Absence of warmth permits epigenetic memory of winter in Arabidopsis

Hepworth, Jo; Antoniou-Kourounioti, Rea L; Bloomer, Rebecca; Selga, Catja; Berggren, Kristina; Cox, Deborah; Harris, Barley Rose Collier; Irwin, Judith A.; Holm, Svante; Säll, Torbjörn; Howard, Martin; Dean, Caroline

doi:10.1038/s41467-018-03065-7

Cited by 89 publications

(144 citation statements)

References 48 publications

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“…However, Arabidopsis accessions are known to use the spectral quality of ambient light to differentiate the proximity of kin versus nonkin (Crepy & Casal, 2015), resulting in phenotype matching among kin (Till-Bottraud & de Villemereuil, 2015). This lends support to our hypothesis that S NIL acceleration is due to phytochrome-mediated shade avoid- (Angel et al, 2015;Burghardt et al, 2016;Duncan et al, 2015;Hepworth et al, 2018;Shindo, Lister, Crevillen, Nordborg, & Dean, 2006). On the other hand, increased temperature in the summer accelerated reproduction, likely mediated by FLM response to high ambient temperature (Lutzet al, 2017(Lutzet al, , 2015Sureshkumar et al, 2016).…”

Section: Discussionsupporting

confidence: 70%

“…The winter annual S NIL switched between two plastic responses to climate warming based on season: delay in the fall and acceleration in the summer. Its future‐fall delay may have been caused by the attenuation of the vernalization signal present in the fall‐modern simulation (Angel et al, ; Burghardt et al, ; Duncan et al, ; Hepworth et al, ; Shindo, Lister, Crevillen, Nordborg, & Dean, ). On the other hand, increased temperature in the summer accelerated reproduction, likely mediated by FLM response to high ambient temperature (Lutzet al, ; Sureshkumar et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Responses to chilling or high temperature are governed by a set of repressor genes that prevent activation of genes promoting flowering (florigens) (Johanson et al, 2000;Li et al, 2014;Mendez-Vigo, Gomaa, Alonso-Blanco, & Pico, 2013;Rosloski, Jali, Balasubramanian, Weigel, & Grbic, 2010;Salome et al, 2011;Stinchcombe et al, 2004;Werner et al, 2005). In particular, FRIGIDA (FRI) activates the floral repressor FLOWERING LOCUS C (FLC), conferring late flowering which can be accelerated by vernalization (Hepworth et al, 2018;Kim & Sung, 2013;Lee & Amasino, 1995;Sung & Amasino, 2004;Wood et al, 2006). Across its range, A. thaliana segregates functional and nonfunctional versions of this gene, resulting in ecotypes that are responsive and nonresponsive to extended cold (Johanson et al, 2000;Shindo et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Phenological and fitness responses to climate warming depend upon genotype and competitive neighbourhood in Arabidopsis thaliana

2019

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Increasing temperatures during climate change are known to alter the phenology across diverse plant taxa, but the evolutionary outcomes of these shifts are poorly understood. Moreover, plant temperature‐sensing pathways are known to interact with competition‐sensing pathways, yet there remains little experimental evidence for how genotypes varying in temperature responsiveness react to warming in realistic competitive settings. We compared flowering time and fitness responses to warming and competition for two near‐isogenic lines (NILs) of Arabidopsis thaliana transgressively segregating temperature‐sensitive and temperature‐insensitive alleles for major‐effect flowering time genes. We grew focal plants of each genotype in intraspecific and interspecific competition in four treatments contrasting daily temperature profiles in summer and fall under contemporary and warmed conditions. We measured phenology and fitness of focal plants to quantify plastic responses to season, temperature and competition and the dependence of these responses on flowering time genotype. The temperature‐insensitive NIL was constitutively early flowering and less fit, except in a future‐summer climate in which its fitness was higher than the later flowering, temperature‐sensitive NIL in low competition. The late‐flowering NIL showed accelerated flowering in response to intragenotypic competition and to increased temperature in the summer but delayed flowering in the fall. However, its fitness fell with rising temperatures in both seasons, and in the fall its marginal fitness gain from decreasing competition was diminished in the future. Functional alleles at temperature‐responsive genes were necessary for plastic responses to season, warming and competition. However, the plastic genotype was not the most fit in every experimental condition, becoming less fit than the temperature‐canalized genotype in the warm summer treatment. Climate change is often predicted to have deleterious effects on plant populations, and our results show how increased temperatures can act through genotype‐dependent phenology to decrease fitness. Furthermore, plasticity is not necessarily adaptive in rapidly changing environments since a nonplastic genotype proved fitter than a plastic genotype in a warming climate treatment. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13262/suppinfo is available for this article.

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Section: Discussionsupporting

confidence: 70%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Phenological and fitness responses to climate warming depend upon genotype and competitive neighbourhood in Arabidopsis thaliana

2019

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“…(), who conducted a 2‐year census of the transcript levels of this well‐known temperature‐dependent flowering time gene to uncover the mechanisms by which environmental factors regulate flowering (Figure ). This ground‐breaking study has since been followed up by others in which FLC transcript levels and chromatin states were measured in different localities and field conditions (Nishio et al ., ; Hepworth et al ., ), which increasingly provided a clearer account of the complexity and relevance of the environment for FLC ‐mediated responses.…”

Section: From Lab To the Field: Plant Genomics And Systems Biology Imentioning

confidence: 99%

Evolutionary and ecological functional genomics, from lab to the wild

2018

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Summary Plant phenotypes are the result of both genetic and environmental forces that act to modulate trait expression. Over the last few years, numerous approaches in functional genomics and systems biology have led to a greater understanding of plant phenotypic variation and plant responses to the environment. These approaches, and the questions that they can address, have been loosely termed evolutionary and ecological functional genomics (EEFG), and have been providing key insights on how plants adapt and evolve. In particular, by bringing these studies from the laboratory to the field, EEFG studies allow us to gain greater knowledge of how plants function in their natural contexts.

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“…This approach has also been proposed in attempts to engineer crop traits starting from genetics or from genomes (Welch et al , 2005; Yin and Struik, 2008, 2010; Parent and Tardieu, 2014; Wu et al , 2016; Chenu et al , 2018), where simpler models have demonstrated both the potential of crop modelling in general and the significant demands of detailed models for empirical data that varies in availability (Hammer et al , 2006; Asseng et al , 2013). For microorganisms, comprehensive models link the metabolic and molecular level with the cellular (Karr et al , 2012) and population growth scales (Weiße et al , 2015), whereas contemporary work in more complex organisms has necessarily focused more narrowly (Buckley and Mott, 2013; Lynch, 2013; Zhu et al , 2013; Klose et al , 2015; Le Novere, 2015; Hepworth et al., 2018).…”

Section: Introductionmentioning

confidence: 99%