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SUMMARY Schrenkiella parvula , a leading extremophyte model in Brassicaceae, can grow and complete its lifecycle under multiple environmental stresses, including high salinity. Yet, the key physiological and structural traits underlying its stress‐adapted lifestyle are unknown along with trade‐offs when surviving salt stress at the expense of growth and reproduction. We aimed to identify the influential adaptive trait responses that lead to stress‐resilient and uncompromised growth across developmental stages when treated with salt at levels known to inhibit growth in Arabidopsis and most crops. Its resilient growth was promoted by traits that synergistically allowed primary root growth in seedlings, the expansion of xylem vessels across the root‐shoot continuum, and a high capacity to maintain tissue water levels by developing thicker succulent leaves while enabling photosynthesis during salt stress. A successful transition from vegetative to reproductive phase was initiated by salt‐induced early flowering, resulting in viable seeds. Self‐fertilization in salt‐induced early flowering was dependent upon filament elongation in flowers otherwise aborted in the absence of salt during comparable plant ages. The maintenance of leaf water status promoting growth, and early flowering to ensure reproductive success in a changing environment, were among the most influential traits that contributed to the extremophytic lifestyle ofS. parvula . -
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Summary Plant 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.We generated an
A. hierochuntica reference transcriptome and identified extremophyte adaptations by comparingArabidopsis thaliana andA. hierochuntica transcriptome responses to heat, and detecting positively selected genes inA. hierochuntica .The 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, theA. hierochuntica global transcriptome as well as heat‐responsive orthologs, display a lower basal and higher heat‐induced expression than inA. thaliana . Genes positively selected in multiple extremophytes are associated with stomatal opening, nutrient acquisition, and UV‐B induced DNA repair while those unique toA. hierochuntica are consistent with its photoperiod‐insensitive, early‐flowering phenotype.We 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.
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Abstract The rapid invasion of the non‐native
Phragmites australis (Poaceae, subfamily Arundinoideae) is a major threat to native wetland ecosystems in North America and elsewhere. We describe the first reference genome forP .australis and compare invasive (ssp.australis ) and native (ssp.americanus ) genotypes collected from replicated populations across the Laurentian Great Lakes to deduce genomic bases driving its invasive success. Here, we report novel genomic features including aPhragmites 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. Comparative transcriptomic analyses revealed that genes associated with biotic stress and defence responses were expressed at a higher basal level in invasive genotypes, but native genotypes showed a stronger induction of defence responses when challenged by a fungal endophyte. The reference genome and transcriptomes, combined with previous ecological and environmental data, add to our understanding of mechanisms leading to invasiveness and support the development of novel, genomics‐assisted management approaches for invasivePhragmites . -
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Abstract As an essential micronutrient for many organisms, sodium plays an important role in ecological and evolutionary dynamics. Although plants mediate trophic fluxes of sodium, from substrates to higher trophic levels, relatively little comparative research has been published about plant growth and sodium accumulation in response to variation in substrate sodium. Accordingly, we carried out a systematic review of plants' responses to variation in substrate sodium concentrations.
We compared biomass and tissue‐sodium accumulation among 107 cultivars or populations (67 species in 20 plant families), broadly expanding beyond the agricultural and model taxa for which several generalizations previously had been made. We hypothesized a priori response models for each population's growth and sodium accumulation as a function of increasing substrate NaCl and used Bayesian Information Criterion to choose the best model. Additionally, using a phylogenetic signal analysis, we tested for phylogenetic patterning of responses across taxa.
The influence of substrate sodium on growth differed across taxa, with most populations experiencing detrimental effects at high concentrations. Irrespective of growth responses, tissue sodium concentrations for most taxa increased as sodium concentration in the substrate increased. We found no strong associations between the type of growth response and the type of sodium accumulation response across taxa. Although experiments often fail to test plants across a sufficiently broad range of substrate salinities, non‐crop species tended toward higher sodium tolerance than domesticated species. Moreover, some phylogenetic conservatism was apparent, in that evolutionary history helped predict the distribution of total‐plant growth responses across the phylogeny, but not sodium accumulation responses.
Our study reveals that saltier plants in saltier soils proves to be a broadly general pattern for sodium across plant taxa. Regardless of growth responses, sodium accumulation mostly followed an increasing trend as substrate sodium levels increased.
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Summary Boron toxicity is a world‐wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants.
We employed a cross‐species comparison between boron stress‐sensitive
Arabidopsis thaliana and its boron stress‐tolerant extremophyte relativeSchrenkiella parvula , and a multi‐omics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.Schrenkiella parvula maintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron.Schrenkiella parvula excludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyteS. parvula facilitates critical cellular processes while maintaining the pool of ribose‐containing compounds that can bind with boric acid.The
S. parvula transcriptome is pre‐adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron‐stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity. -
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.more » « less
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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.more » « less
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Plant vascular systems can translocate the entomopathogen Bacillus thuringiensis from the soil into plant tissues. However, whether other soil dwelling entomopathogens utilize plant vascular tissue for movement has not yet been fully explored. We used Spodoptera frugiperda multiple nucleopolyhedrovirus (SfMNPV) to evaluate whether baculoviruses, a common entomopathogen and bioinsecticide, can be transported through the plant vascular pathways of Zea mays. We found that our treatments did not allow a sufficient virus translocation into the plant to induce a lethal infection in insects, which was confirmed by a molecular analysis. While other entomopathogens translocate, baculoviruses may not be one of them.more » « less
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