Inhibition of FUSCA3 degradation at high temperature is dependent on ABA signaling and is regulated by the ABA/GA ratio

Abstract

During seed imbibition at supra-optimal temperature, an increase in the abscisic acid (ABA)/gibberellin (GA) ratio imposes secondary dormancy to prevent germination (thermoinhibition). FUSCA3 (FUS3), a positive regulator of seed dormancy, accumulates in seeds imbibed at high temperature and increases ABA levels to inhibit germination. Recently, we showed that ABA inhibits FUS3 degradation at high temperature, and that ABA and high temperature also inhibit the ubiquitin-proteasome system, by dampening both proteasome activity and protein polyubiquitination. Here, we investigated the role of ABA signaling components and the ABA antagonizing hormone, GA, in the regulation of FUS3 levels. We show that the ABA receptor mutant, pyl1-1, is less sensitive to ABA and thermoinhibition. In this mutant background, FUS3 degradation in vitro is faster. Similarly, GA alleviates thermoinhibition and also increases FUS3 degradation. These results indicate that inhibition of FUS3 degradation at high temperature is dependent on a high ABA/GA ratio and a functional ABA signaling pathway. Thus, FUS3 constitutes an important node in ABA-GA crosstalk during germination at supra-optimal temperature. KEYWORDS ABA; dormancy; FUSCA3; GA; germination; high temperature; protein degradation; proteasome; thermoinhibition; ubiquitin proteasome system; UPS Seed dormancy is an important adaptive trait that prevents seedling establishment under unfavourable conditions to maximize plant survival. Dormancy prevents pre-harvest sprouting of mature seeds and precocious germination or vivipary of immature seeds when still attached to the mother plant. These processes can lead to severe yield loss in agricultural crops. While primary dormancy is induced during seed maturation, secondary dormancy can be imposed in mature seeds with non-deep dormancy to prevent their germination under unfavourable growth conditions such as high temperature. [1][2] In Arabidopsis, the transcription factor FUSCA3 (FUS3) is essential for seed maturation and regulates several processes including the establishment of primary dormancy during embryogenesis. Loss-of-function fus3 embryos skip dormancy and can germinate precociously, while mutants ectopically expressing FUS3 post-embryonically display increased dormancy and show delayed germination, growth and flowering among several other phenotypes. 3-6 FUS3 represses developmental phase transitions by increasing the levels of the dormancy-promoting hormone, abscisic acid (ABA), while repressing the synthesis of the germination/growth-promoting hormone, gibberellin A (GA). 5,7,8 FUS3 is itself regulated by these hormones: the protein is more abundant in the presence of ABA and less abundant in the presence of GA. Exogenous GA application or reduction of endogenous ABA both partially rescue FUS3 overexpression phenotypes, such as the delayed growth, flowering and reduced cell cycling. 5 While FUS3 was shown to directly bind and repress GA biosynthetic genes, 4,8 the mechanisms behind the regulation of FUS3 protein levels...

Effect of Temperature, Light, and Storage Time on the Seed Germination of Pinus bungeana Zucc. ex Endl.: The Role of Seed-Covering Layers and Abscisic Acid Changes

“…Heynh. [56], etc. However, the rate of inhibitory substances or ABA catabolism depends on the oxygen concentration, and the oxygen availability in an imbibed seed is largely determined by low temperatures, which improve the dissolved oxygen levels in nearby water [57].…”

Abscisic Acid and Gibberellins Antagonistically Mediate Plant Development and Abiotic Stress Responses

“…Moreover, the NF-YC-RGL2-ABI5 cascades, which integrate GA and ABA signaling pathways to precisely regulate seed germination ( Liu X. et al, 2016 ), have been dissected. FOA2 (F-box overexpressed/oppressed ABA signaling), and the transcription factors FUSCA3 and DAG1 (DOF AFFECTING GERMINATION 1) also regulate biosynthesis and signal transduction of GA and ABA during seed germination ( Boccaccini et al, 2014a , b , 2016 ; Chiu et al, 2016a , b ; He et al, 2016 ). Overall, diverse key genes regulate seed germination by mediating ABA and GA biosynthesis and/or signal transduction pathways ( Table 1 ).…”

Quantitative ubiquitylomics approach for characterizing the dynamic change and extensive modulation of ubiquitylation in rice seed germination

“…RING‐type E3 ligase KEEP ON GOING (KEG) ubiquitinates ABI5 and regulates its abundance (Bueso et al , ). In addition, ABA inhibits the completion of seed germination by repressing UPS activity and protecting some dormancy‐related proteins, for example FUSCA3 (Chiu et al , ). Although these findings underscore the importance of protein ubiquitylation during seed germination, the process has not yet been studied at a systemic level.…”