PLEIOTROPY IN THE WILD: THE DORMANCY GENE<i>DOG1</i>EXERTS CASCADING CONTROL ON LIFE CYCLES

Chiang, George C. K.; Barua, Deepak; Dittmar, Emily L.; Kramer, Elena M.; Casas, Rafael Rubio de; Donohue, Kathleen

doi:10.1111/j.1558-5646.2012.01828.x

Cited by 80 publications

(119 citation statements)

References 60 publications

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“…S3) (20), as might be expected from the suppression of expression of GA biosynthetic enzymes by high temperatures in Arabidopsis and lettuce (25,28,34). Ecological genetics studies have shown that, under natural seasonal variation, DOG1 can influence seed germination and flowering times (48). Although, initially, the effects of DOG1 on flowering were suggested to be an indirect response to the seasonal timing of germination, further study showed that the alleviation of seed dormancy resulted in an acceleration of flowering that was independent of germination timing (49).…”

Section: Discussionmentioning

confidence: 92%

“…As the miR156/SPL/miR172 pathway is involved in modulating the inputs from a diverse array of environmental signals and transducing them into developmental responses (6,7,32,59), interaction of DOG1 with this system would enable it to play an integrating role by matching the environmental sensitivities of seed dormancy and flowering to current or anticipated conditions. A dual role in sensing environmental signals (e.g., temperature) and coordinating developmentalphase transitions in the plant life cycle would explain the repeated identification of DOG1 as a significant locus in ecological genetics studies of flowering phenotypes (22,23,48). 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).…”

Section: Discussionmentioning

confidence: 99%

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

Huo

Wei

Bradford

2016

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

166

149

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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...

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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

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

Huo

Wei

Bradford

2016

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

166

149

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“…In particular, dormancy, a form of developmental arrest, can determine the temporal distribution of progeny that are metabolically active. Just as the location of spatial dispersal can greatly influence the environmental conditions experienced by progeny, so too can the timing of dormancy breakage and emergence determine the environmental conditions experienced by progeny at later life stages (Donohue et al 2010;Chiang et al 2013). Both spatial and temporal dispersal therefore can influence the distribution of progeny across heterogeneous environments in ways that influence fitness and the potential for gene flow.…”

Section: Introductionmentioning

confidence: 99%

Gene-flow through space and time: dispersal, dormancy and adaptation to changing environments

et al. 2015

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Dispersal through space or time (via dormancy) determines gene flow and influences demography. Because of their functional similarities, a covariation between dispersal and dormancy is expected. Dispersal and dormancy are anatomically linked in plants, because they both depend on attributes of the seed, albeit this anatomical association is rarely considered when analyzing interactions between dispersal and dormancy. In this paper, we investigate the extent to which dispersal and dormancy can be expected to correlate and how each might influence adaptation to novel environments such as those brought on by climate change. We review the theoretical and empirical literature on the subject with a focus on seed plants. We find that although a negative correlation between dispersal and dormancy has been theoretically anticipated, several models predict deviations from this expectation under scenarios of environmental heterogeneity. The empirical evidence does not support any specific covariation pattern, likely because the interaction between dispersal and dormancy is affected by multiple environmental and developmental constraints. From a climate change perspective, the effects of dispersal and dormancy on population structure are not equivalent: dormancy-mediated gene flow is intrinsically asymmetric (from the past towards the future) whereas spatial dispersal is not necessarily directional. As a result, selection on traits linked to dormancy and dispersal might differ qualitatively. In particular, gene flow through dormancy can only be adaptive if future environmental conditions are similar to those of the past, or if it contributes to novel allelic combinations. We conclude that, in spite of a long tradition of research, we are unable to anticipate a universal relationship between dispersal and dormancy. More work is needed to predict the relative contributions of spatial dispersal and dormancy to gene flow and adaptation to novel environments.

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“…S3). We found wild-type levels of the germination inhibitors abscisic acid and 12-oxophytodienoic acid in mature ft-1 seeds, alongside increased gibberellin GA 4 and jasmonate (JA) levels. (Fig.…”

mentioning

confidence: 99%

“…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)(4)(5). Seed dormancy is established during seed maturation and is imposed by control of hormone signaling and the action of the maternal seed coat.…”

mentioning

confidence: 99%

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

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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...

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PLEIOTROPY IN THE WILD: THE DORMANCY GENEDOG1EXERTS CASCADING CONTROL ON LIFE CYCLES

Cited by 80 publications

References 60 publications

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

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

Gene-flow through space and time: dispersal, dormancy and adaptation to changing environments

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

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