Changing Responses to Changing Seasons: Natural Variation in the Plasticity of Flowering Time

For plants that live in seasonally changing environments, timing is everything. Matching developmental transitions with the best times of year for growth and reproduction is necessary to maintain high fitness. Consequently, plants employ many mechanisms to sense and integrate multiple predictive seasonal cues to regulate their major developmental shifts. As the annual timing with which the growing season starts and ends changes across the landscape, natural selection has led to the evolution of the mechanisms that regulate the developmental plasticity of flowering among populations or varieties of species and crop plants that inhabit broad geographic ranges. There has been significant recent progress in describing the diversity of this variation in flowering time plasticity and in identifying the specific genetic changes responsible. Such work is an essential step toward understanding the processes that have shaped current and past adaptation, managing genetic diversity and improving crops in the face of climate change, and forecasting how populations may respond plastically and evolutionarily to future environmental challenges. In this Update, I review the findings of recent studies of natural variation in the plasticity of flowering to photoperiod, vernalization, and ambient temperature, and the implications and open questions raised by this work are considered. A fundamental adaptation of plants inhabiting seasonal environments is their ability to match the annual timing of major life history transitions to the local growing season. Most species achieve this synchrony through developmental plasticity. In other words, individuals sense how environmental cues like daylength and temperature change from winter to spring to summer to fall. The information gleaned from these cycles is then integrated molecularly so that germination, flowering, and other key transitions occur during periods favorable for growth, reproduction, and seed set. However, as the climate changes over the 21st century and the relative timing of annual cycles in temperature and precipitation shifts, once adaptive responses will no longer effectively predict the best calendar dates to initiate these essential developmental events (Nicotra et al., 2010; Wilczek et al., 2010). Because natural populations and cultivated landraces of many taxa have evolved to thrive in geographically diverse habitats and climates as their ranges have expanded, they harbor natural variants that may prove instructive in breeding crops and conserving native plant diversity in the face of future environmental challenges. Thus, a critical objective in plant biology is not only to understand the mechanisms by which plants interpret seasonal cues to guide development but also to learn how evolution has historically altered the underlying molecular bases of these responses as plants have adapted to cope with environmental heterogeneity across the landscape. Flowering time has emerged as a model trait for investigating the evolutionary genetics of developmental plasticity. A deep history of physiological studies in crop and wild taxa has demonstrated that several seasonal cues, photoperiod, ambient temperature, and exposure to prolonged cold (vernalization), among others, regulate the floral transition in many species (Allard and Garner, 1940; Chouard, 1960; Lang, 1965; Thomas and Vince-Prue, 1997; Kim et al., 2009; Amasino, 2010). Moreover, these early studies revealed important aspects of these responses, including that leaves produce a mobile inductive signal in response to inductive photoperiods (Knott, 1934; Zeevaart, 1962) and that the perception of vernalization directly in the shoot apical meristem leads to a mitotically stable memory of winter (Chouard, 1960; Lang, 1965). Building on this history of investigation, many genetic studies performed over the past two decades in the genetic model plants Arabidopsis (thale cress, Arabidopsis thaliana) and rice (Oryza sativa) as well as an increasingly broad array of additional organisms have produced abundant insight into the underlying molecular basis of these responses. As reviewed elsewhere, including in this issue, environmental cues modulate the timing of flowering through diverse transcriptional and posttranscriptional regulatory mechanisms, including DNA methylation, chromatin modification, small and long noncoding RNA activity, protein degradation, and protein transport (Andrés and Coupland, 2012). As we continue to learn more, it is hard not to be impressed by how the complex, interacting mechanisms involved achieve a high level of specificity in the type and duration of cues required to trigger floral initiation as well as the degree of reversibility and the quality of the induced response. And yet, despite their critical functions, the pathways that regulate the plasticity of flowering to environmental signals are not all that highly conserved compared with other developmental networks. These mechanisms differ extensively between model taxa, indicating that the flowering time gene regulatory network has the flexibility to evolve in myriad ways. For instance, although homologs of the core photoperiod pathway genes all regulate floral induction by daylength cues in Arabidopsis and rice, by long days and short days, respectively, their regulatory relationships have been rewired (Hayama et al., 2003). Moreover, additional pathways by which photoperiod cues regulate flowering exist in monocots that have no clear counterpart in dicots (Itoh et al., 2010), and whether homologs of the key integrator gene CONSTANS contribute to flowering regulation has been questioned in several dicot species (Hsu et al., 2012; Wong et al., 2014; Simon et al., 2015). Likewise, the pathways by which the memory of winter is retained in Arabidopsis and grasses share few details in common (Ream et al., 2012). However, such macroevolutionary differences likely reflect long-term convergence and/or developmental system drift (True and Haag, 2001) and may bear little resemblance to the types of genetic alterations by which populations have incrementally adapted to environmental gradients across space or will adapt to climate change through time. Thus, particularly as more genetic and genomic tools have been adopted in new systems, many investigators have begun concentrating on how wild and crop plants have adapted to thrive in diverse habitats that vary in the timing and predictability of the growing season across both broad and fine geographic scales. In doing so, they have found abundant variation in the plasticity of flowering, ranging from subtle tweaks in particular parameters to abolition or full reversal of the direction of responses. Understanding the genetic architecture of this diversity, whether divergence occurs rapidly through allelic substitutions of major effect at few loci or through the accumulation of changes at many minor loci, can inform our outlook on whether populations may be able to adapt at a rate that can keep pace with a changing climate (Chevin et al., 2010). Likewise, if developmental plasticity often evolves through selection on alleles already segregating as standing genetic variation in populations rather than awaiting new adaptive de novo mutations to arise, the prognosis for species to adapt in the face of a changing climate may be more optimistic. Finally, characterizing how the causal variants impact seasonal phenology and fitness across field locations and years as well as assessing whether they have pleiotropic effects on other traits is essential (Wilczek et al., 2009, 2010; Anderson et al., 2012). Only by doing so can we gain a comprehensive view of the adaptive value of this variation and model how its impacts on whole-plant biology may constrain or enhance responses to selection imposed by future, potentially novel climates. Here, my goal is to review how the ever-growing recent literature on the ecological genetics of natural variation in the developmental plasticity of flowering has begun to shed light on these questions. Focusing on the three cues that have received the greatest attention, photoperiod, vernalization, and ambient temperature, I will explore how surveys of natural populations and landraces are revealing that perception and responses to these cues change along diverse axes of variation, often structured along environmental gradients. I will also consider in turn what genetic studies have shown to be the genetic architecture and molecular basis of this natural variation in plasticity. Finally, I will consider how these findings that have come from dissecting this variation under controlled conditions can be extended to move us toward understanding the evolution of seasonal phenology in past, current, or future field conditions. Photoperiod responses can be facultative or obligate, and they generally fall into one of two categories. Short-day plants flower earlier (or only) in short days, and long-day plants flower earlier (or only) in long days (Allard and Garner, 1940). Facultative responses are approximately sigmoidal with two threshold photoperiods. Below one threshold, noninductive conditions fail to further delay flowering; above the other threshold, inductive conditions fail to further accelerate flowering. A final major category is day-neutral flowering; these plants do not exhibit photoperiod-sensitive flowering. More complex, but rarer, types also occur (Thomas and Vince-Prue, 1997). For instance, ambiphotoperiodic plants flower earlier in long and short days relative to intermediate conditions. Other species require a succession of long days before short days (or vice versa) to flower. In both long-day and short-day species, intraspecific transitions to day neutrality are observed frequently. These transitions are generally quantitative and clinal, resulting from incremental reductions in the magnitude of the response, rather than abrupt losses, and thus are covered separately below. Transitions from long-day to short-day flowering, or vice versa, are far less common on the microevolutionary scale (Thomas and Vince-Prue, 1997). A few cases have recently received attention. Notably, they all implicate alterations to the control of floral induction in the shoot apex rather than divergence in the measurement of photoperiod in the leaf. First, long-day flowering evolved from short-day flowering as wild populations of the common sunflower (Helianthus annuus) expanded the species range into southern Texas (Blackman et al., 2011). reversal is with differences in the photoperiod of shoot apical but not of homologs of the floral cultivated varieties of the plants and have been for flowering relative to a short-day mutations in homologs of the floral the seasonal to flowering, to flowering et al., 2012; et al., 2012). However, as this is more to day-neutral flowering and the long-day response in on an with ambient temperature and to flowering as less of reversal in plasticity as the change in In species with facultative responses to photoperiod, the between flowering time under inductive and noninductive photoperiods often evolves along geographic For instance, among wild sunflower the in flowering time between inductive short days and noninductive long days with such that populations are day flowering in short growing (Blackman et al., 2011). are observed in long-day likely the growth into the and found at seed et al., and quantitative trait studies of photoperiod response have from a to as many as loci to intraspecific variation et al., 2010; Anderson et al., et al., 2012; et al., 2014; et al., of these loci allelic and of the loci may be to produce day-neutral et al., et al., the magnitude of photoperiod response occur the flowering regulation by and light or the and of floral or In two long-day and variants in homologs of a of the and its earlier flowering under noninductive short-day are in cultivated and may have into et al., 2012). and induced mutations in the also have to the of cultivated in the short growing of et al., 2012; et al., 2012). In cultivated at loci, including variants to in two to A and a of to the such that photoperiod with et al., et al., et al., These alleles do not a in wild variation in several genes that at the of and light have been in the evolution of photoperiod responses the of to environments in et al., et al., et al., rice et al., et al., et al., and et al., 2012; et al., In the final a the and photoperiod response by the of this floral in noninductive long days et al., The likely and a selection in changes homologs of the floral also have to changes in photoperiod during or the of crop A in a sunflower segregating at in wild populations a during and studies in Arabidopsis that this a delay in flowering through with the of (Blackman et al., 2010; work also has variants in homologs of et al., and et al., with the evolution of day-neutral Finally, has been in the photoperiod of one Arabidopsis et al., 2011). In many species, the floral transition is on a critical Below a threshold daylength or above a threshold plants do not flower (Thomas and Vince-Prue, 1997). studies of the common an long-day species with both annual and have begun to explore of and genetic variation in this populations of the annual critical photoperiod with the and variation in the annual of the growing season et al., 2015). Notably, time to flower in inductive conditions evolves along in growing season these two aspects of seasonal phenology adapt environmental parameters that the allelic variation trait occurs in of photoperiod also the annual and populations require at days to only annual populations at high and require such and In a and often has evolved a critical photoperiod earlier seasonal flowering than et al., in a few controlled that the differences in critical photoperiod among or species are for by a few loci of major effect and et al., but the and evolutionary of the underlying alleles The diversity and genetics of natural variation in threshold parameters have received less in short-day species and species with facultative responses. it is the critical that between two of the short-day plant and this is with a in the of for two (Hayama et al., In facultative long-day the photoperiod which days no longer delay flowering is and the critical photoperiod above which longer days no longer accelerate flowering is between in these parameters to a few major et al., 2010). species in the summer or fall and before the of flowering in the response, or the or of flowering by prolonged exposure to is often an adaptation that flowering in species with such seasonal In Arabidopsis the gene the which the of in the and in the shoot apex and Amasino, et al., et al., this to flowering. of a of and flowering by vernalization is also observed in crops and wild grasses in the core However, the is the and a not to and by prolonged cold is for its et al., et al., et al., of vernalization response species is to a at a major For instance, in spring annual that are able to and seed in a growing season have evolved as many as times through mutations in et al., et al., et al., 2011). In the of vernalization response in the also in the has evolved through multiple or regulatory mutations in its in the floral rather than its et al., 2012). of winter annual to spring annual varieties by of vernalization response in cultivated and have evolved through allelic variation in the floral et al., alleles among spring including a a in the and a of the full Likewise, the gene is from spring et al., with vernalization responses may vary in how long winter be to accelerate flowering or in the temperature that vernalization et al., et al., et al., and et al., variation in the has been best in the it changes at a few loci et al., et al., et al., et al., variation in is the major of the of a vernalization in to be the of variation in the of the vernalization response et al., et al., 2012). For instance, Arabidopsis for major two with vernalization and three with vernalization et al., 2012; et al., 2015). For one of these a of noncoding impacts how prolonged cold the accumulation of chromatin on and gene et al., 2012; et al., A in impacts the of the long noncoding RNA from the to an vernalization et al., 2015). and studies have also variation in flowering time or vernalization response with in the homologs of and et al., 2010; et al., 2012; et al., 2012; et al., For instance, one of two major in is by cold exposure more than the other et al., In the species a a new resulting in a and of the open and thus but not vernalization response et al., 2012). Notably, a in an of is found in multiple geographic and also is with flowering time variation et al., but its impact on vernalization response is not The temperature threshold parameters which plants vernalization or that in the greatest response to vernalization may also vary among et al., and Amasino, 2012; et al., 2014; et al., 2015). For instance, can be by as high as require (Ream et al., In the magnitude of the vernalization response is at although the response is less for and for In the of one the is to differences in the of cold in of et al., 2015). The temperature threshold to a vernalization response of magnitude in Arabidopsis from to and Amasino, 2012). In many species, both daylength and prolonged exposure to cold can to accelerate flowering, and the magnitude of response to one may be or on whether a plant inductive or noninductive conditions with to the other For vernalization flowering by days under long days than under short days in However, in species, of a vernalization or photoperiod response or can directly on the other For instance, all populations of flower rapidly under long days, but populations of are raised in short days, they then require vernalization in for long days to flowering and in the regulation of homologs of the and to whether populations exhibit this vernalization or not et al., In of both and its wild differ from annual in that the of flowering vernalization et al., 2010). variation in a this between and and this gene is in the as the that flowering variation in and rice et al., 2012). temperature, as in growing degree days or other is to developmental that predict flowering time in crop and wild species et al., 2015). However, of adaptive natural variation in this response and the questions of whether and how the of flowering has been altered by have received attention. For instance, although multiple studies have found that natural variation in the response is abundant in Arabidopsis et al., et al., et al., few have in more than two temperature or demonstrated that the of developmental plasticity to the geographic of environmental et al., for future surveys to more and more natural variation and between species in this response. For species, a threshold may exist such that on one of that threshold earlier flowering and on the other of the threshold delay flowering. Moreover, of these responses may on whether temperature is or et al., they may be photoperiod et al., and at ambient temperature and vernalization responses may both be and Amasino, 2012). The genetics of natural variation in the ambient temperature response also has received attention, in the underlying mechanisms have been only recently and then only in As reviewed et al., 2014; et al., these studies have variation in and other genes as well as of in the plasticity of flowering to ambient temperature et al., et al., 2012; et al., et al., et al., et al., 2014; et al., 2015). and studies in Arabidopsis have and as genes natural variants that the ambient temperature response et al., 2009; et al., et al., and these the only causal that has been from both molecular and evolutionary is a in the of et al., 2015). The is and temperature but the is necessary and to accelerate flowering, under by and The once and in but field that the is adaptive to be As reviewed the plasticity of flowering to environmental cues can vary among wild populations and cultivated diversity multiple parameters threshold, and and alterations may be or Because the of variation segregating or among natural populations is by natural understanding the genetic of this variation may into the flowering time network not through also the to identifying the types of adaptive variation for crop and and for further improving and gene network of seasonal phenology to how populations will respond to future, potentially climates et al., et al., et al., this has on natural variation in plasticity to photoperiod, vernalization, and ambient temperature, studies of diverse taxa have revealed that the timing of flowering may respond to a of additional environmental including ambient and among and et al., et al., and that diversity in responses may a to explore how plants their life cycles to cope with environmental For instance, accelerate flowering in Arabidopsis but delay flowering in rice et al., Moreover, alterations to pathways by which or regulate the of floral have likely been critical for the evolution of flowering and in many species et al., et al., work has the physiological parameters that these responses, the genetic mechanisms that the to flowering or whether these responses vary or among species in that that the has been shaped by past Because flowering time and its plasticity often vary along or investigators for and that variation is likely to be an adaptive response to imposed by the seasonal timing of like and However, as The of seed and vary seasonally and geographically and their cycles are changing with the changing climate as Thus, to the that these cycles can be by seasonally such also may maintain or divergence in flowering time plasticity. from the genetic findings reviewed above I and Most the genetic architecture of natural variation in flowering time plasticity may differ on the and of vernalization response a by substitutions of alleles that impact a small core of and In or of the photoperiod response often several to many loci, and these variants a gene of the flowering that many genes the vernalization response (Andrés and Coupland, these likely reflect a for the vernalization variants in few genes have impacts on plasticity and fitness with pleiotropic and 2011). For relationships are the of the gene in Arabidopsis is of that the gene that the of a vernalization in is more to that photoperiod response than to that the vernalization response in For relationships are the of the gene in Arabidopsis is of that the gene that the of a vernalization in is more to that photoperiod response than to that the vernalization response in multiple alleles that these responses relative to the in a all are the multiple alleles that these responses relative to the in a all are the is also that variants or the of genes more contribute to the evolution of flowering time plasticity than regulatory and mutations rather than gene may in reflect a more mutations gene than or new Consequently, of a favorable the adaptive rate is and evolution through allelic like for in Arabidopsis et al., in grasses et al., et al., et al., or et al., et al., are more these are on an increasingly of are For instance, approximately of the vernalization alleles are from a few taxa in the Moreover, all variants in the evolution of flowering have been cultivated taxa to selection in cultivated may not be of responses to in wild and can differ between and natural and the and of selection on a may often be during and These differences may to pleiotropic impacts of variants may be for local adaptation in wild populations with small like of particularly if adaptive variants with more specific effects by or are by gene less and these variants that have been us a to these are found (or and what these how best to crops or populations for future climates. the growth to understanding how these variants in organisms and in field environments is essential to this cues in may not under the natural and seasonal cycles of many environmental For instance, it has been observed that flowering time in controlled conditions have no effect on flowering in field conditions et al., Anderson et al., 2011). flowering time plasticity may often impact other traits as For instance, the photoperiod and vernalization pathways can also impact traits et al., 2009; et al., architecture et al., 2010), and et al., et al., and at flowering et al., Such pleiotropic effects may that the on seasonal For instance, alleles do not have fitness relative to alleles they also shoot architecture et al., and have a with traits et al., Finally, if we consider the many natural variants at flowering loci shown by genetic studies to vary with environmental or to of et al., et al., an of variants to I have not reviewed these as the multiple of many genes that regulate flowering time plasticity the of in the of a recent found that variation in the of the its and fitness but not its flowering time in field conditions et al., these studies alleles of evolutionary and into their molecular and will be of quantitative trait