Illuminating COI1

Abstract

A significant portion of developmental and environmental responses in plants is mediated through phytohormone signaling, often if not always integrated with outputs from other signals. We have recently shown that CORONATINE INSENSITIVE1 (COI1), a component of a jasmonate receptor complex, is involved in ethylene-induced root growth inhibition of Arabidopsis, in the light. This response is neither due to elevated levels of jasmonates in response to ethylene treatment nor dependent on the known jasmonate signal-transduction cascade, except that it requires COI1. Further, we have shown that the ethylene-induced COI1-mediated pathway functions in parallel with, and additively to, the conventional ethylene signaling pathway, and that the light requirement is primarily for long photoperiods. This unexpected interaction of COI1 with ethylene signaling has also been extended to other developmental processes including germination and fertility. This addendum summarizes the earlier findings with some new insights, and describes and speculates on the mechanisms by which these processes are regulated, in the context of the interaction between COI1 and ethylene signaling.

Jasmonates (JAs) regulate essential physiological processes including fertility, senescence and defense against biotic and abiotic stresses.¹ Ethylene, meanwhile, regulates an overlapping set of essential processes that includes germination, fruit ripening, programmed cell death and defense.² Examples of the interaction of JA and ethylene signaling are both synergistic or antagonistic. A common effect of both regulators is that they inhibit root growth. CORONATINE INSENSITIVE1 (COI1) is a component of the JA receptor complex in Arabidopsis thaliana.^3,4 Our recent studies indicate that Arabidopsis root growth inhibition by ethylene and its immediate precursor 1-aminocyclopropane-1-carboxylic acid (ACC) partly requires COI1, and this occurs only in the light.⁵ This is indicated by the phenotype of a JA-insensitive mutant coi1-16, which is less responsive to ACC-induced root growth inhibition compared to the wild-type in the light, but not in the dark.^5,6 JA biosynthesis mutants allene oxide synthase (aos)^7,8 and 12-oxophytodienoate reductase3 (opr3),⁹ however, show wild-type-response to ACC,⁵ indicating that the observed root growth inhibition is not caused by ACC-induced JA production. JA-insensitive mutants, jasmonate resistant1 (jar1-1) which is impaired in forming the biologically active JA-Ile,^10,11 and jasmonate insensitive1 (jin1), in which the AtMYC2 transcriptional activator is not functional,^12,13 also show wild-type-response to ACC,⁵ suggesting that the conventional JA signaling pathway is not involved in ACC-induced root growth inhibition in the light. This leads to the inevitable conclusion that COI1 has additional functions along with the known role in the JA signal pathway. In the dark, in contrast, coi1-16 shows wild-type-response to ACC and its response decreases in long photoperiods.⁵ Our preliminary results also show that coi1-16 is even less responsive to ACC at a higher light intensity (120 µmol/m²/sec), suggesting a dose-dependency. Photoreceptor mutants including phyA, phyB, phot1, phot2, cry1 and cry2, however, show wild type-response to ACC in the light.⁵ Our preliminary results indicate that coi1-16 does not display an altered phenotype against 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), a photosynthetic electron transport inhibitor and N,N'-dimethyl-4,4'-bipyridinium dichloride (paraquat), which produces hydrogen peroxide from photosystem I electrons. Taken together, these results indicate that the light requirement for COI1 involvement in ACC-induced root growth inhibition is not wavelength-specific, and is unrelated to photosynthesis and accumulated hydrogen peroxide caused by high light dose. The interaction between COI1 and light signaling has been suggested,¹⁴ and recent findings have revealed that COI1 is required for some far-red light responses.¹⁵ It is, therefore, possible that a dose-dependent light signal directly or indirectly activates the COI1-pathway in response to ACC, although further investigation is required to clarify this point.

Double mutant assays using ethylene insensitive mutants have revealed that the ACC-induced COI1-mediated pathway functions in parallel to and additively with the conventional ethylene pathway.⁵ Ethylene receptor mutants, ethylene response1 (etr1-1), ethylene response sensor1 (ers1-1) and ers2-1, and ethylene signal-perception mutants, ethylene insensitive2 (ein2-1) and ein3-1, show strong insensitivity to ACC in the dark⁵—the basis for their original characterization.^16–20 However, they show some response to ACC in the light.⁵ Introduction of the coi1-16 mutation into these backgrounds renders their response to ACC almost negligible in the light.⁵ These results indicate that the COI1-pathway and the conventional ethylene pathway are not linear but are both parallel and additive. Apparently therefore, the conventional ethylene pathway inhibits root growth primarily in the dark whereas the contribution of the novel ethylene-activated COI1-pathway to root growth inhibition increases as the light dose increases. Although we have focused on the accumulative effect of light and ACC (seven-day exposure), it will be interesting to investigate whether the temporal exposure to light regulates the COI1-pathway: for example, does the ethylene perception-response mechanism in the day differ from that in the night?

COI1 is involved in both JA-induced and ACC-induced root growth inhibition, however, the mechanisms by which the COI1 protein functions in each pathway may be different.⁵ The COI1 protein contains an F-box motif and leucine-rich repeats (LRRs), and forms an E3 ubiquitin ligase SCF^COI1 complex^21–23 to target downstream negative regulators of JA signaling for proteolysis in response to the JA-Ile conjugate.^24,25 Complementation assay indicates that the LRR domain of COI1 is sufficient to restore wild type-response to ACC in coi1-16 but not the F-box domain.⁵ This suggests that SCF complex assembly is probably not required for COI1 function in the ethylene response unlike in the JA response which requires the intact COI1 protein⁵ in a functional SCF complex.²³

Interaction between the ethylene pathway and COI1 is not restricted to root growth. The etr1-1 mutant germinates poorly on MeJA-supplemented media but the etr1-1;coi1-16 double mutant germinates like the wild-type.⁵ ETR1 is a negative regulator of the ethylene pathway and the etr1-1 mutant is incapable of binding ethylene and of activating the downstream pathway. This suggests that JAs inhibit germination through COI1 and simultaneously activate the ethylene pathway to antagonise this effect. This notion is also supported by the observation that on MeJA-supplemented media, there is low germination of ein2-1 (33.3% in the dark, 73.3% in the light), but there is recovery of germination in ein2-1;coi1-16 (80.0% in the dark, 100% in the light). Whether this activation is due to JA-induced ethylene production is yet to be elucidated. Fertility is also affected by interaction between the ethylene pathway and COI1. JAs are known to be essential for male fertility in Arabidopsis and therefore, coi1 mutants are compromised in fertility.²⁶ In contrast, excess ethylene signaling is suggested to inhibit fertility by the findings that loss-of-function double mutants etr1;ers1 are both male- and female-sterile, and that this phenotype is restored in etr1;ers1;ein2 triple mutants.²⁷ These notions are further reinforced by our observation of the ctr1-1;coi1-16 sterile phenotype.⁵ CONSTITUTIVE TRIPLE RESPONSE (CTR1) encodes a negative regulator of ethylene signaling and ctr1 mutants show constitutive ethylene response.²⁸ This may suggest that JAs promote fertility in a COI1-dependent manner while ethylene signaling antagonises this effect. Interestingly, expressing a transgenic COI1 gene, whose product is incapable of making a SCF complex, partly recovers male sterility of the null coi1-1 mutant,⁵ suggesting that there is a COI1-dependent fertility mechanism that does not require SCF complex assembly.

Our previous study focused on the interaction between COI1 and the ethylene pathway on the root growth inhibition of Arabidopsis, and here we also point out that this interaction plays important roles in other developmental processes such as germination and fertility. Model pathways are presented in Figure 1.

Figure 1.

Model networks for the interaction of COI1 and the ethylene perception-response pathway in physiological processes such as root growth, germination and fertility in Arabidopsis.

Addendum to: Adams E, Turner J. COI1, a jasmonate receptor, is involved in ethylene-induced inhibition of Arabidopsis root growth in the light. J Exp Bot. 2010;61:4373–4386. doi: 10.1093/jxb/erq240.