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Abstract Waterlogging stress (WLS) negatively impacts the growth and yield of crops resulting in heavy losses to agricultural production. Previous studies have revealed that WLS induces a systemic response in shoots that is partially dependent on the plant hormones ethylene and abscisic acid. However, the role of rapid cell-to-cell signaling pathways, such as the reactive oxygen species (ROS) and calcium waves, in systemic responses of plants to WLS is unknown at present. Here, we reveal that an abrupt WLS treatment of Arabidopsis (Arabidopsis thaliana) plants growing in peat moss triggers systemic ROS and calcium wave responses and that the WLS-triggered ROS wave response of Arabidopsis is dependent on the ROS-generating RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD), calcium-permeable channels GLUTAMATE-LIKE RECEPTOR 3.3 and 3.6 (GLR3.3 and GLR3.6), and aquaporin PLASMA MEMBRANE INTRINSIC PROTEIN 2;1 (PIP2;1) proteins. We further show that WLS is accompanied by a rapid systemic transcriptomic response that is evident as early as 10 min following waterlogging initiation, includes many hypoxia-response transcripts, and is partially dependent on RBOHD. Interestingly, the abrupt WLS of Arabidopsis resulted in the triggering of a rapid hydraulic wave response and the transient opening of stomata on leaves. In addition, it induced in plants a heightened state of tolerance to a subsequent submergence stress. Taken together, our findings reveal that the initiation of WLS in plants is accompanied by rapid systemic physiological and transcriptomic responses that involve the ROS, calcium, and hydraulic waves, as well as the induction of hypoxia acclimation mechanisms in systemic tissues.more » « less
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Abstract The plant-specific TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) transcription factor family is most closely associated with regulating plant developmental programs. Recently, TCPs were also shown to mediate host immune signaling, both as targets of pathogen virulence factors and as regulators of plant defense genes. However, comprehensive characterization of TCP gene targets is still lacking. Loss of function of the class I TCP gene AtTCP8 attenuates early immune signaling and, when combined with mutations in AtTCP14 and AtTCP15, additional layers of defense signaling in Arabidopsis (Arabidopsis thaliana). Here, we focus on TCP8, the most poorly characterized of the three to date. We used chromatin immunoprecipitation and RNA sequencing to identify TCP8-bound gene promoters and differentially regulated genes in the tcp8 mutant; these datasets were heavily enriched in signaling components for multiple phytohormone pathways, including brassinosteroids (BRs), auxin, and jasmonic acid. Using BR signaling as a representative example, we showed that TCP8 directly binds and activates the promoters of the key BR transcriptional regulatory genes BRASSINAZOLE-RESISTANT1 (BZR1) and BRASSINAZOLE-RESISTANT2 (BZR2/BES1). Furthermore, tcp8 mutant seedlings exhibited altered BR-responsive growth patterns and complementary reductions in BZR2 transcript levels, while TCP8 protein demonstrated BR-responsive changes in subnuclear localization and transcriptional activity. We conclude that one explanation for the substantial targeting of TCP8 alongside other TCP family members by pathogen effectors may lie in its role as a modulator of BR and other plant hormone signaling pathways.more » « less
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Cuypers, Ann (Ed.)Abstract Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to prevent either deficiency or toxicity. Cadmium (Cd) is a non-essential element that induces both Fe deficiency and toxicity; however, the mechanisms behind these Fe/Cd-induced responses are still elusive. Here we explored Cd- and Fe-associated responses in wild-type Arabidopsis and in a mutant that overaccumulates Fe (opt3-2). Gene expression profiling revealed a large overlap between transcripts induced by Fe deficiency and Cd exposure. Interestingly, the use of opt3-2 allowed us to identify additional gene clusters originally induced by Cd in the wild type but repressed in the opt3-2 background. Based on the high levels of H2O2 found in opt3-2, we propose a model where reactive oxygen species prevent the induction of genes that are induced in the wild type by either Fe deficiency or Cd. Interestingly, a defined cluster of Fe-responsive genes was found to be insensitive to this negative feedback, suggesting that their induction by Cd is more likely to be the result of an impaired Fe sensing. Overall, our data suggest that Fe deficiency responses are governed by multiple inputs and that a hierarchical regulation of Fe homeostasis prevents the induction of specific networks when Fe and H2O2 levels are elevated.more » « less
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Abstract Plants are capable of synthesizing all the molecules necessary to complete their life cycle from minerals, water, and light. This plasticity, however, comes at a high energetic cost and therefore plants need to regulate their economy and allocate resources accordingly. Iron–sulfur (Fe–S) clusters are at the center of photosynthesis, respiration, amino acid, and DNA metabolism. Fe–S clusters are extraordinary catalysts, but their main components (Fe2+ and S2−) are highly reactive and potentially toxic. To prevent toxicity, plants have evolved mechanisms to regulate the uptake, storage, and assimilation of Fe and S. Recent advances have been made in understanding the cellular economy of Fe and S metabolism individually, and growing evidence suggests that there is dynamic crosstalk between Fe and S networks. In this review, we summarize and discuss recent literature on Fe sensing, allocation, use efficiency, and, when pertinent, its relationship to S metabolism. Our future perspectives include a discussion about the open questions and challenges ahead and how the plant nutrition field can come together to approach these questions in a cohesive and more efficient way.more » « less
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SUMMARY The first draft of the Arabidopsis genome was released more than 20 years ago and despite intensive molecular research, more than 30% of Arabidopsis genes remained uncharacterized or without an assigned function. This is in part due to gene redundancy within gene families or the essential nature of genes, where their deletion results in lethality (i.e., thedark genome). High‐throughput plant phenotyping (HTPP) offers an automated and unbiased approach to characterize subtle or transient phenotypes resulting from gene redundancy or inducible gene silencing; however, access to commercial HTPP platforms remains limited. Here we describe the design and implementation ofOPEN leaf, an open‐source phenotyping system with cloud connectivity and remote bilateral communication to facilitate data collection, sharing and processing.OPEN leaf, coupled with our SMART imaging processing pipeline was able to consistently document and quantify dynamic changes at the whole rosette level and leaf‐specific resolution when plants experienced changes in nutrient availability. Our data also demonstrate that VIS sensors remain underutilized and can be used in high‐throughput screens to identify and characterize previously unidentified phenotypes in a leaf‐specific time‐dependent manner. Moreover, the modular and open‐source design ofOPEN leafallows seamless integration of additional sensors based on users and experimental needs.more » « less
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SUMMARY Global warming, climate change, and industrial pollution are altering our environment subjecting plants, microbiomes, and ecosystems to an increasing number and complexity of abiotic stress conditions, concurrently or sequentially. These conditions, termed, “multifactorial stress combination” (MFSC), can cause a significant decline in plant growth and survival. However, the impacts of MFSC on reproductive tissues and yield of major crop plants are largely unknown. We subjected soybean (Glycine max) 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 their 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 of soybean are linked to the effects of MFSC on different vegetative, physiological, and/or reproductive parameters. Our study identified networks and pathways associated with reactive oxygen species, ascorbic acid and aldarate, and iron/copper signaling/metabolism as promising targets for future biotechnological efforts to augment the resilience of reproductive tissues of major crop plants to MFSC. In addition, we provide unique phenotypic and transcriptomic datasets for dissecting the mechanistic effects of MFSC on the vegetative, physiological, and reproductive processes of a crop plant.more » « less
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