skip to main content


Title: Cold tolerance in the genus Arabidopsis
Premise

Cold tolerance is an important factor limiting the geographic distribution and growing season for many plant species, yet few studies have examined variation in cold tolerance extensively within and among closely related species and compared that to their geographic distribution.

Methods

This study examines cold tolerance within and among species in the genusArabidopsis. We assessed cold tolerance by measuring electrolyte leakage from detached leaves in multiple populations of fiveArabidopsistaxa. The temperature at which 50% of cells were lysed was considered the lethal temperature (LT50).

Results

We found variability within and among taxa in cold tolerance. There was no significant within‐species relationship between latitude and cold tolerance. However, the northern taxa,A. kamchatica,A. lyratasubsp.petraea, andA. lyratasubsp.lyrata, were more cold tolerant thanA. thalianaandA. hallerisubsp.gemmiferaboth before and after cold acclimation. Cold tolerance increased after cold acclimation (exposure to low, but nonfreezing temperatures) for all taxa, although the difference was not significant forA. hallerisubsp.gemmifera. For all taxa exceptA. lyratasubsp.lyrata, theLT50values for cold‐acclimated plants were higher than the January mean daily minimum temperature (Tmin), indicating that if plants were not insulated by snow cover, they would not likely survive winter at the northern edge of their range.

Conclusions

Arabidopsis lyrataandA. kamchaticawere far more cold tolerant thanA. thaliana. These extremely cold‐tolerant taxa are excellent candidates for studying both the molecular and ecological aspects of cold tolerance.

 
more » « less
NSF-PAR ID:
10458734
Author(s) / Creator(s):
 ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
American Journal of Botany
Volume:
107
Issue:
3
ISSN:
0002-9122
Page Range / eLocation ID:
p. 489-497
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Premise

    Despite myriad examples of local adaptation, the phenotypes and genetic variants underlying such adaptive differentiation are seldom known. Recent work on freezing tolerance and local adaptation in ecotypes ofArabidopsis thalianafrom Italy and Sweden provides an essential foundation for uncovering the genotype–phenotype–fitness map for an adaptive response to a key environmental stress.

    Methods

    We examined the consequences of a naturally occurring loss‐of‐function (LOF) mutation in an Italian allele of the gene that encodes the transcription factorCBF2,which underlies a major freezing‐tolerance locus. We used four lines with a Swedish genetic background, each containing aLOFCBF2allele. Two lines had introgression segments containing the ItalianCBF2allele, and two contained deletions created usingCRISPR‐Cas9. We used a growth chamber experiment to quantify freezing tolerance and gene expression before and after cold acclimation.

    Results

    Freezing tolerance was lower in the Italian (11%) compared to the Swedish (72%) ecotype, and all four experimentalCBF2LOFlines had reduced freezing tolerance compared to the Swedish ecotype. Differential expression analyses identified 10 genes for which allCBF2LOFlines, and theITecotype had similar patterns of reduced cold responsive expression compared to theSWecotype.

    Conclusions

    We identified 10 genes that are at least partially regulated byCBF2that may contribute to the differences in cold‐acclimated freezing tolerance between the Italian and Swedish ecotypes. These results provide novel insight into the molecular and physiological mechanisms connecting a naturally occurring sequence polymorphism to an adaptive response to freezing conditions.

     
    more » « less
  2. Premise

    Determining how species perform in novel climatic environments is essential for understanding (1) responses to climate change and (2) evolutionary consequences of biological invasions. For the vast majority of species, the number of population characteristics that will predict performance and patterns of natural selection in novel locations in the wild remains limited.

    Methods

    We evaluated phenological, vegetative, architectural, and fitness‐related traits in experimental gardens in contrasting climates (Ontario, Canada, and South Carolina,USA) in the North American non‐native distribution ofArabidopsis thaliana. We assessed the effects of climatic distance, geographic distance, and genetic features of history on performance and patterns of natural selection in the novel garden settings.

    Results

    We found that plants had greater survivorship, flowered earlier, were larger, and produced more fruit in the south, and that genotype‐by‐environment interactions were significant between gardens. However, our analyses revealed similar patterns of natural selection between gardens in distinct climate zones. After accounting for genetic ancestry, we also detected that population climatic distance best predicted performance within gardens.

    Conclusions

    These data suggest that colonization success in novel, non‐native environments is determined by a combination of climate and genetic history. When performance at novel sites was assessed with seed sources from geographically and genetically disparate, established non‐native populations, proximity to the garden alone was insufficient to predict performance. Our study highlights the need to evaluate seed sources from diverse origins to describe comprehensively phenotypic responses to novel environments, particularly for taxa in which many source populations may contribute to colonization.

     
    more » « less
  3. Abstract Questions

    What are the primary biotic and abiotic factors driving composition and abundance of naturally regenerated tree seedlings across forest landscapes of Maine? Do seedling species richness (SR) and density (SD) decrease with improved growing conditions (climate and soil), but increase with increased diversity of overstorey composition and structure? Does partial harvesting disproportionately favour relative dominance of shade‐intolerant hardwoods (PIHD) over shade‐tolerant softwoods (PTSD)?

    Location

    Forest landscapes across the diverse eco‐regions and forest types of Maine,USA.

    Methods

    This study usedUSDAForest Service Forest Inventory Analysis permanent plots (n = 10 842), measured every 5 yr since 1999. The best models for each response variable (SR,SD,PIHDandPTSD) were developed based onAICand biological interpretability, while considering 35 potential explanatory variables incorporating climate, soil, site productivity, overstorey structure and composition, and past harvesting.

    Results

    Mean annual temperature was the most important abiotic factor, whereas overstorey tree size diversity was the most important biotic factor forSRandSD. Both mean annual temperature and overstorey tree size diversity had a curvilinear relationship withSRandSD. Average overstorey shade tolerance and percentage tolerant softwood basal area in the overstorey were the top predictor variables ofPIHDandPTSD,respectively. Partial harvesting favouredPIHDbut notPTSD.

    Conclusions

    This is one of the first studies to comprehensively evaluate a number of factors influencing naturally established tree seedlings at a broad landscape scale in the Northern Forest region of the easternUSAand Canada. Despite limitations associated with relatively small plot size, large seedling size class and lack of direct measurements of light, water and nutrients, this study documents the influence of these factors amid high variability associated with patterns of natural regeneration. The curvilinear relationship between mean annual temperature withSRandSDsupports the argument that species richness and abundance usually have unimodal relationships with productivity indicators, whereas the curvilinear relationship between overstorey tree size diversity andSRandSDsuggest that moderate overstorey diversity incorporates multiple species as well as higher seedling individuals.

     
    more » « less
  4. Abstract

    Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole,Anolis carolinensis, we integrate measures of cold tolerance (CTmin), standard metabolic rate, heart size, blood lactate concentration andRNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co‐expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity‐limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.

     
    more » « less
  5. Abstract

    The Olympia oyster (Ostrea lurida) is a foundation species inhabiting estuaries along the North American west coast. In California estuaries,O. luridais adapted to local salinity regimes and populations differ in low salinity tolerance. In this study, oysters from three California populations were reared for two generations in a laboratory common garden and subsequently exposed to low salinity seawater. Comparative transcriptomics was then used to understand species‐level responses to hyposmotic stress and population‐level mechanisms underlying divergent salinity tolerances. Gene expression patterns indicate Olympia oysters are sensitive to hyposmotic stress: All populations respond to low salinity by up‐regulating transcripts indicative of protein unfolding,DNAdamage and cell cycle arrest after sub‐lethal exposure. AmongO. luridapopulations, transcriptomic profiles differed constitutively and in response to low salinity. Despite two generations in common‐garden conditions, transcripts encoding apoptosis modulators were constitutively expressed at significantly different levels in the most tolerant population. Expression of cell death regulators may facilitate cell fate decisions when salinity declines. Following low salinity exposure, oysters from the more tolerant population expressed a small number of mRNAs at significantly higher levels than less tolerant populations. Proteins encoded by these transcripts regulate ciliary activity within the mantle cavity and may function to prolong valve closure and reduce mortality in low salinity seawater. Collectively, gene expression patterns suggest sub‐lethal impacts of hyposmotic stress in Olympia oysters are considerable and that even oysters with greater low salinity tolerance may be vulnerable to future freshwater flooding events.

     
    more » « less