DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature- and gibberellin-dependent control of seed germination

Abstract

Seed germination is an important life-cycle transition because it determines subsequent plant survival and reproductive success. To detect optimal spatiotemporal conditions for germination, seeds act as sophisticated environmental sensors integrating information such as ambient temperature. Here we show that the DELAY OF GERMI-NATION 1 (DOG1) gene, known for providing dormancy adaptation to distinct environments, determines the optimal temperature for seed germination. By reciprocal gene-swapping experiments between Brassicaceae species we show that the DOG1-mediated dormancy mechanism is conserved. Biomechanical analyses show that this mechanism regulates the material properties of the endosperm, a seed tissue layer acting as germination barrier to control coat dormancy. We found that DOG1 inhibits the expression of gibberellin (GA)-regulated genes encoding cell-wall remodeling proteins in a temperaturedependent manner. Furthermore we demonstrate that DOG1 causes temperature-dependent alterations in the seed GA metabolism. These alterations in hormone metabolism are brought about by the temperature-dependent differential expression of genes encoding key enzymes of the GA biosynthetic pathway. These effects of DOG1 lead to a temperature-dependent control of endosperm weakening and determine the optimal temperature for germination. The conserved DOG1-mediated coat-dormancy mechanism provides a highly adaptable temperature-sensing mechanism to control the timing of germination.dormancy gene DOG1 | gibberellin metabolism | germination temperature | cell-wall remodelling | Lepidium sativum

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

“…This additional effect of dog1-3 in the presence of ABA biosynthesis mutants is in contrast to reports that ABA biosynthesis and functional DOG1 are required for induction of primary dormancy (18,19). However, consistent with previous reports (17)(18)(19)(20), overexpression of LsDOG1 under the CaMV35S promoter in Arabidopsis Col plants resulted in deep seed dormancy that could not be alleviated by the ABA biosynthesis inhibitor fluridone, but could be alleviated by GA (SI Appendix, Fig. S3).…”

“…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).…”

“…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).…”

“…Deeper dormancy of freshly harvested seeds is associated with high DOG1 transcript levels, which decrease in after-ripened (nondormant) and germinating seeds (18,19). 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).…”

“…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).…”