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Holm, Svante
Publications (10 of 28) Show all publications
Hepworth, J., Antoniou-Kourounioti, R. L., Bloomer, R. H., Selga, C., Berggren, K., Cox, D., . . . Dean, C. (2018). Absence of warmth permits epigenetic memory of winter in Arabidopsis. Nature Communications, 9(1), Article ID 639.
Open this publication in new window or tab >>Absence of warmth permits epigenetic memory of winter in Arabidopsis
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2018 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, no 1, article id 639Article in journal (Refereed) Published
Abstract [en]

Plants integrate widely fluctuating temperatures to monitor seasonal progression. Here, we investigate the temperature signals in field conditions that result in vernalisation, the mechanism by which flowering is aligned with spring. We find that multiple, distinct aspects of the temperature profile contribute to vernalisation. In autumn, transient cold temperatures promote transcriptional shutdown of Arabidopsis FLOWERING LOCUS C (FLC), independently of factors conferring epigenetic memory. As winter continues, expression of VERNALIZATION INSENSITIVE3 (VIN3), a factor needed for epigenetic silencing, is upregulated by at least two independent thermosensory processes. One integrates long-term cold temperatures, while the other requires the absence of daily temperatures above 15 °C. The lack of spikes of high temperature, not just prolonged cold, is thus the major driver for vernalisation. Monitoring of peak daily temperature is an effective mechanism to judge seasonal progression, but is likely to have deleterious consequences for vernalisation as the climate becomes more variable. 

National Category
Biological Sciences
Identifiers
urn:nbn:se:miun:diva-33270 (URN)10.1038/s41467-018-03065-7 (DOI)000424748700010 ()29434233 (PubMedID)2-s2.0-85042029461 (Scopus ID)
Available from: 2018-03-14 Created: 2018-03-14 Last updated: 2018-03-19Bibliographically approved
Antoniou-Kourounioti, R. L., Hepworth, J., Heckmann, A., Duncan, S., Qüesta, J., Rosa, S., . . . Howard, M. (2018). Temperature Sensing Is Distributed throughout the Regulatory Network that Controls FLC Epigenetic Silencing in Vernalization. Cell systems, 7(6), 643-655
Open this publication in new window or tab >>Temperature Sensing Is Distributed throughout the Regulatory Network that Controls FLC Epigenetic Silencing in Vernalization
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2018 (English)In: Cell systems, ISSN 2405-4712, Vol. 7, no 6, p. 643-655Article in journal (Refereed) Published
Abstract [en]

Many organisms need to respond to complex, noisy environmental signals for developmental decision making. Here, we dissect how Arabidopsis plants integrate widely fluctuating field temperatures over month-long timescales to progressively upregulate VERNALIZATION INSENSITIVE3 (VIN3) and silence FLOWERING LOCUS C (FLC), aligning flowering with spring. We develop a mathematical model for vernalization that operates on multiple timescales-long term (month), short term (day), and current (hour)-and is constrained by experimental data. Our analysis demonstrates that temperature sensing is not localized to specific nodes within the FLC network. Instead, temperature sensing is broadly distributed, with each thermosensory process responding to specific features of the plants' history of exposure to warm and cold. The model accurately predicts FLC silencing in new field data, allowing us to forecast FLC expression in changing climates. We suggest that distributed thermosensing may be a general property of thermoresponsive regulatory networks in complex natural environments. 

Keywords
climate change, epigenetics, FLC, FLOWERING LOCUS C, gene regulation, mathematical modeling, phenology, temperature sensing, vernalization, VERNALIZATION INSENSITIVE3, VIN3
National Category
Biological Sciences
Identifiers
urn:nbn:se:miun:diva-35416 (URN)10.1016/j.cels.2018.10.011 (DOI)000454344300008 ()30503646 (PubMedID)2-s2.0-85059223084 (Scopus ID)
Available from: 2019-01-09 Created: 2019-01-09 Last updated: 2019-01-10Bibliographically approved
Plötner, B., Nurmi, M., Fischer, A., Watanabe, M., Schneeberger, K., Holm, S., . . . Laitinen, R. A. E. (2017). Chlorosis caused by two recessively interacting genes reveals a role of RNA helicase in hybrid breakdown in Arabidopsis thaliana. The Plant Journal, 91(2), 251-262
Open this publication in new window or tab >>Chlorosis caused by two recessively interacting genes reveals a role of RNA helicase in hybrid breakdown in Arabidopsis thaliana
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2017 (English)In: The Plant Journal, ISSN 0960-7412, E-ISSN 1365-313X, Vol. 91, no 2, p. 251-262Article in journal (Refereed) Published
Abstract [en]

Hybrids often differ in fitness from their parents. They may be superior, translating into hybrid vigour or heterosis, but they may also be markedly inferior, because of hybrid weakness or incompatibility. The underlying genetic causes for the latter can often be traced back to genes that evolve rapidly because of sexual or host-pathogen conflicts. Hybrid weakness may manifest itself only in later generations, in a phenomenon called hybrid breakdown. We have characterized a case of hybrid breakdown among two Arabidopsis thaliana accessions, Shahdara (Sha, Tajikistan) and Lövvik-5 (Lov-5, Northern Sweden). In addition to chlorosis, a fraction of the F2 plants have defects in leaf and embryo development, and reduced photosynthetic efficiency. Hybrid chlorosis is due to two major-effect loci, of which one, originating from Lov-5, appears to encode an RNA helicase (AtRH18). To examine the role of the chlorosis allele in the Lövvik area, in addition to eight accessions collected in 2009, we collected another 240 accessions from 15 collections sites, including Lövvik, from Northern Sweden in 2015. Genotyping revealed that Lövvik collection site is separated from the rest. Crosses between 109 accessions from this area and Sha revealed 85 cases of hybrid chlorosis, indicating that the chlorosis-causing allele is common in this area. These results suggest that hybrid breakdown alleles not only occur at rapidly evolving loci, but also at genes that code for conserved processes.

Keywords
Arabidopsis thaliana, Chlorosis, Hybrid breakdown, Local adaptation, RNA helicase
National Category
Biological Sciences
Identifiers
urn:nbn:se:miun:diva-30991 (URN)10.1111/tpj.13560 (DOI)000404795500006 ()28378460 (PubMedID)2-s2.0-85019677417 (Scopus ID)
Note

Version of record online: 30 May 2017

Available from: 2017-06-26 Created: 2017-06-26 Last updated: 2018-02-27Bibliographically approved
Novikova, P. Y., Tsuchimatsu, T., Simon, S., Nizhynska, V., Voronin, V., Burns, R., . . . Nordborg, M. (2017). Genome Sequencing Reveals the Origin of the Allotetraploid Arabidopsis suecica. Molecular biology and evolution, 34(4), 957-968
Open this publication in new window or tab >>Genome Sequencing Reveals the Origin of the Allotetraploid Arabidopsis suecica
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2017 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 34, no 4, p. 957-968Article in journal (Refereed) Published
Abstract [en]

Polyploidy is an example of instantaneous speciation when it involves the formation of a new cytotype that is incompatible with the parental species. Because new polyploid individuals are likely to be rare, establishment of a new species is unlikely unless polyploids are able to reproduce through self-fertilization (selfing), or asexually. Conversely, selfing (or asexuality) makes it possible for polyploid species to originate from a single individual-a bona fide speciation event. The extent to which this happens is not known. Here, we consider the origin of Arabidopsis suecica, a selfing allopolyploid between Arabidopsis thaliana and Arabidopsis arenosa, which has hitherto been considered to be an example of a unique origin. Based on whole-genome re-sequencing of 15 natural A. suecica accessions, we identify ubiquitous shared polymorphism with the parental species, and hence conclusively reject a unique origin in favor of multiple founding individuals. We further estimate that the species originated after the last glacial maximum in Eastern Europe or central Eurasia (rather than Sweden, as the name might suggest). Finally, annotation of the self-incompatibility loci in A. suecica revealed that both loci carry non-functional alleles. The locus inherited from the selfing A. thaliana is fixed for an ancestral non-functional allele, whereas the locus inherited from the outcrossing A. arenosa is fixed for a novel loss-offunction allele. Furthermore, the allele inherited from A. thaliana is predicted to transcriptionally silence the allele inherited from A. arenosa, suggesting that loss of self-incompatibility may have been instantaneous.

Keywords
polyploidy, Arabidopsis suecica, Arabidopsis thaliana, Arabidopsis arenosa, shared polymorphism, speciation, hybridization
National Category
Biological Sciences
Identifiers
urn:nbn:se:miun:diva-30566 (URN)10.1093/molbev/msw299 (DOI)000396762200014 ()2-s2.0-85018944369 (Scopus ID)
Available from: 2017-04-03 Created: 2017-04-03 Last updated: 2017-11-29Bibliographically approved
Alonso-Blanco, C., Andrade, J., Becker, C., Bemm, F., Bergelson, J., Borgwardt, K. M., . . . Zhou, X. (2016). 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana. Cell, 166(2), 481-491
Open this publication in new window or tab >>1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana
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2016 (English)In: Cell, ISSN 0092-8674, E-ISSN 1097-4172, Vol. 166, no 2, p. 481-491Article in journal (Refereed) Published
Abstract [en]

Arabidopsis thaliana serves as a model organism for the study of fundamental physiological, cellular, and molecular processes. It has also greatly advanced our understanding of intraspecific genome variation. We present a detailed map of variation in 1,135 high-quality re-sequenced natural inbred lines representing the native Eurasian and North African range and recently colonized North America. We identify relict populations that continue to inhabit ancestral habitats, primarily in the Iberian Peninsula. They have mixed with a lineage that has spread to northern latitudes from an unknown glacial refugium and is now found in a much broader spectrum of habitats. Insights into the history of the species and the fine-scale distribution of genetic diversity provide the basis for full exploitation of A. thaliana natural variation through integration of genomes and epigenomes with molecular and non-molecular phenotypes.

Place, publisher, year, edition, pages
Elsevier, 2016
Keywords
Arabidopsis thaliana, 1001 Genomes, glacial refugia, GWAS, population expansion
Identifiers
urn:nbn:se:miun:diva-30670 (URN)10.1016/j.cell.2016.05.063 (DOI)
Available from: 2017-04-27 Created: 2017-04-27 Last updated: 2017-08-09Bibliographically approved
Kawakatsu, T., Huang, S.-s. C., Jupe, F., Sasaki, E., Schmitz, R. J., Urich, M. A., . . . Schork, N. J. (2016). Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions. Cell, 166(2), 492-505
Open this publication in new window or tab >>Epigenomic Diversity in a Global Collection of Arabidopsis thaliana Accessions
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2016 (English)In: Cell, ISSN 0092-8674, E-ISSN 1097-4172, Vol. 166, no 2, p. 492-505Article in journal (Refereed) Published
Abstract [en]

The epigenome orchestrates genome accessibility, functionality, and three-dimensional structure. Because epigenetic variation can impact transcription and thus phenotypes, it may contribute to adaptation. Here, we report 1,107 high-quality single-base resolution methylomes and 1,203 transcriptomes from the 1001 Genomes collection of Arabidopsis thaliana. Although the genetic basis of methylation variation is highly complex, geographic origin is a major predictor of genome-wide DNA methylation levels and of altered gene expression caused by epialleles. Comparison to cistrome and epicistrome datasets identifies associations between transcription factor binding sites, methylation, nucleotide variation, and co-expression modules. Physical maps for nine of the most diverse genomes reveal how transposons and other structural variants shape the epigenome, with dramatic effects on immunity genes. The 1001 Epigenomes Project provides a comprehensive resource for understanding how variation in DNA methylation contributes to molecular and non-molecular phenotypes in natural populations of the most studied model plant.

Place, publisher, year, edition, pages
Elsevier, 2016
National Category
Natural Sciences
Identifiers
urn:nbn:se:miun:diva-30669 (URN)10.1016/j.cell.2016.06.044 (DOI)
Available from: 2017-04-27 Created: 2017-04-27 Last updated: 2017-08-09Bibliographically approved
Novikova, P. Y., Hohmann, N., Nizhynska, V., Tsuchimatsu, T., Ali, J., Muir, G., . . . Nordborg, M. (2016). Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism. Nature Genetics, 48(9), 1077-1082
Open this publication in new window or tab >>Sequencing of the genus Arabidopsis identifies a complex history of nonbifurcating speciation and abundant trans-specific polymorphism
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2016 (English)In: Nature Genetics, ISSN 1061-4036, E-ISSN 1546-1718, Vol. 48, no 9, p. 1077-1082Article in journal (Refereed) Published
Abstract [en]

The notion of species as reproductively isolated units related through a bifurcating tree implies that gene trees should generally agree with the species tree and that sister taxa should not share polymorphisms unless they diverged recently and should be equally closely related to outgroups. It is now possible to evaluate this model systematically. We sequenced multiple individuals from 27 described taxa representing the entire Arabidopsis genus. Cluster analysis identified seven groups, corresponding to described species that capture the structure of the genus. However, at the level of gene trees, only the separation of Arabidopsis thaliana from the remaining species was universally supported, and, overall, the amount of shared polymorphism demonstrated that reproductive isolation was considerably more recent than the estimated divergence times. We uncovered multiple cases of past gene flow that contradict a bifurcating species tree. Finally, we showed that the pattern of divergence differs between gene ontologies, suggesting a role for selection. © 2016 Nature America, Inc. All rights reserved.

National Category
Genetics
Identifiers
urn:nbn:se:miun:diva-28930 (URN)10.1038/ng.3617 (DOI)000382398800021 ()2-s2.0-84978732423 (Scopus ID)
Note

CODEN: NGENE

Available from: 2016-09-27 Created: 2016-09-27 Last updated: 2017-08-09Bibliographically approved
Duncan, S., Holm, S., Questa, J., Irwin, J., Grant, A. & Dean, C. (2015). Seasonal shift in timing of vernalization as an adaptation to extreme winter. eLIFE, 4(JULY)
Open this publication in new window or tab >>Seasonal shift in timing of vernalization as an adaptation to extreme winter
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2015 (English)In: eLIFE, ISSN 2050-084X, Vol. 4, no JULYArticle in journal (Refereed) Published
Abstract [en]

The requirement for vernalization, a need for prolonged cold to trigger flowering, aligns reproductive development with favorable spring conditions. In Arabidopsis thaliana vernalization depends on the cold-induced epigenetic silencing of the floral repressor locus FLC. Extensive natural variation in vernalization response is associated with A. thaliana accessions collected from different geographical regions. Here, we analyse natural variation for vernalization temperature requirement in accessions, including those from the northern limit of the A. thaliana range. Vernalization required temperatures above 0°C and was still relatively effective at 14°C in all the accessions. The different accessions had characteristic vernalization temperature profiles. One Northern Swedish accession showed maximum vernalization at 8°C, both at the level of flowering time and FLC chromatin silencing. Historical temperature records predicted all accessions would vernalize in autumn in N. Sweden, a prediction we validated in field transplantation experiments. The vernalization response of the different accessions was monitored over three intervals in the field and found to match that when the average field temperature was given as a constant condition. The vernalization temperature range of 0–14°C meant all accessions fully vernalized before snowfall in N. Sweden. These findings have important implications for understanding the molecular basis of adaptation and for predicting the consequences of climate change on flowering time.

National Category
Biological Sciences Climate Research
Identifiers
urn:nbn:se:miun:diva-25895 (URN)10.7554/eLife.06620.001 (DOI)000373848800001 ()2-s2.0-85016070229 (Scopus ID)
Available from: 2015-09-23 Created: 2015-09-23 Last updated: 2017-07-03Bibliographically approved
Carlsson, F., Edman, M., Holm, S. & Jonsson, B. G. (2014). Effect of heat on interspecific competition in saprotrophic wood fungi. Fungal ecology, 11, 100-106
Open this publication in new window or tab >>Effect of heat on interspecific competition in saprotrophic wood fungi
2014 (English)In: Fungal ecology, ISSN 1754-5048, E-ISSN 1878-0083, Vol. 11, p. 100-106Article in journal (Refereed) Published
Abstract [en]

Some boreal wood fungi that are associated with forest fire or open dry habitats have an increased resistance to heat in comparison to species associated with a less specific distribution or species found in mesic forests. We hypothesize that extreme temperature-stress experienced during fires will favor species adapted to heat and, ultimately, the composition of species inhabiting logs in such habitats will change. Competitiveness after temperature stress was examined in three fire-associated species – Dichomitus squalens, Gloeophyllum sepiarium and Phlebiopsis gigantea – and three non fire-associated species – Ischnoderma benzoinum, Phellinus pini and Fomitopsis pinicola. There was a difference between the fire-associated species and the non fire-associated species with respect to competitive strength after heat stress. All fire-associated species had an advantage after heat treatment, colonizing a larger volume of wood than any non-fire-associated competitor. Our findings suggest that increased heat tolerance of mycelia can exert a competitive balance shift after forest fire. It shows that a system governed by forest fire will be dominance controlled under certain conditions. Furthermore, from a management perspective, during a prescribed burning, certain species already present in the ecosystem will be favored if the fire is not allowed to totally consume the substrates.

Keywords
Fungi, fire, dead wood, Basidiomycetes; Community interactions; Forest fire; Heat resistance; Mycelia; Wood fungi
National Category
Ecology
Identifiers
urn:nbn:se:miun:diva-21408 (URN)10.1016/j.funeco.2014.05.003 (DOI)000342244000011 ()2-s2.0-84906738682 (Scopus ID)
Available from: 2014-02-20 Created: 2014-02-20 Last updated: 2017-12-06Bibliographically approved
Carlsson, F., Edman, M., Holm, S., Eriksson, A.-M. & Jonsson, B. G. (2012). Increased heat resistance in mycelia from wood fungi prevalent in forests characterized by fire: a possible adaptation to forest fire.. Fungal Biology, 116(10), 1025-1031
Open this publication in new window or tab >>Increased heat resistance in mycelia from wood fungi prevalent in forests characterized by fire: a possible adaptation to forest fire.
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2012 (English)In: Fungal Biology, ISSN 1878-6146, E-ISSN 1878-6162, Vol. 116, no 10, p. 1025-1031Article in journal (Refereed) Published
Abstract [en]

Abstract

Forest fire has for a long time been the major stand replacing/modifying disturbance in boreal forests. For organisms to adopt to this phenomenon different strategies for protective measurements has evolved. This study focuses on the organism group of wood fungi, and one of several possibilities for adaptation to forest fire - increased heat resistance in the mycelia. 16 species of wood fungi where selected and sorted a priori according to their prevalence for fire affected substrate. These were isolated and re-inoculated on pine wood before testing. Experiments where done in a series where the mycelia was exposed to 100, 140, 180, 220°C for 5, 10, 15, 20, 15 min. A very clear difference was found, the group containing species with a prevalence for a fire affected substrate had a much higher survival rate over all combinations of time and temperature compared to species with a more general ecology. This data suggests that increased heat resistance in mycelia could be a possible adaptation to forest fire. This in turn has major impacts on the ecology and population dynamics of wood fungi. An increase in temperature could shift the population structure in a log, allowing minor non fruiting mycelia content to expand on the expense of earlier dominant colonizers. Furthermore this study has implications on how to control prescribed restoration burning events. When burning areas where the dead wood content is dominated by early decay stages, loss of species can be avoided by proper management.

Keywords
Adaptation; Basidiomycetes; Competition; Dead wood; Ecology; Forest fire; Mycelia; Resistance to heat; Restoration fires; Saprotrophic
National Category
Natural Sciences
Identifiers
urn:nbn:se:miun:diva-15883 (URN)10.1016/j.funbio.2012.07.005 (DOI)000311182700001 ()2-s2.0-84867427474 (Scopus ID)
Available from: 2012-02-16 Created: 2012-02-16 Last updated: 2017-12-07Bibliographically approved
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