids; all of which have roles in stress tolerance and plant defense. Isoprene also influences key gene expression patterns in the terpenoid biosynthetic pathways, and the jasmonic acid, gibberellic acid and cytokinin signaling networks that have important roles in controlling inducible defense responses and influencing plant growth and development, particularly following defoliation. In this synthesis paper, using past studies of transgenic poplar, tobacco and Arabidopsis, we present the evidence for isoprene acting as a metabolite that coordinates aspects of cellular signaling, resulting in enhanced chemical defense during periods of climate stress, while minimizing costs to growth. This perspective represents a major shift in our thinking away from direct effects of isoprene, for example, by changing membrane properties or quenching ROS, to indirect effects, through changes in gene expression and protein abundances. Recognition of isoprene’s role in the growth-defense tradeoff provides new perspectives on evolution of the trait, its contribution to plant adaptation and resilience, and the ecological niches in which it is most effective. 

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3. Subcellular dynamics of ethylene signaling drive plant plasticity to growth and stress: Spatiotemporal control of ethylene signaling in Arabidopsis

   https://doi.org/10.1002/bies.202400043  

   Chien, Yuan‐Chi; Yoon, Gyeong_Mee (April 2024, BioEssays)

   Abstract Volatile compounds, such as nitric oxide and ethylene gas, play a vital role as signaling molecules in organisms. Ethylene is a plant hormone that regulates a wide range of plant growth, development, and responses to stress and is perceived by a family of ethylene receptors that localize in the endoplasmic reticulum. Constitutive Triple Response 1 (CTR1), a Raf‐like protein kinase and a key negative regulator for ethylene responses, tethers to the ethylene receptors, but undergoes nuclear translocation upon activation of ethylene signaling. This ER‐to‐nucleus trafficking transforms CTR1 into a positive regulator for ethylene responses, significantly enhancing stress resilience to drought and salinity. The nuclear trafficking of CTR1 demonstrates that the spatiotemporal control of ethylene signaling is essential for stress adaptation. Understanding the mechanisms governing the spatiotemporal control of ethylene signaling elements is crucial for unraveling the system‐level regulatory mechanisms that collectively fine‐tune ethylene responses to optimize plant growth, development, and stress adaptation. 

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4. Intensive leaf cooling promotes tree survival during a record heatwave

   https://doi.org/10.1073/pnas.2408583121  

   Posch, Bradley C; Bush, Susan E; Koepke, Dan F; Schuessler, Alexandra; Anderegg, Leander LD; Aparecido, Luiza MT; Blonder, Benjamin W; Guo, Jessica S; Kerr, Kelly L; Moran, Madeline E; et al (October 2024, Proceedings of the National Academy of Sciences)

   Increasing heatwaves are threatening forest ecosystems globally. Leaf thermal regulation and tolerance are important for plant survival during heatwaves, though the interaction between these processes and water availability is unclear. Genotypes of the widely distributed foundation tree speciesPopulus fremontiiwere studied in a controlled common garden during a record summer heatwave—where air temperature exceeded 48 °C. When water was not limiting, all genotypes cooled leaves 2 to 5 °C below air temperatures. Homeothermic cooling was disrupted for weeks following a 72-h reduction in soil water, resulting in leaf temperatures rising 3 °C above air temperature and 1.3 °C above leaf thresholds for physiological damage, despite the water stress having little effect on leaf water potentials. Tradeoffs between leaf thermal safety and hydraulic safety emerged but, regardless of water use strategy, all genotypes experienced significant leaf mortality following water stress. Genotypes from warmer climates showed greater leaf cooling and less leaf mortality after water stress in comparison with genotypes from cooler climates. These results illustrate how brief soil water limitation disrupts leaf thermal regulation and potentially compromises plant survival during extreme heatwaves, thus providing insight into future scenarios in which ecosystems will be challenged with extreme heat and unreliable soil water access. 

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5. Coordinated resource allocation to plant growth–defense tradeoffs

   https://doi.org/10.1111/nph.17773  

   Monson, Russell K.; Trowbridge, Amy M.; Lindroth, Richard L.; Lerdau, Manuel T. (October 2021, New Phytologist)

   Summary Plant resource allocation patterns often reveal tradeoffs that favor growth (G) over defense (D), or vice versa. Ecologists most often explain G–D tradeoffs through principles of economic optimality, in which negative trait correlations are attributed to the reconciliation of fitness costs. Recently, researchers in molecular biology have developed ‘big data’ resources including multi‐omic (e.g. transcriptomic, proteomic and metabolomic) studies that describe the cellular processes controlling gene expression in model species. In this synthesis, we bridge ecological theory with discoveries in multi‐omics biology to better understand how selection has shaped the mechanisms of G–D tradeoffs. Multi‐omic studies reveal strategically coordinated patterns in resource allocation that are enabled by phytohormone crosstalk and transcriptional signal cascades. Coordinated resource allocation justifies the framework of optimality theory, while providing mechanistic insight into the feedbacks and control hubs that calibrate G–D tradeoff commitments. We use the existing literature to describe the coordinated resource allocation hypothesis (CoRAH) that accounts for balanced cellular controls during the expression of G–D tradeoffs, while sustaining stored resource pools to buffer the impacts of future stresses. The integrative mechanisms of the CoRAH unify the supply‐ and demand‐side perspectives of previous G–D tradeoff theories. 

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