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  1. Abstract Background and aims

    Hakea prostrata(Proteaceae) is a highly phosphorus-use-efficient plant native to southwest Australia. It maintains a high photosynthetic rate at low leaf phosphorus (P) and exhibits delayed leaf greening, a convergent adaptation that increases nutrient-use efficiency. This study aimed to provide broad physiological and gene expression profiles across leaf development, uncovering pathways leading from young leaves as nutrient sinks to mature leaves as low-nutrient, energy-transducing sources.

    Methods

    To explore gene expression underlying delayed greening, we analysed a de novo transcriptome forH. prostrataacross five stages of leaf development. Photosynthesis and respiration rates, and foliar pigment, P and nitrogen (N) concentrations were determined, including the division of P into five biochemical fractions.

    Key results

    Transcripts encoding functions associated with leaf structure generally decreased in abundance across leaf development, concomitant with decreases in foliar concentrations of 85% for anthocyanins, 90% for P and 70% for N. The expression of genes associated with photosynthetic function increased during or after leaf expansion, in parallel with increases in photosynthetic pigments and activity, much later in leaf development than in species that do not have delayed greening. As leaves developed, transcript abundance for cytosolic and mitochondrial ribosomal proteins generally declined, whilst transcripts for chloroplast ribosomal proteins increased.

    Conclusions

    There was a much longer temporal separation of leaf cell growth from chloroplast development inH. prostratathan is found in species that lack delayed greening. Transcriptome-guided analysis of leaf development inH. prostrataprovided insight into delayed greening as a nutrient-saving strategy in severely phosphorus-impoverished landscapes.

     
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  2. Abstract

    Model species continue to underpin groundbreaking plant science research. At the same time, the phylogenetic resolution of the land plant Tree of Life continues to improve. The intersection of these two research paths creates a unique opportunity to further extend the usefulness of model species across larger taxonomic groups. Here we promote the utility of the Arabidopsis thaliana model species, especially the ability to connect its genetic and functional resources, to species across the entire Brassicales order. We focus on the utility of using genomics and phylogenomics to bridge the evolution and diversification of several traits across the Brassicales to the resources in Arabidopsis, thereby extending scope from a model species by establishing a “model clade”. These Brassicales-wide traits are discussed in the context of both the model species Arabidopsis thaliana and the family Brassicaceae. We promote the utility of such a “model clade” and make suggestions for building global networks to support future studies in the model order Brassicales.

     
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    Free, publicly-accessible full text available October 12, 2024
  3. SUMMARY

    Cell differentiation and morphogenesis are crucial for the establishment of diverse cell types and organs in multicellular organisms. Trichome cells offer an excellent paradigm for dissecting the regulatory mechanisms of plant cell differentiation and morphogenesis due to their unique growth characteristics. Here, we report the isolation of an Arabidopsis mutant,aberrantlybranchedtrichome 3–1(abt3‐1), with a reduced trichome branching phenotype. Positional cloning and molecular complementation experiments confirmed thatabt3‐1is a new mutant allele ofAuxin resistant 1(AXR1), which encodes the N‐terminal half of ubiquitin‐activating enzyme E1 and functions in auxin signaling pathway. Meanwhile, we found that transgenic plants expressing constitutively active version ofROP2(CA‐ROP2) caused a reduction of trichome branches, resembling that ofabt3‐1. ROP2 is a member of Rho GTPase of plants (ROP) family, serving as versatile signaling switches involved in a range of cellular and developmental processes. Our genetic and biochemical analyses showedAXR1genetically interacted withROP2and mediated ROP2 protein stability. The loss ofAXR1aggravated the trichome defects ofCA‐ROP2and induced the accumulation of steady‐state ROP2. Consistently, elevatedAXR1expression levels suppressedROP2expression and partially rescued trichome branching defects inCA‐ROP2plants. Together, our results presented a new mutant allele ofAXR1, uncovered the effects ofAXR1andROP2during trichome development, and revealed a pathway ofROP2‐mediated regulation of plant cell morphogenesis in Arabidopsis.

     
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    Free, publicly-accessible full text available November 1, 2024
  4. Summary

    In superrosid species, root epidermal cells differentiate into root hair cells and nonhair cells. In some superrosids, the root hair cells and nonhair cells are distributed randomly (Type I pattern), and in others, they are arranged in a position‐dependent manner (Type III pattern). The model plant Arabidopsis (Arabidopsis thaliana) adopts the Type III pattern, and the gene regulatory network (GRN) that controls this pattern has been defined. However, it is unclear whether the Type III pattern in other species is controlled by a similar GRN as in Arabidopsis, and it is not known how the different patterns evolved.

    In this study, we analyzed superrosid speciesRhodiola rosea,Boehmeria nivea, andCucumis sativusfor their root epidermal cell patterns. Combining phylogenetics, transcriptomics, and cross‐species complementation, we analyzed homologs of the Arabidopsis patterning genes from these species.

    We identifiedR. roseaandB. niveaas Type III species andC. sativusas Type I species. We discovered substantial similarities in structure, expression, and function of Arabidopsis patterning gene homologs inR. roseaandB. nivea, and major changes inC. sativus.

    We propose that in superrosids, diverse Type III species inherited the patterning GRN from a common ancestor, whereas Type I species arose by mutations in multiple lineages.

     
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  5. 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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  6. Summary

    Plant adaptation to a desert environment and its endemic heat stress is poorly understood at the molecular level. The naturally heat‐tolerant Brassicaceae speciesAnastatica hierochunticais an ideal extremophyte model to identify genetic adaptations that have evolved to allow plants to tolerate heat stress and thrive in deserts.

    We generated anA. hierochunticareference transcriptome and identified extremophyte adaptations by comparingArabidopsis thalianaandA. hierochunticatranscriptome responses to heat, and detecting positively selected genes inA. hierochuntica.

    The two species exhibit similar transcriptome adjustment in response to heat and theA. hierochunticatranscriptome does not exist in a constitutive heat ‘stress‐ready’ state. Furthermore, theA. hierochunticaglobal 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. hierochunticaare 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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  7. Abstract

    The rapid invasion of the non‐nativePhragmites australis(Poaceae, subfamily Arundinoideae) is a major threat to native wetland ecosystems in North America and elsewhere. We describe the first reference genome forPaustralisand 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 aPhragmiteslineage‐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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  8. 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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  9. 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‐sensitiveArabidopsis thalianaand 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 parvulamaintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron.Schrenkiella parvulaexcludes 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. parvulafacilitates critical cellular processes while maintaining the pool of ribose‐containing compounds that can bind with boric acid.

    TheS. parvulatranscriptome 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.

     
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  10. Free, publicly-accessible full text available August 3, 2024