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Coupland, G.

Publications and source records attributed to Coupland, G..

11 recordsLinked to original sources

Time-dependent bistability leads to critical slowing down during floral transition in Arabidopsis

Developmental transitions occur in the life cycles of all multicellular organisms. Despite their fundamental relevance, the underlying dynamics remain poorly understood. In plants, floral transition is a key developmental process whereby the shoot apical meristem changes from producing leaves to forming flowers. Using quantitative imaging, developmental genetics and dynamical systems theory, we show that a time-dependent bistable switch between expression of APETALA2, a key floral inhibitor, and the floral activators SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 and FRUITFULL, can explain the dynamics of floral transition in Arabidopsis. Notably, we detect a slowing down of the inhibitor dynamics, consistent with the system crossing a critical point of a bistable switch and transiently experiencing a ghost attractor. We demonstrate that this time-dependent bistability is essential to generate the range of dynamical behaviours measured across genotypes, including oscillations in the inhibitor, and that it also confers robustness in the transition. Collectively, our work provides quantitative evidence of time-dependent bistability underlying floral transition, which introduces a new timescale to this developmental process.

systems biology↗

Adaptation to seasonal drought in Arabis alpina is linked to the demographic history and climatic changes since the last glacial maximum

Understanding how species adapt to new environments is a central goal in evolutionary biology, and a topical question in climate change research. Here, we sequenced the genomes of 426 individuals of the perennial, Arctic-alpine herb Arabis alpina to study demography and adaptation, with a focus on populations in Northern Spain, that experience warm and dry summers. Our inference supports a scenario in which A. alpina colonized Northern Spain in a range expansion event that started near the Alps around 216 thousand years ago (kya). During the last glacial episode (115 to 12 kya), this expansion proceeded Westward, and effective population sizes were large across Europe, likely due to a larger suitable habitat for A. alpina. These ancient demographic events gave rise to a highly diverged genetic lineage in Northern Spain. In the present interglacial (between 12 kya and present), populations became increasingly fragmented, and lost genetic diversity across Europe. Furthermore, we detected signatures of selection at genes associated with responses to abiotic stress, including drought stress, and regulation of growth, for instance at SC5D and NAC055, which reflects the climatic changes since the last glacial period. Notably, an ancient polymorphism at the gene FRL1 emerged as a candidate for conferring variation in flowering behavior, and for contributing to adaptation to drought. Our study suggests that the combination of ancestral variation in flowering behavior, and positive selection on new mutations involved in drought responses, underlies the evolution of a new trait syndrome, and adaptation to climate change.

evolutionary biology↗

A regulatory gene network that couples floral transition to shoot apical meristem morphology in Arabidopsis

Plants flower in response to environmental signals. These signals change the shape and developmental identity of the shoot apical meristem (SAM), causing it to form flowers and inflorescences rather than leaves. How the changes in SAM shape and identity are coordinated is poorly understood. Using genetics, confocal microscopy and RNA sequencing, we show that reciprocal repression of the APETALA2 (AP2) and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) transcription factors in the SAM is crucial in coupling these processes. During vegetative development, AP2 represses SOC1 transcription to delay floral transition. Later, SOC1 is activated during floral transition in response to environmental cues and represses AP2 transcription. However, during floral transition and prior to its stable repression by SOC1, AP2 rapidly promotes an increase in the size, and changes in the morphology, of the SAM. Thus, direct reciprocal repression of AP2 and SOC1 couples floral transition and changes in SAM morphology, which initiate inflorescence development.

plant biology↗

AGAMOUS mediates timing of guard cell formation during gynoecium development

In Arabidopsis thaliana, stomata are composed of two guard cells that control the aperture of a central pore to facilitate gas exchange between the plant and its environment, which is particularly important during photosynthesis. Although leaves are the primary photosynthetic organs of higher plants, floral organs are also photosynthetically active. In the Brassicaceae, evidence suggests that silique photosynthesis is important for optimal seed oil content. A group of transcription factors containing MADS DNA binding domains is necessary and sufficient to confer floral organ identity. Elegant models, such as the ABCE model of flower development and the floral quartet model, have been instrumental in describing the molecular mechanisms by which these floral organ identity proteins govern flower development. However, we lack a complete understanding of how the floral organ identity genes interact with the underlying leaf development program. Here, we show that the MADS domain transcription factor AGAMOUS (AG) represses stomatal development on the gynoecial valves, so that maturation of stomatal complexes coincides with fertilization. We present evidence that this regulation by AG is mediated by direct transcriptional repression of the master regulator of the stomatal lineage, MUTE, and that this interaction is conserved among the Brassicaceae. This work extends on our understanding of the mechanisms underlying floral organ formation and provides a framework to decipher the mechanisms that control floral organ photosynthesis.

plant biology↗

Local adaptation of life-history traits within urban populations of Arabidopsis thaliana

O_LIThe challenges to which plants are exposed in urban environments represent, in miniature, the challenges plants face as a result of global environmental change. Hence, urban habitats provide a unique opportunity to assess whether processes of local adaptation are taking place despite the short temporal and geographical scales that characterize the Anthropocene. C_LIO_LIWe quantified the ecological diversity of urban habitats hosting A. thaliana populations. Using plant community indicators, we show that these patches differ in their levels of soil nutrient content and disturbance. Accordingly, plants in each patch displayed a range of flowering time, size and fitness. C_LIO_LIUsing a deep sampling approach coupled with reduced genome-sequencing, we demonstrate that most individuals can be assigned to a limited set of clonal lineages; the genetic diversity of these lineages is a sample of the diversity observed in western European populations of the species, indicating that established urban populations originate from a broad regional pool of lineages. C_LIO_LIWe assessed the genetic and phenotypic diversity of these lineages in a set of common garden experiments. We report marked genetic differences in life-history traits, including time of primary and secondary dormancy as well as of flowering. These genetic differences in life-history traits are not randomly distributed but sorted out by ecological differences among sites of origin. C_LIO_LISynthesis: Our study shows that the genetically diverse phenology of a regional A. thaliana gene pool is not randomly distributed but filtered by heterogeneity in the urban environment. To out knowledge, this report is the first to show a pattern indicative of environmental filtering enhancing local genetic adaptation within urban environments. We conclude that environmental filtering helps maintain functional diversity within species. C_LI

evolutionary biology↗

Energy status-promoted growth and development of Arabidopsis require copper deficiency response transcriptional regulator SPL7

Copper (Cu) is a cofactor of around 300 Arabidopsis proteins including photosynthetic and mitochondrial electron transfer chain enzymes critical for ATP production and carbon fixation. Plant acclimation to Cu deficiency requires the transcription factor SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE7 (SPL7). We report that in the wild type and in the spl7-1 mutant, respiratory electron flux via Cu-dependent cytochrome c oxidase remained unaffected under both normal and low-Cu cultivation conditions. Contrary to the wild type, supplementing Cu-deficient media with exogenous sugar failed to stimulate growth of spl7-1. The spl7-1 mutant accumulated carbohydrates including the signaling sugar trehalose 6-phosphate, as well as ATP and NADH, also under normal Cu supply and without sugar supplementation. Late flowering of spl7-1 was in agreement with its attenuated sugar responsiveness. Functional TOR and SnRK1 kinase signaling in spl7-1 suggested against fundamental defects in these energy-signaling hubs. Sequencing of chromatin immunoprecipitates combined with transcriptomics identified direct targets of SPL7-mediated positive regulation, including FE SUPEROXIDE DISMUTASE1 (FSD1), COPPER-DEFICIENCY-INDUCED TRANSCRIPTION FACTOR1 (CITF1) and uncharacterized bHLH23 (CITF2), as well as an enriched upstream GTACTRC motif. In summary, transducing energy availability into growth and reproductive development requires the function of SPL7. Our results could help to increase crop yields, especially on Cu-deficient soils.

plant biology↗

Unraveling the role of MADS transcription factor complexes in apple tree dormancy using sequential DAP-seq

BackgroundThe effect of global warming on dormancy and flowering patterns of crop trees threatens world-wide fruit production and food security. In Rosaceous tree species, it is believed that a group of genes encoding MADS transcription factors (TFs) controls temperature-mediated dormancy cycle. These genes are similar to SHORT VEGETATIVE PHASE (SVP) from Arabidopsis thaliana and referred as DORMANCY-ASSOCIATED MADS-BOX (DAM) genes. ResultsBy making use of apple tree (Malus x domestica) as a model for Rosaceous species, we have investigated the function of MADS TFs during the dormancy cycle. We found that MdDAM and other dormancy related MADS TFs form multimeric complexes with MdSVPa, and that MdSVPa is essential for the transcriptional complex activity. Then, for the first time in non-model plant species, we performed sequential DNA Affinity Purification sequencing (seq-DAP-seq) to define the genome-wide binding sites of these MADS TF complexes. Target genes associated with the binding sites were identified by combining seq-DAP-seq data with transcriptomics datasets obtained by the inducible glucocorticoid receptor expression system, and reanalyzing preexisting data related to dormancy cycle in apple trees. ConclusionWe have determined a gene regulatory network formed by MdSVPa-containing complexes that regulate the dormancy cycle in apple trees in response to environmental cues. Key genes identified with our genomic approach and the elucidated regulatory relationships provide leads for breeding fruit trees better adapted to changing climate conditions. Moreover, we provide novel molecular evidence on the evolutionary functional segregation between DAM and SVP proteins in the Rosaceae family.

plant biology↗

On the origin of photoperiod non-responsiveness in barley

In barley, the transition from the vegetative to reproductive phase is complex and under the control of photoperiodic and temperature conditions. One major gene involved is PPD-H1, a PSEUDO-RESPONSE REGULATOR 7 (PRR7) that encodes a component of the circadian clock. Mutation at PPD-H1 resulted in the photoperiod non-responsive ppd-H1 alleles that are beneficial under high latitudinal environments as they allow vegetative growth during the long-day summer conditions whereby higher yields are harvested by farmers. Utilizing a diverse GWAS panel of world-wide origin and a genome-wide gene-based set of 50K SNP markers, a strong association of days to heading with the PPD-H1 gene was detected in multi-location field trials. Re-sequencing of the gene spanning putative causative SNPs, SNP22 (Turner et al. 2005) and SNP48 (Jones et al. 2008), detected recombination between the two, previously reported to be in complete LD. Phenotyping of the recombinants and phylogenetic relationships among haplotypes supported the original conclusion of Turner et al. (2005) that SNP22, present in the CCT domain, is the most likely causative SNP. To infer the origin of non-responsiveness, the PPD-H1 gene was re-sequenced in a geo-referenced collection of 2057 wild and domesticated barleys and compared with the allelic status of the 6000-year-old barley sample from the Yoram cave in the Masada cliff. A monophyletic and post-domestication origin in the Fertile Crescent was found in contrast to the pre-domestication origin proposed by Jones et al. (2008). We show that the photoperiod non-responsiveness originated from Desert type wild barley in the Southern Levant.Competing Interest StatementThe authors have declared no competing interest.View Full Text

plant biology↗

Cytokinin-promoted secondary growth and nutrient storage in the perennial stem zone of Arabis alpina

Perennial plants maintain their life span through several growth seasons. Arabis alpina serves as model Brassicaceae species to study perennial traits. A. alpina lateral stems have a proximal vegetative zone with a dormant bud zone, and a distal senescing seed-producing inflorescence zone. We addressed the questions of how this zonation is distinguished at the anatomical level, whether it is related to nutrient storage, and which signals affect the zonation. We found that the vegetative zone exhibits secondary growth, which we termed the perennial growth zone (PZ). High-molecular weight carbon compounds accumulate there in cambium and cambium derivatives. Neither vernalization nor flowering were requirements for secondary growth and sequestration of storage compounds. The inflorescence zone with only primary growth, termed annual growth zone (AZ), or roots exhibited different storage characteristics. Following cytokinin application, cambium activity was enhanced and secondary phloem parenchyma was formed in the PZ and also in the AZ. In transcriptome analysis cytokinin-related genes represented enriched gene ontology terms and were expressed at higher level in PZ than AZ. Thus, A. alpina uses primarily the vegetative PZ for nutrient storage, coupled to cytokinin-promoted secondary growth. This finding lays a foundation for future studies addressing signals for perennial growth. HighlightArabis alpina stems have a perennial zone with secondary growth, where cambium and derivatives store high-molecular weight compounds independent of vernalization. Cytokinins are signals for the perennial secondary growth zone.

plant biology↗

PERPETUAL FLOWERING2 coordinates the vernalization response and perennial flowering in Arabis alpina

The floral repressor APETALA2 (AP2) in Arabidopsis regulates flowering through the age pathway. The AP2 orthologue in the alpine perennial Arabis alpina, PERPETUAL FLOWERING 2 (PEP2), was previously reported to regulate flowering through the vernalization pathway by enhancing the expression of another floral repressor PERPETUAL FLOWERING 1 (PEP1), the orthologue of Arabidopsis FLOWERING LOCUS C (FLC). However, PEP2 also regulates flowering independently of PEP1. To characterize the function of PEP2 we analyzed the transcriptomes of pep2 and pep1 mutants. The majority of differentially expressed genes were detected between pep2 and the wild type or between pep2 and pep1, highlighting the importance of the PEP2 role that is independent of PEP1. Here we demonstrate that PEP2 prevents the upregulation of the A. alpina floral meristem identity genes FRUITFUL (AaFUL), LEAFY (AaLFY) and APETALA1 (AaAP1) which ensure floral commitment during vernalization. Young pep2 seedlings respond to vernalization, suggesting that PEP2 regulates the age-dependent response to vernalization independently of PEP1. The major role of PEP2 through the PEP1-dependent pathway takes place after vernalization, when it facilitates PEP1 activation both in the main shoot apex and in the axillary branches. These multiple roles of PEP2 in vernalization response contribute to the A. alpina life-cycle.\n\nHIGHLIGHTThe Arabis alpina APETALA2 orthologue, PERPETUAL FLOWERING2, regulates the age-dependent response to vernalization and it is required to facilitate the activation of the A. alpina FLOWERING LOCUS C after vernalization.

plant biology↗

Demography And Mating System Shape The Genome-Wide Impact Of Purifying Selection In Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation, and can affect the impact of natural selection. While theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, both mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.\n\nSignificanceIntermediate outcrossing rates are theoretically predicted to maintain effective selection against harmful alleles, but few studies have empirically tested this prediction using genomic data. We used whole-genome resequencing data from alpine rock-cress to study how genetic variation and purifying selection vary with mating system. We find that populations with intermediate outcrossing rates have similar levels of genetic diversity as outcrossing populations, and that purifying selection against harmful alleles is efficient in mixed-mating populations. In contrast, self-fertilizing populations from Scandinavia have strongly reduced genetic diversity, and accumulate harmful mutations, likely as a result of demographic effects of postglacial colonization. Our results suggest that mixed-mating populations can avoid the negative evolutionary consequences of high self-fertilization rates.

evolutionary biology↗