JXB Advance Access originally published online on March 14, 2005
Journal of Experimental Botany 2005 56(415):1359-1367; doi:10.1093/jxb/eri137
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RESEARCH PAPER |
The climacteric-like behaviour of young, mature and wounded citrus leaves
The Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, PO Box 12, Rehovot 76100, Israel
* Present address and to whom correspondence should be sent: University of California, Department of Plant Sciences, Mail Stop 5, One Shields Avenue, Davis, CA 95616, USA. Fax: +1 530 752 2278. E-mail: ekatz{at}ucdavis.edu
Received 9 September 2004; Accepted 10 February 2005
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Abstract |
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Although leaves and other vegetative tissues are generally considered as non-climacteric, citrus leaves show a climacteric system II behaviour after detachment. Upon harvest, young, fully expanded ‘Valencia’ orange (Citrus sinensis) leaves (
60-d-old) exhibited two phases of ethylene production. The first phase, up to 6 d after detachment, was characterized by a low and constant ethylene production (system I pathway), associated with a constitutive expression of ACC synthase 2 (CsACS2), CsERS1, and CsETR1. ACC synthase 1 (CsACS1) was not expressed during this phase and autoinhibition of ethylene production was apparent following treatment with exogenous ethylene or propylene. The second phase, 7–12 d after detachment, was characterized by a climacteric rise in ethylene production, preceded by the induction of CsACS1 and ACC oxidase 1 (CsACO1) gene expression in the system II pathway. This induction was accelerated and augmented by exogenous ethylene or propylene, indicating an autocatalytic system II ethylene biosynthesis. Mature leaves (6–8-months-old) behaved similarly, except that the climacteric peak in ethylene production occurred earlier (day 5). Young and mature leaves varied in the timing of the climacteric ethylene rise and CsACS1 and CsACO1 induction. The two phases of ethylene production, system I and system II, were also detected in wounded leaf discs of both young and mature leaves. The first phase peaked 15 min after excision and the second phase peaked after 6 h. Key words: ACC oxidase, ACC synthase, citrus leaves, ethylene, non-climacteric fruit, systems I and II, senescence, wounding
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Introduction |
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The plant hormone ethylene has profound effects on plant growth and development (Abeles et al., 1992
). During the course of the plant life cycle, ethylene affects seed germination, cell elongation, cell differentiation, sex determination, fruit ripening, senescence, and abscission. Ethylene is also a key regulator of the response to biotic and abiotic stresses such as drought, flooding, wounding, chilling injury, pathogen infection, and chemical inducers.
Ethylene biosynthesis and perception are important factors in ethylene action in plant tissues. Ethylene is produced from methionine via the conversion of S-adenosyl-L-methionine to 1-aminocyclopropane-1-carboxylate (ACC), catalysed by ACC synthase, and the subsequent oxidation of ACC to ethylene by ACC oxidase. ACC synthase, the key enzyme in this pathway, is encoded by a multigene family. The expression of ACC synthase genes is differentially and tightly regulated by various developmental, environmental, and hormonal signals (Kende, 1993; Zarembinski and Theologis, 1994; Fluhr and Mattoo, 1996; Alexander and Grierson, 2002). ACC oxidase is encoded by a small gene family and there is evidence for a differential regulation of ACC oxidase gene expression (Barry et al., 1996; Nakatsuka et al., 1997, 1998; Mita et al., 1998, 1999).
Ethylene is perceived by a family of integral membrane receptors that are similar to the bacterial two-component histidine kinase receptors (Bleecker, 1999; Chang and Shockey, 1999; Stepanova and Ecker, 2000). In Arabidopsis thaliana and tomato, this family includes at least five members (in arabidopsis, ETR1, ETR2, EIN4, ERS1, and ERS2) (Chang et al., 1993; Hua et al., 1995, 1998; Sakai et al., 1998; Stepanova and Ecker, 2000; Ciardi and Klee, 2001). Genetic studies suggest that ethylene binding inactivates the receptors (Hua and Meyerowitz, 1998). In the absence of ethylene, the receptors are predicted to activate a Raf-like serine/threonine kinase, CTR1, a negative regulator of the transduction pathway (Kieber et al., 1993). Other components of the ethylene signal transduction pathway have also been identified (Johnson and Ecker, 1998; Bleecker, 1999; Chang and Shockey, 1999; Stepanova and Ecker, 2000; Chang and Stadler, 2001).
Several reports have demonstrated that ethylene production in attached or detached leaves of various species increased during senescence or in response to exogenous ethylene in a climacteric-like pattern (Aharoni et al., 1979; Alejar et al., 1988; McGlasson et al., 1975; Morgan and Durham, 1980; Gepstein and Thimann, 1981; Riov and Yang, 1982; Morgan et al., 1992). A similar phenomenon was observed in leaf discs following wounding and particularly in response to ethylene treatment (Aharoni et al., 1979; Riov and Yang, 1982). Riov and Yang (1982) showed that treatment of citrus leaf discs with ethylene exerted both autocatalytic and autoinhibitory effects, phenomena which are characteristic of ethylene production during climacteric fruit development. However, ethylene production in leaves sometimes differed from that observed in fruits. For example, in attached tobacco leaves ethylene production decreased during the onset of senescence and increased only during the advanced stages of senescence (Aharoni et al., 1979). In addition, the autocatalytic ethylene production in citrus leaf discs was dependent on a continuous presence of exogenous ethylene and decreased rapidly upon its removal (Riov and Yang, 1982). In contrast to fruit, in which the molecular control of ethylene production and sensing has been extensively investigated, very little has been done on these topics in leaves.
In the present study, the regulation of ethylene evolution in whole and wounded citrus leaves of different ages was examined using exogenous ethylene and ethylene-action inhibitor treatments. The expression of genes involved in ethylene biosynthesis and perception, which have recently been isolated from citrus fruit, was followed (Katz et al., 2004). The data demonstrate a climacteric-like behaviour of citrus leaves, which was reflected in the induction of ethylene biosynthesis genes and autocatalytic ethylene production. The results suggest the existence of the two systems of ethylene production, system I and system II (McMurchie et al., 1972), in citrus leaves.
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Materials and methods |
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Plant material
‘Valencia’ orange (Citrus sinensis L. Osbeck) leaves were harvested and stored in the dark at 25 °C under 100% relative humidity. For ethylene and propylene treatments, leaves were sealed in 3.2 l jars into which the gasses were injected to give final concentrations of 10 and 1000 µl l–1, respectively. Both treatments were applied continuously unless otherwise specified. Ethylene or propylene gas mixtures were renewed every day after aeration of the jars. Leaves or leaf discs samples were frozen immediately in liquid nitrogen and stored at –70 °C until analysis.
For wounding experiments, leaf discs, 8 mm in diameter, were excised and punctured with a biological needle to increase the wounding effect. Discs were placed in Petri dishes and incubated in darkness at 25 °C and 100% relative humidity. Whole detached leaves were used as controls in the wounding experiments.
Ethylene evolution
Ethylene evolution was determined daily. Each leaf was placed for 2 h into an 18 ml tube that was sealed with a serum cap. Leaf discs were sealed in 6 ml tubes. One ml air samples were withdrawn from the tubes and injected into a Varian 3300 gas chromatograph equipped with an alumina column at 100 °C and a flame ionization detector at 120 °C. Ethylene concentration was calculated based on an ethylene standard of a known concentration which was injected into the GC before and after sample analysis, incubation time, tube volume, and leaf or leaf discs weight.
2,5-NBD treatment
2,5-NBD (2,5-norbornadiene) (Aldrich Chemical Co., Milwaukee, WI, USA) was pipetted onto Whatman No. 1 filter paper held in glass beakers. The beakers were placed in the containers, which were closed immediately. Fresh 2,5-NBD was introduced every day after aeration of the containers.
RNA extraction and northern blot analysis
Total RNA was isolated from citrus leaves according to Izhaki et al. (2001). RNA (20 µg) was size-fractionated in a 1% agarose gel containing formaldehyde and blotted onto a Hybond-N+ filter (Amersham-Pharmacia Biotech, Buckinghamshire, UK). Following electrophoresis, the gel was briefly stained with ethidium bromide and photographed before blotting to ensure that equal amounts of RNA had been used for each sample. The blots were hybridized in 0.263 M Na2HPO4, 7% SDS, 1 mM EDTA, and 1% BSA at 60 °C with 32P-labelled cDNA probes (Rediprime; Amersham-Pharmacia Biotech) of CsACS1, CsACS2, CsACO1, CsERS1, and CsETR1 (Li et al., 2000; Katz et al., 2004). After hybridization, the membranes were washed twice in 2x SSC (0.3 M NaCl, 30 mM Na-citrate, pH 7.0) and 0.1% SDS at 60 °C for 15 min each and exposed to X-ray film (Fuji, Tokyo, Japan) with two intensifying screens at –70 °C.
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Results |
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Ethylene evolution by young and mature leaves in the presence and absence of exogenous ethylene or propylene
Enhanced ethylene evolution by detached, fully expanded young,
60-d-old, ‘Valencia’ leaves, was first detected 7 d after harvest, reaching a peak after 9–12 d (Fig. 1A). This rise in ethylene evolution was accompanied by petiole abscission. Exogenous ethylene accelerated the rise in ethylene evolution of these leaves, which peaked on day 4, about 5 d before untreated leaves. After 7 d of exposure to ethylene, the young leaves were degenerated, as can be seen by the degradation of rRNA (Fig. 1C). Therefore, analyses of ethylene evolution and gene expression in the following experiments were terminated on day 7, even though these leaves continued to produce ethylene.
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Ethylene production by detached mature,
8-month-old, leaves started to increase 5 d after detachment, preceding the ethylene rise in young leaves by 2 d (Fig. 1B). The increased ethylene production reached a sharp peak on day 9. Exogenous ethylene accelerated ethylene evolution of mature leaves, which peaked on day 3, 6 d before the control. After 6 d of exposure to ethylene, mature leaves were also completely degenerated, as can be seen again by the degradation of rRNA (Fig. 1D). Therefore, similar to young leaves, analysis of ethylene evolution in ethylene-treated leaves was terminated at that time. Exposure of young or mature leaves for a relatively short period (48 h) to exogenous ethylene induced ethylene evolution in a similar pattern to that observed under continuous ethylene (data not shown).
To ensure that the ethylene evolved by young and mature leaves was indeed endogenous ethylene and did not result from the externally applied ethylene, mature leaves were treated with propylene, an ethylene analogue (McMurchie et al., 1972). Propylene treatment resulted in increased ethylene evolution by young (data not shown) or mature (Fig. 2) leaves, similar to that obtained by ethylene treatment (Fig. 1).
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Gene expression in young and mature leaves after detachment in the presence and absence of exogenous ethylene
The molecular mechanisms involved in ethylene biosynthesis and sensing in control and ethylene-treated detached leaves was investigated further. The differential expression of genes involved in these two processes in young and mature ‘Valencia’ leaves is shown in Fig. 1C and D. In control young and mature leaves, the kinetics of CsACS1 expression coincided with ethylene evolution. The expression of this gene was undetectable immediately after detachment in both types of leaves, but was induced after 2 d, decreased, and induced again after 5 d in mature leaves. In control young leaves, CsACS1 was undetectable during the experimental period, but was induced after 6 d (data not shown). CsACO1 was detectable immediately after detachment in both young and mature leaves. In mature leaves, CsACO1 expression was more or less constant (Fig. 1D), while in young leaves its expression decreased after 2 d to a constant level (Fig. 1C).
Ethylene treatment caused an earlier and stronger induction of CsACS1 in both young and mature leaves, detectable after 3 d and 1 d, respectively, which coincided with ethylene evolution. Ethylene treatment enhanced CsACO1 expression as well. CsACS2, CsERS1, and CsETR1 were constantly expressed after detachment in both types of leaves and were not affected by ethylene (Fig. 1C, D) or propylene (data not shown) treatments.
Effect of the ethylene-action inhibitor, 2,5-NBD, on ethylene evolution and gene expression
2,5-NBD, which has previously been shown to be very effective in this species (Goldschmidt et al., 1993), was used in the present study for the inhibition of ethylene action. 2,5-NBD treatment almost completely inhibited the significant rise in ethylene evolution in mature control leaves (Fig. 3A). In ethylene-treated leaves, 2,5-NBD also inhibited the accelerated rise in ethylene evolution, but the extent of inhibition was smaller than that obtained in control leaves.
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2,5-NBD treatment reduced the expression of CsACS1 and CsACO1 in mature leaves with or without ethylene treatment (Fig. 3B). CsACS2, CsERS1, and CsETR1 were again constantly expressed and were unaffected by either ethylene or 2,5-NBD treatment (Fig. 3B).
Autoinhibition of ethylene production
Immediately after harvest, leaves produced very low and constant amounts of ethylene. Treating mature leaves during this particular period with ethylene (data not shown) or propylene (Fig. 4A) revealed an autoinhibition of ethylene evolution. This autoinhibition was accompanied by a slight decrease in CsERS1 and CsETR1 expression and a slight increase in CsACO1 expression. CsACS1 was not detected during the experimental period and CsACS2 was constantly expressed (Fig. 4B).
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Ethylene evolution and gene expression in wounded leaf discs
Wounded leaf discs revealed two phases of increased ethylene evolution, an early rise, which peaked 15 min after excision, followed by a decrease up to 120 min, and then a second rise, which peaked after 6 h (Fig. 5). The first rise in ethylene evolution was not accompanied by any changes in gene expression, except for CsACO1 expression, which was apparent after 30–60 min (Fig. 6A). The second phase involved an up-regulation of CsACS1, starting 3 h after wounding (Fig. 6B). Ethylene application to the wounded discs did not affect gene expression, including that of CsACO1, during the first rise in ethylene (Fig. 6A).
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A short ethylene pretreatment (6 h) of leaves before disc excision inhibited the wound-induced ethylene (Fig. 7A). This was demonstrated by a smaller rise in ethylene evolution in wounded leaf discs pretreated with ethylene compared with untreated ones. On the other hand, a prolonged (24 h) ethylene pretreatment activated ethylene production in a climacteric-like pattern (Fig. 7B).
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Discussion |
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Two systems of ethylene production are operating in citrus leaves
The present paper provides data on the control of ethylene biosynthesis in citrus leaves, demonstrating their climacteric-like behaviour. Besides the contribution to the basic knowledge of ethylene biosynthesis and perception in plant organs, the authors believe that it increases current understanding of the role of ethylene in citrus leaf ontogeny, particularly of leaf senescence. Although detached leaves were used, there is similarity between ethylene evolution during natural senescence and detachment-induced-senescence.
In general, leaves evolve increased levels of ethylene during natural senescence as they do after detachment (Aharoni et al., 1979; Alejar et al., 1988; McGlasson et al., 1975; Morgan and Durham, 1980; Gepstein and Thimann, 1981; Riov and Yang, 1982; Morgan et al., 1992). This is also true for citrus leaves (Fig. 1; E Katz, unpublished data). In addition, the advent of natural senescence of citrus leaves is slow (Freeman et al., 1978) and likewise, the senescence of detached citrus leaves is very slow, and does not reveal the usual yellowing symptoms. Although citrus leaves undergo a slow senescence process, the data from this study show that they have the capability to produce high levels of ethylene. Based on the role of ethylene in senescence (see below), it is reasonable to assume that it is also plays a role in citrus leaf senescence.
Riov and Yang (1982) showed that citrus leaves responded to exogenous ethylene shortly after detachment by increased ethylene production. In the present study it was found that detached mature and young leaves produced high levels of ethylene without ethylene treatment when stored for more than 5 or 7 d, respectively (Fig. 1A, B). Ethylene production rates of detached citrus leaves, especially mature ones, were in the same range as those observed during the ripening phase of climacteric fruits (Katz et al., 2004). The results show that the two systems of ethylene production, system I and system II, operate in citrus leaves. During the first phase (3–5 d and 6–7 d after detachment in mature and young leaves, respectively) system I is operating. During this phase leaves produced low and constant amounts of ethylene after detachment (Fig. 1A, B), and upon treatment with ethylene or propylene they exhibited an autoinhibition of ethylene production (Figs 4, 7), an additional characteristic of system I (Riov and Yang, 1982). This autoinhibition did not involve changes in CsACS2 expression and CsACS1 was not detected at all during this period, suggesting a post-transcriptional regulation of ethylene biosynthesis enzymes. Other possibilities are reduction in the expression of other gene-family members which were not analysed in the present study or increased malonylation of ACC by ethylene (Liu et al., 1985a). Similar data were also obtained in mature citrus fruit (Katz et al., 2004), which represent a typical system I. It, therefore, seems that factors controlling the activity of system I were operating during the first phase after leaf detachment (Fig. 4B).
During the second phase, which started 5 d and 7 d after harvest in mature and young leaves, respectively, system II of ethylene production was initiated and ethylene evolution became autocatalytic and climacteric-like, which is typical of system II (Fig. 1A, B). In this phase, leaves produced relatively high levels of ethylene. Young and mature leaves differed both in the timing of the initiation of the autocatalytic ethylene production and in ethylene levels. Ethylene or propylene treatments enhanced ethylene evolution and induced an earlier climacteric-like peak (Fig. 1A, B), thus accelerating the initiation of system II activity. These results show that ethylene production by detached citrus leaves during the second phase is truly climacteric and follows the characteristics of system II ethylene production in fruits.
CsACS1, which was induced during the second phase, was responsible for the massive increase in ethylene production (Fig. 1). The expression of this gene was enhanced by ethylene treatment (Fig. 1C, D) and reduced by 2,5-NBD, an ethylene action inhibitor (Fig. 3B). 2,5-NBD antagonized not only the ethylene responses but also ethylene biosynthesis by down-regulating CsACS1 and CsACO1 expression (Fig. 3). This suggests the operation of a feedback regulation of ethylene biosynthesis, which interferes with autocatalysis, another indication for the presence of system II. The data also suggest that CsACS1, which is a key factor in the climacteric rise of ethylene production in citrus leaves, is regulated by ethylene, as previously shown for citrus fruitlets (Katz et al., 2004).
The difference in the initiation of the climacteric ethylene rise between young and mature leaves was apparently due to the difference in the timing of the induction of CsACS1 and CsACO1 expression (Fig. 1C, D). CsACS1 expression in young leaves was not observed during the first 6 d after detachment and its absence prolonged the first phase which was characterized by a low ethylene evolution. In mature leaves, CsACS1 was detected 2 d after detachment and was induced again on the fifth day, thereby reducing the duration of the first phase (Fig. 1). Another difference between the two types of leaves was the stronger expression level of CsACO1 in mature leaves (Fig. 1C, D).
CsERS1 expression in leaves during system II activity was different from that observed during system II activity in citrus fruitlets (Fig. 1C, D; Katz et al., 2004). CsERS1 expression was constant in both types of leaves irrespective of ethylene treatment (Fig. 1C, D), while in young fruitlets, CsERS1 was induced after harvest and in response to ethylene treatment. Treatment with 2,5-NBD was unable to inhibit CsERS1 expression in leaves (Fig. 3B), in contrast to the fruitlets system, suggesting that CsERS1 probably has a different regulatory role in leaves.
CsETR1 which has been shown to be constantly expressed in young and mature leaves (Figs 1C, D, 3), during fruit development (Katz et al., 2004), and in flowers (data not shown) is probably involved in system I in citrus. A similar pattern of expression was reported for its tomato homologue (Lashbrook et al., 1998; Nakatsuka et al., 1998). CsETR1 expression was not affected by ethylene treatment or ethylene action inhibitors, suggesting that it is not regulated by ethylene.
Wounded leaf discs have served as a useful system to study ethylene production during leaf senescence for many years. This system was also used to study the regulation of ethylene biosynthesis in citrus leaves. In response to wounding there were two phases of ethylene evolution. In the first phase, which was characterized by a low level of ethylene, no changes in gene expression were observed (Fig. 6A), suggesting the involvement of other members of ethylene biosynthesis genes or post-transcriptional regulation. Since discs were prepared from freshly detached leaves, they were in the system I ethylene production phase. This resulted in autoinhibition following ethylene or propylene treatments (Fig. 4A). Additional evidence for the activity of system I was the absence of CsACS1 expression (Fig. 6A, B). In the second phase, system II was activated, resulting in a much higher rise in ethylene (Fig. 5). This rise was accompanied by CsACS1 induction, which was detected 3 h after excision (Fig. 6B). Pretreatment with ethylene for at least 12 h before excision was sufficient to induce system II activity shortly after excision (Fig. 7B), skipping phase I. It can be concluded that in the leaf discs system, similar to fruit peel discs (Katz et al., 2004), both ethylene biosynthesis systems are operating and CsACS1 plays a major role in regulating ethylene evolution.
Ethylene has been considered to be involved in the regulation of leaf senescence (Smart, 1994). However, studies with transgenic plants and ethylene response mutants showed that ethylene is not necessary or not sufficient by itself to induce senescence, which led to the suggestion that ethylene operates via age-related factors in controlling this process (Bleecker et al., 1988; Kieber et al., 1993; Lanahan et al., 1994; Grbic and Bleecker, 1995; Buchanan-Wollaston, 1997; Chao et al., 1997; Oh et al., 1997; Hua and Meyerowitz, 1998). Jing et al. (2002) hypothesized that leaves have a defined age ‘window’ in which ethylene can affect senescence. Ethylene-effect windows were reported for other developmental events, such as curvature of the apical hook in etiolated seedlings (Raz and Ecker, 1999), release of seed dormancy and promotion of germination (Beaudoin et al., 2000), induction of epinasty in young tomato leaves but not in old ones (Abeles et al., 1992), induction of fruit ripening in mature green tomato fruits but not in immature ones (Liu et al., 1985b), and induction of massive ethylene production by young citrus fruitlets but not by mature fruit (Katz et al., 2004). Such ethylene-effect windows are accompanied by the activation of system II as has been found during fruit ripening (Nakatsuka et al., 1998; Barry et al., 2000) and following detachment and wounding of citrus leaves (this study).
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Acknowledgements |
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The financial support to EK, by a fellowship granted by the Israeli Citrus Marketing Board, is gratefully acknowledged.
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Footnotes |
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Abbreviations: ACC, 1-aminocyclopropane-1-carboxylate; CsACS1, CsACS2, ACC synthase; CsACO1, ACC oxidase; CsERS1, CsETR1, ethylene receptors; 2,5-NBD, 2,5-norbornadiene.
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Abeles FB, Morgan PW, Saltveit Jr ME. 1992. Ethylene in plant biology. San Diego: Academic Press.
Aharoni N, Lieberman M, Sisler HD. 1979. Patterns of ethylene production in senescing leaves. Plant Physiology 64, 796–800.
Alejar AA, Visser RD, Spencer MS. 1988. Ethylene production by attached leaves or intact shoots of tobacco cultivars differing in their speed of yellowing during curing. Plant Physiology 88, 329–332.
Alexander L, Grierson D. 2002. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. Journal of Experimental Botany 53, 2039–2055.
Barry CS, Blume B, Bouzayen M, Cooper W, Hamilton AJ, Grierson D. 1996. Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. The Plant Journal 9, 525–535.[CrossRef][Web of Science][Medline]
Barry CS, Llop-Tous MI, Grierson D. 2000. The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiology 123, 979–986.
Beaudoin N, Serizet C, Gosti F, Giraudat J. 2000. Interactions between abscisic acid and ethylene signaling cascades. The Plant Cell 12, 1103–1115.
Bleecker AB. 1999. Ethylene perception and signaling: an evolutionary perspective. Trends in Plant Science 4, 269–274.[CrossRef][Web of Science][Medline]
Bleecker AB, Estelle MA, Somerville C, Kende H. 1988. Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241, 1086–1089.
Buchanan-Wollaston V. 1997. The molecular biology of leaf senescence. Journal of Experimental Botany 48, 181–199.
Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. 1993. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262, 539–544.
Chang C, Shockey JA. 1999. The ethylene-response pathway: signal perception to gene regulation. Current Opinion in Plant Biology 2, 352–358.[CrossRef][Web of Science][Medline]
Chang C, Stadler R. 2001. Ethylene hormone receptor action in Arabidopsis. Bioessays 23, 619–627.[CrossRef][Web of Science][Medline]
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker JR. 1997. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133–1144.[CrossRef][Web of Science][Medline]
Ciardi J, Klee H. 2001. Regulation of ethylene-mediated responses at the level of the receptor. Analytical Botany 88, 813–822.
Fluhr R, Mattoo AK. 1996. Ethylene-biosynthesis and perception. Critical Reviews in Plant Science 15, 479–523.
Freeman BA, Platt-Aloia K, Mudd JB, Thomson WW. 1978. Ultrastructure and lipid changes associated with aging of citrus leaves. Protoplasma 94, 221–233.[CrossRef]
Gepstein S, Thimann KV. 1981. The role of ethylene in the senescence of oat leaves. Plant Physiology 68, 349–350.
Goldschmidt EE, Huberman M, Goren R. 1993. Probing the role of endogenous ethylene in the degreening of citrus fruit with ethylene antagonists. Plant Growth Regulation 12, 325–329.[CrossRef][Web of Science]
Grbic V, Bleecker AB. 1995. Ethylene regulates the timing of leaf senescence. The Plant Journal 8, 595–602.[CrossRef][Web of Science]
Hua J, Chang C, Sun Q, Meyerowitz EM. 1995. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269, 1712–1714.
Hua J, Meyerowitz EM. 1998. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 94, 261–271.[CrossRef][Web of Science][Medline]
Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB, Ecker JR, Meyerowitz EM. 1998. EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. The Plant Cell 10, 1321–1332.
Izhaki A, Swain SM, Tseng TS, Borochov A, Olszewski NE, Weiss D. 2001. The role of SPY and its TPR domain in the regulation of gibberellin action throughout the life cycle of Petunia hybrida plants. The Plant Journal 28, 181–190.[CrossRef][Web of Science][Medline]
Jing HC, Sturre JGM, Hille J, Dijkwel PP. 2002. Arabidopsis onset of leaf death mutants identify a regulatory pathway controlling leaf senescence. The Plant Journal 32, 51–63.[CrossRef][Web of Science][Medline]
Johnson PR, Ecker JR. 1998. The ethylene gas signal transduction pathway: a molecular perspective. Annual Review of Genetics 32, 227–254.[CrossRef][Web of Science][Medline]
Katz E, Lagunes PM, Riov J, Weiss D, Goldschmidt EE. 2004. Molecular and physiological evidence suggests the existence of system II-like pathway of ethylene production, in non-climacteric Citrus fruit. Planta 219, 243–252.[CrossRef][Web of Science][Medline]
Kende H. 1993. Ethylene biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 44, 283–307.[CrossRef][Web of Science]
Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR. 1993. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72, 427–441.[CrossRef][Web of Science][Medline]
Lanahan MB, Yen HC, Giovannoni JJ, Klee HJ. 1994. The Never ripe mutation blocks ethylene perception in tomato. The Plant Cell 6, 521–530.[Abstract]
Lashbrook CC, Tieman DM, Klee HJ. 1998. Differential regulation of the tomato ETR gene family throughout plant development. The Plant Journal 15, 243–252.[CrossRef][Web of Science][Medline]
Li CY, Zhong GY, Goren R, Jacob-Wilk D, Holland D. 2000. Cloning of a full-length cDNA encoding an ethylene receptor ERS homologue from Citrus. Acta Horticulturae 535, 119–125.
Liu Y, Hoffman NE, Yang SF. 1985a. Ethylene-promoted malonylation of 1-aminocyclopropane-1-carboxylic acid participates in autoinhibition of ethylene synthesis in grapefruit flavedo discs. Planta 164, 565–568.[CrossRef][Web of Science]
Liu Y, Hoffman NE, Yang SF. 1985b. Promotion by ethylene of the capability to convert 1-aminocyclopropane-1-carboxylic acid to ethylene in preclimacteric tomato and cantaloupe fruits. Plant Physiology 77, 407–411.
McGlasson WB, Poovaiah BW, Dostal HC. 1975. Ethylene production and respiration in aging leaf segments and in disks of fruit tissue of normal and mutant tomatoes. Plant Physiology 56, 547–549.
McMurchie EJ, McGlasson WB, Eaks IL. 1972. Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature 237, 235–236.[CrossRef][Medline]
Mita S, Kawamura S, Yamawaki K, Nakamura K, Hyodo H. 1998. Differential expression of genes involved in the biosynthesis and perception of ethylene during ripening of passion fruit (Passiflora edulis Sims). Plant Cell Physiology 39, 1209–1217.
Mita S, Kirita C, Kato M, Hyodo H. 1999. Expression of ACC synthase is enhanced earlier than that of ACC oxidase during fruit ripening of mume (Prunus mume). Physiologia Plantarum 107, 319–328.[CrossRef]
Morgan PW, Durham JI. 1980. Ethylene production and leaflet abscission in Melia azedarach L. Plant Physiology 66, 88–92.
Morgan PW, He CJ, Drew MC. 1992. Intact leaves exhibit a climacteric-like rise in ethylene production before abscission. Plant Physiology 100, 1587–1590.
Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A. 1998. Differential expression and internal feedback regulation of 1- aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiology 118, 1295–1305.
Nakatsuka A, Shiomi S, Kubo Y, Inaba A. 1997. Expression and internal feedback regulation of ACC synthase and ACC oxidase genes in ripening tomato fruit. Plant and Cell Physiology 38, 1103–1110.
Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG. 1997. Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. The Plant Journal 12, 527–535.[CrossRef][Web of Science][Medline]
Raz V, Ecker JR. 1999. Regulation of differential growth in the apical hook of Arabidopsis. Development 126, 3661–3668.[Abstract]
Riov J, Yang SF. 1982. Effects of exogenous ethylene on ethylene production in citrus leaf tissue. Plant Physiology 70, 136–141.
Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, Bleecker AB, Meyerowitz EM. 1998. ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proceedings of the National Academy of Sciences, USA 95, 5812–5817.
Smart C. 1994. Gene expression during leaf senescence. New Phytologist 126, 419–448.[CrossRef][Web of Science]
Stepanova AN, Ecker JR. 2000. Ethylene signaling: from mutants to molecules. Current Opinion in Plant Biology 3, 353–360.[CrossRef][Web of Science][Medline]
Zarembinski TI, Theologis A. 1994. Ethylene biosynthesis and action: a case of conservation. Plant Molecular Biology 26, 1579–1597.[CrossRef][Web of Science][Medline]
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