Ethylene

Abstract

Ethylene, a simple hydrocarbon gas, is a plant growth regulator that profoundly affects growth and development. Ethylene plays an important role in a wide range of processes, including fruit ripening, abscission, senescence and responses to biotic and abiotic stresses. Plants synthesise ethylene in response to diverse developmental factors and environmental stimuli. Responses to ethylene occur through a conserved ethylene signalling pathway that was first elucidated by molecular genetic dissection in the plant Arabidopsis thaliana. The ethylene‐signalling pathway comprises a unique combination of signalling components, beginning with ethylene receptors localised primarily at the endoplasmic reticulum membrane. Ethylene signalling leads to changes in gene expression in the nucleus. Ethylene also exhibits complex interactions with the signalling pathways of a number of other plant signals. An understanding of the regulatory mechanisms involved in ethylene biosynthesis and ethylene signalling has important agricultural and economic implications.

Key Concepts:

  • Ethylene gas (C2H4) is a plant growth regulator that has profound effects on growth and development.

  • Plants synthesise ethylene from the amino acid l‐methionine via a simple biosynthetic pathway consisting of three enzymatic steps.

  • Gene family members encoding the ethylene biosynthesis enzymes are differentially expressed in response to diverse developmental and environmental factors; additionally, ACC synthase isozymes, which catalyse the penultimate step in the pathway, are regulated by protein turnover.

  • The ethylene signalling pathway, which was genetically dissected in the reference plant Arabidopsis, is conserved in plants and involves a unique combination of signalling components.

  • The ethylene signal is perceived by protein complexes residing at the ER membrane and transduction of the signal activates a transcriptional cascade resulting in rapid changes in gene expression.

  • Protein turnover plays a critical role in both ethylene biosynthesis and ethylene signalling.

  • Ethylene displays complex interactions with a variety of other signals to control a wide array of processes.

  • The ability to control ethylene biology has far‐reaching consequences in agriculture and horticulture.

Keywords: ethylene; plant hormone; plant growth regulator; plant growth and development; signal transduction; Arabidopsis thaliana; agriculture

Figure 1.

Ethylene responses in Arabidopsis. (a) A 4‐day old dark‐grown seedling germinated in the presence of exogenously applied ethylene exhibits the characteristic triple response phenotype (right). The defining features of the triple response include inhibition of cell elongation in the hypocotyl and the root, radial swelling of the hypocotyl, exaggerated curvature of the apical hook and a proliferation of root hairs. The 4‐day old dark‐grown seedling (left) has not been treated with ethylene and displays the same phenotype as an ethylene‐insensitive mutant. (b) The ctr1 null mutant (right) exhibits inhibition of cell expansion in leaves compared with a wild‐type plant (left) of the same age. (c) A wild‐type plant treated with 100 μL/L ethylene gas for 3 days exhibits leaf senescence (right) in comparison to an untreated wild‐type plant (left).

Figure 2.

Model of the ethylene‐signalling pathway in Arabidopsis. Ethylene is perceived by a family of five ethylene receptors predominantly localised to the ER membrane. These receptors (represented by the ETR1 receptor) form homodimers and require a copper cofactor to bind ethylene. The delivery of copper is dependent on the transporter RAN1 in the Golgi membrane. Signalling by receptor ETR1 is facilitated by interaction with RTE1. In the absence of ethylene (left half of figure), the receptors repress downstream ethylene responses through the CTR1 protein kinase, which phosphorylates EIN2, an integral membrane protein with sequence similarity to the Nramp family of metal‐ion transporters. Upon ethylene binding (right half of figure), the receptors inactivate CTR1. The lack of phosphorylation results in the EIN2 C‐terminal domain being cleaved and translocated into the nucleus. The EIN2 C‐terminal domain is a positive regulator of ethylene responses that leads to the activation of the EIN3/EIL1 family of transcription factors. EIN3 and EIL1 are regulated by two F‐box proteins (EBF1/EBF2), which in the absence of ethylene, target EIN3 for degradation through the 26S proteasome pathway. EBF1 and EBF2 are negatively regulated at the mRNA level indirectly through a 5′–3′ exoribonuclease XRN4 (EIN5). Upon ethylene binding, EIN3 is stabilised, enabling it to activate a transcriptional cascade resulting in the expression of ethylene‐response genes. Figure is modified from Figure 4 in Ju et al. .

Figure 3.

The ethylene biosynthesis pathway. In higher plants, ethylene is produced from the amino acid l‐methionine, which is converted into AdoMet by AdoMet synthetase. Next, AdoMet is converted into ACC by ACC synthase, which is the rate‐limiting step in ethylene biosynthesis. Finally, ACC is converted into ethylene through the action of the enzyme ACC oxidase.

Figure 4.

Posttranslational modifications of ACS proteins regulate ethylene synthesis. The three ACS isozyme types are defined by their C‐terminal amino acid sequence motifs; representative members of each type are shown. Consensus sites for MAPK and CDPK phosphorylation are shown as purple and turquoise ovals, respectively. Several factors and signals that affect the stability of type 1 and type 2 isozymes through action on C‐terminal motifs are indicated, with positive regulators shown in blue and negative regulators shown in red. In the absence of a stabilising input, type 1 and type 2 isozymes are rapidly degraded by the 26S proteasome. Evidence for CDPK regulation of type 1 isozymes has been obtained in tomato fruits; dashed lines indicate that this role has not yet been established in Arabidopsis. Although the C‐terminus of type 2 isozymes can be phosphorylated by CDPKs in vitro, a regulatory role for CDPK phosphorylation of these proteins has not been demonstrated in vivo; the grey arrow indicates possible CDPK input. The eto2 and eto3 mutations are stabilising alleles of ACS5 and ACS9, respectively. Not depicted in this cartoon are ACS4 and ACS8, two additional type 2 isozymes, and ACS1, a catalytically inactive type 1 isozyme. Copyright: © Skottke et al.. This is an open‐access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited. © PLoS.

Figure 5.

The ethylene receptor family in Arabidopsis. The five ethylene receptors in Arabidopsis, which are similar in sequence and structure to two‐component histidine protein kinase receptors, fall into two subfamilies. Subfamily I receptors contain all motifs necessary for functional histidine kinase activity (indicated by horizontal black lines), and have been demonstrated to have histidine kinase activity in vitro. Subfamily II receptors lack most or all of these motifs and instead appear to function as serine/threonine kinases. All receptors (shown here as monomers) contain a highly conserved transmembrane ethylene‐binding domain, with three membrane‐spanning regions in subfamily I receptors and four in subfamily II, a GAF‐like domain implicated in protein–protein interactions, and a histidine protein kinase domain. Three of the five receptors (ETR1, EIN4 and ETR2) also contain a domain that is conserved with two‐component receiver domains. The GAF, histidine kinase and receiver domains comprise the region believed to be important for signal transmission.

close

References

Abeles FB, Morgan PW and Saltveit ME Jr (1992) Ethylene in Plant Biology, 2nd edn. San Diego, CA: Academic Press.

Adie B, Chico JM, Rubio‐Somoza I and Solano R (2007) Modulation of plant defenses by ethylene. Journal of Plant Growth Regulation 26: 160–177.

Alonso JM, Stepanova AN, Leisse TJ et al. (2003) Genome‐wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

An F, Zhao Q, Ji Y et al. (2010) Ethylene‐induced stabilization of ETHYLENE INSENSITIVE3 and EIN3‐LIKE1 is mediated by proteasomal degradation of EIN3 binding F‐box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 22: 2384–2401.

Argueso CT, Hansen M and Kieber JJ (2007) The regulation of ethylene biosynthesis. Journal of Plant Growth Regulation 26: 92–105.

Barry CS and Giovannoni JJ (2006) Ripening in the tomato Green‐ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling. Proceedings of the National Academy of Sciences of the USA 103: 7923–7928.

Beaudoin N, Serizet C, Gosti F and Giraudat J (2000) Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12: 1103–1115.

Bisson MMA and Groth G (2010) New insight in ethylene signaling: autokinase activity of ETR1 modulates the interaction of receptors and EIN2. Molecular Plant 3: 882–889.

Bleecker AB, Estelle MA, Somerville C and Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241: 1086–1089.

Chang C, Kwok SF, Bleecker AB and Meyerowitz EM (1993) Arabidopsis ethylene‐response gene ETR1: similarity of product to two‐component regulators. Science 262: 539–544.

Chen YF, Etheridge N and Schaller GE (2005) Ethylene signal transduction. Annals of Botany 95: 901–915.

Chen YF, Randlett MD, Findell JL and Schaller GE (2002) Localization of the ethylene receptor ETR1 to the endoplasmic reticulum of Arabidopsis. Journal of Biological Chemistry 277: 19861–19866.

Clark KL, Larsen PB, Wang X and Chang C (1998) Association of the Arabidopsis CTR1 Raf‐like kinase with the ETR1 and ERS ethylene receptors. Proceedings of the National Academy of Sciences of the USA 95: 5401–5406.

Gao Z, Wen CK, Binder BM et al. (2008) Heteromeric interactions among ethylene receptors mediate signaling in Arabidopsis. Journal of Biological Chemistry 283: 23801–23810.

Guzman P and Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene‐related mutants. Plant Cell 2: 513–523.

Hall BP, Shakeel SN, Amir M et al. (2012) Histidine kinase activity of the ethylene receptor ETR1 facilitates the ethylene response in Arabidopsis. Plant Physiology 159: 682–695.

Hua J and Meyerowitz EM (1998) Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94: 261–271.

Hirayama T, Kieber JJ, Hirayama N et al. (1999) RESPONSIVE‐TO‐ANTAGONIST1, a Menkes/Wilson disease‐related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97: 383–393.

Ju C, Yoon GM, Shemansky JM et al. (2012) CTR1 phosphorylates EIN2 to control ethylene signaling from the ER membrane to the nucleus. Proceedings of the National Academy of Sciences of the USA 109: 19486–19491.

Kende H (1993) Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44: 283–307.

Klee HJ and Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annual Review of Genetics 45: 41–59.

Li GJ, Meng XZ, Wang RG et al. (2012) Dual‐level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genetics 8: e1002767.

Maruyama‐Nakashita A, Nakamura Y, Tohge T, Saito K and Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulphur response and metabolism. Plant Cell 18: 3235–3251.

McManus MT (2012) Annual Plant Reviews Volume 44: The Plant Hormone Ethylene. Oxford, UK: Wiley Blackwell.

Mount SM and Chang C (2002) Evidence for a plastid origin of plant ethylene receptor genes. Plant Physiology 130: 10–14.

Muday GK, Rahman A and Binder BM (2012) Auxin and ethylene: collaborators or competitors? Trends in Plant Science 17: 181–195.

Qiao H, Chang KN, Yazaki J and Ecker JR (2009) Interplay between ethylene, ETP1/ETP2 F‐box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes & Development 23: 512–521.

Resnick JS, Wen CK, Shockey JA and Chang C (2006) REVERSION‐TO‐ETHYLENE SENSITIVITY1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 103: 7917–7922.

Robert‐Seilaniantz A, Grant M and Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate–salicylate antagonism. Annual Review of Phytopathology 49: 317–343.

Rodríguez FI, Esch JJ, Hall AE et al. (1999) A copper cofactor for the ethylene receptor ETR1 from Arabidopsis. Science 283: 996–998.

Skottke KR, Yoon GM, Kieber JJ and DeLong A (2011) Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genetics 7: e1001370.

Solano R, Stepanova A, Chao Q and Ecker JR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE‐INSENSITIVE3 and ETHYLENE‐RESPONSE‐FACTOR1. Genes & Development 12: 3703–3714.

Stepanova AN and Alonso JM (2009) Ethylene signaling and response: where different regulatory modules meet. Current Opinion in Plant Biology 12: 548–555.

Wilkinson JQ, Lanahan MB, Clark DG et al. (1997) A dominant mutant receptor from Arabidopsis confers ethylene insensitivity in heterologous plants. Nature Biotechnology 15: 444–448.

Zhu Z, An F, Feng Y et al. (2011) Derepression of ethylene‐stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 108: 12539–12544.

Further Reading

Alexander L and Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. Journal of Experimental Botany 53: 2039–2055.

Arshad M and Frankenberger WT Jr (2002) Ethylene: Agricultural Sources and Applications. New York: Kluwer Academic/Plenum Publishers.

Barry CS and Giovannoni JJ (2007) Ethylene and fruit ripening. Journal of Plant Growth Regulation 26: 143–159.

Gazzarrini S and McCourt P (2003) Cross‐talk in plant hormone signalling: what Arabidopsis mutants are telling us. Annals of Botany 91: 605–612.

Hall BP, Qureshi SN and Schaller GE (2007) Ethylene receptors: ethylene perception and signal transduction. Journal of Plant Growth Regulation 26: 118–130.

Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiology 13: 660–667.

Mattoo AK and Suttle JC (1991) The Plant Hormone Ethylene. Boca Raton: CRC Press, Inc.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Chang, Caren, Schaller, G Eric, and Resnick, Josephine S(Jun 2013) Ethylene. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020099.pub2]