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

Abstract

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...

The pivotal role of small non-coding RNAs in the regulation of seed development

“…miRNAs, and namely miR156, have been implicated in the regulation of the transition to germination (Huang et al 2013). Very recently, the DELAY OF GERMINATION1 (DOG1) gene has been shown to regulate seed dormancy, and flowering times, in response to temperature by affecting the levels of miR156 and miR172 (Huo et al 2016). In fact, the authors showed that miR156 and miR172 affect seed germination.…”

“…As suggested by Luo et al (2006), the strong expression of miR397 in pro-embryogenic cells results in downregulation of laccase genes. These interactions may be fundamental for maintaining the characteristic thin walls of the embryonic cells and their meristematic Huo et al (2016) features. Inversely, decreasing the expression of miR397 allows laccases to accumulate, with a resulting lignification of cell walls during the transition from meristematic to a mature cell state (Luo et al 2006).…”

“…The potential interactions of the DOG1-miR156-miR172 module in regulating developmental phase transitions, including dormancy to germination and adult to flowering transitions, have also been recently depicted by Huo et al (2016), to illustrate how DOG1 regulates dormancy (and flowering time) through miRNA pathways. The elucidation of other specific networks will largely depend on quantitative and qualitative information derived from genome-wide screenings, including information of the small non-coding elements, and functional approaches conducted in different plant taxonomic groups.…”

Control of seed dormancy in Arabidopsis by a cis -acting noncoding antisense transcript

“…Genetically, DOG1 has been shown to control a gibberellin-dependent endosperm-weakening mechanism in Arabidopsis and other Brassicaceae family members (12). DOG1 is also required for the miRNA156-mediated delay of flowering and germination (13).…”

easyGWAS: A Cloud-Based Platform for Comparing the Results of Genome-Wide Association Studies

“…Significantly associated hits are distributed across 30 different genes on four different chromosomes (1, 2, 4, and 5), as shown in the Shared Genes view in easyGWAS and in Supplemental Data Set 1. The 87 shared peaks include the dormancy regulator DOG1 (At5g45830), which has recently been shown to affect flowering time (Huo et al, 2016); FLOWERING LOCUS C (FLC; At5G10140), and FRIGIDA (At4G00650), which are linked to flowering time variation Amasino, 1999, 2001;Méndez-Vigo et al, 2013, 2016Sanchez-Bermejo and Balasubramanian, 2016); and ANTHOCYANINLESS2 (ANL2; At4G00730), which is involved in root development (Kubo and Hayashi, 2011). Furthermore, easyGWAS makes it possible to investigate the LD and gene information in close proximity to a focal SNP.…”