DOG1-imposed dormancy mediates germination responses to temperature cues

Murphey, Michael; Kovach, Katherine; Elnacash, Tarek; He, Hanzi; Bentsink, Leónie; Donohue, Kathleen

doi:10.1016/j.envexpbot.2014.11.013

Cited by 30 publications

(41 citation statements)

References 62 publications

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“…Although its mechanism of action remains unknown, DOG1 has been demonstrated to be a positive regulator for the establishment and maintenance of primary seed dormancy in several species (19,20,35). DOG1 is involved in transducing maternal environmental conditions during seed development into effects on seed dormancy and in the loss of dormancy through dry after-ripening or moist chilling (2,5,17,45,46). ABA is also a strong positive regulator of seed dormancy (12) and promoted DOG1 expression in imbibed Lepidium sativum seeds (47).…”

Section: Discussionmentioning

confidence: 99%

“…Functional analyses have shown that DOG1 and ABA are essential for establishing primary seed dormancy (18,19,21), although DOG1 can act independently of ABA to delay germination of less dormant seeds (20). Overexpression of DOG1 also increases the sensitivity of seed germination to inhibition by warm temperatures (5,20). In addition, genome-wide association and genetic linkage mapping studies revealed that the DOG1 locus was associated with flowering phenotypes across diverse accessions and locations (22,23).…”

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confidence: 99%

“…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 dormancy to germination (13-16), suggesting that seed dormancy and flowering may be coordinately regulated through overlapping molecular pathways.In Arabidopsis, expression of the DELAY OF GERMINATION1 (DOG1) gene responds to seed maturation temperature and determines the depth of seed dormancy (2,3,5,(17)(18)(19)(20). Deeper dormancy of freshly harvested seeds is associated with high DOG1 transcript levels, which decrease in after-ripened (nondormant) and germinating seeds (18,19).…”

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confidence: 99%

“…In Arabidopsis, expression of the DELAY OF GERMINATION1 (DOG1) gene responds to seed maturation temperature and determines the depth of seed dormancy (2,3,5,(17)(18)(19)(20). Deeper dormancy of freshly harvested seeds is associated with high DOG1 transcript levels, which decrease in after-ripened (nondormant) and germinating seeds (18,19).…”

mentioning

confidence: 99%

“…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)(2)(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).…”

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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: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

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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The seed dormancy allele TaSdr-A1a associated with pre-harvest sprouting tolerance is mainly present in Chinese wheat landraces

Zhang

Xia

2016

Theor Appl Genet

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We cloned TaSdr - A1 gene, and developed a gene-specific marker for TaSdr - A1 . A QTL for germination index at the TaSdr - A1 locus was identified in the Yangxiaomai/Zhongyou 9507 RIL population. Pre-harvest sprouting (PHS) affects yield and end-use quality in bread wheat (Triticum aestivum L.). In the present study we found an association between the TaSdr-A1 gene and PHS tolerance in bread wheat. TaSdr-A1 on chromosome 2A was cloned using a homologous cloning approach. Sequence analysis of TaSdr-A1 revealed an SNP at position 643, with the G allele being present in genotypes with lower germination index (GI) values and A in those with higher GI. These alleles were designated as TaSdr-A1a and TaSdr-A1b, respectively. A cleaved amplified polymorphism sequence (CAPS) marker Sdr2A based on the SNP was developed, and linkage mapping and QTL analysis were conducted to confirm the association between TaSdr-A1 and seed dormancy. Sdr2A was located in a 2.9 cM interval between SSR markers Xgwm95 and Xgwm372. A QTL for GI at the TaSdr-A1 locus explained 6.6, 7.3, and 8.2 % of the phenotypic variances in a Yangxiaomai/Zhongyou 9507 RIL population grown at Beijing, Shijiazhuang, and the averaged data from the two environments, respectively. Two sets of Chinese wheat cultivars used for validating the TaSdr-A1 polymorphism and the corresponding gene-specific marker Sdr2A showed that TaSdr-A1 was significantly associated with GI. Among 29 accessions with TaSdr-A1a, 24 (82.8 %) were landraces, indicating the importance of Chinese wheat landraces as sources of PHS tolerance. This study identified a novel PHS resistance allele TaSdr-A1a mainly presented in Chinese landraces and it is likely to be the causal gene for QPhs.ccsu-2A.3, providing new information for an understanding of seed dormancy.

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Secondary dormancy dynamics depends on primary dormancy status inArabidopsis thaliana

et al. 2015

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Seed dormancy can prevent germination under unfavourable conditions that reduce the chances of seedling survival. Freshly harvested seeds often have strong primary dormancy that depends on the temperature experienced by the maternal plant and which is gradually released through afterripening. However, seeds can be induced into secondary dormancy if they experience conditions or cues of future unfavourable conditions. Whether this secondary dormancy induction is influenced by seed-maturation conditions and primary dormancy has not been explored in depth. In this study, we examined secondary dormancy induction in seeds of Arabidopsis thaliana matured under different temperatures and with different levels of afterripening. We found that low water potential and a range of temperatures, from 8°C to 35°C, induced secondary dormancy. Secondary dormancy induction was affected by the state of primary dormancy of the seeds. Specifically, afterripening had a non-monotonic effect on the ability to be induced into secondary dormancy by stratification; first increasing in sensitivity as afterripening proceeded, then declining in sensitivity after 5 months of afterripening, finally increasing again by 18 months of afterripening. Seed-maturation temperature sometimes had effects that were independent of expressed primary dormancy, such that seeds that had matured at low temperature, but which had comparable germination proportions as seeds matured at warmer temperatures, were more easily induced into secondary dormancy. Because seed-maturation temperature is a cue of when seeds were matured and dispersed, these results suggest that the interaction of seed-maturation temperature, afterripening and post-dispersal conditions all combine to regulate the time of year of seed germination.

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DOG1-imposed dormancy mediates germination responses to temperature cues

Cited by 30 publications

References 62 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

The seed dormancy allele TaSdr-A1a associated with pre-harvest sprouting tolerance is mainly present in Chinese wheat landraces

Secondary dormancy dynamics depends on primary dormancy status inArabidopsis thaliana

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