Co-Variation between Seed Dormancy, Growth Rate and Flowering Time Changes with Latitude in Arabidopsis thaliana

158

138

Seasonal behavior is important for fitness in temperate environments but it is unclear how progeny gain their initial seasonal entrainment. Plants use temperature signals to measure time of year, and changes to life histories are therefore an important consequence of climate change. Here we show that in Arabidopsis the current and prior temperature experience of the mother plant is used to control germination of progeny seeds, via the activation of the florigen Flowering Locus T (FT) in fruit tissues. We demonstrate that maternal past and current temperature experience are transduced to the FT locus in silique phloem. In turn, FT controls seed dormancy through inhibition of proanthocyanidin synthesis in fruits, resulting in altered seed coat tannin content. Our data reveal that maternal temperature history is integrated through FT in the fruit to generate a metabolic signal that entrains the behavior of progeny seeds according to time of year.M any organisms use annual changes in temperature to control their phenology, resulting in predictable timing of key life history events, such as flowering, spawning, and migration (1-3). Understanding crop and ecosystem response to climate change requires knowledge of the temperature control of key developmental transitions, but how new generations achieve seasonal orientation is currently unclear. Seed germination is the first step in plant life history and therefore plays a central role in the control of plant phenology (4) and is extremely sensitive to environmental temperature (3-5). Seed dormancy is established during seed maturation and is imposed by control of hormone signaling and the action of the maternal seed coat. Nearly 30 y ago it was found that environmental signaling throughout the whole maternal life history can affect seed dormancy control in wild oats, and that temperature experience in the vegetative phase before flowering affected progeny seed dormancy (6). Here we show that this response is conserved on the model species Arabidopsis. Our data show that fruit tissues carry a memory of past temperature experience and that flowering pathways control a transgenerational metabolic signal of maternal past temperature experience, which modulates progeny dormancy according to time of year.To test whether past parental temperature experience affected progeny dormancy in the model species Arabidopsis thaliana, we grew plants until the first sign of flowering at either 22°C or 16°C and then placed plants side by side to set seed at 22°C in long days (LDs) (Fig. 1A). We found that in Landsberg erecta (Ler) lower temperature during the vegetative phase caused a large increase in the dormancy of seeds produced later on the plants (Fig. 1A). Lower temperatures during seed set also increase progeny dormancy (6), but we observed no effect of photoperiod on dormancy either before or after flowering, as has been reported previously (7, 8). Therefore, temperature signals before seed fertilization are remembered by the parent plant and used to control offspring behavior.P...

Section: Analysis Ofsupporting

confidence: 92%

Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year

Chen

MacGregor

Dave

et al. 2014

158

138

“…It would also make evolutionary sense, as seed dormancy and germination timing influence the environment in which subsequent flowering and reproduction occur, and vice versa (16,44,50). An integrated mechanism for coordinating these two major life cycle transitions having significant impacts on fitness and survival would be subject to coselection to optimize (or bet-hedge) both (9,11,43,49,50). Much remains to be done to fully understand these complex interactions between plant life cycles and the environment, but our results demonstrate that DOG1 functions as an important molecular integrator that exerts its effects on developmental phase changes at least in part through miRNAregulated pathways.…”

Section: Discussionmentioning

confidence: 83%

“…Similarly, in many plants the transition from vegetative to floral development occurs in response to environmental cues, particularly temperature and day length (6,7). Ecological and evolutionary studies have found that seed germination and flowering traits within species are coadapted across habitat ranges (8)(9)(10)(11). Seed dormancy and germination are regulated primarily by the antagonistic actions of the plant hormones gibberellin (GA; promotive) and abscisic acid (ABA; inhibitory), whose synthesis and action vary in response to environmental signals (12).…”

mentioning

confidence: 99%

DELAY OF GERMINATION1 ( DOG1 ) regulates both seed dormancy and flowering time through microRNA pathways

Huo

Wei

Bradford

2016

162

149

Seed germination and flowering, two critical developmental transitions in plant life cycles, are coordinately regulated by genetic and environmental factors to match plant establishment and reproduction to seasonal cues. The DELAY OF GERMINATION1 (DOG1) gene is involved in regulating seed dormancy in response to temperature and has also been associated genetically with pleiotropic flowering phenotypes across diverse Arabidopsis thaliana accessions and locations. Here we show that DOG1 can regulate seed dormancy and flowering times in lettuce (Lactuca sativa, Ls) and Arabidopsis through an influence on levels of microRNAs (miRNAs) miR156 and miR172. In lettuce, suppression of LsDOG1 expression enabled seed germination at high temperature and promoted early flowering in association with reduced miR156 and increased miR172 levels. In Arabidopsis, higher miR156 levels resulting from overexpression of the MIR156 gene enhanced seed dormancy and delayed flowering. These phenotypic effects, as well as conversion of MIR156 transcripts to miR156, were compromised in DOG1 loss-of-function mutant plants, especially in seeds. Overexpression of MIR172 reduced seed dormancy and promoted early flowering in Arabidopsis, and the effect on flowering required functional DOG1. Transcript levels of several genes associated with miRNA processing were consistently lower in dry seeds of Arabidopsis and lettuce when DOG1 was mutated or its expression was reduced; in contrast, transcript levels of these genes were elevated in a DOG1 gain-of-function mutant. Our results reveal a previously unknown linkage between two critical developmental phase transitions in the plant life cycle through a DOG1-miR156-miR172 interaction.T he life cycles of flowering plants are characterized by distinct phase transitions such as from seed to seedling (germination) or from vegetative to reproductive development (flowering) (1). The timing of germination and flowering both require precise environmental sensing and integrated responses to multiple inputs so that developmental transitions can be accurately matched to seasonal conditions (1-3). Seeds use temperature as a signal of the seasonal and current environmental conditions to determine opportune times to germinate with respect to the potential for seedling survival (2, 4, 5). Similarly, in many plants the transition from vegetative to floral development occurs in response to environmental cues, particularly temperature and day length (6, 7). Ecological and evolutionary studies have found that seed germination and flowering traits within species are coadapted across habitat ranges (8-11). Seed dormancy and germination are regulated primarily by the antagonistic actions of the plant hormones gibberellin (GA; promotive) and abscisic acid (ABA; inhibitory), whose synthesis and action vary in response to environmental signals (12). Recent studies indicate that canonical genes regulating flowering, such as FLOWERING LOCUS T (FT) and FLOWERING LOCUS C (FLC), are also involved in the transition from seed dormanc...

“…4), and latitudinal gradients in dormancy observed in A. thaliana and also in the sea beet Beta vulgaris ssp. maritima (34)(35)(36).…”

Section: Discussionmentioning

confidence: 99%

“…In many species, the timing of germination is controlled by seed dormancy, which is a heritable trait (30,31) that shows evidence of adaptive differentiation. Up to 90% of the plant species in temperate regions produce seeds that are dormant at maturation (31), and intraspecific genetic variation in seed dormancy has been documented along altitudinal (32,33) and latitudinal gradients (34)(35)(36). Moreover, sequence variation in the dormancy gene DELAY OF GERMINATION 1 (DOG1) in Arabidopsis thaliana indicates local adaptation (34), and the level of seed dormancy has been shown to be important for establishment success in novel environments (37).…”

mentioning

confidence: 99%

Early life stages contribute strongly to local adaptation in Arabidopsis thaliana

Postma

Ågren

2016

120

171

The magnitude and genetic basis of local adaptation is of fundamental interest in evolutionary biology. However, field experiments usually do not consider early life stages, and therefore may underestimate local adaptation and miss genetically based tradeoffs. We examined the contribution of differences in seedling establishment to adaptive differentiation and the genetic architecture of local adaptation using recombinant inbred lines (RIL) derived from a cross between two locally adapted populations (Italy and Sweden) of the annual plant Arabidopsis thaliana. We planted freshly matured, dormant seeds (>180 000) representing >200 RILs at the native field sites of the parental genotypes, estimated the strength of selection during different life stages, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on seed dormancy. We found that selection during the seedling establishment phase contributed strongly to the fitness advantage of the local genotype at both sites. With one exception, local alleles of the eight distinct establishment QTL were favored. The major QTL for establishment and total fitness showed evidence of a fitness tradeoff and was located in the same region as the major seed dormancy QTL and the dormancy gene DELAY OF GERMINATION 1 (DOG1). RIL seed dormancy could explain variation in seedling establishment and fitness across the life cycle. Our results demonstrate that genetically based differences in traits affecting performance during early life stages can contribute strongly to adaptive differentiation and genetic tradeoffs, and should be considered for a full understanding of the ecology and genetics of local adaptation.I dentifying the ecological and genetic mechanisms underlying local adaptation, defined as the local genotype outperforming nonlocal genotypes (1), is a central problem in evolutionary biology. Local adaptation is common in both plant and animal species (2-5), promotes the maintenance of genetic variation (6, 7), and is a key component of models of speciation (8, 9). However, the relative importance of traits contributing to adaptive differentiation and their underlying genetic architecture remain poorly known (1,7,10,11). One key question is whether local adaptation results from genetic tradeoffs (antagonistic pleiotropy) in which locally favored alleles reduce fitness elsewhere or is caused by alleles that are conditionally neutral (favored in the home environment but selectively neutral in other environments). Empirical studies have rarely detected genetic tradeoffs (12)(13)(14), but these studies typically include only part of the life cycle (3,5,15), possibly resulting in a systematic underestimation of the magnitude of adaptive differentiation and of the occurrence of genetically based tradeoffs.Early life stages can be expected to play a prominent role in local adaptation. First, selection can be particularly severe during the first part of the life cycle when organisms are vulnerable and suffer from high mortality rates (15)(16)(...