DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways
Significance Annual plants adapt to their environments by matching their life cycles, particularly seed germination and flowering, to the appropriate seasons. Although genetic evidence has suggested connections among genes regulating seed dormancy and flowering, specific mechanisms for such coordination are unknown. We report that a gene [DELAY OF GERMINATION1 (DOG1) involved in determining the depth of seed dormancy, and therefore the seasonal timing of germination, also influences the timing of flowering in Arabidopsis and lettuce. We further show that this gene acts through influencing the production of microRNAs that govern the progression of developmental phase transitions through the plant life cycle, providing a molecular genetic mechanism for the coordinate adaptation of seed dormancy and flowering phenotypes to environmental conditions. 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.
Proceedings of the National Academy of Sciences