Revisiting the Role of Ethylene and N-End Rule Pathway on Chilling-Induced Dormancy Release in Arabidopsis Seeds

Abstract

Dormant Arabidopsis (Arabidopsis thaliana) seeds do not germinate easily at temperatures higher than 10–15 °C. Using mutants affected in ethylene signaling (etr1, ein2 and ein4) and in the N-end-rule pathway of the proteolysis (prt6 and ate1-ate2) we have investigated the effects of cold and ethylene on dormancy alleviation. Ethylene (10–100 ppm) and 2–4 days chilling (4 °C) strongly stimulate the germination of wild type (Col-0) seeds at 25 °C. Two to four days of chilling promote the germination at 25 °C of all the mutants suggesting that release of dormancy by cold did not require ethylene and did not require the N-end-rule pathway. One mutant (etr1) that did not respond to ethylene did not respond to GA3 either. Mutants affected in the N-end rule (prt6 and ate1-ate2) did not respond to ethylene indicating that also this pathway is required for dormancy alleviation by ethylene; they germinated after chilling and in the presence of GA3. Cold can activate the ethylene signaling pathway since it induced an accumulation of ETR1, EINI4, and EIN2 transcripts, the expression of which was not affected by ethylene and GA3. Both cold followed by 10 h at 25 °C and ethylene downregulated the expression of PRT6, ATE1, ATE2, and of ABI5 involved in ABA signaling as compared to dormant seeds incubated at 25 °C. In opposite, the expression of RGA, GAI, and RGL2 encoding three DELLAs was induced at 4 °C but downregulated in the presence of ethylene.

Retrograde signalling from the mitochondria to the nucleus translates the positive effect of ethylene on dormancy breaking of Arabidopsis thaliana seeds

“…In the presence of ethylene, dormant seeds fully germinated in these conditions (Fig. 1) showing that ethylene released seed dormancy, as already demonstrated for several species (Corbineau et al ., 2014; Kigel, 2017; Mattoo, 2018), including Arabidopsis (Wang et al ., 2018). This effect has been proposed to rely, at least partially, on its antagonistic relationship with ABA metabolism and signalling (Arc et al ., 2013; Corbineau et al ., 2014).…”

“…Ethylene is a gaseous plant hormone that regulates a number of developmental processes including vegetative growth, flowering time, fruit ripening, organ senescence and abscission, and seed germination (Yoo et al ., 2009; Muday et al ., 2012; Arc et al ., 2013; Corbineau et al ., 2014). Ethylene improves the germination of nondormant seeds incubated in nonoptimal environmental conditions (see Corbineau et al ., 2014, for review) including Arabidopsis (Wang et al ., 2018). The ethylene signalling cascade is well described in Arabidopsis (Alonso & Stepanova, 2004; Guo & Ecker, 2004).…”

“…In the nucleus, the components acting downstream from EIN2 are two major transcription factors, ETHYLENE INSENSITIVE 3 (EIN3) and its homologue EIN3‐LIKE 1 (EIL1), which regulate the majority of gene expression mediated by ethylene, including ethylene response factors (ERFs). The positive effect of ethylene on seed germination can be explained by its antagonistic effect on ABA metabolic and signalling pathways (Arc et al ., 2013) and by a crosstalk with the GA signalling pathway (Corbineau et al ., 2014; Wang et al ., 2018). In addition it has also been proposed that ethylene and ROS could act in concert to control seed dormancy release (Corbineau et al ., 2014; El‐Maarouf‐Bouteau et al ., 2014).…”

Expression of abscisic and gibberellic acid signalling factors in Fagus sylvatica L. seeds during dormancy breaking and germination

“…Interestingly, this decrease was inhibited by ABA (Wang et al, 2013). The expression of RGL2 was induced during chilling-induced dormancy release in Arabidopsis seeds but downregulated in the presence of ethylene (Wang et al, 2018). Piskurewicz et al (2009Piskurewicz et al ( , 2008 indicated that RGL2 inhibited germination by stimulating both ABI5 and ABI3 activity, and ABA synthesis.…”

The plant N‐degron pathways of ubiquitin‐mediated proteolysis

“…These data indicate that the PRT6 N‐degron pathway inactivates core component(s) that inhibit germination. Ethylene‐stimulated germination was shown to be abolished in prt6 and ate1 ate2 mutants indicating an interaction between this hormone and the PRT6 pathway (Wang et al ). The PRT6 N‐degron pathway was also shown to influence the proteome of etiolated (dark germinated) seedlings, with upregulation of 45 protein groups in prt6 , including ERFVII‐regulated storage proteins (Zhang et al ).…”