Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana

Introduced species frequently show geographic differentiation, and when differentiation mirrors the ancestral range, it is often taken as evidence of adaptive evolution. The mouse-ear cress (Arabidopsis thaliana) was introduced to North America from Eurasia 150-200 years ago, providing an opportunity to study parallel adaptation in a genetic model organism. Here, we test for clinal variation in flowering time using 199 North American (NA) accessions of A. thaliana, and evaluate the contributions of major flowering time genes FRI, FLC, and PHYC as well as potential ecological mechanisms underlying differentiation. We find evidence for substantial within population genetic variation in quantitative traits and flowering time, and putatively adaptive longitudinal differentiation, despite low levels of variation at FRI, FLC, and PHYC and genome-wide reductions in population structure relative to Eurasian (EA) samples. The observed longitudinal cline in flowering time in North America is parallel to an EA cline, robust to the effects of population structure, and associated with geographic variation in winter precipitation and temperature. We detected major effects of FRI on quantitative traits associated with reproductive fitness, although the haplotype associated with higher fitness remains rare in North America. Collectively, our results suggest the evolution of parallel flowering time clines through novel genetic mechanisms.     

Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis

Extensive natural variation has been described for the timing of flowering initiation in many annual plants, including the model wild species Arabidopsis (Arabidopsis thaliana), which is presumed to be involved in adaptation to different climates. However, the environmental factors that might shape this genetic variation, as well as the molecular bases of climatic adaptation by modifications of flowering time, remain mostly unknown. To approach both goals, we characterized the flowering behavior in relation to vernalization of 182 Arabidopsis wild genotypes collected in a native region spanning a broad climatic range. Phenotype-environment association analyses identified strong altitudinal clines (0-2600 m) in seven out of nine flowering-related traits. Altitudinal clines were dissected in terms of minimum winter temperature and precipitation, indicating that these are the main climatic factors that might act as selective pressures on flowering traits. In addition, we used an association analysis approach with four candidate genes, FRIGIDA (FRI), FLOWERING LOCUS C (FLC), PHYTOCHROME C (PHYC), and CRYPTOCHROME2, to decipher the genetic bases of this variation. Eleven different loss-of-function FRI alleles of low frequency accounted for up to 16% of the variation for most traits. Furthermore, an FLC allelic series of six novel putative loss- and change-of-function alleles, with low to moderate frequency, revealed that a broader FLC functional diversification might contribute to flowering variation. Finally, environment-genotype association analyses showed that the spatial patterns of FRI, FLC, and PHYC polymorphisms are significantly associated with winter temperatures and spring and winter precipitations, respectively. These results support that allelic variation in these genes is involved in climatic adaptation.     

Quantifying latitudinal clines to light responses in natural populations of Arabidopsis thaliana (Brassicaceae)

Evidence of adaptation in Arabidopsis thaliana (Brassicaceae) phenotypic traits has rarely been shown. We demonstrate latitudinal clines in two A. thaliana traits: hypocotyl responses to red and far-red light. Natural populations of A. thaliana were sampled along a latitudinal gradient from southern to northern Norway. Seeds from maternal families within each population were subjected to 1 wk of constant red, far-red, blue, white, and dark treatments. Hypocotyl lengths were measured for each maternal family within each population. Significant variability within and among populations in hypocotyl responses for the various treatments was found. There was a significant latitudinal cline in hypocotyl responses for red and far-red treatments, with northern populations being more de-etiolated than southern populations. These results suggest that northern populations are more responsive to red and far-red light than southern populations. Thus, differentiation of seedling traits in natural populations of A. thaliana seems in part to be mediated by the phytochrome pathway. There was no correlation between hypocotyl responses and flowering time for any treatment. This suggests that flowering time variability and variability in hypocotyl responses may not be governed by genes shared between the pathways, such as those involved in photoreception or the circadian clock.     

Evidence for a link between local and seasonal cycles in gene frequencies and latitudinal gene clines in a cyclic parthenogen

In an earlier study (Rhombergh et al., Can. J. Genet. Cytol. 27: 224-232, 1985) of natural populations of the cyclic parthenogenetic Rose aphids, Macrosiphum rosae, 6 out of 31 loci were found to be polymorphic and one locus (Esterase-4) showed cyclic seasonal changes in gene and genotypic frequencies. Assuming that the Est-4 polymorphism was balanced and due to some climatic factor that varies seasonally, and realizing that most environmental factors that vary seasonally also vary latitudinally, we predicted existence of a latitudinal gene cline at this locus. In the present study we surveyed four polymorphic loci (chosen to be used as markers) in six geographic populations spanning over 1200 km between the United States and Canada and found all four loci to have latitudinal clines. We think that the gene clines are due to a latitudinal cline in the degree of advancement of local populations through the seasonal cycle, and have called such a pattern a 'seasonal phase cline'. The results are discussed in relation to the temporal instability of local patterns and persistence of genetic variability on the large scale in aphids. It is argued that population structure of aphids makes retention of selectively neutral or weakly selected polymorphisms difficult.     

The Genetic Architecture of Flowering Time and Photoperiod Sensitivity in Maize as Revealed by QTL Review and Meta Analysis

The control of flowering is not only important for reproduction,but also plays a key role in the processes of domestication and adaptation.To reveal the genetic architecture for flowering time and photoperiod sensitivity,a comprehensive evaluation of the relevant literature was performed and followed by meta analysis.A total of 25 synthetic consensus quantitative trait loci(QTL)and four hot-spot genomic regions were identified for photoperiod sensitivity including 11 genes related to photoperiod response or flower morphogenesis and development.Besides,a comparative analysis of the QTL for flowering time and photoperiod sensitivity highlighted the regions containing shared and unique QTL for the two traits.Candidate genes associated with maize flowering were identified through integrated analysis of the homologous genes for flowering time in plants and the consensus QTL regions for photoperiod sensitivity in maize(Zea mays L.).Our results suggest that the combination of literature review,meta-analysis and homologous blast is an efficient approach to identify new candidate genes and create a global view of the genetic architecture for maize photoperiodic flowering.Sequences of candidate genes can be used to develop molecular markers for various models of marker-assisted selection,such as marker-assisted recurrent selection and genomic selection that can contribute significantly to crop environmental adaptation.     

Influence of seasonal time constraints on growth and development of common frog tadpoles: a photoperiod experiment

Organisms living in seasonal environments are often limited by the time available to complete their development. Especially individuals in northern populations may face severe time constraints in their need of completing development before the end of the growth season. Larval amphibians have been widely used in studies of phenotypic plasticity. However, their responses to changes in photoperiod, the main seasonal cue in many organisms, are unknown. In a laboratory experiment, we studied whether common frog (Rana temporaria) tadpoles originating from two populations (separated latitudinally by 1600 km) adjust their growth and development according to the progress of the season by using photoperiodic cues, and whether these responses are temperature dependent. We hypothesised that if frogs use photoperiod as a cue, they should increase growth and development rates as a response to photoperiodic treatments mimicking progressing season. Although our predictions were not verified in either of the populations, photoperiod manipulations had effects on larval life history in both populations. When exposed to progressing season treatments and high temperature, tadpoles from the southern population ceased feeding, which led to delayed metamorphosis and increased mortality. In the northern population, age at metamorphosis was unaffected by the photoperiod treatments, but growth rate until metamorphosis and metamorphic size were slightly larger in the treatments with shorter (increasing or decreasing) day length. Irrespective of photoperiod treatments, growth and development rates, size at metamorphosis and food consumption were higher in the northern as compared to the southern population. These results indicate that in contrast to several insect species, the critical life history decisions in amphibian larvae may not be strongly influenced by photoperiodic cues, but different populations seem to differ in this respect. However, the strong temperature×photoperiod interactions in several traits in the southern population suggest that the role of photoperiodic cues may be affected by other environmental factors, although the ecological significance of these differences remains unclear.     

Seasonal and plant-density dependency for quantitative trait loci affecting flowering time in multiple populations of Arabidopsis thaliana

Multiple environmental cues regulate the transition to flowering. In natural environments, plants perceive seasonal progression by changes in day length and growth temperature, and plant density is monitored by changes in the light quality reflected from neighbouring vegetation. To understand the seasonal and plant-density dependence associated with natural allelic variation in flowering time, we conducted a quantitative trait loci (QTL) mapping study in Ler x Cvi, Bay x Sha and Ler x No-0 recombinant inbred line (RIL) populations of Arabidopsis thaliana. Days and total leaf number to bolting were examined under low and high plant density (200 or 1600 plants m(-2)) in autumn-winter and spring seasons. We found between 4 and 10 QTLs associated with seasonal and density variations in each RIL population. For Ler x Cvi and Bay x Sha RIL populations, a major proportion of QTLs showed seasonal and density interaction (up to 63%) and four QTLs were common to all environments (21%). Only three QTLs showed seasonal or density dependency. By aligning the linkage maps onto a common physical map, we detected at least one QTL at chromosome 2 and two QTLs at chromosome 5 that overlap between the three RIL populations, suggesting that these QTLs play a crucial role in the adaptive control of flowering time.     

Adaptive patterns of phenotypic plasticity in laboratory and field environments in Drosophila melanogaster

Identifying mechanisms of adaptation to variable environments is essential in developing a comprehensive understanding of evolutionary dynamics in natural populations. Phenotypic plasticity allows for phenotypic change in response to changes in the environment, and as such may play a major role in adaptation to environmental heterogeneity. Here, the plasticity of stress response in Drosophila melanogaster originating from two distinct geographic regions and ecological habitats was examined. Adults were given a short‐term, 5‐day exposure to combinations of temperature and photoperiod to elicit a plastic response for three fundamental aspects of stress tolerance that vary adaptively with geography. This was replicated both in the laboratory and in outdoor enclosures in the field. In the laboratory, geographic origin was the primary determinant of the stress response. Temperature and the interaction between temperature and photoperiod also significantly affected stress resistance. In the outdoor enclosures, plasticity was distinct among traits and between geographic regions. These results demonstrate that short‐term exposure of adults to ecologically relevant environmental cues results in predictable effects on multiple aspects of fitness. These patterns of plasticity vary among traits and are highly distinct between the two examined geographic regions, consistent with patterns of local adaptation to climate and associated environmental parameters.     

Selection for population‐specific adaptation shaped patterns of variation in the photoperiod pathway genes in Arabidopsis lyrata during post‐glacial colonization

Spatially varying selection can lead to population‐specific adaptation, which is often recognized at the phenotypic level; however, the genetic evidence is weaker in many groups of organisms. In plants, environmental shifts that occur due to colonization of a novel environment may require adaptive changes in the timing of growth and flowering, which are often governed by location‐specific environmental cues such as day length. We studied locally varying selection in 19 flowering time loci in nine populations of the perennial herb Arabidopsis lyrata, which has a wide but patchy distribution in temperate and boreal regions of the northern hemisphere. The populations differ in their recent population demographic and colonization histories and current environmental conditions, especially in the growing season length. We searched for population‐specific molecular signatures of directional selection by comparing a set of candidate flowering time loci with a genomic reference set within each population using multiple approaches and contrasted the patterns of different populations. The candidate loci possessed approximately 20% of the diversity of the reference loci. On average the flowering time loci had more rare alleles (a smaller Tajima's D) and an excess of highly differentiated sites relative to the reference, suggesting positive selection. The strongest signal of selection was detected in photoperiodic pathway loci in the colonizing populations of Northwestern Europe, whereas no evidence of positive selection was detected in the Central European populations. These findings emphasized the population‐specific nature of selection and suggested that photoperiodic adaptation was important during postglacial colonization of the species.     

Salicylic acid regulates flowering time and links defence responses and reproductive development

Flowering relies on signaling networks that integrate endogenous and external cues. Normally, plants flower at a particular season, reflecting day length and/or temperature cues. However, plants can surpass this seasonal regulation and show precocious flowering under stress environmental conditions. Here, we show that UV-C light stress activates the transition to flowering in Arabidopsis thaliana through salicylic acid (SA). Moreover, SA also regulates flowering time in non-stressed plants, as SA-deficient plants are late flowering. The regulation of flowering time by SA seems to involve the photoperiod and autonomous pathways, but it does not require the function of the flowering time genes CONSTANS (CO), FCA, or FLOWERING LOCUS C (FLC).     

Vernalization sensitivity in Arabidopsis thaliana (Brassicaceae): the effects of latitude and FLC variation

Latitudinal variation in climate is predicted to select for latitudinal differentiation in sensitivity to the environmental cues that signal plants to flower at the appropriate time for a given climate. In Arabidopsis thaliana, flowering is promoted by exposure to cold temperatures (vernalization), and several vernalization pathway loci are known. To test whether natural variation in vernalization sensitivity could account for a previously observed latitudinal cline in flowering time in A. thaliana, we exposed 21 European accessions to 0, 10, 20, or 30 d of vernalization and observed leaf number at flowering under short days in a growth chamber. We observed a significant latitudinal cline in vernalization sensitivity: southern accessions were more sensitive to vernalization than northern accessions. In addition, accessions that were late flowering in the absence of vernalization were more sensitive to vernalization cues. Allelic variation at the flowering time regulatory gene FLC was not associated with mean vernalization sensitivity, but one allele class exhibited greater variance in vernalization sensitivity.     

PHOTOPERIODIC ADAPTATION IN DESERT POPULATIONS OF XANTHIUM STRUMARIUM

Reproductive adaptation to photoperiod is diverse among desert populations of Xanthium. Chihuahuan Desert populations require dark periods of 9.5–10.5 hr for reproduction, and Sonoran Desert populations require 9–10.5 hr. Many Chihuahuan populations from western Texas two weeks from sowing need only 10 cycles of 11-hr nights to produce 100% flowering, but Sonoran populations from western Mexico four weeks from sowing need 18 cycles or more. Some Sonoran plants produce buds only at a cooler temperature program, 24–15 C, but Chihuahuan plants produce them more readily under the warmer program, 30–24 C. Chihuahuan plants that were germinated under 11-hr nights and four different temperature programs were induced to flower in each condition. Differences in photoperiod and ripeness-to-flower (maturity) responses were also demonstrated under natural day lengths in central Texas. Although desert populations occurring at approximately the same latitude in either the Chihuahuan or Sonoran Desert are exposed to similar day lengths, each population may be adapted to different photoperiod cues that maximize its utilization of the local growing conditions.     

Evidence for a link between local and seasonal cycles in gene frequencies and latitudinal gene clines in a cyclic parthenogen

In an earlier study (Rhombergh et al., Can. J. Genet. Cytol. 27: 224–232, 1985) of natural populations of the cyclic parthenogenetic Rose aphids, Macrosiphum rosae, 6 out of 31 loci were found to be polymorphic and one locus (Esterase-4) showed cyclic seasonal changes in gene and genotypic frequencies. Assuming that the Est-4 polymorphism was balanced and due to some climatic factor that varies seasonally, and realizing that most environmental factors that vary seasonally also vary latitudinally, we predicted existence of a latitudinal gene cline at this locus. In the present study we surveyed four polymorphic loci (chosen to be used as markers) in six geographic populations spanning over 1200 km between the United States and Canada and found all four loci to have latitudinal clines. We think that the gene clines are due to a latitudinal cline in the degree of advancement of local populations through the seasonal cycle, and have called such a pattern a seasonal phase cline. The results are discussed in relation to the temporal instability of local patterns and persistence of genetic variability on the large scale in aphids. It is argued that population structure of aphids makes retention of selectively neutral or weakly selected polymorphisms difficult.     

Parallel flowering time clines in native and introduced ragweed populations are likely due to adaptation

As introduced species expand their ranges, they often encounter differences in climate which are often correlated with geography. For introduced species, encountering a geographically variable climate sometimes leads to the re‐establishment of clines seen in the native range. However, clines can also be caused by neutral processes, and so it is important to gather additional evidence that population differentiation is the result of selection as opposed to nonadaptive processes. Here, we examine phenotypic and genetic differences in ragweed from the native (North America) and introduced (European) ranges. We used a common garden to assess phenotypic differentiation in size and flowering time in ragweed populations. We found significant parallel clines in flowering time in both North America and Europe. Height and branch number had significant clines in North America, and, while not statistically significant, the patterns in Europe were the same. We used SNP data to assess population structure in both ranges and to compare phenotypic differentiation to neutral genetic variation. We failed to detect significant patterns of isolation by distance, geographic patterns in population structure, or correlations between the major axes of SNP variation and phenotypes or latitude of origin. We conclude that the North American clines in size and the parallel clines seen for flowering time are most likely the result of adaptation.     

Molecular mechanisms for the photoperiodic regulation of flowering in soybean

Photoperiodic flowering is one of the most important factors affecting regional adaptation and yield in soybean (Glycine max). Plant adaptation to long-day conditions at higher latitudes requires early flowering and a reduction or loss of photoperiod sensitivity; adaptation to short-day conditions at lower latitudes involves delayed flowering, which prolongs vegetative growth for maximum yield potential. Due to the influence of numerous major loci and quantitative trait loci (QTLs), soybean has broad adaptability across latitudes. Forward genetic approaches have uncovered the molecular basis for several of these major maturity genes and QTLs. Moreover, the molecular characterization of orthologs of Arabidopsis thaliana flowering genes has enriched our understanding of the photoperiodic flowering pathway in soybean. Building on early insights into the importance of the photoreceptor phytochrome A, several circadian clock components have been integrated into the genetic network controlling flowering in soybean: E1, a repressor of FLOWERING LOCUS T orthologs, plays a central role in this network. Here, we provide an overview of recent progress in elucidating photoperiodic flowering in soybean, how it contributes to our fundamental understanding of flowering time control, and how this information could be used for molecular design and breeding of high-yielding soybean cultivars.     

Flowering responses to light and temperature

Light and temperature signals are the most important environmental cues regulating plant growth and development. Plants have evolved various strategies to prepare for, and adapt to environmental changes. Plants integrate environmental cues with endogenous signals to regulate various physiological processes, including flowering time. There are at least five distinct pathways controlling flowering in the model plant Arabidopsis thaliana: the photoperiod pathway, the vernalization/thermosensory pathway, the autonomous floral initiation, the gibberellins pathway, and the age pathway. The photoperiod and temperature/vernalization pathways mainly perceive external signals from the environment, while the autonomous and age pathways transmit endogenous cues within plants. In many plant species, floral transition is precisely controlled by light signals(photoperiod) and temperature to optimize seed production in specific environments. The molecular mechanisms by which light and temperature control flowering responses have been revealed using forward and reverse genetic approaches. Here we focus on the recent advances in research on flowering responses to light and temperature.     

The role of a pseudo-response regulator gene in life cycle adaptation and domestication of beet

Life cycle adaptation to latitudinal and seasonal variation in photoperiod and temperature is a major determinant of evolutionary success in flowering plants. Whereas the life cycle of the dicotyledonous model species Arabidopsis thaliana is controlled by two epistatic genes, FLOWERING LOCUS C and FRIGIDA, three unrelated loci (VERNALIZATION) determine the spring and winter habits of monocotyledonous plants such as temperate cereals. In the core eudicot species Beta vulgaris, whose lineage diverged from that leading to Arabidopsis shortly after the monocot-dicot split 140 million years ago, the bolting locus B is a master switch distinguishing annuals from biennials. Here, we isolated B and show that the pseudo-response regulator gene BOLTING TIME CONTROL 1 (BvBTC1), through regulation of the FLOWERING LOCUS T genes, is absolutely necessary for flowering and mediates the response to both long days and vernalization. Our results suggest that domestication of beets involved the selection of a rare partial loss-of-function BvBTC1 allele that imparts reduced sensitivity to photoperiod that is restored by vernalization, thus conferring bienniality, and illustrate how evolutionary plasticity at a key regulatory point can enable new life cycle strategies.     

Selection in heterogeneous environments maintains the gene arrangement polymorphism of Drosophila pseudoobscura

Chromosomal rearrangements may play an important role in how populations adapt to a local environment. The gene arrangement polymorphism on the third chromosome of Drosophila pseudoobscura is a model system to help determine the role that inversions play in the evolution of this species. The gene arrangements are the likely target of strong selection because they form classical clines across diverse geographic habitats, they cycle in frequency over seasons, and they form stable equilibria in population cages. A numerical approach was developed to estimate the fitness sets for 15 gene arrangement karyotypes in six niches based on a model of selection-migration balance. Gene arrangement frequencies in the six different niches were able to reach a stable meta-population equilibrium that matched the observed gene arrangement frequencies when recursions used the estimated fitnesses with a variety of initial inversion frequencies. These analyses show that a complex pattern of selection is operating in the six niches to maintain the D. pseudoobscura gene arrangement polymorphism. Models of local adaptation predict that the new inversion mutations were able to invade populations because they held combinations of two to 13 local adaptation loci together.     

Natural variation involving deletion alleles of FRIGIDA modulate temperature‐sensitive flowering responses in Arabidopsis thaliana

Ambient temperature is one of the major environmental factors that modulate plant growth and development. There is extensive natural genetic variation in thermal responses of plants exemplified by the variation exhibited by the accessions of Arabidopsis thaliana. In this work we have studied the enhanced temperature response in hypocotyl elongation and flowering shown by the Tsu‐0 accession in long days. Genetic mapping in the Col‐0 × Tsu‐0 recombinant inbred line (RIL) population identified several QTLs for thermal response including three major effect loci encompassing candidate genes FRIGIDA (FRI), FLOWERING LOCUS C (FLC) and FLOWERING LOCUS T (FT). We confirm and validate these QTLs. We show that the Tsu‐0 FRI allele, which is the same as FRI‐Ler is associated with late flowering but only at lower temperatures in long days. Using transgenic lines and accessions, we show that the FRI‐Ler allele confers temperature‐sensitive late flowering confirming a role for FRI in photoperiod‐dependent thermal response. Through quantitative complementation with heterogeneous inbred families, we further show that cis‐regulatory variation at FT contributes to the observed hypersensitivity of Tsu‐0 to ambient temperature. Overall our results suggest that multiple loci that interact epistatically govern photoperiod‐dependent thermal responses of A. thaliana.     

Genome-Wide Patterns of Adaptation to Temperate Environments Associated with Transposable Elements in Drosophila

Investigating spatial patterns of loci under selection can give insight into how populations evolved in response to selective pressures and can provide monitoring tools for detecting the impact of environmental changes on populations. Drosophila is a particularly good model to study adaptation to environmental heterogeneity since it is a tropical species that originated in sub-Saharan Africa and has only recently colonized the rest of the world. There is strong evidence for the adaptive role of Transposable Elements (TEs) in the evolution of Drosophila, and TEs might play an important role specifically in adaptation to temperate climates. In this work, we analyzed the frequency of a set of putatively adaptive and putatively neutral TEs in populations with contrasting climates that were collected near the endpoints of two known latitudinal clines in Australia and North America. The contrasting results obtained for putatively adaptive and putatively neutral TEs and the consistency of the patterns between continents strongly suggest that putatively adaptive TEs are involved in adaptation to temperate climates. We integrated information on population behavior, possible environmental selective agents, and both molecular and functional information of the TEs and their nearby genes to infer the plausible phenotypic consequences of these insertions. We conclude that adaptation to temperate environments is widespread in Drosophila and that TEs play a significant role in this adaptation. It is remarkable that such a diverse set of TEs located next to a diverse set of genes are consistently adaptive to temperate climate-related factors. We argue that reverse population genomic analyses, as the one described in this work, are necessary to arrive at a comprehensive picture of adaptation.