Nejvíce citovaný článek - PubMed ID 30230555
Dispersal biophysics and adaptive significance of dimorphic diaspores in the annual Aethionema arabicum (Brassicaceae)
BACKGROUND: The biomechanical, morphological and ecophysiological properties of plant seed/fruit structures are adaptations that support survival in unpredictable environments. High phenotypic variability of noxious and invasive weed species such as Raphanus raphanistrum (wild radish) allow diversification into new environmental niches. Dry indehiscent fruits (thick and lignified pericarp [fruit coat] enclosing seeds) have evolved many times independently. METHODS: A multiscale biomechanics and imaging (microscopy, X-ray, finite element stress simulation, puncture force analysis) approach was used to comparatively investigate the indehiscent fruits of R. raphanistrum (global weed), R. pugioniformis (endemic weed) and R. sativus (cultivated radish). RESULTS: The hard pericarp of Raphanus species (Brassicaceae) imposes mechanical dormancy by preventing full phase-II water uptake of the enclosed seeds. The apparently unilocular fruits of Raphanus species develop from two fused valves, pericarp rupture to permit germination is confined to the midvalve regions, and each midvalve region contains a predetermined breaking zone that is biomechanically defined by the internal shape of the seed chambers. Direct biomechanical analysis revealed great variability in within-fruit and between-fruits pericarp resistances. CONCLUSIONS: Variability in pericarp-imposed dormancy provides a bet-hedging strategy to affect soil seed bank persistence and prolong the germinability period.
- Klíčová slova
- Functional morphology, finite element stress simulation, fruit coat biomechanics, pericarp-imposed mechanical dormancy, predetermined breaking zone, soil seed bank persistence,
- MeSH
- analýza metodou konečných prvků MeSH
- biomechanika MeSH
- klíčení * fyziologie MeSH
- ovoce * fyziologie anatomie a histologie MeSH
- Raphanus * fyziologie anatomie a histologie MeSH
- semena rostlinná fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- srovnávací studie MeSH
Plants in habitats with unpredictable conditions often have diversified bet-hedging strategies that ensure fitness over a wider range of variable environmental factors. A striking example is the diaspore (seed and fruit) heteromorphism that evolved to maximize species survival in Aethionema arabicum (Brassicaceae) in which external and endogenous triggers allow the production of two distinct diaspores on the same plant. Using this dimorphic diaspore model, we identified contrasting molecular, biophysical, and ecophysiological mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained by pericarp (fruit coat) removal from IND fruits. Large-scale comparative transcriptome and hormone analyses of M+ seeds, IND fruits, and M- seeds provided comprehensive datasets for their distinct thermal responses. Morph-specific differences in co-expressed gene modules in seeds, as well as in seed and pericarp hormone contents, identified a role of the IND pericarp in imposing coat dormancy by generating hypoxia affecting abscisic acid (ABA) sensitivity. This involved expression of morph-specific transcription factors, hypoxia response, and cell wall remodeling genes, as well as altered ABA metabolism, transport, and signaling. Parental temperature affected ABA contents and ABA-related gene expression and altered IND pericarp biomechanical properties. Elucidating the molecular framework underlying the diaspore heteromorphism can provide insight into developmental responses to globally changing temperatures.
- MeSH
- Brassicaceae * genetika fyziologie metabolismus MeSH
- klíčení * genetika fyziologie MeSH
- kyselina abscisová metabolismus MeSH
- ovoce * genetika fyziologie růst a vývoj metabolismus MeSH
- regulace genové exprese u rostlin * MeSH
- regulátory růstu rostlin metabolismus MeSH
- semena rostlinná * genetika fyziologie růst a vývoj metabolismus MeSH
- teplota * MeSH
- transkriptom genetika MeSH
- vegetační klid genetika fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- kyselina abscisová MeSH
- regulátory růstu rostlin MeSH
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 2 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 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.
The transition from germinating seeds to emerging seedlings is one of the most vulnerable plant life cycle stages. Heteromorphic diaspores (seed and fruit dispersal units) are an adaptive bet-hedging strategy to cope with spatiotemporally variable environments. While the roles and mechanisms of seedling traits have been studied in monomorphic species, which produce one type of diaspore, very little is known about seedlings in heteromorphic species. Using the dimorphic diaspore model Aethionema arabicum (Brassicaceae), we identified contrasting mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained from IND fruits by pericarp (fruit coat) removal. What follows the completion of germination is the pre-emergence seedling growth phase, which we investigated by comparative growth assays of early seedlings derived from the M+ seeds, bare M- seeds, and IND fruits. The dimorphic seedlings derived from M+ and M- seeds did not differ in their responses to ambient temperature and water potential. The phenotype of seedlings derived from IND fruits differed in that they had bent hypocotyls and their shoot and root growth was slower, but the biomechanical hypocotyl properties of 15-day-old seedlings did not differ between seedlings derived from germinated M+ seeds, M- seeds, or IND fruits. Comparison of the transcriptomes of the natural dimorphic diaspores, M+ seeds and IND fruits, identified 2,682 differentially expressed genes (DEGs) during late germination. During the subsequent 3 days of seedling pre-emergence growth, the number of DEGs was reduced 10-fold to 277 root DEGs and 16-fold to 164 shoot DEGs. Among the DEGs in early seedlings were hormonal regulators, in particular for auxin, ethylene, and gibberellins. Furthermore, DEGs were identified for water and ion transporters, nitrate transporter and assimilation enzymes, and cell wall remodeling protein genes encoding enzymes targeting xyloglucan and pectin. We conclude that the transcriptomes of seedlings derived from the dimorphic diaspores, M+ seeds and IND fruits, undergo transcriptional resetting during the post-germination pre-emergence growth transition phase from germinated diaspores to growing seedlings.
The view on the role of light during seed germination stems mainly from studies with Arabidopsis (Arabidopsis thaliana), where light is required to initiate this process. In contrast, white light is a strong inhibitor of germination in other plants, exemplified by accessions of Aethionema arabicum, another member of Brassicaceae. Their seeds respond to light with gene expression changes of key regulators converse to that of Arabidopsis, resulting in opposite hormone regulation and prevention of germination. However, the photoreceptors involved in this process in A. arabicum remain unknown. Here, we screened a mutant collection of A. arabicum and identified koy-1, a mutant that lost light inhibition of germination due to a deletion in the promoter of HEME OXYGENASE 1, the gene for a key enzyme in the biosynthesis of the phytochrome chromophore. koy-1 seeds were unresponsive to red- and far-red light and hyposensitive under white light. Comparison of hormone and gene expression between wild type and koy-1 revealed that very low light fluence stimulates germination, while high irradiance of red and far-red light is inhibitory, indicating a dual role of phytochromes in light-regulated seed germination. The mutation also affects the ratio between the 2 fruit morphs of A. arabicum, suggesting that light reception via phytochromes can fine-tune several parameters of propagation in adaptation to conditions in the habitat.
- MeSH
- Arabidopsis * metabolismus MeSH
- Brassicaceae * genetika MeSH
- fytochrom * genetika metabolismus MeSH
- hormony metabolismus MeSH
- klíčení genetika MeSH
- proteiny huseníčku * genetika metabolismus MeSH
- semena rostlinná genetika MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- fytochrom * MeSH
- hormony MeSH
- proteiny huseníčku * MeSH
Aethionema arabicum is an important model plant for Brassicaceae trait evolution, particularly of seed (development, regulation, germination, dormancy) and fruit (development, dehiscence mechanisms) characters. Its genome assembly was recently improved but the gene annotation was not updated. Here, we improved the Ae. arabicum gene annotation using 294 RNA-seq libraries and 136 307 full-length PacBio Iso-seq transcripts, increasing BUSCO completeness by 11.6% and featuring 5606 additional genes. Analysis of orthologs showed a lower number of genes in Ae. arabicum than in other Brassicaceae, which could be partially explained by loss of homeologs derived from the At-α polyploidization event and by a lower occurrence of tandem duplications after divergence of Aethionema from the other Brassicaceae. Benchmarking of MADS-box genes identified orthologs of FUL and AGL79 not found in previous versions. Analysis of full-length transcripts related to ABA-mediated seed dormancy discovered a conserved isoform of PIF6-β and antisense transcripts in ABI3, ABI4 and DOG1, among other cases found of different alternative splicing between Turkey and Cyprus ecotypes. The presented data allow alternative splicing mining and proposition of numerous hypotheses to research evolution and functional genomics. Annotation data and sequences are available at the Ae. arabicum DB (https://plantcode.online.uni-marburg.de/aetar_db).
- Klíčová slova
- Aethionema arabicum, Brassicaceae evolution, Iso-seq, alternative splicing, genome annotation, seed germination, transcription factors,
- MeSH
- Brassicaceae genetika metabolismus fyziologie MeSH
- genom rostlinný genetika MeSH
- klíčení genetika fyziologie MeSH
- regulace genové exprese u rostlin genetika fyziologie MeSH
- semena rostlinná genetika metabolismus fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Plasticity in plant dispersal traits can maximise the ability of a plant species to survive in stressful environments during colonization. Aethionema arabicum (Brassicaceae) is a dimorphic annual species that is hypothesized to survive stressful conditions during colonization due to adaptive plasticity in life-phase (vegetative vs sexual) and fruit morph (dehiscent [DEH] vs indehiscent fruits [IND]). We tested for adaptive plasticity in life-phase and fruit morphs along laboratory environmental stress gradients found in the natural habitats of Ae. arabicum. We considered optimal environmental conditions (750-2000 m above sea level) to be those that resulted in the following fitness parameters: higher biomass and a higher total number of fruits compared to stressful habitats. We found evidence of plasticity in life-phase and fruit-morph along a stressful environmental gradient. High hydrothermal stress proportionally increased the number of dehiscent morphs and non-dormant seeds germinating in autumn. This offsets natural phenology towards dry and cold winter (less hydrothermal stress), yielding fewer fruits that dehisce in the next generation. We conclude that the plastic responses of Ae. arabicum to natural stress gradients constitute a strategy of long-term adaptive benefits and favouring potential pathways of colonisation of the optimal habitat.
BACKGROUND: RNA-sequencing analysis is increasingly utilized to study gene expression in non-model organisms without sequenced genomes. Aethionema arabicum (Brassicaceae) exhibits seed dimorphism as a bet-hedging strategy - producing both a less dormant mucilaginous (M+) seed morph and a more dormant non-mucilaginous (NM) seed morph. Here, we compared de novo and reference-genome based transcriptome assemblies to investigate Ae. arabicum seed dimorphism and to evaluate the reference-free versus -dependent approach for identifying differentially expressed genes (DEGs). RESULTS: A de novo transcriptome assembly was generated using sequences from M+ and NM Ae. arabicum dry seed morphs. The transcripts of the de novo assembly contained 63.1% complete Benchmarking Universal Single-Copy Orthologs (BUSCO) compared to 90.9% for the transcripts of the reference genome. DEG detection used the strict consensus of three methods (DESeq2, edgeR and NOISeq). Only 37% of 1533 differentially expressed de novo assembled transcripts paired with 1876 genome-derived DEGs. Gene Ontology (GO) terms distinguished the seed morphs: the terms translation and nucleosome assembly were overrepresented in DEGs higher in abundance in M+ dry seeds, whereas terms related to mRNA processing and transcription were overrepresented in DEGs higher in abundance in NM dry seeds. DEGs amongst these GO terms included ribosomal proteins and histones (higher in M+), RNA polymerase II subunits and related transcription and elongation factors (higher in NM). Expression of the inferred DEGs and other genes associated with seed maturation (e.g. those encoding late embryogenesis abundant proteins and transcription factors regulating seed development and maturation such as ABI3, FUS3, LEC1 and WRI1 homologs) were put in context with Arabidopsis thaliana seed maturation and indicated that M+ seeds may desiccate and mature faster than NM. The 1901 transcriptomic DEG set GO-terms had almost 90% overlap with the 2191 genome-derived DEG GO-terms. CONCLUSIONS: Whilst there was only modest overlap of DEGs identified in reference-free versus -dependent approaches, the resulting GO analysis was concordant in both approaches. The identified differences in dry seed transcriptomes suggest mechanisms underpinning previously identified contrasts between morphology and germination behaviour of M+ and NM seeds.
- Klíčová slova
- Aethionema arabicum, Dimorphic seeds, RNA-seq, Reference and reference-free, Transcriptome,
- MeSH
- anotace sekvence MeSH
- Brassicaceae genetika růst a vývoj MeSH
- genom rostlinný MeSH
- genová ontologie MeSH
- klíčení MeSH
- regulace genové exprese u rostlin * MeSH
- rostlinné proteiny genetika MeSH
- semena rostlinná genetika růst a vývoj MeSH
- stanovení celkové genové exprese MeSH
- transkriptom * MeSH
- vysoce účinné nukleotidové sekvenování MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- rostlinné proteiny MeSH
