Induction of Dormancy in Arabidopsis Summer Annuals Requires Parallel Regulation of DOG1 and Hormone Metabolism by Low Temperature and CBF Transcription Factors

Abstract

Summer annuals overwinter as seeds in the soil seed bank. This is facilitated by a cold-induced increase in dormancy during seed maturation followed by a switch to a state during seed imbibition in which cold instead promotes germination. Here, we show that the seed maturation transcriptome in Arabidopsis thaliana is highly temperature sensitive and reveal that low temperature during seed maturation induces several genes associated with dormancy, including DELAY OF GERMINATION1 (DOG1), and influences gibberellin and abscisic acid levels in mature seeds. Mutants lacking DOG1, or with altered gibberellin or abscisic acid synthesis or signaling, in turn show reduced ability to enter the deeply dormant states in response to low seed maturation temperatures. In addition, we find that DOG1 promotes gibberellin catabolism during maturation. We show that C-REPEAT BINDING FACTORS (CBFs) are necessary for regulation of dormancy and of GA2OX6 and DOG1 expression caused by low temperatures. However, the temperature sensitivity of CBF transcription is markedly reduced in seeds and is absent in imbibed seeds. Our data demonstrate that inhibition of CBF expression is likely a critical feature allowing cold to promote rather than inhibit germination and support a model in which CBFs act in parallel to a low-temperature signaling pathway in the regulation of dormancy.

Seed dormancy is a dynamic state: variable responses to pre- and post-shedding environmental signals in seeds of contrastingArabidopsisecotypes

“…Similarly, seeds of the Col ecotype matured at 158C were also reported to have decreased germination in response to cold stratification compared to those matured at higher temperatures (e.g. 208C) (Donohue et al, 2008;Kendall et al, 2011).…”

“…This takes the form of sensing the maternal environment (light, nitrate and temperature) (Sawhney et al, 1985;Alboresi et al, 2005;Kendall et al, 2011;Kendall and Penfield, 2012;Penfield and Springthorpe, 2012;He et al, 2014;Huang et al, 2014) and the environment of the soil seed bank (light, nitrate and temperature) (Footitt et al, 2011(Footitt et al, , 2013Finch-Savage and Footitt, 2012;Penfield and Springthorpe, 2012). This enables seeds to use environmental signals to determine the time and place of seed germination and subsequent seedling emergence (Baskin and Baskin, 1998;Finch-Savage and LeubnerMetzger, 2006;Footitt et al, 2011Footitt et al, , 2013Footitt et al, , 2014.…”

“…This enables seeds to use environmental signals to determine the time and place of seed germination and subsequent seedling emergence (Baskin and Baskin, 1998;Finch-Savage and LeubnerMetzger, 2006;Footitt et al, 2011Footitt et al, , 2013Footitt et al, , 2014. Within a species, the initial depth of primary dormancy is determined during seed development by ecotype genetics and the prevailing environment (Baskin and Baskin, 1998;Kendall et al, 2011;Donohue, 2014;He et al, 2014;Huang et al, 2014). If seeds are not exposed to suitable environmental signals for dormancy removal upon shedding, they enter the soil seed bank.…”

Spatiotemporal Seed Development Analysis Provides Insight into Primary Dormancy Induction and Evolution of theLepidium DELAY OF GERMINATION1Genes

“…For seed dormancy, analysis of Arabidopsis natural genetic variation has led to the cloning of AtDOG1 as the first specific seed dormancy gene (Bentsink et al, 2006) and has been shown to be important for local adaptation to different environments (Huang et al, 2010;Chiang et al, 2011;Footitt et al, 2011;Kendall et al, 2011;Kronholm et al, 2012). Homologs of the AtDOG1 gene are also known for the Brassicaceae species B. rapa (BrDOG1) and Lepidium sativum (Lesa-DOG1; Graeber et al, 2010).…”

“…Recent work shows that the AtDOG1 protein accumulates during seed maturation and, unlike the transcript, remains stable throughout imbibition of Arabidopsis seeds . The mother plant environment, especially the ambient temperature during seed development, controls AtDOG1 gene expression during seed maturation as well as the seed dormancy status (Kendall et al, 2011;Nakabayashi et al, 2012).…”