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1. Hydroxyl radical scavenging by cerium oxide nanoparticles improves Arabidopsis salinity tolerance by enhancing leaf mesophyll potassium retention

   https://doi.org/10.1039/C8EN00323H  

   Wu, Honghong ; Shabala, Lana ; Shabala, Sergey ; Giraldo, Juan Pablo ( January 2018 , Environmental Science: Nano)

   null (Ed.)

   Salinity is a widespread environmental stress that severely limits crop yield worldwide. Cerium oxide nanoparticles (nanoceria) have the unique capability of catalytically reducing levels of stress-induced reactive oxygen species (ROS) including hydroxyl radicals (˙OH) that lack enzymatic scavenging pathways. The underlying mechanisms of how nanoceria ROS scavenging augments plant tolerance to environmental stress are not well understood. Herein, we demonstrate that catalytic ˙OH scavenging by nanoceria in Arabidopsis thaliana leaves significantly improves mesophyll K + retention, a key trait associated with salinity stress tolerance. Leaves with mesophyll cells interfaced with 50 mg L −1 poly(acrylic acid) coated nanoceria (PNC) have significantly higher ( P < 0.05) carbon assimilation rates (85%), quantum efficiency of photosystem II (9%), and chlorophyll content (14%) compared to controls after being exposed to 100 mM NaCl for 3 days. PNC infiltrated leaves (PNC-leaves) under salinity stress exhibit lower ROS levels – including hydroxyl radical (41%) and its precursor hydrogen peroxide (44%) – and one fold higher ( P < 0.05) cytosolic K + dye intensity in leaf mesophyll cells relative to controls. Non-invasive microelectrode ion flux electrophysiological (MIFE) measurements indicated that PNC-leaves have about three-fold lower NaCl-induced K + efflux from leaf mesophyll cells compared to controls upon exposure to salinity stress. The ROS-activated nonselective cation channels (ROS-NSCC) in the plasma membrane of leaf mesophyll cells were identified as the main ˙OH-inducible K + efflux channels. Long term catalytic scavenging of ˙OH in leaves by PNC enhances plant photosynthetic performance under salinity stress by enabling plasma membrane channels/transporters to coordinately retain higher levels of K + in the leaf mesophyll cell cytosol. PNC augmented plant ROS scavenging provides a key tool for understanding and improving plant tolerance against abiotic stresses such as salinity. 

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2. Photosymbiosis reduces the environmental stress response under a heat challenge in a facultatively symbiotic coral

   https://doi.org/10.1038/s41598-024-66057-2  

   Wuitchik, D M ; Aichelman, H E ; Atherton, K F ; Brown, C M ; Chen, X ; DiRoberts, L ; Pelose, G E ; Tramonte, C A ; Davies, S W ( December 2024 , Scientific Reports)

   The symbiosis between corals and dinoflagellates of the family Symbiodiniaceae is sensitive to environmental stress. The oxidative bleaching hypothesis posits that extreme temperatures lead to accumulation of photobiont-derived reactive oxygen species ROS, which exacerbates the coral environmental stress response (ESR). To understand how photosymbiosis modulates coral ESRs, these responses must be explored in hosts in and out of symbiosis. We leveraged the facultatively symbiotic coralAstrangia poculata, which offers an opportunity to uncouple the ESR across its two symbiotic phenotypes (brown, white). Colonies of both symbiotic phenotypes were exposed to three temperature treatments for 15 days: (i) control (static 18 °C), (ii) heat challenge (increasing from 18 to 30 °C), and (iii) cold challenge (decreasing from 18 to 4 °C) after which host gene expression was profiled. Cold challenged corals elicited widespread differential expression, however, there were no differences between symbiotic phenotypes. In contrast, brown colonies exhibited greater gene expression plasticity under heat challenge, including enrichment of cell cycle pathways involved in controlling photobiont growth. While this plasticity was greater, the genes driving this plasticity were not associated with an amplified environmental stress response (ESR) and instead showed patterns of a dampened ESR under heat challenge. This provides nuance to the oxidative bleaching hypothesis and suggests that, at least during the early onset of bleaching, photobionts reduce the host’s ESR under elevated temperatures inA. poculata.

    

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3. Thermal stress triggers productive viral infection of a key coral reef symbiont

   https://doi.org/10.1038/s41396-022-01194-y  

   Grupstra, Carsten G. B. ; Howe-Kerr, Lauren I. ; Veglia, Alex J. ; Bryant, Reb L. ; Coy, Samantha R. ; Blackwelder, Patricia L. ; Correa, Adrienne M. S. ( January 2022 , The ISME Journal)

   Climate change-driven ocean warming is increasing the frequency and severity of bleaching events, in which corals appear whitened after losing their dinoflagellate endosymbionts (family Symbiodiniaceae). Viral infections of Symbiodiniaceae may contribute to some bleaching signs, but little empirical evidence exists to support this hypothesis. We present the first temporal analysis of a lineage of Symbiodiniaceae-infecting positive-sense single-stranded RNA viruses (“dinoRNAVs”) in coral colonies, which were exposed to a 5-day heat treatment (+2.1 °C). A total of 124 dinoRNAV major capsid protein gene “aminotypes” (unique amino acid sequences) were detected from five colonies of two closely related Pocillopora-Cladocopium (coral-symbiont) combinations in the experiment; most dinoRNAV aminotypes were shared between the two coral-symbiont combinations (64%) and among multiple colonies (82%). Throughout the experiment, seventeen dinoRNAV aminotypes were found only in heat-treated fragments, and 22 aminotypes were detected at higher relative abundances in heat-treated fragments. DinoRNAVs in fragments of some colonies exhibited higher alpha diversity and dispersion under heat stress. Together, these findings provide the first empirical evidence that exposure to high temperatures triggers some dinoRNAVs to switch from a persistent to a productive infection mode within heat-stressed corals. Over extended time frames, we hypothesize that cumulative dinoRNAV production in the Pocillopora-Cladocopium system could affect colony symbiotic status, for example, by decreasing Symbiodiniaceae densities within corals. This study sets the stage for reef-scale investigations of dinoRNAV dynamics during bleaching events.

    

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4. Symbiotic dinoflagellates divert energy away from mutualism during coral bleaching recovery

   https://doi.org/10.1007/s13199-023-00901-3  

   Allen-Waller, Luella ; Barott, Katie L. ( March 2023 , Symbiosis)

   The future of coral reefs in a warming world depends on corals’ ability to recover from bleaching, the loss of their symbiotic dinoflagellate algae (Symbiodiniaceae) during marine heatwaves. Heat-tolerant symbiont species can remain in symbiosis during heat stress, but often provide less photosynthate to the host than heat-sensitive species under ambient conditions. Understanding how heat stress changes the dynamics of this tradeoff between stress tolerance and mutualism contribution is crucial for predicting coral success under climate change. To test how symbiont resource allocation affects coral recovery from heat stress, we exposed the coral Montipora capitata hosting either heat-sensitive Cladocopium C31 (C) or heat-tolerant Durusdinium glynnii (D) to heat stress. D regained symbiont density and photochemical efficiency faster after heat treat- ment than C, but symbiont recovery did not restore coral biomass or calcification rates to pre-bleaching levels in the initial recovery period. D populations also contributed less photosynthate to the host relative to C, even during heat stress. Further, higher-density symbiont populations of both species retained more photosynthate than lower-density populations, and corals receiving less photosynthate exhibited reduced calcification rates and lower intracellular pH. This is the first evidence that symbiont density and carbon translocation are negatively related, and the first to establish a link between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest the energy demand of symbiont regrowth after bleaching reduces their mutualism contribution and can thus delay host recovery. Reestablishing a beneficial endos- ymbiosis imposes additional costs as holobionts overcome stress, and may explain latent mortality among coral populations after alleviation of heat stress in the field. 

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5. Comparison of 15 dinoflagellate genomes reveals extensive sequence and structural divergence in family Symbiodiniaceae and genus Symbiodinium

   https://doi.org/10.1186/s12915-021-00994-6  

   González-Pech, Raúl A. ; Stephens, Timothy G. ; Chen, Yibi ; Mohamed, Amin R. ; Cheng, Yuanyuan ; Shah, Sarah ; Dougan, Katherine E. ; Fortuin, Michael D. ; Lagorce, Rémi ; Burt, David W. ; et al ( December 2021 , BMC Biology)

   Abstract Background Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians (such as corals) and other coral reef organisms. Breakdown of the coral-dinoflagellate symbiosis due to environmental stress (i.e. coral bleaching) can lead to coral death and the potential collapse of reef ecosystems. However, evolution of Symbiodiniaceae genomes, and its implications for the coral, is little understood. Genome sequences of Symbiodiniaceae remain scarce due in part to their large genome sizes (1–5 Gbp) and idiosyncratic genome features. Results Here, we present de novo genome assemblies of seven members of the genus Symbiodinium , of which two are free-living, one is an opportunistic symbiont, and the remainder are mutualistic symbionts. Integrating other available data, we compare 15 dinoflagellate genomes revealing high sequence and structural divergence. Divergence among some Symbiodinium isolates is comparable to that among distinct genera of Symbiodiniaceae. We also recovered hundreds of gene families specific to each lineage, many of which encode unknown functions. An in-depth comparison between the genomes of the symbiotic Symbiodinium tridacnidorum (isolated from a coral) and the free-living Symbiodinium natans reveals a greater prevalence of transposable elements, genetic duplication, structural rearrangements, and pseudogenisation in the symbiotic species. Conclusions Our results underscore the potential impact of lifestyle on lineage-specific gene-function innovation, genome divergence, and the diversification of Symbiodinium and Symbiodiniaceae. The divergent features we report, and their putative causes, may also apply to other microbial eukaryotes that have undergone symbiotic phases in their evolutionary history. 

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