Annals of Botany 89: 689-693, 2002
© 2002 Annals of Botany Company
Effect of Ethylene on Flower Abscission: a Survey
Agrotechnological Research Institute (ATO), Wageningen University and Research Centre, PO Box 17, 6700 AA Wageningen, The Netherlands
* For correspondence. Fax +31 317 475347, e-mail w.g.vandoorn{at}ato.wag-ur.nl
Received: 9 January 2002; Returned for revision: 11 February 2002; Accepted: 22 February 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The effect of ethylene on flower abscission was investigated in monocotyledons and eudicotyledons, in about 300 species from 50 families. In all species studied except Cymbidium, flower abscission was highly sensitive to ethylene. Flower fall was not consistent among the species in any family studied. It also showed no relationship with petal senescence or abscission, nor with petal colour changes or flower closure. Results suggest that flower abscission is generally mediated by endogenous ethylene, but that some exceptional ethylene-insensitive abscission occurs in the Orchidaceae.
Key words: Ethylene sensitivity, flower abscission, petal wilting and abscission, petal senescence.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Flower fall seems a wasteful strategy as it involves the loss of a considerable amount of energy and nutrients. However, the strategy appears primarily related to strong internal competition, in which a rapid purge of sink tissue may be useful.
Flower abscission occurs both before and after fertilization. In some species the mere lack of pollination, after a critical period, activates the abscission zones, and in other species the lack of fertilization, again after a critical period, does so (Gärtner, 1844). Unfertilized flowers often abscise due to competition for carbohydrates (Aufhämmer et al., 1987; Aloni et al., 1996). Abscission of fertilized flowers is also often stimulated by stress, such as adverse growth conditions, lack of nutrients and by competition for assimilates (Stephenson, 1981; Lee, 1988).
Abscission of flowers reportedly occurs in many families, both in the monocotyledons and the eudicotyledons. In most species, the abscission zone is found in the pedicel, the stem segment that subtends the ovary. The zone usually occurs either towards the top or base of the pedicel, but exceptions are found, for example, in some Rosaceae, where the abscission zone is located in the lower part of the floral cup, which consists of fused basal portions of sepals, petals and stamens (van Doorn and Stead, 1997).
We have previously investigated the role of ethylene in petal abscission and petal wilting in about 300 species from 50 families. Petal abscission was rare in the monocotyledonous flowers tested, and common in the eudicotyledons. It was generally ethylene sensitive and tended to occur in all species of a (sub)family tested. In contrast, petal wilting was either ethylene sensitive or insensitive, and this was also generally consistent within families or subfamilies (Woltering and van Doorn, 1988; van Doorn, 2001). The incidence of flower abscission in these species is reported here. Results were compared for their consistency within families, and were related to the petal responses to ethylene treatment. The flowers were neither pollinated nor fertilized.
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MATERIALS AND METHODS |
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Plant material
Flowers or potted plants were bought at the flower auction in Aalsmeer or at retail outlets in Wageningen, The Netherlands. The plants were well watered, and used for experiments on the day of purchase. Several other species were obtained as cut parts, either from the Botanical Garden of the Agricultural University in Wageningen, or from the field. After severing, the flowering stems were immediately placed in water. The stems were transported in water to the laboratory, within an hour of cutting, and were used immediately. Cut flowers from a few other species were bought at the Aalsmeer flower auction. These were brought dry to the laboratory and arrived within 3 h. The stems of these flowers were recut under water, and used the same day for experimentation. The tested species are described in Woltering and van Doorn (1988) and van Doorn (2001).
Ethylene treatment
Treatments were carried out in stainless steel chambers at 20 ± 1 °C, in darkness, as described previously (Woltering and van Doorn, 1988). Briefly, the plants or flowers were exposed to 0·3 (0·28–0·33) Pa ethylene for 24 h. Excess carbon dioxide was absorbed by the presence of 10 g calcium hydroxide in the chamber. Partial pressures of ethylene and carbon dioxide were checked regularly during the treatments. Control flowers were stored under identical conditions except that ethylene was removed (the concentration remained below 0·001 Pa) using Ethysorb (aluminium oxide and potassium permanganate; Stay Fresh Ltd, London, UK). In each experiment, at least three potted plants or at least five flowers were used per chamber, and two replicate chambers were used. Each species was tested at least twice.
In additional tests with Cymbidium, inflorescences were placed in vials containing deionized water and put in airtight 1 x 1 m perspex boxes into which ethylene was injected, either as a pulse of 3 ppm for 24 h on day 0–1 or as a continuous 0·3 ppm treatment starting on day 14. Two replicate boxes were used, with five inflorescences in each. The temperature was held at 20 ± 1 °C, and relative humidity (RH) was about 80 %. Excess carbon dioxide was absorbed by the presence of 10 g calcium hydroxide in the boxes. The two control boxes contained Ethysorb to remove ethylene.
Classification of ethylene sensitivity
Following ethylene treatment, potted plants and flowers were placed under controlled environmental conditions of 12 h fluorescent white light (15 µmol m–2 s–1) and 12 h darkness, 60 % RH and 20 ± 1 °C. Observations were made daily. The effects were expressed as the percentage of the time taken for the symptoms to occur, compared with the controls. For example, a 100 % response indicates that clear symptoms occurred within 1 d of treatment. Similarly, a 50 % response indicates that the symptoms occurred within half the time taken by the controls. These percentages were then grouped according to five classes as follows: class 0, no response (not sensitive); class 1, up to 33 % effect (low sensitivity); class 2, between 33 and 66 % effect (intermediate sensitivity); class 3, 66–99 % effect (high sensitivity); and class 4, 100 % response by the end of 24 h treatment (very high sensitivity).
Taxonomic classification
Plants were grouped into families according to the classification of the Angiosperm Phylogeny Group (APG, 1998), which is partially based on molecular techniques. Compared with older classifications, such as that of Heywood (1978), APG (1998) subtracts the basal-most angiosperms from the dicotyledons, and calls the remaining dicots ‘eudicotyledons’.
Statistical analysis
Quantitative results were compared by ANOVA and t-tests (P > 0·05), using the GENSTAT V program. Experiments were duplicated at least twice.
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RESULTS |
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Ethylene sensitivity
A relatively small number of the approx. 300 species tested showed floral abscission. It was observed in only 28 of the approx. 250 genera tested. Abscission of flowers was generally highly sensitive to exogenous ethylene (Table 1). A notable exception was Cymbidum: inflorescences treated with ethylene exhibited rapid discolouration, starting at the flower lip and then extending to the whole flower. The time taken for 50 % of all open flowers to fall was not affected by ethylene treatment (Table 2). In the Cymbidum cultivars ‘Gymer Cookbridge’ and ‘Holkinson Piedmont’, 50 % of the flowers had abscised after 17 and 22 d, respectively. This is long after the 24 h exposure to ethylene. This lack of effect could relate to the lack of sensitivity of the abscission zones to ethylene at the time of ethylene exposure, but the abscission zones could become more sensitive later on. To test this, another experiment was performed in which the ethylene treatment began on day 14, about 5 d prior to flower fall, and continued until more than half of the flowers in all inflorescences had fallen. Flower fall was still not affected by ethylene following this delayed treatment (Table 2).
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Types of response
Flowers usually fell when their petals were fully turgid, but in a few species in the Solanaceae (Lycopersicon spp. and Solanum spp.) petals had wilted by the time of flower abscission. Flowers on Plumbago auriculata plants showed petal wilting and flower closure concomitant with flower abscission.
Shedding of flowers was also observed in plants growing in the garden or field, e.g. Yucca, Lathyrus and Oenothera. In the latter species, the flowers of plants growing in the field usually fell after petal wilting, whereas following exposure to exogenous ethylene, the petals were turgid when the flowers were shed. Symptoms observed in the field may therefore differ from those observed following ethylene treatment.
Relationship with taxonomic groups
Flower abscission occurred in monocotyledons and eudicotyledons. A comparison of the species in Table 1 with lists of all species tested (Woltering and van Doorn, 1988; van Doorn, 2001) showed that flower fall was not consistent within any of the families studied (results not shown).
Relationship with ethylene effects in petals
In the monocotyledons tested, flower fall occurred in several families in which most species exhibit ethylene-insensitive petal wilting, but also occurred in the Orchidaceae which generally exhibit ethylene-sensitive petal wilting (Table 1).
Flower fall in the eudicotyledons tested occurred in families in which the flowers generally exhibit ethylene-sensitive petal wilting or petal abscission. It was also found in the Saxifragaceae, which contain species that exhibit ethylene-insensitive petal wilting (Table 1). In some species in the eudicotyledons the effects of ethylene exposure on petals could not be assessed as the flowers tested all abscised within the 24 h period of ethylene treatment (Begoniaceae, Euphorbiaceae, Myrtaceae and Onagraceae; Table 1).
Some flowers showed hastened closure or a colour change after ethylene treatment. These petal changes showed no relationship with flower fall (results not shown).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Although it is often assumed that abscission of plant parts is regulated by endogenous ethylene, and is therefore sensitive to ethylene treatment, Addicott (1982) reported that ethylene had little effect on abscission in some vegetative tissues. Similarly, we have previously found that abscission of generative organs such as petals is generally sensitive to ethylene, but that it is insensitive in some species (Sexton et al., 2000; van Doorn, 2001). We now report that flower abscission, although generally ethylene sensitive (Table 1), shows no response to ethylene in Cymbidium flowers (Table 2). Similarly, preliminary experiments also indicate ethylene-insensitive flower fall in Dendrobium orchids (S. Ketsa, pers. comm. 2001). This indicates that ethylene-insensitive flower abscission occurs in some species in the Orchidaceae.
In some experiments with Cymbidium, the flowers abscised after symptoms of senescence. Thus, flower fall in this species could be taken to be a result of cell death following perianth senescence. However, there are three reasons for assuming that the fall is due to true abscission: (1) flower fall also occurred in experiments in which flowers did not show any visible symptoms of senescence; (2) the separation zone was smooth and clear-cut; and (3) abscission always occurred at the same place, about 0.5 cm above the pedicel base.
Comparison of Table 1 with the species tested (published previously) shows that flower abscission was not consistently found in all species of a family. Nevertheless, in some families such as the Solanaceae, flower fall seems to be relatively frequent. The literature indicates that flower fall is also rather frequent in families such as Agavaceae (it was observed in at least six genera besides Yucca investigated here), Arecaceae (observed in Phoenix, Rhopalostylis, Washingtonia), Asphodelaceae (also in Gasteria and Haworthia, besides Kniphofia tested here), Euphorbiaceae (Hevea, Mercurialis, Ricinus, in addition to Euphorbia examined here), Fabaceae (Cicer, Glycine, Lupinus, Medicago, Phaseolus, Vicia, Vigna, in addition to three genera tested here) and Rosaceae (Malus, Prunus, Pyrus, Rosa) (McKenzie and Lovell, 1992; van Doorn and Stead, 1997; Saxena et al., 2000).
As the number of species tested in each family was small, flower abscission may occur in several families in which it was not observed during the present study, both in the monocotyledons and eudicotyledons. We did not observe flower fall in several families of monocotyledons (Alismataceae, Alstroemeriaceae, Amaryl lidaceae, Cannaceae, Colchicaceae, Commelinaceae, Haemodoraceae, Hemerocallidaceae, Hyacinthaceae and Iridaceae). However, the literature indicates that some flower fall occurs in the Amaryllidaceae (Clivia miniata), Cannaceae (Canna x generalis), Hemerocallidaceae (Hemerocallis) and Iridaceae (Diplarrhena moraea, Iris wattii, Sysirynchium striatum) (McKenzie and Lovell, 1992; van Doorn and Stead, 1997). Some of these species were tested in the present experiments (Canna, Hemerocallis and Hosta), but no flower fall was observed. It is not clear from the reports in the literature whether flower fall occurred before or after fertilization. In the present experiments flowers had not been pollinated—and thus not fertilized—when exposed to ethylene. Some flowers may not be sensitive to ethylene at this stage, whereas they are more sensitive following fertilization.
The literature reports floral fall in several other species in the monocotyledons, for example in Ophiopogon jaburan (Convallariaceae), Sansevieria trifasciata (Draceanaceae), Maranta leuconora (Marantaceae), Dianella nigra and Phormium tenax (Phormiaceae). The effect of ethylene in these flowers has not been reported to date (McKenzie and Lovell, 1992). In the monocotyledons, therefore, flower fall occurs in many families. This is in contrast with petal fall, which is uncommon in the monocots.
In the eudicotyledons, flower fall was not observed in several families tested (Acanthaceae, Aizoaceae, Boraginaceae, Campanulaceae, Convolvulaceae, Crassulaceae, Cruciferae, Ericaceae, Fumariaceae, Gentian aceae, Gesneriaceae, Hydrangeaceae, Lobeliaceae, Oleaceae, Papaveraceae, Portulacaceae, Primulaceae, Rubiaceae, Scrophulariaceae and Valerianaceae). The literature, however, does report flower fall in the Primulaceae (Anagallis spp. and Primula spp.) and the Scrophulariaceae (Antirrhinum majus, Verbascum spp. and Veronica spp.) (Wang et al., 1977; van Doorn and Stead, 1997). It may also occur in other families.
The wilting symptoms accompanying flower fall may depend on conditions during the experiment. In most species the flowers fell while still turgid, but in some they showed wilting or withering at the time of fall. When Cymbidium flowers were held at 20 °C and 60 % RH, flowers were shed after they began to wilt and turned brown at the distal parts. In the experiments shown in Table 2, however, the flowers fell when still completely turgid. In these tests, inflorescences were placed in perspex boxes where the temperature was 20 °C but RH was close to 100 %. This may also explain differences between ethylene experiments and symptoms observed in the field (see Results). The RH during the 24 h of ethylene exposure was high, whereas it was 60 % during the days thereafter.
It is concluded that floral abscission occurs in several families in the monocotyledons and eudicotyledons. This is in contrast to petal abscission which is common in the latter and rare in the former group. Floral fall is apparently not consistent within families. Like petal abscission, flower abscission is generally sensitive to ethylene. However, at least in Cymbidium, it was ethylene insensitive. Therefore, floral abscission, seems to be generally—but not universally—regulated by endogenous ethylene.
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ACKNOWLEDGEMENTS |
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I thank Jan J. Bos (Department of Taxonomy, Wageningen University) for permission to pick flowers in the botanical garden and for relevant taxonomic literature, and Ernst Woltering for valuable advice.
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LITERATURE CITED |
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Addicott FT. 1982. Abscission. Berkeley: University of California Press.
Aloni B, Karni L, Zaidman Z, Schaffer AA. 1996. Changes of carbohydrates in pepper (Capsicum annuum L.) flowers in relation to their abscission under different shading regimes. Annals of Botany 78: 163–168.
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van Doorn WG. 2001. Categories of petal senescence and abscission: a re-evaluation. Annals of Botany 87: 447–456.
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Wang CY, Baker JE, Hardenburg RE, Lieberman M. 1977. Effects of two analogs of rhizobitoxine and sodium benzoate on senescence of snapdragons. Journal of the American Society of Horticultural Science 102: 517–520.
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