Adaptive significance of flowering time variation across natural seasonal environments in Arabidopsis thaliana.

The relevance of flowering time variation and plasticity to climate adaptation requires a comprehensive empirical assessment. We investigated natural selection and the genetic architecture of flowering time in Arabidopsis through field experiments in Europe across multiple sites and seasons. We estimated selection for flowering time, plasticity and canalization. Loci associated with flowering time, plasticity and canalization by genome-wide association studies were tested for a geographic signature of climate adaptation. Selection favored early flowering and increased canalization, except at the northernmost site, but was rarely detected for plasticity. Genome-wide association studies revealed significant associations with flowering traits and supported a substantial polygenic inheritance. Alleles associated with late flowering, including functional FRIGIDA variants, were more common in regions experiencing high annual temperature variation. Flowering time plasticity to fall vs spring and summer environments was associated with GIGANTEA SUPPRESSOR 5, which promotes early flowering under decreasing day length and temperature. The finding that late flowering genotypes and alleles are associated with climate is evidence for past adaptation. Real-time phenotypic selection analysis, however, reveals pervasive contemporary selection for rapid flowering in agricultural settings across most of the species range. The response to this selection may involve genetic shifts in environmental cuing compared to the ancestral state.

Large-effect flowering time mutations reveal conditionally adaptive paths through fitness landscapes in Arabidopsis thaliana.

Contrary to previous assumptions that most mutations are deleterious, there is increasing evidence for persistence of large-effect mutations in natural populations. A possible explanation for these observations is that mutant phenotypes and fitness may depend upon the specific environmental conditions to which a mutant is exposed. Here, we tested this hypothesis by growing large-effect flowering time mutants of Arabidopsis thaliana in multiple field sites and seasons to quantify their fitness effects in realistic natural conditions. By constructing environment-specific fitness landscapes based on flowering time and branching architecture, we observed that a subset of mutations increased fitness, but only in specific environments. These mutations increased fitness via different paths: through shifting flowering time, branching, or both. Branching was under stronger selection, but flowering time was more genetically variable, pointing to the importance of indirect selection on mutations through their pleiotropic effects on multiple phenotypes. Finally, mutations in hub genes with greater connectedness in their regulatory networks had greater effects on both phenotypes and fitness. Together, these findings indicate that large-effect mutations may persist in populations because they influence traits that are adaptive only under specific environmental conditions. Understanding their evolutionary dynamics therefore requires measuring their effects in multiple natural environments.

Fluctuating, warm temperatures decrease the effect of a key floral repressor on flowering time in Arabidopsis thaliana.

The genetic basis of growth and development is often studied in constant laboratory environments; however, the environmental conditions that organisms experience in nature are often much more dynamic. We examined how daily temperature fluctuations, average temperature, day length and vernalization influence the flowering time of 59 genotypes of Arabidopsis thaliana with allelic perturbations known to affect flowering time. For a subset of genotypes, we also assessed treatment effects on morphology and growth. We identified 17 genotypes, many of which have high levels of the floral repressor FLOWERING LOCUS C (FLC), that bolted dramatically earlier in fluctuating - as opposed to constant - warm temperatures (mean = 22°C). This acceleration was not caused by transient VERNALIZATION INSENSITIVE 3-mediated vernalization, differential growth rates or exposure to high temperatures, and was not apparent when the average temperature was cool (mean = 12°C). Further, in constant temperatures, contrary to physiological expectations, these genotypes flowered more rapidly in cool than in warm environments. Fluctuating temperatures often reversed these responses, restoring faster bolting in warm conditions. Independently of bolting time, warm fluctuating temperature profiles also caused morphological changes associated with shade avoidance or 'high-temperature' phenotypes. Our results suggest that previous studies have overestimated the effect of the floral repressor FLC on flowering time by using constant temperature laboratory conditions.

Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes.

Organisms develop through multiple life stages that differ in environmental tolerances. The seasonal timing, or phenology, of life-stage transitions determines the environmental conditions to which each life stage is exposed and the length of time required to complete a generation. Both environmental and genetic factors contribute to phenological variation, yet predicting their combined effect on life cycles across a geographic range remains a challenge. We linked submodels of the plasticity of individual life stages to create an integrated model that predicts life-cycle phenology in complex environments. We parameterized the model for Arabidopsis thaliana and simulated life cycles in four locations. We compared multiple "genotypes" by varying two parameters associated with natural genetic variation in phenology: seed dormancy and floral repression. The model predicted variation in life cycles across locations that qualitatively matches observed natural phenology. Seed dormancy had larger effects on life-cycle length than floral repression, and results suggest that a genetic cline in dormancy maintains a life-cycle length of 1 year across the geographic range of this species. By integrating across life stages, this approach demonstrates how genetic variation in one transition can influence subsequent transitions and the geographic distribution of life cycles more generally.

Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana.

Relating molecular variation to phenotypic diversity is a central goal in evolutionary biology. In Arabidopsis thaliana, FLOWERING LOCUS C (FLC) is a major determinant of variation in vernalization--the acceleration of flowering by prolonged cold. Here, through analysis of 1307 A. thaliana accessions, we identify five predominant FLC haplotypes defined by noncoding sequence variation. Genetic and transgenic experiments show that they are functionally distinct, varying in FLC expression level and rate of epigenetic silencing. Allelic heterogeneity at this single locus accounts for a large proportion of natural variation in vernalization that contributes to adaptation of A. thaliana.

Lagging adaptation to warming climate in Arabidopsis thaliana.

If climate change outpaces the rate of adaptive evolution within a site, populations previously well adapted to local conditions may decline or disappear, and banked seeds from those populations will be unsuitable for restoring them. However, if such adaptational lag has occurred, immigrants from historically warmer climates will outperform natives and may provide genetic potential for evolutionary rescue. We tested for lagging adaptation to warming climate using banked seeds of the annual weed Arabidopsis thaliana in common garden experiments in four sites across the species' native European range: Valencia, Spain; Norwich, United Kingdom; Halle, Germany; and Oulu, Finland. Genotypes originating from geographic regions near the planting site had high relative fitness in each site, direct evidence for broad-scale geographic adaptation in this model species. However, genotypes originating in sites historically warmer than the planting site had higher average relative fitness than local genotypes in every site, especially at the northern range limit in Finland. This result suggests that local adaptive optima have shifted rapidly with recent warming across the species' native range. Climatic optima also differed among seasonal germination cohorts within the Norwich site, suggesting that populations occurring where summer germination is common may have greater evolutionary potential to persist under future warming. If adaptational lag has occurred over just a few decades in banked seeds of an annual species, it may be an important consideration for managing longer-lived species, as well as for attempts to conserve threatened populations through ex situ preservation.

Pathogen-triggered ethylene signaling mediates systemic-induced susceptibility to herbivory in Arabidopsis.

Multicellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites. We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemic-induced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.

Paths to selection on life history loci in different natural environments across the native range of Arabidopsis thaliana.

Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment-specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2-5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.

An augmented Arabidopsis phenology model reveals seasonal temperature control of flowering time.

• In this study, we used a combination of theoretical (models) and experimental (field data) approaches to investigate the interaction between light and temperature signalling in the control of Arabidopsis flowering. • We utilised our recently published phenology model that describes the flowering time of Arabidopsis grown under a range of field conditions. We first examined the ability of the model to predict the flowering time of field plantings at different sites and seasons in light of the specific meteorological conditions that pertained. • Our analysis suggested that the synchrony of temperature and light cycles is important in promoting floral initiation. New features were incorporated into the model that improved its predictive accuracy across seasons. Using both laboratory and field data, our study has revealed an important seasonal effect of night temperatures on flowering time. Further model adjustments to describe phytochrome (phy) mutants supported our findings and implicated phyB in the temporal gating of temperature-induced flowering. • Our study suggests that different molecular pathways interact and predominate in natural environments that change seasonally. Temperature effects are mediated largely during the photoperiod during spring/summer (long days) but, as days shorten in the autumn, night temperatures become increasingly important.

Contrasting patterns of transgenerational plasticity in ecologically distinct congeners.

Stressful parental environments can influence offspring size and development either adaptively or maladaptively, yet little is known about species' differences in this complex aspect of phenotypic plasticity. We performed a reciprocal split-brood experiment to compare transgenerational plasticity in response to drought stress in two closely related annual plant species. We raised inbred replicate parent plants of eight genotypes per species in dry vs. moist soil to generate offspring of each genetic line that differed only in parental environment, then monitored seedling development in both dry and moist conditions. Individuals of the two species expressed contrasting patterns of transgenerational plasticity for traits important to seedling drought tolerance. In Polygonum persicaria, a weedy generalist found in moist, dry, and variably dry sites, drought-stressed plants produced offspring with longer and more rapidly extending root systems and greater biomass when growing in dry soil. In contrast, in P. hydropiper, a non-weedy congener restricted to moist habitats, the offspring of drought-stressed parents had reduced root system development and seedling biomass in dry soil. In P. persicaria, transgenerational and immediate adaptive plasticity combined to produce drought-adapted seedling phenotypes. These results make clear that characteristic patterns of transgenerational plasticity can contribute to ecological diversity among species.

Effects of genetic perturbation on seasonal life history plasticity.

Like many species, the model plant Arabidopsis thaliana exhibits multiple different life histories in natural environments. We grew mutants impaired in different signaling pathways in field experiments across the species' native European range in order to dissect the mechanisms underlying this variation. Unexpectedly, mutational loss at loci implicated in the cold requirement for flowering had little effect on life history except in late-summer cohorts. A genetically informed photothermal model of progression toward flowering explained most of the observed variation and predicted an abrupt transition from autumn flowering to spring flowering in late-summer germinants. Environmental signals control the timing of this transition, creating a critical window of acute sensitivity to genetic and climatic change that may be common for seasonally regulated life history traits.