Tree ‘memory’: new insights on temperature-induced priming effects during early embryogenesis

Trontin, Jean-François; Raschke, Juliane; Rupps, Andrea

doi:10.1093/treephys/tpaa150

Cited by 11 publications

(7 citation statements)

References 32 publications

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“…Our results demonstrate the need to include within-generation carryover effects not only in assessments of individual and population performance as others have done (Donelan & Trussell, 2019;Stuligross & Williams, 2021) but also in assessments of ecosystem-level processes. Mounting evidence suggests that carryover effects operate in a diversity of species (Donelan & Trussell, 2019;Stuligross & Williams, 2021;Sutton et al, 2021;Trontin et al, 2020), so their…”

Section: Discussionmentioning

confidence: 99%

“…However, organism phenotypes are also shaped by past environments such as those experienced during previous life stages. These within‐generation carryover effects are widespread across taxa (Sutton et al, 2021; Trontin et al, 2020) and affect functional traits similar to those that respond plastically to current environmental conditions, including growth (Donelan & Trussell, 2019), fecundity (Stuligross & Williams, 2021), foraging (Van Allen et al, 2010), and disease transmission (Roux et al, 2015). Mounting evidence suggests that phenotypic changes caused by within‐generation carryover effects in individuals cascade to impact population (Stuligross & Williams, 2021) and community dynamics (Van Allen & Rudolf, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Legacy of past exposure to hypoxia and warming regulates an ecosystem service provided by oysters

Donelan

Ogburn

Breitburg

2023

Global Change Biology

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Climate change is altering patterns and processes across all levels of biological organization (Pinsky et al., 2020). Phenotypic plasticity is an important component of organismal responses to rapid environmental change (Fox et al., 2019) and can facilitate individual survival in response to changing and variable environments (Merilä & Hendry, 2014). Plasticity in traits such as growth, fecundity, and foraging influence not only individual performance and population growth (Green et al., 2022;Snell-Rood et al., 2018) but can also scale

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Legacy of past exposure to hypoxia and warming regulates an ecosystem service provided by oysters

Donelan

Ogburn

Breitburg

2023

Global Change Biology

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“…It was first characterized by its ability to promote cell division ( Skoog and Miller, 1957 ), and since then, its roles in many cellular processes have been reported ( Kieber and Schaller, 2014 ). In conifers, there is now some discussed evidence that cytokinins are involved in maintenance of the embryogenic state ( Gautier et al, 2019 ), embryo development ( Li et al, 2017 ) as well as transduction of environmental signals resulting in plant phenotypic plasticity ( Castander-Olarieta et al, 2021 ; Trontin et al, 2021 ). The GARP family includes regulatory genes involved in the control of plant responses to nutrients and it has been proposed to also include nutrient sensors ( Safi et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

“…Most knowledge has been gained from short-lived angiosperms (especially Arabidopsis ) and little is known from perennials including gymnosperms. Yet, embryogenesis is a short but crucial phase for seed production and also for imprinting molecular patterns involved in delayed phenotypic plasticity of trees in response to environmental stress ( Trontin et al, 2021 ). Understanding molecular aspects of both somatic (SE) and zygotic embryo (ZE) development in conifers is therefore of undoubted interest ( Trontin et al, 2016c ) at both fundamental and applied levels for (i) comparative studies between angiosperms and gymnosperms, (ii) understanding seed development and (iii) to optimize SE production for conservation, rescue, breeding and deployment issues of selected or natural genetic resources.…”

Section: Introductionmentioning

confidence: 99%

Identification of Metabolic Pathways Differentially Regulated in Somatic and Zygotic Embryos of Maritime Pine

et al. 2022

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Embryogenesis is a complex phase of conifer development involving hundreds of genes, and a proper understanding of this process is critical not only to produce embryos with different applied purposes but also for comparative studies with angiosperms. A global view of transcriptome dynamics during pine somatic and zygotic embryogenesis is currently missing. Here, we present a genome-wide transcriptome analysis of somatic and zygotic embryos at three developmental stages to identify conserved biological processes and gene functions during late embryogenesis. Most of the differences became more significant as the developmental process progressed from early to cotyledonary stages, and a higher number of genes were differentially expressed in somatic than in zygotic embryos. Metabolic pathways substantially affected included those involved in amino acid biosynthesis and utilization, and this difference was already observable at early developmental stages. Overall, this effect was found to be independent of the line (genotype) used to produce the somatic embryos. Additionally, transcription factors differentially expressed in somatic versus zygotic embryos were analyzed. Some potential hub regulatory genes were identified that can provide clues as to what transcription factors are controlling the process and to how the observed differences between somatic and zygotic embryogenesis in conifers could be regulated.

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“…However, organism phenotypes are also shaped by past environments such as those experienced during previous life stages. These within-generation carryover effects are widespread across taxa (13)(14)(15) and can affect important functional traits, including those that respond plastically to current environmental change and affect ecosystem functioning. For example, early life exposure to drought reduces beech tree growth and leaf production (16), which may ultimately influence their ability to sequester carbon, an important ecosystem service, as has been shown in response to current drought (17).…”

Section: Introductionmentioning

confidence: 99%

Legacy of past exposure to hypoxia and warming regulates ecosystem service provided by oysters

Donelan

Ogburn

Breitburg

2022

Preprint

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Climate change is having substantial impacts on organism fitness and ability to deliver critical ecosystem services, but these effects are often examined only in response to current environments. Past exposure to stress can also affect individuals via carryover effects, and whether these effects scale from individuals to influence ecosystem function and services is unclear. We explored carryover effects of two coastal climate change stressors – hypoxia and warming – on oyster (Crassostrea virginica) growth and nitrogen bioassimilation, an important ecosystem service. Oysters were exposed to a factorial combination of two temperature and two diel-cycling dissolved oxygen treatments at three-months-old and again one year later. Carryover effects of hypoxia and warming influenced oyster growth and nitrogen storage, with early life stress generally reducing nitrogen storage and relative tissue growth, particularly in warm environments. When extrapolated to the reef scale, carryover effects reduced estimated nitrogen storage by a restored oyster reef by as much as 41%, a substantial decline in a critical ecosystem service. Even brief exposure to climate change stressors early in life has persistent, negative effects on an ecosystem service one year later. Carryover effects on individuals impact processes at the ecological scale and must be considered in assessments of and management plans for species and ecosystems threatened by anthropogenic change.Significance StatementAnthropogenic change threatens organisms’ ability to provide ecosystem services through effects on individual phenotypes. Past experiences with anthropogenic stress can have delayed, persistent impacts on organisms via carryover effects, but how carryover effects scale to influence ecosystem function and services is not yet established. In marine systems, foundation species such as oysters mitigate effects of eutrophication by storing nutrients like nitrogen in their tissue and shell. We show that past exposure to two interacting climate change stressors (hypoxia and warming) reduces nitrogen stored by oysters by as much as 41% one year after initial exposure. Our results reveal carryover effects as a novel pathway through which climate change affects ecosystem processes that should be incorporated into conservation and management plans.

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Tree ‘memory’: new insights on temperature-induced priming effects during early embryogenesis

Cited by 11 publications

References 32 publications

Legacy of past exposure to hypoxia and warming regulates an ecosystem service provided by oysters

Legacy of past exposure to hypoxia and warming regulates an ecosystem service provided by oysters

Identification of Metabolic Pathways Differentially Regulated in Somatic and Zygotic Embryos of Maritime Pine

Legacy of past exposure to hypoxia and warming regulates ecosystem service provided by oysters

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