Ethylene: The Gaseous Hormone
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1 Ethylene: The Gaseous Hormone History: th century: coal gas was used for street illumination, it was observed that trees in the vicinity of streetlamps defoliated more extensively than other trees. 2. In 1901, Dimitry Neljubov, a graduate student in Russia, first found etiolated pea seedlings in the laboratory exhibited triple response. 3. In 1910, H. H. Cousins first indication that ethylene is a natural product of plant tissues. Emanation from orange stored in a chamber caused banana ripening. 4. In 1934, R. Gane and others identified ethylene chemically as a natural product of plant metabolism, and because of its dramatic effects on the plant it was classified as a hormone. 1
2 Structure, Biosynthesis, and Measurement of Ethylene Structure: the simplest olefin ( 石蠟 ), Mr=28 Biosynthesis: almost all tissues leaf abscission, flower senescence, fruit ripening stress, disease Measurement: gas chromatography (GC) 氣相層析儀 2
3 Ethylene biosynthetic pathway N Mnlonyl ACC, a conjuated form of ACC), may play an important role in the control of ethylene biosynthesis. 3 ACC deaminase:
4 Catabolism 1, 4 cyclohexadiene 14 C 2 H 4 carbon dioxide, ethylene oxide, ethylene glycol, and the glucose conjugate of ethylene glycol Ethylene catabolism does not appear to play a significant role in regulating the level of the hormone. 4
5 Ethylene biosynthesis is promoted by several factors 1. Fruit ripening: ACC synthase (ACS), ACC oxidase (ACO) ACC and ethylene ACC treats with unripe fruits only slightly enhances ethylene production. ACO is the rate limiting step in ripening. 2. Stress: drought, flooding, chilling, exposure to ozone, and mechanical wounding. This stress ethylene leads to the onset of stress responses such as abscission, senescence, wound healing and increased disease resistance. 5
6 Ethylene biosynthesis is promoted by several factors 3. Circadian: ethylene high at midday and low at midnight. Circadian regulates a subset of ACSs, which is mediated by the TOC1/CCA1 clock in Arabidopsis. 4. Auxin induced: Auxin promotes ethylene biosynthesis by enhancing ACS activity, such as flowering in pineapple and inhibition of stem elongation. 6
7 Inhibitors of ethylene biosynthesis or signaling Epinasty (a downward curvature of leaves) caused by ethylene and high auxin conc. Studies using inhibitors showed that ethylene is the primary effector of epinasty and that auxin acts indirectly by causing a substantial increase in ethylene production. Inhibitors of ethylene biosynthesis: AVG: aminoethoxy vinylglycine (for ACS) AOA: aminooxyacetic acid (for ACS) AIBA: α aminoisobytyric acid (for ACO) Co 2+ : cobalt ions (for ACO) Inhibitors of ethylene action (signaling): Silver ions (Ag + ): silver nitrate (AgNO 3 ), silver thiosulfate [Ag(S 2 O 3 ) 2 3 ] CO 2 : at high conc (5 to 10%) trans cyclooctene: a strong competitive inhibitor MCP: 1 Methylcyclopropene, a irreversible binding Epinasty phenotype Ethylene absorbent: Potassium permanganate (KMnO 4 ) 7
8 Ethylene Signal Transduction Pathways Triple response: Etiolated seedlings show short hypocotyls (epicotyp), short roots and exaggerated apical hoods at the presence of ethylene. How to isolate ethylene signaling mutants? Mutagenized Arabidopsis seeds were grown on agar plates with or without ethylene in the dark. 1. Ethylene resistant or ethylene insensitive mutants. 2. Constitutive mutants ctr1: constitutive triple response Biosynthesis: Met ACC ethylene Signal transduction: Receptor TF ERE promoter Transcription factor (TF) Ethylene responsive gene 8
9 Ethylene Signal Transduction Pathways Ethylene receptors are related to bacterial two component system histidine kinase The first ethylene insensitive mutant isolated was etr1 (ethylene response1). The C terminal half of etr1 is similar to bacterial two component histidine kinase. ERS: ETHYLENE RESPONSE SENSOR 1 EIN: ETHYLENE INSENSITIVE All of these five receptors share at least two domains: 1. Membrane spanning domain at N terminus. 2. Histidine kinase catalytic domains. These five receptors may interact with each other to form large multisubunit complexes. Binding of ethylene induces degradation of the receptors via the 26S proteasome. 9
10 Bacterial two component system 10
11 Ethylene Signal Transduction Pathways High affinity binding of ethylene to its receptor requires a copper cofactor Analysis of the ETR1 ethylene receptor expressed in yeast demonstrated that copper was necessary for high affinity ethylene binding. Evidence: RAN1 (RESPONSE TO ANTAGONIST1), a protein required for the transfer of a copper ion to an iron transport protein. The ran1 mutant blocks the formation of functional ethylene receptors. Silver ion could substitute for copper to yield high affinity binding, which indicates that silver blocks the actin of ethylene not by interfering with ethylene binding, but by preventing the changes in the protein that normally occur when ethylene binds to the receptor. 11
12 Ethylene Signal Transduction Pathways Receptors (ETR1 etc) CTR1 EIN2 EIN3 etc ethylene response A serine/threonine protein kinase is also involved in ethylene signaling ctr1: constitutive triple response 1, a recessive mutant 1. The ctr1 mutant caused an activation of the ethylene response suggests that the wildtype protein, like the ethylene receptors, acts as a negative regulator of the response pathway. 2. CTR1: a Raf like kinase, a MAPKKK (mitogen activated protein kinase kinase kinase) type of serine/threonine protein kinase. 3. CTR1 protein directly interacts with the ethylene receptors, forming part of a protein complex. EIN2 encodes a transmembrane protein 1. The ein2 mutant completely blocks ethylene signaling. 2. EIN2: a protein with 12 membrane spanning domains, similar to the N RAMP (natural resistance associated macrophage protein) family of cation transporters in animals, suggesting that it may act as a channel or pore. 3. The EIN2 protein is rapidly degraded by 26S proteasome, and ethylene inhibits the degradation of EIN2. 12
13 Developmental and Physiological Effects of Ethylene Ethylene promotes the ripening of some fruits Fruit ripening includes the enzymatic breakdown of the cell walls, starch hydrolysis, sugar accumulation, and the disappearance of organic acids and phenolic compounds. Fruits that respond to ethylene exhibit a climacteric Climacteric fruits have a characteristic respiratory rise before ripening phase. Such fruits also show a spike of ethylene production immediately before the respiratory rise, such as apples, bananas, avocados, and tomatoes In climacteric fruits, treatment with ethylene induces the fruit to produce additional ethylene, a response called autocatalytic. Nonclimacteric fruits: grapes 13
14 Developmental and Physiological Effects of Ethylene Practical application: 1. Exogenous application of ethylene to the climacteric fruits leads to uniform ripening. 2. Inhibitors of ethylene biosynthesis or action delay or prevent ripening. 3. Transgenic tomatoes expressing antisense ACS or ACO genes block fruit ripening and application of exogenous ethylene restored ripening. 14
15 Developmental and Physiological Effects of Ethylene The receptors of never ripe mutants of tomato fail to bind ethylene The never ripe mutant is due to a mutation in an ethylene receptor that rendered it unable to bind ethylene and block ripening. 60 DPA 42 DPA 60 DPA Gr: green ripe mutant Nr: never ripe mutant Barry et al., 2005; Plant Physiol 138:
16 Developmental and Physiological Effects of Ethylene Ethylene breaks seed and bud dormancy in some species 1. Ethylene breaks dormancy and initiate germination in certain seeds, such as cereals. 2. Ethylene can also break bud dormancy, and ethylene treatment is sometimes used to promote bud sprouting in potato and other tubers. Ethylene induces the formation of roots and root hairs 1. Ethylene induces adventitious root formation in leaves, stems, and even other roots. 2. Auxin induction of adventitious roots is mediated by ethylene. e.g., ein mutant with little effect. 3. Ethylene acts as a positive regulator of root hair formation in several species. 16
17 Developmental and Physiological Effects of Ethylene Ethylene promotes the elongation growth of submerged aquatic species 1. Although usually thought of as an inhibitor of stem elongation, ethylene is able to promote stem and petiole elongation in various submerged or partially submerged aquatic plants. 2. Deep water rice: Submergence induces rapid internode elongation, which allow the leaves or upper parts of the shoot to remain above water. 3. Ethylene stimulates internode elongation in deep water rice by increasing the amount of, and the sensitivity to, GA in the cells of the intercalary meristem. 4. Ethylene mediated expression of SNORKEL1 and SNORKEL2 was identified to trigger the dramatic internode elongation. 17
18 Ethylene and flooding tolerance strategies in rice From the following article: Plant biology: Genetics of high-rise rice Laurentius A. C. J. Voesenek & Julia Bailey-Serres Nature 460, (20 August 2009) doi: /460959a The elongation of stem and leaf cells is positively regulated by the hormone gibberellic acid (GA). In normal circumstances, a second hormone, abscisic acid (ABA), inhibits GA activity. When plants are submerged, ethylene, a gaseous plant hormone, accumulates owing to its slow outward diffusion in water. This promotes the breakdown of ABA, increasing the production of, or responsiveness to, GA, ultimately stimulating cell elongation. a, The escape strategy of deepwater varieties involves fast stem elongation to rise above the water level. Elongation growth and possibly GA accumulation or action are stimulated by transcription factors encoded by two ethylene regulated genes, SNORKEL1 andsnorkel2 (SK1 and SK2) (dashed arrow) 1. b, In the quiescence strategy of submergence tolerant varieties, shoot elongation is suppressed so as to conserve carbohydrates and increase survival under flash flood conditions. GA signalling and thus elongation are inhibited by the ethylene induced action of a SUBMERGENCE gene (SUB1A 1) on the growth inhibiting genes SLENDER RICE 1 (SLR1) and SLR LIKE 1 (SLRL1). 18
19 Developmental and Physiological Effects of Ethylene Ethylene regulates flowering and sex determination in some species Promote flowering: pineapple and mango Sex determination: On plants that have separate male and female flowers (monoecious species), ethylene may change the sex of developing flowers. e.g., cucumber. Ethylene mediates some defense responses 1. Ethylene production generally increases in response to pathogen attack in both compatible (i.e., pathogenic) and noncompatible (nonpathogenic) interaction. 2. On the other hand, ethylene in combination with the plant hormone jasmonic acid, is required for the activation of several plant defense genes. 19
20 Developmental and Physiological Effects of Ethylene Ethylene acts on the abscission layer Abscission: The shedding of leaves, fruits, flowers, and other plant organs. Abscission layer: Abscission takes place in specific layers of cells. birch tree ( 樺樹 ) Transgenic plant expressing Arabidopsis etr1 mutant gene 20
21 Developmental and Physiological Effects of Ethylene Schematic view of the roles of auxin and ethylene during leaf abscission Removal of the leaf blade promotes petiole abscission. 21
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