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Dassanayake, M.

Publications and source records attributed to Dassanayake, M..

At least 19 recordsLinked to original sources

Convergent genome evolution reveals shared routes to salt tolerance in flowering plants

Transitions to saline environments pose formidable challenges to plants, yet halophytism has evolved independently across many flowering plant lineages. We assembled a comparative angiosperm gene catalog of ~10 million protein-coding genes from 232 genomes spanning 55 families, with similar representation of halophytes and salt-sensitive relatives, to identify convergent genomic signatures of halophytism. Halophytes show remarkable convergence with recurrent genomic trends in salt-response genes, including lower copy numbers, higher basal expression, more constrained expression variation, distinct evolutionary rates, and independent positive selection on select genes at the same amino acid sites across multiple halophyte lineages. Crops and their wild halophytic relatives differ in gene family evolution, particularly in stress-response pathways. These findings reveal repeatedly tested evolutionary routes to halophytism and establish a genomic foundation for translating convergent adaptations into salt-tolerant crops.

genomics↗

Spatial and developmental reprogramming enables root growth under high salinity in the extremophyte Schrenkiella parvula

High salinity severely restricts root growth in most plants, yet the extremophyte model Schrenkiella parvula maintains growth under otherwise inhibitory conditions through a previously unrecognized developmental reorganization of the primary root. Under high salinity, the elongation zone rapidly reorganizes into two distinct states: the bulged and gap zones. These zones form in response to ionic stress and emerge during a transient growth pause followed by resumed tip growth and localized lateral root emergence from the gap zone. Jasmonic acid (JA) is necessary to initiate this developmental transition, while cell-layer-resolved hormone profiling revealed spatiotemporally coordinated JA and auxin accompanying the maintenance of the distinct zones. The zone-specific expression profiling resolved transcriptomic networks spanning core development and broad or zone-specific stress responses, revealing spatial regulation of hormone signaling, cell-wall remodeling, and osmotic and oxidative stress pathways. Raman spectroscopy, metabolite profiling, and cellular imaging supported localized regulation of water availability, ionic balance, and suppression of ROS accumulation and cell death. These networks also identified orthologous genes co-opted for novel functions potentially used to sustain growth. Together, these findings reveal a spatially coordinated mechanism for maintaining root growth under salt stress and provide a framework for discovering genetic mechanisms that optimize growth under stress.

plant biology↗

Distinct molecular mechanisms shape thermal tolerance and its plasticity in a splash pool copepod

Understanding how organisms respond to changes in temperature is becoming increasingly important in our rapidly changing world. While species differ substantially in their thermal tolerance, the exact molecular mechanisms underpinning this trait variation remain largely unknown. Species with broad geographical distribution provide a unique opportunity to examine variable responses to temperature, as populations experience a diverse range of thermal regimes that differ in the intensity, frequency, and duration of thermal stress. We used a splash pool copepod (Tigriopus californicus) with a large geographic range across the North American coast (Baja California to Alaska) to examine variation in thermotolerance and the plasticity of thermotolerance in five populations sampled across 12 degrees of latitude. We found that populations with higher heat tolerance (southern) showed lower plasticity (measured as increased survival at higher temperatures after a prior exposure to sub-lethal temperature). Our comparative transcriptomic analyses revealed that higher heat tolerance was associated with maintaining elevated expression of genes coding for peptidases even in absence of heat shock and higher plasticity of heat tolerance was associated with an increase in gene expression plasticity of genes coding for chitin and extracellular matrix (ECM). Our results highlight ontology-specific patterns associated with changes in the trait means and plasticity of heat tolerance across populations. These findings improve our mechanistic knowledge of thermotolerance as a trait and our ability to predict which populations are most vulnerable to extinction based on the trade-off between fixed thermal limits and plastic responses.

evolutionary biology↗

Comparative genomics reveals potential mechanisms of invasion in Phragmites australis (common reed)

Biological invasions are transforming ecosystems worldwide, yet the genomic bases enabling certain species to dominate new environments remain poorly understood. Phragmites australis, a widespread wetland grass with invasive and native subspecies co-occurring in North America, provides a powerful system to investigate genomic mechanisms of invasiveness. We generated independent chromosome-scale genome assemblies for invasive P. australis ssp. australis and co-occurring native ssp. americanus and used comparative genomic and transcriptomic analyses to identify lineage-specific innovations associated with invasive success. The invasive subspecies exhibits genomic novelties through functionally-biased single-copy orthologs, intronless genes, and subgenome expression asymmetry, along with a stress-ready basal transcriptome relative to the native subspecies. Following the removal of aboveground shoots ("cutback"), which measures the ability to recover from damage, the invasive subspecies undergoes stronger transcriptional reprogramming, increased shoot production, and higher biomass accumulation compared to the native. It also displays expansion of gene families and coordinately expressed gene modules that support resource mobilization, growth responses to light, and stress tolerance. Beyond Phragmites, comparative analyses across multiple grass genomes, including eight invasive species with related non-invasive species, revealed repeated expansion of gene families associated with abiotic stress tolerance and developmental regulation, suggesting convergent adaptive strategies in the grass family for invasive success. Together, these results demonstrate genomic architecture linked to invasion success and highlight potential targets for managing invasive grasses.

Plant Biology↗

The curious case of a Chilean copepod (Tigriopus aff. angulatus) genome assembly

Tigriopus copepods are found in splash pools on all seven continents from the equator to Arctic and Antarctic regions. Given their geographic distribution, frequent exposure to extreme environmental conditions, and strong signatures of local adaptation, these copepods have become models for exploring patterns of adaptation to stressful environments. However, most studies focus on a small subset of Tigriopus species, and there are few genome resources representing the diversity of Tigriopus species and populations. Here, we combine long-read, Pacific Biosciences HiFi data with short-read, Illumina HiC and RNA-seq data to assemble and annotate a genome representing a Tigriopus population from the coast of central Chile. Based on the level of divergence that we observed in mitochondrial genes, we also performed a comparison of morphological characteristics between this population and members of the T. angulatus complex. The assembly that we generated (qhTigAngs1.1.pri) includes 12 major scaffolds (N50 19Mbp, L50 7), equivalent to the number of chromosomes in other Tigriopus species. BUSCO and k-mer analyses of the assembly and BUSCO analyses of gene models are relatively complete (89-99%) with respect to gene or k-mer content. The level of divergence that we observed, morphological differences we recorded, and the spatial distance of this population from the type locality suggest that this Chilean population of Tigriopus may represent a novel species that we call Tigriopus aff. angulatus. These genomic resources will help us understand the diversity and structure of Tigriopus species and populations as well as facilitate future comparisons of adaptation across parallel environmental gradients.

genomics↗

Genetic assimilation and accommodation shape adaptation to heat stress in a splash pool copepod

Understanding how organisms respond to variable environments is becoming increasingly important in our rapidly changing world. Beyond genetic adaptation, plastic responses to the environment can alter phenotypes and fitness, ultimately driving evolution. However, the interaction between plasticity and adaptation during environmental change is complex and hard to measure in natural systems. Here, we used two populations of Tigriopus californicus copepods, a thermally tolerant southern population and a thermally sensitive northern population, to conduct a fully factorial split brood experiment where we exposed animals as larvae and adults to either a sublethal heat stress or control (no heat treatment) before measuring heat tolerance and gene expression patterns. We found that increased thermal tolerance across populations came at the expense of physiological plasticity and evolved through higher baseline expression of heat stress response genes across environmental contexts as well as increased gene expression plasticity in response to heat stress. In the thermally sensitive northern population, developmental exposure to heat stress led to higher adult tolerance and lower physiological plasticity underpinned by higher gene expression plasticity. Importantly, we found that the same set of genes were largely responsible for both the evolved higher tolerance in the southern population and the developmentally induced tolerance in the northern population suggesting that in this system, a shared molecular response contributes to acclimation and adaptation across both populations. These results link existing physiological plasticity with long-term evolutionary responses providing insight into how these populations will adapt and respond to future environmental change. SIGNIFICANCEUnderstanding plastic and evolutionary responses to dynamic environments is critical to anticipating species vulnerability to climate change. In this study, we compared gene expression and physiological responses to heat stress across two populations of a marine copepod that differ in thermal tolerance to investigate mechanisms of adaptation. We found evidence for plasticity-led evolution in this system, with the same set of genes contributing to long-term evolutionary changes across populations and to short-term physiological adjustments within populations. Our results suggest that populations with a reservoir of plasticity have a greater potential to evolve as the climate continues to warm, but that there may be a limit to this adaptive capacity.

evolutionary biology↗

Transcriptome responses of two Halophila stipulacea seagrass populations from pristine and impacted habitats, to single and combined thermal and excess nutrient stressors, reveal local adaptive features and core stress-response genes

In their natural habitats, seagrasses face multiple abiotic stressors, which can often occur simultaneously. However, most studies investigating the effects of environmental stressors on seagrasses have focused on growth and physiological responses to single stressors. Here, we examined the transcriptome responses of the tropical seagrass Halophila stipulacea collected from a northern Gulf of Aqaba pristine site (South Beach - SB) and an anthropogenically-impacted site (Tur Yam - TY), grown in a mesocosm, and exposed to ecologically-relevant, single and combined, thermal and excess nutrient stressors. The combined thermal and nutrient stressor elicited greater transcriptome reprogramming than the single stressors in both populations and induced the expression of a combination-specific set of genes involved in abiotic and biotic stress responses. Furthermore, thermal stress exerted a more dominant influence than excess nutrient stress upon the transcriptome response to the combined stress. Transcriptomes of plants from the impacted TY site displayed reduced plasticity, the presence of genes exhibiting a "stress-ready" mode of expression under all stresses, and increased resilience (recovery to control transcriptomes). We also identified core stress-response genes that could be leveraged as early indicators of stress in the field. Overall, our data suggest that environmental conditions in seagrass habitats can drive local molecular adaptation, and that the response of seagrasses to combined stressors associated with climate change and coastal anthropogenic stressors cannot be predicted from the response to single stressors.

plant biology↗

Diversification of gene expression across extremophytes and stress-sensitive species in the Brassicaceae

Plants are composed of diverse cell types that facilitate adaptations to the environment, yet cross-species comparisons of such response programs at single-cell resolution remain scarce. To explore this diversity, here we profiled >200,000 root cells from five Brassicaceae species, including stress-sensitive species (Arabidopsis thaliana, Sisymbrium irio), extremophytes (Eutrema salsugineum, Schrenkiella parvula), and the polyploid crop Camelina sativa under control, NaCl, and abscisic acid (ABA) treatments. We developed a computational pipeline to characterize the conservation and divergence of cell-type gene expression across the Brassicaceae, revealing that approximately half of previously defined Arabidopsis cell-type markers fail to maintain conserved expression in one or more non-Arabidopsis species. Therefore, we curated a refined set of pan-Brassicaceae markers and identified orthologs whose expression profiles have diverged across lineages. Using in situ hybridization, we mapped distinct cortex subpopulations to specific cortical layers across species, and found flavonoid biosynthesis programs preferentially localized to the inner cortex layer, linking cortex-layer specification to metabolic specialization. Cell-type contributions to stress responses differed among species and across treatments, with lineage-specific losses of responsiveness occurring less frequently but evolutionarily more favored than lineage-specific gains. In C. sativa, sub-genomes contributed equally to stress responses, and homeologs with divergent responses typically lacked other signatures of functional divergence. Together, this work establishes a foundational root single-cell atlas and an analytical framework for multi-species comparative transcriptomics, providing insights into how stress responses diversify across cell types, stress-sensitive to stress-adapted species, and in crop lineages.

plant biology↗

Studies of CrHCF244 reveal similarities and differences in psbA translation between Chlamydomonas reinhardtii and Arabidopsis thaliana

Translation of psbA, the chloroplast gene that encodes the D1 subunit of Photosystem II (PSII), is important for both PSII biogenesis and repair. The translation of the psbA transcript in the chloroplast is under the control of nuclear gene products. Using a Chlamydomonas forward genetic screen and whole genome sequencing, we found a mutant defective in PSII activity and mapped the causative gene to be the homolog of Arabidopsis High Fluorescence (HCF244) gene, or CrHCF244. We then demonstrated that CrHCF244 is required for psbA translation in the alga, consistent with the function of HCF244 in Arabidopsis. The Arabidopsis HCF244 gene also partially complemented the algal mutant. These results experimentally support the functional conservation of the homologs in green algae and land plants. Intriguingly, the CrHCF244 mutant also exhibited a relatively high rate of suppressor mutants, pointing to the presence of alternative factor(s)/pathway(s) for D1 translation control. The establishment of CrHCF244 as a psbA translation factor in Chlamydomonas showed the similarities in psbA translation regulation in algae and plants. The future identification of the alternative factor(s) in this alga will provide insights on psbA translation in plants. HighlightWe identified CrHCF244 as a translation factor of psbA in Chlamydomonas. Arabidopsis HCF244 partially complements Chlamydomonas {Delta}CrHCF244 mutant, indicating semi-conservation of the function of this gene between organisms. Suppressor mutants of {Delta}CrHCF244 suggest the presence of alternative translation factors in psbA translation.

plant biology↗

The Tofu mutation restores female fertility to Drosophila with a null BEAF mutation

Compensatory mutations offer clues to deciphering the role of a particular protein in cellular processes. Here we investigate an unknown compensatory mutation, present in the BEAFNP6377 fly line, that provides sufficient rescue of the defective ovary phenotype caused by null BEAF alleles to allow maintenance of fly stocks lacking the chromatin domain insulator proteins Boundary Element-Associated Factors BEAF-32A and BEAF-32B. We call this mutation Tofu. We employ both classical genetics and genomic sequencing to attempt to identify the mutation. We find evidence that points to a mutation in a predicted Polycomb response element upstream of the ribbon gene, which may lead to aberrant rib expression.

genetics↗

Spatiotemporal gene expression atlas of the extremophyte Schrenkiella parvula

Extremophytes are naturally selected to survive environmental stresses, but scarcity of genetic resources for them developed with spatiotemporal resolution limit their use in stress biology. Schrenkiella parvula is one of the leading extremophyte models with initial molecular genomic resources developed to study its tolerance mechanisms to high salinity. Here we present a transcriptome atlas for S. parvula with subsequent analyses to highlight its diverse gene expression networks associated with salt responses. We included spatiotemporal expression profiles, expression specificity of each gene, and co-expression and functional gene networks representing 115 transcriptomes sequenced from 35 tissue and developmental stages examining their responses before and after 27 salt treatments in our current study. The highest number of tissue-preferentially expressed genes were found in seeds and siliques while genes in seedlings showed the broadest expression profiles among developmental stages. Seedlings had the highest magnitude of overall transcriptomic responses to salinity compared to mature tissues and developmental stages. Differentially expressed genes in response to salt were largely mutually exclusive but shared common stress response pathways spanning across tissues and developmental stages. Our foundational dataset created for S. parvula representing a stress-adapted wild plant lays the groundwork for future functional, comparative, and evolutionary studies using extremophytes aiming to uncover novel stress tolerant mechanisms. SIGNIFICANCE STATEMENTConcerted transcriptomic responses coordinated across developmental stages and tissues are required to complete a plant lifecycle under salt stress. Transcriptomic resources created with spatiotemporal resolution for plants are rare and for stress-adapted plants rarer. We present a transcriptome atlas enabling discovery of genes and networks evolved as adaptations to salt stress in a model extremophyte, Schrenkiella parvula. The spatiotemporally resolved gene expression networks are largely non-overlapping but functionally connected through synergistic stress responsive pathways.

plant biology↗

Alternative splicing preferentially increases transcript diversity associated with stress responses in the extremophyte Schrenkiella parvula

Alternative splicing extends the coding potential of genomes by creating multiple isoforms from one gene. Isoforms can render transcript specificity and diversity to initiate multiple responses required during transcriptome adjustments in stressed environments. Although the prevalence of alternative splicing is widely recognized, how diverse isoforms facilitate stress adaptation in plants that thrive in extreme environments are unexplored. Here we examine how an extremophyte model, Schrenkiella parvula, coordinates alternative splicing in response to high salinity compared to a salt-stress sensitive model, Arabidopsis thaliana. We use Iso-Seq to generate full length reference transcripts and RNA-seq to quantify differential isoform usage in response to salinity changes. We find that single-copy orthologs where S. parvula has a higher number of isoforms than A. thaliana as well as S. parvula genes observed and predicted using machine learning to have multiple isoforms are enriched in stress associated functions. Genes that showed differential isoform usage were largely mutually exclusive from genes that were differentially expressed in response to salt. S. parvula transcriptomes maintained specificity in isoform usage assessed via a measure of expression disorderdness during transcriptome reprogramming under salt. Our study adds a novel resource and insight to study plant stress tolerance evolved in extreme environments.

plant biology↗

Multiple paths lead to salt tolerance - pre-adaptation vs dynamic responses from two closely related extremophytes

Salt tolerance is a complex trait with much of the underlying genetic variation and integrated response strategies yet to be discovered from stress adapted plants. Schrenkiella parvula and Eutrema salsugineum are salt-tolerant extremophytes related to Arabidopsis thaliana in Brassicaceae. We investigated their response strategies contrasted against the salt-sensitive model, A. thaliana to cope with salt stresses via transcriptomic, metabolomic, and ionomic adjustments. The extremophytes exemplified divergent routes to achieve nutrient balance, build osmotolerance, boost antioxidant capacity, and extend transcriptomic support for modified ion transport and stress signaling. Those led to similar molecular phenotypes adapted to salt stress in the extremophytes, absent in A. thaliana. The predominant transcriptomic signals in all three species were associated with salt stress. However, root architecture modulation mediated by negative regulation of auxin and ABA signaling supported minimally-affected root growth unique to each extremophyte during salt treatments. Overall, E. salsugineum exhibited pre-adapted responses at the metabolome level, whereas S. parvula showed dynamic metabolomic responses coupled to a pre-adapted transcriptome to survive salt stress. Our work shows that the two extremophytes share common salt tolerance features, but differ substantially in pathways leading to the convergent, adaptive traits.

plant biology↗

Balancing growth amidst salinity stress-lifestyle perspectives from the extremophyte model Schrenkiella parvula

Schrenkiella parvula, a leading extremophyte model in Brassicaceae, can grow and complete its life cycle under multiple environmental stresses, including high salinity. While foundational genomic resources have been created for S. parvula, a comprehensive physiological or structural characterization of its salt stress responses is absent. We aimed to identify the influential traits that lead to stress-resilient growth of this species. We examined salt-induced changes in the physiology and anatomy of S. parvula throughout its lifecycle across multiple tissues. We found that S. parvula maintains or even exhibits enhanced growth during various developmental stages at salt stress levels known to inhibit growth in Arabidopsis and most crops. The resilient growth of S. parvula was associated with key traits that synergistically allow continued primary root growth, expansion of xylem vessels across the root-shoot continuum, and a high capacity to maintain tissue water levels by developing larger and thicker leaves while facilitating continued photosynthesis during salt stress. These traits at the vegetative phase were followed by a successful transition to the reproductive phase via early flowering, development of larger siliques, and production of viable seeds during salt stress. Additionally, the success of self-fertilization during early flowering stages was dependent on salt-induced filament elongation in flowers that aborted in the absence of salt. Our results suggest that the maintenance of leaf water status and enhancement of selfing in early flowers to ensure reproductive success, are among the most influential traits that contribute to the extremophyte lifestyle of S. parvula in its natural habitat. One sentence summarySchrenkiella parvula salt-resilient growth is facilitated by uncompromised primary root growth, expansion of xylem vessels, maintenance of leaf water status and photosynthesis, and early flowering.

plant biology↗

Living with high potassium: an asset or a hindrance

O_LIHigh potassium (K) in the growth medium is more toxic to plants than Na at similar concentrations. However, the molecular mechanisms underlying plant responses to K-induced salt stress are virtually unknown. C_LIO_LIWe examined Arabidopsis thaliana and its extremophyte relative Schrenkiella parvula, using a comparative multi-omics approach to identify cellular processes affected by excess K and understand which deterministic regulatory pathways are active to avoid tissue damage while sustaining growth. C_LIO_LIA. thaliana showed limited capacity to curb excess K accumulation and prevent nutrient depletion contrasting to S. parvula which could limit excess K accumulation without restricting nutrient uptake. Facilitated by a targeted transcriptomic response, promoting nitrogen uptake along with other key nutrients and uninterrupted N assimilation into primary metabolites during excess K-stress allowed S. parvula to boost its antioxidant and osmolyte pools concurrently leading to sustained growth. Antithetically, A. thaliana showed transcriptional responses indicative of a poor balance between stress signaling, increased ROS levels, and reduced photosynthesis, subsequently leading to inhibited growth. C_LIO_LIThe ability to regulate independent nutrient uptake and a coordinated transcriptomic response to avoid non-specific stress signaling are two main deterministic steps towards building stress resilience to excess K+-induced salt stress. C_LI

plant biology↗

Positive Selection and Heat-Response Transcriptomes Reveal Adaptive Features of the Arabidopsis Desert Relative, Anastatica hierochuntica

O_LIPlant adaptation to a desert environment and its endemic heat stress is poorly understood at the molecular level. The naturally heat-tolerant Brassicaceae species Anastatica hierochuntica is an ideal extremophyte model to identify genetic adaptations that have evolved to allow plants to tolerate heat stress and thrive in deserts. C_LIO_LIWe generated an A. hierochuntica reference transcriptome and pinpointed extremophyte adaptations by comparing Arabidopsis thaliana and A. hierochuntica transcriptome responses to heat and identifying positively selected genes in A. hierochuntica. C_LIO_LIThe two species exhibit similar transcriptome adjustment in response to heat and the A. hierochuntica transcriptome does not exist in a constitutive heat "stress-ready" state. Furthermore, the A. hierochuntica global transcriptome as well as heat-responsive orthologs, display a lower basal and higher heat-induced expression than in A. thaliana. Genes positively selected in multiple extremophytes are associated with stomatal opening, nutrient acquisition, and UV-B induced DNA repair while those unique to A. hierochuntica are consistent with its photoperiod-insensitive, early-flowering phenotype. C_LIO_LIWe suggest that evolution of a flexible transcriptome confers the ability to quickly react to extreme diurnal temperature fluctuations characteristic of a desert environment while positive selection of genes involved in stress tolerance and early flowering could facilitate an opportunistic desert lifestyle. C_LI

plant biology↗

Novel genome characteristics contribute to the invasiveness of Phragmites australis (common reed)

The rapid invasion of the non-native Phragmites australis (Poaceae, subfamily Arundinoideae) is a major threat to native ecosystems in North America. We describe a 1.14 Gbp reference genome for P. australis and compare invasive (ssp. australis) and native (ssp. americanus) genotypes collected across the Laurentian Great Lakes to deduce genomic bases driving its invasive success. We report novel genomic features including a lineage-specific whole genome duplication, followed by gene loss and preferential retention of genes associated with transcription factors and regulatory functions in the remaining duplicates. The comparative transcriptomic analyses revealed that genes associated with biotic stress and defense responses were expressed at a higher basal level in invasive genotypes, but the native genotypes showed a stronger induction of defense responses following fungal inoculation. The reference genome and transcriptomes, combined with previous ecological and environmental data, support the development of novel, genomics-assisted management approaches for invasive Phragmites.

plant biology↗

Divergence in a stress-associated gene regulatory network underlies differential growth control in the Brassicaceae family

The phytohormone abscisic acid (ABA) is a central regulator of acclimation during environmental stress. While some plants exhibit tremendous stress resilience, it has been unclear whether differences in ABA response underlie such adaptations. Here we establish a cross-species gene regulatory network (GRN) for ABA to identify broadly conserved, core components of the ABA signaling network and peripheral pathways exhibiting species-specific connectivity. Genes that are broadly conserved in the network share promoter architecture and patterns of gene expression. Networks associated with growth hormones exhibited highly divergent wiring of their ABA network leading to changes in the physiological outcome of signaling. Together our study provides a model for understanding how GRN subcircuits deploy different growth regulatory states across ecologically diverse species. One Sentence SummaryComparative studies reveal core and peripheral stress-mediated gene networks driving divergent growth control in plants.

plant biology↗