Linker histone H1 modulates defense priming and immunity in plants.

Linker H1 histones play an important role in animal and human pathogenesis, but their function in plant immunity is poorly understood. Here, we analyzed mutants of the three canonical variants of Arabidopsis H1 histones, namely H1.1, H1.2 and H1.3. We observed that double h1.1h1.2 and triple h1.1h1.2h1.3 (3h1) mutants were resistant to Pseudomonas syringae and Botrytis cinerea infections. Transcriptome analysis of 3h1 mutant plants showed H1s play a key role in regulating the expression of early and late defense genes upon pathogen challenge. Moreover, 3h1 mutant plants showed enhanced production of reactive oxygen species and activation of mitogen activated protein kinases upon pathogen-associated molecular pattern (PAMP) treatment. However, 3h1 mutant plants were insensitive to priming with flg22, a well-known bacterial PAMP which induces enhanced resistance in WT plants. The defective defense response in 3h1 upon priming was correlated with altered DNA methylation and reduced global H3K56ac levels. Our data place H1 as a molecular gatekeeper in governing dynamic changes in the chromatin landscape of defense genes during plant pathogen interaction.

A role of frontal association cortex in long-term object recognition memory of objects with complex features in rats.

Perirhinal cortex is a brain area that has been considered crucial for the object recognition memory (ORM). However, with the use of an ORM enhancer named RGS14414 as gain-in-function tool, we show here that frontal association cortex and not the Perirhinal cortex is essential for the ORM of objects with complex features that consisted of detailed drawing on the object surface (complex ORM). An expression of RGS14414, in rat brain frontal association cortex, induced the formation of long-term complex ORM, whereas the expression of the same memory enhancer in Perirhinal cortex failed to produce this effect. Instead, RGS14414 expression in Perirhinal cortex caused the formation of ORM of objects with simple features that consisted of the shape of object (simple ORM). Further, a selective elimination of frontal association cortex neurons by treatment with an immunotoxin Ox7-SAP completely abrogated the formation of complex ORM. Thus, our results suggest that frontal association cortex plays a key role in processing of a high-order recognition memory information in brain.

Disparate population and holobiont structure of pocilloporid corals across the Red Sea gradient demonstrate species-specific evolutionary trajectories.

Global habitat degradation heightens the need to better understand patterns of genetic connectivity and diversity of marine biota across geographical ranges to guide conservation efforts. Corals across the Red Sea are subject to pronounced environmental differences, but studies so far suggest that animal populations are largely connected, excepting evidence for a genetic break between the northern-central and southern regions. Here, we investigated population structure and holobiont assemblage of two common pocilloporid corals, Pocillopora verrucosa and Stylophora pistillata, across the Red Sea. We found little evidence for population differentiation in P. verrucosa, except for the southernmost site. Conversely, S. pistillata exhibited a complex population structure with evidence for within-reef and regional genetic differentiation, in line with differences in their reproductive mode (P. verrucosa is a broadcast spawner and S. pistillata is a brooder). Analysis for genomic loci under positive selection identified 85 sites (18 of which were in coding sequences) that distinguished the southern P. verrucosa population from the remainder of the Red Sea population. By comparison, we found 128 loci (24 of which were residing in coding sequences) in S. pistillata with evidence for local adaptation at various sites. Functional annotation of the underlying proteins revealed putative roles in the response to stress, lipid metabolism, transport, cytoskeletal rearrangement, and ciliary function (among others). Microbial assemblages of both coral species showed pervasive association with microalgal symbionts from the genus Symbiodinium (former clade A) and bacteria from the genus Endozoicomonas that exhibited significant differences according to host genotype and environment. The disparity of population genetic and holobiont assemblage patterns even between closely related species (family Pocilloporidae) highlights the need for multispecies investigations to better understand the role of the environment in shaping evolutionary trajectories. It further emphasizes the importance of networks of reef reserves to achieve conservation of genetic variants critical to the future survival of coral ecosystems.

Rapid shifts in thermal reaction norms and tolerance of brooded coral larvae following parental heat acclimation.

Thermal priming of reef corals can enhance their heat tolerance; however, the legacy effects of heat stress during parental brooding on larval resilience remain understudied. This study investigated whether preconditioning adult coral Pocillopora damicornis to high temperatures (29°C and 32°C) could better prepare their larvae for heat stress. Results showed that heat-acclimated adults brooded larvae with reduced symbiont density and shifted thermal performance curves. Reciprocal transplant experiments demonstrated higher bleaching resistance and better photosynthetic and autotrophic performance in heat-exposed larvae from acclimated adults compared to unacclimated adults. RNA-seq revealed strong cellular stress responses in larvae from heat-acclimated adults that could have been effective in rescuing host cells from stress, as evidenced by the widespread upregulation of genes involved in cell cycle and mitosis. For symbionts, a molecular coordination between light harvesting, photoprotection and carbon fixation was detected in larvae from heat-acclimated adults, which may help optimize photosynthetic activity and yield under high temperature. Furthermore, heat acclimation led to opposing regulations of symbiont catabolic and anabolic pathways and favoured nutrient translocation to the host and thus a functional symbiosis. Notwithstanding, the improved heat tolerance was paralleled by reduced light-enhanced dark respiration, indicating metabolic depression for energy saving. Our findings suggest that adult heat acclimation can rapidly shift thermal tolerance of brooded coral larvae and provide integrated physiological and molecular evidence for this adaptive plasticity, which could increase climate resilience. However, the metabolic depression may be maladaptive for long-term organismal performance, highlighting the importance of curbing carbon emissions to better protect corals.

RGS14414-Mediated Activation of the 14-3-3ζ in Rodent Perirhinal Cortex Induces Dendritic Arborization, an Increase in Spine Number, Long-Lasting Memory Enhancement, and the Prevention of Memory Deficits.

The remedy of memory deficits has been inadequate, as all potential candidates studied thus far have shown limited to no effects and a search for an effective strategy is ongoing. Here, we show that an expression of RGS14414 in rat perirhinal cortex (PRh) produced long-lasting object recognition memory (ORM) enhancement and that this effect was mediated through the upregulation of 14-3-3ζ, which caused a boost in BDNF protein levels and increase in pyramidal neuron dendritic arborization and dendritic spine number. A knockdown of the 14-3-3ζ gene in rat or the deletion of the BDNF gene in mice caused complete loss in ORM enhancement and increase in BDNF protein levels and neuronal plasticity, indicating that 14-3-3ζ-BDNF pathway-mediated structural plasticity is an essential step in RGS14414-induced memory enhancement. We further observed that RGS14414 treatment was able to prevent deficits in recognition, spatial, and temporal memory, which are types of memory that are particularly affected in patients with memory dysfunctions, in rodent models of aging and Alzheimer's disease. These results suggest that 14-3-3ζ-BDNF pathway might play an important role in the maintenance of the synaptic structures in PRh that support memory functions and that RGS14414-mediated activation of this pathway could serve as a remedy to treat memory deficits.

Host under epigenetic control: A novel perspective on the interaction between microorganisms and corals.

Coral reefs have been challenged by the current rate and severity of environmental change that might outpace their ability to adapt and survive. Current research focuses on understanding how microbial communities and epigenetic changes separately affect phenotypes and gene expression of corals. Here, we provide the hypothesis that coral-associated microorganisms may directly or indirectly affect the coral's phenotypic response through the modulation of its epigenome. Homologs of ankyrin-repeat protein A and internalin B, which indirectly cause histone modifications in humans, as well as Rv1988 histone methyltransferase, and the DNA methyltransferases Rv2966c, Mhy1, Mhy2, and Mhy3 found in coral-associated bacteria indicate that there are potential host epigenome-modifying proteins in the coral microbiome. With the ideas presented here, we suggest that microbiome manipulation may be a means to alter a coral's epigenome, which could aid the current efforts to protect coral reefs. Also see the video abstract here: https://youtu.be/CW9GbChjKM4.

Histone modifications and DNA methylation act cooperatively in regulating symbiosis genes in the sea anemone Aiptasia.

BACKGROUND: The symbiotic relationship between cnidarians and dinoflagellates is one of the most widespread endosymbiosis in our oceans and provides the ecological basis of coral reef ecosystems. Although many studies have been undertaken to unravel the molecular mechanisms underlying these symbioses, we still know little about the epigenetic mechanisms that control the transcriptional responses to symbiosis. RESULTS: Here, we used the model organism Exaiptasia diaphana to study the genome-wide patterns and putative functions of the histone modifications H3K27ac, H3K4me3, H3K9ac, H3K36me3, and H3K27me3 in symbiosis. While we find that their functions are generally conserved, we observed that colocalization of more than one modification and or DNA methylation correlated with significantly higher gene expression, suggesting a cooperative action of histone modifications and DNA methylation in promoting gene expression. Analysis of symbiosis genes revealed that activating histone modifications predominantly associated with symbiosis-induced genes involved in glucose metabolism, nitrogen transport, amino acid biosynthesis, and organism growth while symbiosis-suppressed genes were involved in catabolic processes. CONCLUSIONS: Our results provide new insights into the mechanisms of prominent histone modifications and their interaction with DNA methylation in regulating symbiosis in cnidarians.

Nutritional control regulates symbiont proliferation and life history in coral-dinoflagellate symbiosis.

BACKGROUND: The coral-Symbiodiniaceae symbiosis is fundamental for the coral reef ecosystem. Corals provide various inorganic nutrients to their algal symbionts in exchange for the photosynthates to meet their metabolic demands. When becoming symbionts, Symbiodiniaceae cells show a reduced proliferation rate and a different life history. While it is generally believed that the animal hosts play critical roles in regulating these processes, far less is known about the molecular underpinnings that allow the corals to induce the changes in their symbionts. RESULTS: We tested symbiont cell proliferation and life stage changes in vitro in response to different nutrient-limiting conditions to determine the key nutrients and to compare the respective symbiont transcriptomic profiles to cells in hospite. We then examined the effects of nutrient repletion on symbiont proliferation in coral hosts and quantified life stage transitions in vitro using time-lapse confocal imaging. Here, we show that symbionts in hospite share gene expression and pathway activation profiles with free-living cells under nitrogen-limited conditions, strongly suggesting that symbiont proliferation in symbiosis is limited by nitrogen availability. CONCLUSIONS: We demonstrate that nitrogen limitation not only suppresses cell proliferation but also life stage transition to maintain symbionts in the immobile coccoid stage. Nutrient repletion experiments in corals further confirmed that nitrogen availability is the major factor limiting symbiont density in hospite. Our study emphasizes the importance of nitrogen in coral-algae interactions and, more importantly, sheds light on the crucial role of nitrogen in symbiont life history regulation.

The Evolution of Calcification in Reef-Building Corals.

Corals build the structural foundation of coral reefs, one of the most diverse and productive ecosystems on our planet. Although the process of coral calcification that allows corals to build these immense structures has been extensively investigated, we still know little about the evolutionary processes that allowed the soft-bodied ancestor of corals to become the ecosystem builders they are today. Using a combination of phylogenomics, proteomics, and immunohistochemistry, we show that scleractinian corals likely acquired the ability to calcify sometime between ∼308 and ∼265 Ma through a combination of lineage-specific gene duplications and the co-option of existing genes to the calcification process. Our results suggest that coral calcification did not require extensive evolutionary changes, but rather few coral-specific gene duplications and a series of small, gradual optimizations of ancestral proteins and their co-option to the calcification process.

Projecting coral responses to intensifying marine heatwaves under ocean acidification.

Over this century, coral reefs will run the gauntlet of climate change, as marine heatwaves (MHWs) become more intense and frequent, and ocean acidification (OA) progresses. However, we still lack a quantitative assessment of how, and to what degree, OA will moderate the responses of corals to MHWs as they intensify throughout this century. Here, we first projected future MHW intensities for tropical regions under three future greenhouse gas emissions scenario (representative concentration pathways, RCP2.6, RCP4.5 and RCP8.5) for the near-term (2021-2040), mid-century (2041-2060) and late-century (2081-2100). We then combined these MHW intensity projections with a global data set of 1,788 experiments to assess coral attribute performance and survival under the three emissions scenarios for the near-term, mid-century and late-century in the presence and absence of OA. Although warming and OA had predominately additive impacts on the coral responses, the contribution of OA in affecting most coral attributes was minor relative to the dominant role of intensifying MHWs. However, the addition of OA led to greater decreases in photosynthesis and survival under intermediate and unrestricted emissions scenario for the mid- and late-century than if intensifying MHWs were considered as the only driver. These results show that role of OA in modulating coral responses to intensifying MHWs depended on the focal coral attribute and extremity of the scenario examined. Specifically, intensifying MHWs and OA will cause increasing instances of coral bleaching and substantial declines in coral productivity, calcification and survival within the next two decades under the low and intermediate emissions scenario. These projections suggest that corals must rapidly adapt or acclimatize to projected ocean conditions to persist, which is far more likely under a low emissions scenario and with increasing efforts to manage reefs to enhance resilience.

Host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia.

The metabolic symbiosis with photosynthetic algae allows corals to thrive in the oligotrophic environments of tropical seas. Different aspects of this relationship have been investigated using the emerging model organism Aiptasia. However, many fundamental questions, such as the nature of the symbiotic relationship and the interactions of nutrients between the partners remain highly debated. Using a meta-analysis approach, we identified a core set of 731 high-confidence symbiosis-associated genes that revealed host-dependent recycling of waste ammonium and amino acid synthesis as central processes in this relationship. Subsequent validation via metabolomic analyses confirmed that symbiont-derived carbon enables host recycling of ammonium into nonessential amino acids. We propose that this provides a regulatory mechanism to control symbiont growth through a carbon-dependent negative feedback of nitrogen availability to the symbiont. The dependence of this mechanism on symbiont-derived carbon highlights the susceptibility of this symbiosis to changes in carbon translocation, as imposed by environmental stress.

CATION-CHLORIDE CO-TRANSPORTER 1 (CCC1) Mediates Plant Resistance against Pseudomonas syringae.

Plasma membrane (PM) depolarization functions as an initial step in plant defense signaling pathways. However, only a few ion channels/transporters have been characterized in the context of plant immunity. Here, we show that the Arabidopsis (Arabidopsis thaliana) Na+:K+:2Cl- (NKCC) cotransporter CCC1 has a dual function in plant immunity. CCC1 functions independently of PM depolarization and negatively regulates pathogen-associated molecular pattern-triggered immunity. However, CCC1 positively regulates plant basal and effector-triggered resistance to Pseudomonas syringae pv. tomato (Pst) DC3000. In line with the compromised immunity to Pst DC3000, ccc1 mutants show reduced expression of genes encoding enzymes involved in the biosynthesis of antimicrobial peptides, camalexin, and 4-OH-ICN, as well as pathogenesis-related proteins. Moreover, genes involved in cell wall and cuticle biosynthesis are constitutively down-regulated in ccc1 mutants, and the cell walls of these mutants exhibit major changes in monosaccharide composition. The role of CCC1 ion transporter activity in the regulation of plant immunity is corroborated by experiments using the specific NKCC inhibitor bumetanide. These results reveal a function for ion transporters in immunity-related cell wall fortification and antimicrobial biosynthesis.

Integrating environmental variability to broaden the research on coral responses to future ocean conditions.

Our understanding of the response of reef-building corals to changes in their physical environment is largely based on laboratory experiments, analysis of long-term field data, and model projections. Experimental data provide unique insights into how organisms respond to variation of environmental drivers. However, an assessment of how well experimental conditions cover the breadth of environmental conditions and variability where corals live successfully is missing. Here, we compiled and analyzed a globally distributed dataset of in-situ seasonal and diurnal variability of key environmental drivers (temperature, pCO2 , and O2 ) critical for the growth and livelihood of reef-building corals. Using a meta-analysis approach, we compared the variability of environmental conditions assayed in coral experimental studies to current and projected conditions in their natural habitats. We found that annual temperature profiles projected for the end of the 21st century were characterized by distributional shifts in temperatures with warmer winters and longer warm periods in the summer, not just peak temperatures. Furthermore, short-term hourly fluctuations of temperature and pCO2 may regularly expose corals to conditions beyond the projected average increases for the end of the 21st century. Coral reef sites varied in the degree of coupling between temperature, pCO2 , and dissolved O2 , which warrants site-specific, differentiated experimental approaches depending on the local hydrography and influence of biological processes on the carbonate system and O2 availability. Our analysis highlights that a large portion of the natural environmental variability at short and long timescales is underexplored in experimental designs, which may provide a path to extend our understanding on the response of corals to global climate change.

Widespread bleaching in the One Tree Island lagoon (Southern Great Barrier Reef) during record-breaking temperatures in 2020.

The global marine environment has been impacted significantly by climate change. Ocean temperatures are rising, and the frequency, duration and intensity of marine heatwaves are increasing, particularly affecting coral reefs. Coral bleaching events are becoming more common, with less recovery time between events. Anomalous temperatures at the start of 2020 caused widespread bleaching across the Great Barrier Reef (GBR), extending to southern, previously less affected reefs such as One Tree Island. Here, nine video transects were conducted at One Tree Island, in the Capricorn Bunker Group, and analysed for community composition and diversity, and the extent of bleaching across taxa. Average live hard coral cover across the area was 11.62%, and almost half of this was identified as severely bleached. This bleaching event is concerning as it occurred in an area previously considered a potential refuge for corals and associated fauna from the risks of climate warming. Due to the global impacts of COVID-19 during 2020, this report provides one of potentially few monitoring efforts of coral bleaching.

Unfamiliar partnerships limit cnidarian holobiont acclimation to warming.

Enhancing the resilience of corals to rising temperatures is now a matter of urgency, leading to growing efforts to explore the use of heat tolerant symbiont species to improve their thermal resilience. The notion that adaptive traits can be retained by transferring the symbionts alone, however, challenges the holobiont concept, a fundamental paradigm in coral research. Holobiont traits are products of a specific community (holobiont) and all its co-evolutionary and local adaptations, which might limit the retention or transference of holobiont traits by exchanging only one partner. Here we evaluate how interchanging partners affect the short- and long-term performance of holobionts under heat stress using clonal lineages of the cnidarian model system Aiptasia (host and Symbiodiniaceae strains) originating from distinct thermal environments. Our results show that holobionts from more thermally variable environments have higher plasticity to heat stress, but this resilience could not be transferred to other host genotypes through the exchange of symbionts. Importantly, our findings highlight the role of the host in determining holobiont productivity in response to thermal stress and indicate that local adaptations of holobionts will likely limit the efficacy of interchanging unfamiliar compartments to enhance thermal tolerance.

RGS14414 treatment induces memory enhancement and rescues episodic memory deficits.

Memory deficits affect a large proportion of the human population and are associated with aging and many neurologic, neurodegenerative, and psychiatric diseases. Treatment of this mental disorder has been disappointing because all potential candidates studied thus far have failed to produce consistent effects across various types of memory and have shown limited to no effects on memory deficits. Here, we show that the promotion of neuronal arborization through the expression of the regulator of G-protein signaling 14 of 414 amino acids (RGS14414) not only induced robust enhancement of multiple types of memory but was also sufficient for the recovery of recognition, spatial, and temporal memory, which are kinds of episodic memory that are primarily affected in patients or individuals with memory dysfunction. We observed that a surge in neuronal arborization was mediated by up-regulation of brain-derived neurotrophic factor (BDNF) signaling and that the deletion of BDNF abrogated both neuronal arborization activation and memory enhancement. The activation of BDNF-dependent neuronal arborization generated almost 2-fold increases in synapse numbers in dendrites of pyramidal neurons and in neurites of nonpyramidal neurons. This increase in synaptic connections might have evoked reorganization within neuronal circuits and eventually supported an increase in the activity of such circuits. Thus, in addition to showing the potential of RGS14414 for rescuing memory deficits, our results suggest that a boost in circuit activity could facilitate memory enhancement and the reversal of memory deficits.-Masmudi-Martín, M., Navarro-Lobato, I., López-Aranda, M. F., Delgado, G., Martín-Montañez, E., Quiros-Ortega, M. E., Carretero-Rey, M., Narváez, L., Garcia-Garrido, M. F., Posadas, S., López-Téllez, J. F., Blanco, E., Jiménez-Recuerda, I., Granados-Durán, P., Paez-Rueda, J., López, J. C., Khan, Z. U. RGS14414 treatment induces memory enhancement and rescues episodic memory deficits.

Condition-specific RNA editing in the coral symbiont Symbiodinium microadriaticum.

RNA editing is a rare post-transcriptional event that provides cells with an additional level of gene expression regulation. It has been implicated in various processes including adaptation, viral defence and RNA interference; however, its potential role as a mechanism in acclimatization has just recently been recognised. Here, we show that RNA editing occurs in 1.6% of all nuclear-encoded genes of Symbiodinium microadriaticum, a dinoflagellate symbiont of reef-building corals. All base-substitution edit types were present, and statistically significant motifs were associated with three edit types. Strikingly, a subset of genes exhibited condition-specific editing patterns in response to different stressors that resulted in significant increases of non-synonymous changes. We posit that this previously unrecognised mechanism extends this organism's capability to respond to stress beyond what is encoded by the genome. This in turn may provide further acclimatization capacity to these organisms, and by extension, their coral hosts.

Synaptic tagging during memory allocation.

There is now compelling evidence that the allocation of memory to specific neurons (neuronal allocation) and synapses (synaptic allocation) in a neurocircuit is not random and that instead specific mechanisms, such as increases in neuronal excitability and synaptic tagging and capture, determine the exact sites where memories are stored. We propose an integrated view of these processes, such that neuronal allocation, synaptic tagging and capture, spine clustering and metaplasticity reflect related aspects of memory allocation mechanisms. Importantly, the properties of these mechanisms suggest a set of rules that profoundly affect how memories are stored and recalled.

Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts.

Corals and their endosymbiotic dinoflagellates of the genus Symbiodinium have a fragile relationship that breaks down under heat stress, an event known as bleaching. However, many coral species have adapted to high temperature environments such as the Red Sea (RS). To investigate mechanisms underlying temperature adaptation in zooxanthellate cnidarians we compared transcriptome- and proteome-wide heat stress response (24 h at 32°C) of three strains of the model organism Aiptasia pallida from regions with differing temperature profiles; North Carolina (CC7), Hawaii (H2) and the RS. Correlations between transcript and protein levels were generally low but inter-strain comparisons highlighted a common core cnidarian response to heat stress, including protein folding and oxidative stress pathways. RS anemones showed the strongest increase in antioxidant gene expression and exhibited significantly lower reactive oxygen species (ROS) levels in hospite However, comparisons of antioxidant gene and protein expression between strains did not show strong differences, indicating similar antioxidant capacity across the strains. Subsequent analysis of ROS production in isolated symbionts confirmed that the observed differences of ROS levels in hospite were symbiont-driven. Our findings indicate that RS anemones do not show increased antioxidant capacity but may have adapted to higher temperatures through association with more thermally tolerant symbionts.