Shuangrong Liu’s research while affiliated with Chinese Academy of Sciences and other places

Seed dormancy enables plants to delay germination until conditions are favorable for the survival of the next generation. Seed dormancy and germination are controlled by a combination of external and internal signals, in which light and ethylene act as critical regulators. However, how light and ethylene are interlinked to control these two processes remains to be investigated. Here, we show that ethylene and its precursor, 1-aminocyclopropane-1-carboxylic acid (ACC), promote seed germination under light. Light facilitates the conversion of ACC to ethylene, in which phytochrome B (phyB) and FAR-RED ELONGATED HYPOCOTYL3 (FHY3) are functionally required. ACC oxidases (ACOs) catalyze the conversion of ACC to ethylene, among which ACO1 is specifically and predominantly expressed in imbibed seeds. Ethylene induces FHY3 protein accumulation in imbibed seeds, whereby FHY3 directly binds to ACO1 promoter and specifically mediates light-promoted ACO1 expression. Light promotes ACO1 protein accumulation. Overexpression of ACO1 significantly promotes seed germination, and almost completely restores the dormant defect of fhy3 loss-of-function mutants. In summary, this study reveals an ethylene-responsive regulatory cascade of phyB-FHY3-ACO1 that integrates external light input with internal factors to regulate seed dormancy and germination.

Seed dormancy and germination are fundamental processes for plant propagation, both of which are tightly regulated by internal and external cues. Phytochrome B (phyB) is a major red/far-red-absorbing photoreceptor that senses light signals that modulate seed dormancy and germination. However, the components that directly transduce that signal downstream of phyB are mostly unknown. Here, we show that the transposase-derived transcription factor FAR-RED ELONGATED HYPOCOTYL3 (FHY3) inhibits seed dormancy and promotes phyB-mediated seed germination in Arabidopsis thaliana. FHY3 physically interacts with phyB in vitro and in vivo. RNA-sequencing and RT-qPCR analyses showed that FHY3 regulates multiple downstream genes, including REVEILLE2 (RVE2), RVE7, and SPATULA (SPT). Yeast one-hybrid, electrophoresis mobility shift, and chromatin immunoprecipitation assays demonstrated that FHY3 directly binds these genes via a conserved FBS cis-element in their promoters. Furthermore, RVE2, RVE7, and GIBBERELLIN 3-OXIDASE 2 (GA3ox2) genetically act downstream of FHY3. Strikingly, light and phyB promote FHY3 protein accumulation. Our study reveals a transcriptional cascade consisting of phyB-FHY3-RVE2/RVE7/SPT-GA3ox2 that relays environmental light signals and thereby controls seed dormancy and germination.

Seed dormancy is an adaptive trait in plants. Breaking seed dormancy determines the timing of germination and is, thereby essential for ensuring plant survival and agricultural production. Seed dormancy and the subsequent germination are controlled by both internal cues (mainly hormones) and environmental signals. In the past few years, the roles of plant hormones in regulating seed dormancy and germination have been uncovered. However, we are only beginning to understand how light signaling pathways modulate seed dormancy and interaction with endogenous hormones. In this review, we summarize current views of the molecular mechanisms by which light controls the induction, maintenance and release of seed dormancy, as well as seed germination, by regulating hormone metabolism and signaling pathways.

Small ubiquitin-like modifier (SUMO) post-translational modification (SUMOylation) plays essential roles in regulating various molecular processes; however, its function and regulation in the plant light signaling pathway are largely unknown. SEUSS (SEU) is a transcriptional co-regulator that integrates light and temperature signaling pathways and thereby regulates plant growth and development in Arabidopsis thaliana. Here, we show that SEU is a substrate of SUMO1, and that substitution of four conserved lysine residues disrupts SUMOylation of SEU, impairs its function in photo- and thermo-morphogenesis, and enhances its interaction with PHYTOCHROME-INTERACTING FACTOR4 transcription factors. Furthermore, the SUMO E3 ligase SIZ1 interacts with SEU and regulates its SUMOylation. Moreover, SEU directly interacts with phytochrome B photoreceptor. Finally, the SUMOylation and stability of SEU are activated by light. Our study reveals a novel post-translational modification mechanism of SEU by which light regulates plant growth and development through SUMOylation-mediated protein stability.

Primary seed dormancy is acquired during seed development and maturation, which is important for plant fitness and survival. DELAY OF GERMINATION1 (DOG1) plays a critical role in inducing seed dormancy. DOG1 expression increases rapidly during seed development, but the precise mechanism underlying this process remains elusive. In this study, we showed that mutants with a loss or reduced function of the chromatin-remodeling factor PICKLE (PKL) exhibit increased seed dormancy. PKL associates with DOG1 chromatin and inhibits its transcription. We found that PKL physically interacts with LUX ARRHYTHMO (LUX), a member of the evening complex (EC) of the circadian clock. Furthermore, LUX directly binds to a specific coding sequence of DOG1, and DOG1 acts genetically downstream of PKL and LUX. Mutations in either LUX or EARLY FLOWERING3 (ELF3) encoding another member of the EC led to increased DOG1 expression and enhanced seed dormancy. Surprisingly, these phenotypes were abolished when the parent plants were grown under continuous light. In addition, we observed that loss of function of either PKL or LUX decreased H3K27me3 levels at the DOG1 locus. Taken together, our study reveals a regulatory mechanism in which EC proteins coordinate with PKL to transmit circadian signals for directly regulating DOG1 expression and seed dormancy during seed development.

Environmental light signal and GAs synergistically regulate seed dormancy and germination. The phytochrome B (phyB) photoreceptor regulates expression of the REVEILLE1 (RVE1) transcription factor, which directly inhibits GIBBERELLIN 3‐OXIDASE2 transcription, suppressing GA biosynthesis. However, whether phyB‐RVE1 coordinates with GA signaling in controlling seed dormancy and germination remains unknown. Here, we demonstrate that RVE1 regulation of seed dormancy and germination requires a DELLA repressor, REPRESSOR OF GA‐LIKE2 (RGL2), in Arabidopsis thaliana. RVE1 interacts with both RGL2 and its E3 ubiquitin ligase SLEEPY1 (SLY1) and promotes RGL2 stability by restraining the RGL2–SLY1 interaction. Furthermore, RVE1 and RGL2 synergistically regulate global transcriptome changes; RGL2 enhances the DNA‐binding capacity and transcriptional activity of RVE1 in regulating downstream gene expression. Moreover, RGL2 expression is repressed by phyB. Our study reveals a novel regulatory mechanism in which the RVE1–RGL2 module coordinately controls seed dormancy and germination by integrating light perception, GA metabolism and GA signaling pathways.