Loss of the ETR1 ethylene receptor reduces the inhibitory effect of far-red light and darkness on seed germination of Arabidopsis thaliana

Abstract

When exposed to far-red light followed by darkness, wild-type Arabidopsis thaliana seeds fail to germinate or germinate very poorly. We have previously shown that the ethylene receptor ETR1 (ETHYLENE RESPONSE1) inhibits and ETR2 stimulates seed germination of Arabidopsis during salt stress.This function of ETR1 requires the full-length receptor.These roles are independent of ethylene levels and sensitivity and are mainly mediated by a change in abscisic acid (ABA) sensitivity. In the current study we find that etr1-6 and etr1-7 loss-offunction mutant seeds germinate better than wild-type seeds after illumination with far-red light or when germinated in the dark indicating an inhibitory role for ETR1. Surprisingly, this function of ETR1 does not require the receiver domain. No differences between these mutants and wild-type are seen when germination proceeds after treatment with white, blue, green, or red light. Loss of any of the other four ethylene receptor isoforms has no measurable effect on germination after far-red light treatment. An analysis of the transcript abundance for genes encoding ABA and gibberellic acid (GA) metabolic enzymes indicates that etr1-6 mutants may produce more GA and less ABA than wild-type seeds after illumination with far-red light which correlates with the better germination of the mutants. Epistasis analysis suggests that ETR1 may genetically interact with the phytochromes (phy), PHYA and PHYB to control germination and growth. This study shows that of the five ethylene receptor isoforms in Arabidopsis, ETR1 has a unique role in modulating the effects of red and far-red light on plant growth and development.

Identification of Regions in the Receiver Domain of the ETHYLENE RESPONSE1 Ethylene Receptor of Arabidopsis Important for Functional Divergence

“…Prior studies showed that ETR1 has a prominent role in the control of several phenotypes, including ethylene-stimulated nutations, growth recovery after removal of ethylene, inhibition of ethylene responses by silver ions, seed germination during salt stress in the light, and seed germination in darkness (Binder et al, 2004bKim et al, 2011;McDaniel and Binder, 2012;Wilson et al, 2014aWilson et al, , 2014b. Interestingly, the ETR1 receiver domain was previously shown to be important for normal growth recovery, ethylene-stimulated nutations, and germination during salt stress in the light (Binder et al, 2004bKim et al, 2011;Wilson et al, 2014b) but not for the control of seed germination in darkness (Wilson et al, 2014a). In this study, we demonstrated that the ETR1 receiver domain also has little or no role in mediating the inhibitory effects of silver ions.…”

“…signaling-independent roles (Gamble et al, 1998;Beaudoin et al, 2000;Desikan et al, 2005;Binder et al, 2006;Wilson et al, 2014aWilson et al, , 2014b, which may underlie these observations. Determining the basis for noncanonical receptor signaling is of wide interest because noncanonical signal transduction has been observed in other signal transduction pathways, including Hedgehog and Wingless/int-1) signaling in animal cells (Jenkins, 2009;Miller and McCrea, 2010) and quorum sensing in bacteria (Federle and Bassler, 2003).…”

“…Mutant seedlings lacking ETR1 fail to nutate when treated with ethylene, whereas mutants lacking the other four isoforms have constitutive nutations in air Kim et al, 2011). Additionally, we recently reported that ETR1 and ETR2 have contrasting roles in the control of Arabidopsis seed germination in darkness or during salt stress in the light where ETR1 inhibits germination and ETR2 stimulates germination (Wilson et al, 2014a(Wilson et al, , 2014b. Correlating with these seed germination results are the observations that etr1 loss-of-function mutants have reduced sensitivity to abscisic acid (ABA), whereas etr2 loss-of-function mutants have increased sensitivity to ABA (Wilson et al, 2014b).…”

“…Even though the receptors have largely overlapping roles for many phenotypes, there are traits where the receptors are not redundant (Binder et al, 2004bPlett et al, 2009aPlett et al, , 2009bLiu et al, 2010;Kim et al, 2011;McDaniel and Binder, 2012;Wilson et al, 2014aWilson et al, , 2014b. For instance, ETR1, ETR2, and EIN4 have a role in normal growth recovery after ethylene removal, whereas ERS1 and ERS2 do not (Binder et al, 2004b).…”

“…Interestingly, this domain is not required for the inhibitory role of ETR1 on seed germination in the dark (Wilson et al, 2014a). Additionally, a common feature of the three receptors that have a role in growth recovery is that they contain a receiver domain, and genetic evidence indicates that ETR1 His autophosphorylation followed by phosphotransfer through these receiver domains is important for normal growth recovery (Binder et al, 2004b;Kim et al, 2011).…”