Environmental and Genetic Influences on the Germination of Arabidopsis Thaliana in the Field

Donohue, Kathleen; Dorn, Lisa A.; Griffith, Converse; Kim, Eunsuk; Aguilera, Anna; Polisetty, Chandra R.; Schmitt, Johanna

doi:10.1554/04-419

Cited by 119 publications

(160 citation statements)

References 56 publications

Supporting

Mentioning

151

Contrasting

Order By: Relevance

“…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.…”

supporting

confidence: 71%

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

Chen

MacGregor

Dave

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

162

138

View full text Add to dashboard Cite

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...

show abstract

supporting

confidence: 71%

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

Chen

MacGregor

Dave

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

162

138

View full text Add to dashboard Cite

show abstract

“…Arabidopsis thaliana, a highly selfing (Abbott and Gomes 1989) annual mustard, matures and disperses seeds in both spring and autumn in New England (see also Thompson 1994), and seasonal environmental factors influence germination timing. In companion papers, we documented highly plastic and genetically variable responses of germination timing to geographic location and season of seed dispersal (Donohue et al 2005a), and we showed that germination timing explained a large proportion of the variation in fitness among genotypes in some conditions but not others (Donohue et al 2005b). Here we examine indirect effects of germination timing on fitness operating through the phenotypic expression of postgermination characters and through natural selection on those postgermination characters.…”

mentioning

confidence: 73%

“…Seeds of Cal, were acquired through the Arabidopsis Biological Resource Center at Ohio State University (stock CS1062), and Tac seeds were collected by T. Mitchell-Olds. Please see Donohue et al (2005a) for details on the lines and their maintenance. …”

mentioning

confidence: 99%

Niche Construction Through Germination Cueing: Life-History Responses to Timing of Germination in Arabidopsis Thaliana

et al. 2005

Self Cite

View full text Add to dashboard Cite

Abstract. Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life-history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life-history traits, and whether germination timing influenced the expression of genetic variation for life-history traits. Adult life-history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life-history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life-history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life-history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life-history traits and the genetic variation of these traits.Key words. Dormancy, maternal effects, natural selection, phenotypic plasticity, seasonal cues.Received October 25, 2004. Accepted January 16, 2005 The timing of seed germination is highly responsive to environmental conditions. For a seed to germinate, certain environmental conditions must be present to break dormancy, and additional environmental conditions must exist subsequently to permit germination (Simpson 1990;Bewley 1997;Baskin and Baskin 1998). The timing of germination can therefore be a precise mechanism of habitat selection or niche construction that determines the environment experienced by the plant (Donohue 2003(Donohue , 2005. If the environmental conditions that elicit germination accurately predict the environment experienced by adults, germination behavior has the potential to influence the environment experienced by the plant throughout its life. It can thereby influence the phenotypic expression of plastic postgermination characters and the mode and strength of natural selection on those characters (Donohue 2002).Niche construction occurs when organisms alter the environment they experience (Odling-Smee et al. 1996), either through direct habitat modification, habitat choice, or resource garnering and depletion (Bazzaz 1991; de Kroon and Hutchins 1995;Huber et al. 1999). The environme...

show abstract

“…Field studies have revealed multiple seasonal germination cohorts in many A. thaliana populations (26,45,46), as well as seasonal differences in natural selection on life history traits (47,48). Moreover, genotypes may differ in phenology and fitness across natural environments (48-51), which may promote reproductive isolation.…”

Section: Discussionmentioning

confidence: 99%

Predicting the evolutionary dynamics of seasonal adaptation to novel climates in Arabidopsis thaliana

Fournier‐Level

Perry

Wang

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

View full text Add to dashboard Cite

Predicting whether and how populations will adapt to rapid climate change is a critical goal for evolutionary biology. To examine the genetic basis of fitness and predict adaptive evolution in novel climates with seasonal variation, we grew a diverse panel of the annual plant Arabidopsis thaliana (multiparent advanced generation intercross lines) in controlled conditions simulating four climates: a present-day reference climate, an increased-temperature climate, a winter-warming only climate, and a poleward-migration climate with increased photoperiod amplitude. In each climate, four successive seasonal cohorts experienced dynamic daily temperature and photoperiod variation over a year. We measured 12 traits and developed a genomic prediction model for fitness evolution in each seasonal environment. This model was used to simulate evolutionary trajectories of the base population over 50 y in each climate, as well as 100-y scenarios of gradual climate change following adaptation to a reference climate. Patterns of plastic and evolutionary fitness response varied across seasons and climates. The increased-temperature climate promoted genetic divergence of subpopulations across seasons, whereas in the winter-warming and poleward-migration climates, seasonal genetic differentiation was reduced. In silico "resurrection experiments" showed limited evolutionary rescue compared with the plastic response of fitness to seasonal climate change. The genetic basis of adaptation and, consequently, the dynamics of evolutionary change differed qualitatively among scenarios. Populations with fewer founding genotypes and populations with genetic diversity reduced by prior selection adapted less well to novel conditions, demonstrating that adaptation to rapid climate change requires the maintenance of sufficient standing variation.climate change | annual plant | genomic prediction | season O ngoing climate change is causing rapid shifts in environmental selective pressures within local populations (1, 2). To persist, populations must track the shifting multivariate trait optimum by phenotypic plasticity or adaptive evolution (3, 4), or migrate to keep up with poleward shifts in their original climate niche (1). The outcome of these responses to climate change will depend upon the seasonal variation a population experiences, particularly in temperate climates, where seasonality is a major source of environmental heterogeneity (5, 6). Understanding adaptation to seasonal environments is critical for predicting the response to climate change in short-lived organisms with multiple generations per year, like many insects and annual plants. Such prediction requires theoretical projections based on solid empirical foundations, tracking phenotypic change in complex traits as well as in the molecular variation present within populations as they adapt to different seasons. Here, we use a genomic prediction model, based on experimental data from Arabidopsis thaliana, to simulate trajectories of adaptation to novel climate scenarios in season...

show abstract

Environmental and Genetic Influences on the Germination of Arabidopsis Thaliana in the Field

Cited by 119 publications

References 56 publications

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

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

Niche Construction Through Germination Cueing: Life-History Responses to Timing of Germination in Arabidopsis Thaliana

Predicting the evolutionary dynamics of seasonal adaptation to novel climates in Arabidopsis thaliana

Contact Info

Product

Resources

About