Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism

MacGregor, Dana R.; Kendall, Sarah L.; Florance, Hannah; Fedi, Fabio; Moore, Karen; Paszkiewicz, Konrad; Smirnoff, Nicholas; Penfield, Steven

doi:10.1111/nph.13090

Cited by 118 publications

(117 citation statements)

References 49 publications

(78 reference statements)

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“…Of these lines, eight showed clear tt phenotypes, underlining the important role of seed coat tannin in the imposition of strongly dormant states and the important role of the seed coat in coat-imposed dormancy in Arabidopsis (Supplemental Fig. S1; Debeaujon et al, 2000;MacGregor et al, 2015). These were not investigated further.…”

Section: Resultsmentioning

confidence: 99%

Awake1, an ABC-Type Transporter, Reveals an Essential Role for Suberin in the Control of Seed Dormancy

Fedi

O’Neill²,

Ménard³

et al. 2017

Plant Physiol.

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The mother plant plays an important dynamic role in the control of dormancy of her progeny seed in response to environmental signals. In order to further understand the mechanisms by which this dormancy control takes place in Arabidopsis (Arabidopsis thaliana), we conducted a forward genetic screen to isolate mutants that fail to enter dormancy in response to variation in temperature during seed set. We show that, for the first of these mutants, designated awake1, the maternal allele is required for entry into strongly dormant states and that awake1 mutants show seed phenotypes shown previously to be associated with the loss of suberin in the seed. We identify awake1 as an allele of ABCG20, an ATP-binding cassette transporter-encoding gene required for the transport of fatty acids during suberin deposition, and show that further suberin-deficient mutants have seed dormancy defects. Seed coat suberin composition is affected by temperature during seed maturation, but this response appears to be independent of ABCG20. We conclude that seed coat suberin is essential for seed dormancy imposition by low temperature and that the exclusion of oxygen and water from the seed by the suberin and tannin layers is important for dormancy imposition.

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Section: Resultsmentioning

confidence: 99%

Awake1, an ABC-Type Transporter, Reveals an Essential Role for Suberin in the Control of Seed Dormancy

Fedi

O’Neill²,

Ménard³

et al. 2017

Plant Physiol.

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“…In kiwifruit SVP overexpression also affects flavonoid synthesis in flowers and seed vigor (36) and can heterodimerize with the SEP proteins as well as control FT expression (19). In seeds, flavonoid pathway gene expression and PA levels are temperature responsive (32). Therefore, it is likely that a complex set of interactions between FT and MADS box transcription factors mediates the control of PA levels in seeds, via TT2.…”

Section: Analysis Ofmentioning

confidence: 99%

“…Our data, together with previously published work, suggest that FT activity may regulate seed tannin levels via the effects of MADS box transcription factor complexes on TT2 expression. To determine whether the temperature regulation of PA synthesis (32) in siliques is contingent on FT, we analyzed gene expression in torpedo-stage embryo-containing siliques from plants that had experienced either 16°C or 22°C BFF (Fig. 4E).…”

Section: Analysis Ofmentioning

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.

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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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“…For experiments investigating gibberellin signaling, media was supplemented with 20 mM paclobutrazol (PAC) and 100 mM gibberellic acid (GA 3 form, both Sigma-Aldrich) with a methanol carrier. Paclobutrazol is effective for studies of GA signaling during development at the concentration of 20 mM (Penfield et al, 2004;MacGregor et al, 2015). For experiments investigating auxin signaling, media was supplemented with N-1-naphthylphthalamic acid (NPA) (Sigma-Aldrich) at up to 10 mM with a DMSO carrier.…”

Section: Plant Materials and Growth Conditionsmentioning

confidence: 99%

The Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation

et al. 2017

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Emerging seedlings respond to environmental conditions such as light and temperature to optimize their establishment. Seedlings grow initially through elongation of the hypocotyl, which is regulated by signaling pathways that integrate environmental information to regulate seedling development. The hypocotyls of Arabidopsis (Arabidopsis thaliana) also elongate in response to sucrose. Here, we investigated the role of cellular sugar-sensing mechanisms in the elongation of hypocotyls in response to Suc. We focused upon the role of SnRK1, which is a sugar-signaling hub that regulates metabolism and transcription in response to cellular energy status. We also investigated the role of TPS1, which synthesizes the signaling sugar trehalose-6-P that is proposed to regulate SnRK1 activity. Under light/dark cycles, we found that Suc-induced hypocotyl elongation did not occur in tps1 mutants and overexpressors of KIN10 (AKIN10/SnRK1.1), a catalytic subunit of SnRK1. We demonstrate that the magnitude of Suc-induced hypocotyl elongation depends on the day length and light intensity. We identified roles for auxin and gibberellin signaling in Suc-induced hypocotyl elongation under short photoperiods. We found that Suc-induced hypocotyl elongation under light/dark cycles does not involve another proposed sugar sensor, HEXOKINASE1, or the circadian oscillator. Our study identifies novel roles for KIN10 and TPS1 in mediating a signal that underlies Suc-induced hypocotyl elongation in light/dark cycles.

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Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism

Cited by 118 publications

References 49 publications

Awake1, an ABC-Type Transporter, Reveals an Essential Role for Suberin in the Control of Seed Dormancy

Awake1, an ABC-Type Transporter, Reveals an Essential Role for Suberin in the Control of Seed Dormancy

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

The Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation

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