Adaptive Value of Phenological Traits in Stressful Environments: Predictions Based on Seed Production and Laboratory Natural Selection

Brachi, Benjamin; Aimé, Carla; Glorieux, Cédric; Cuguen, Joël; Roux, Fabrice

doi:10.1371/journal.pone.0032069

Cited by 50 publications

(61 citation statements)

References 80 publications

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“…Similarly, more recent work showed that the progeny of plants exposed to heat for 3 generations also exhibited early flowering phenotype. 37 Also, Brachi et al (2012), found selection for early bolting in the progeny of water stressed plants, similar to our results for heat stress. …”

Section: Changes To Seed Phenotypesupporting

confidence: 88%

“…Often, changes in response to stress such as temperature are reversible, but in certain cases these modifications, including phenotypic and epigenetic, may be passed on to the progeny. 8,9 Epigenetic systems have the dynamic ability to rapidly induce changes in response to stress, resulting in modifications that may be short or long-term. [10][11][12] For example, environmental stress has been shown to cause hypo-or hypermethylation, altering the accessibility of chromatin to recombination machinery, and thus modifying variability in the genome at a time when it is most needed.…”

Section: Introductionmentioning

confidence: 99%

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Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Migicovsky

Yao

Kovalchuk

2014

Plant Signaling & Behavior

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Abbreviations: ChiP, chromatin immunoprecipitation; DCL, Dicer-like; Dpg, days post germination; gDNA, genomic DNA; "C 1 ," progeny of control plants; "C 1 -", progeny of control plants grown under normal conditions; "C 1 +," progeny of control plants grown under stress conditions; "S 1 ," progeny of stress plants; "S 1 -," progeny of stressed plants grown under normal conditions; "S 1 +," progeny of stressed plants grown under stress conditions; qPCR, quantitative PCR; RdDM, RNA-directed DNA methylation; SAR, systemic acquired resistance; sRNAs, small RNAs; TE, transposable elements exposure to heat stress causes physiological and epigenetic changes in plants, which may also be altered in the progeny. We compared the progeny of stressed and control Arabidopsis thaliana wild type and Dicer-like mutant dcl2, dcl3, and dcl4 plants for variations in physiology and molecular profile, including global genome methylation, mRNa levels, and histone modifications in the subset of differentially expressed genes at normal conditions and in response to heat stress. We found that the immediate progeny of heat-stressed plants had fewer, but larger leaves, and tended to bolt earlier. Transposon expression was elevated in the progeny of heat-stressed plants, and heat stress in the same generation tended to decrease global genome methylation. Progeny of stressed plants had increased expression of HSFA2, and reduction in MSH2, ROS1, and several SUVH genes. Gene expression positively correlated with permissive histone marks and negatively correlated with repressive marks. Overall, the progeny of heat stressed plants varied in both their physiology and epigenome and dcl2 and dcl3 mutants were partially deficient for these changes.

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Section: Changes To Seed Phenotypesupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Migicovsky

Yao

Kovalchuk

2014

Plant Signaling & Behavior

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“…The large-effect nature and low frequency of these new APR2 alleles in the Arabidopsis species-wide collection used in this study are consistent with them being of recent adaptive significance (Brachi et al, 2012;Rockman, 2012). Because of the species-wide nature of the collection of accessions used, locally adaptive alleles would be sampled at a low frequency in the population.…”

Section: Discussionsupporting

confidence: 69%

Variation in Sulfur and Selenium Accumulation Is Controlled by Naturally Occurring Isoforms of the Key Sulfur Assimilation Enzyme ADENOSINE 5′-PHOSPHOSULFATE REDUCTASE2 across the Arabidopsis Species Range

et al. 2014

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Natural variation allows the investigation of both the fundamental functions of genes and their role in local adaptation. As one of the essential macronutrients, sulfur is vital for plant growth and development and also for crop yield and quality. Selenium and sulfur are assimilated by the same process, and although plants do not require selenium, plant-based selenium is an important source of this essential element for animals. Here, we report the use of linkage mapping in synthetic F2 populations and complementation to investigate the genetic architecture of variation in total leaf sulfur and selenium concentrations in a diverse set of Arabidopsis (Arabidopsis thaliana) accessions. We identify in accessions collected from Sweden and the Czech Republic two variants of the enzyme ADENOSINE 59-PHOSPHOSULFATE REDUCTASE2 (APR2) with strongly diminished catalytic capacity. APR2 is a key enzyme in both sulfate and selenate reduction, and its reduced activity in the loss-of-function allele apr2-1 and the two Arabidopsis accessions Hodonín and Shahdara leads to a lowering of sulfur flux from sulfate into the reduced sulfur compounds, cysteine and glutathione, and into proteins, concomitant with an increase in the accumulation of sulfate in leaves. We conclude from our observation, and the previously identified weak allele of APR2 from the Shahdara accession collected in Tadjikistan, that the catalytic capacity of APR2 varies by 4 orders of magnitude across the Arabidopsis species range, driving significant differences in sulfur and selenium metabolism. The selective benefit, if any, of this large variation remains to be explored.

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“…Fruit length is sometimes used as a proxy for seed number and for estimates of fitness in A. thaliana (e.g., Brachi et al 2012). Here, we find that although there is a significant correlation between fruit length and seed number (Table 2), it is far from perfect.…”

Section: Discussionmentioning

confidence: 56%

“…Although his sign test was proposed for QTL studies using intercross between two accessions, its logic can be equally applied to multiparent populations. We argue that there is a very small chance of observing that all alleles that produce large seeds come from the same accession (Bur), when there are 19 parental accessions, if seed size variation was neutral.Thus, we propose that the large seed size observed in the Bur accession is due to directional selection, and that at least some of the variation in seed size within A. thaliana is due to adaptive processes.Fruit length is sometimes used as a proxy for seed number and for estimates of fitness in A. thaliana (e.g., Brachi et al 2012). Here, we find that although there is a significant correlation between fruit length and seed number (Table 2), it is far from perfect.…”

mentioning

confidence: 56%

The Genetic Basis of Natural Variation in Seed Size and Seed Number and Their Trade-Off Using Arabidopsis thaliana MAGIC Lines

Gnan¹,

Priest²,

Kover

2014

Genetics

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Offspring number and size are key traits determining an individual's fitness and a crop's yield. Yet, extensive natural variation within species is observed for these traits. Such variation is typically explained by trade-offs between fecundity and quality, for which an optimal solution is environmentally dependent. Understanding the genetic basis of seed size and number, as well as any possible genetic constraints preventing the maximization of both, is crucial from both an evolutionary and applied perspective. We investigated the genetic basis of natural variation in seed size and number using a set of Arabidopsis thaliana multiparent advanced generation intercross (MAGIC) lines. We also tested whether life history affects seed size, number, and their trade-off. We found that both seed size and seed number are affected by a large number of mostly nonoverlapping QTL, suggesting that seed size and seed number can evolve independently. The allele that increases seed size at most identified QTL is from the same natural accession, indicating past occurrence of directional selection for seed size. Although a significant trade-off between seed size and number is observed, its expression depends on life-history characteristics, and generally explains little variance. We conclude that the trade-off between seed size and number might have a minor role in explaining the maintenance of variation in seed size and number, and that seed size could be a valid target for selection.T HE reproductive output of an organism is a critical lifehistory trait defining its fitness and is the result of both offspring number and quality. In the case of cereal crops, the number and size of seeds are also the main constituents of yield. Thus, understanding the genetic architecture of seed size and number, and any possible genetic constraints to maximizing them, is crucial from both an evolutionary and applied perspective (Sadras 2007;Van Daele et al. 2012;Kesavan et al. 2013). Despite its importance, the genetic basis of natural variation in seed size and number and their interaction with life-history traits remain poorly understood.Previous studies on the genetic basis of seed traits have predominantly used mutant screens and identified genes in key pathways involved in seed development (Garcia et al. 2003;Tzafrir et al. 2004;Adamski et al. 2009;Fang et al. 2012). However, since this approach only allows for the comparison of phenotypic effects of genes that are "on" or "off" (Koornneef et al. 2004), genes' contribution to natural continuous variation in seed size or seed number remain largely uncharacterized. Because the effects of mutants are often dependent on the genetic background (Tonsor et al. 2005;Chou et al. 2011), a QTL mapping approach using multiple parents is ideal to identify genetic factors that can contribute to natural variation in these traits in a heterogeneous genetic background.Identification of genetic factors affecting seed traits is further complicated by potential trade-offs between them. Life-history the...

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Adaptive Value of Phenological Traits in Stressful Environments: Predictions Based on Seed Production and Laboratory Natural Selection

Cited by 50 publications

References 80 publications

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Transgenerational phenotypic and epigenetic changes in response to heat stress inArabidopsis thaliana

Variation in Sulfur and Selenium Accumulation Is Controlled by Naturally Occurring Isoforms of the Key Sulfur Assimilation Enzyme ADENOSINE 5′-PHOSPHOSULFATE REDUCTASE2 across the Arabidopsis Species Range

The Genetic Basis of Natural Variation in Seed Size and Seed Number and Their Trade-Off Using Arabidopsis thaliana MAGIC Lines

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