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Does Ethylene Treatment Mimic the Effects of Pollination on Floral Lifespan and Attractiveness?

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Does Ethylene Treatment Mimic the Effects of Pollination on Floral Lifespan and Attractiveness? Annals of Botany 89: 375±383, 2002 doi:10.1093/aob/mcf053, available online at www.aob.oupjournals.org Does Ethylene Treatment Mimic the Effects of Pollination on Floral Lifespan and Attractiveness? WOUTER G. VAN DOORN1 1Agrotechnological Research Institute (ATO), Wageningen University and Research Centre, PO Box 17, 6700 AA Wageningen, The Netherlands Received: 21 June 2001 Returned for revision: 10 November 2001 Accepted: 15 December 2001 In some species pollination may result in rapid changes in perianth colour and form (petal senescence and abscission, ¯ower closure), rendering the ¯owers less attractive to pollinators. It has been suggested that this effect is mediated by ethylene. Flowers from about 200 species and 50 families were exposed to ethylene (3 ppm for 24 h at 20 °C). The effects on petal senescence and abscission have been described previously. Flower closure and perianth colour changes were generally ethylene-sensitive, but responses showed no consistency within families. Several ¯owers known to respond to pollination by rapid cessation of attractiveness were also exposed to ethylene: this produced the same effect as pollination, both on ¯ower colour and form. Species that respond to pollination by changing ¯ower form or colour were found exclusively in families in which the species are generally ethylene-sensitive (with regard to changes in perianth form and colour). However, several families are generally ethylene-sensitive but contain no species reported to respond to pollination. ã 2002 Annals of Botany Company Key words: Ethylene sensitivity, ¯ower closure, ¯ower longevity, petal abscission, petal colour, petal wilting, petal withering, petal senescence, pollination. INTRODUCTION Woltering et al., 1995, 1997; Hilioti et al., 2000; Llop- Flowers are attractive to pollinators because they provide a Tous et al., 2000). Many ¯owers change colour when their stigmas become source of food, and they advertise this by their form and colour. Petals of ¯owers that remain unpollinated eventually non-receptive. This change coincides with the cessation of nectar production or pollen availability. Pollinators avoid wither or abscise; this may be preceded by a change in ¯owers that no longer produce a reward, and this results in colour or by ¯ower closure. In some species pollination increased pollinator ef®ciency. Retention of the perianth reportedly advances these changes in ¯ower colour or form, beyond stigma receptivity (and pollen availability) is but in other species it does not (Motten, 1986). Where suggested to increase the plant's longer-distance attractive- pollination has an effect, the time course of the symptoms ness to pollinators, whereas at close range the pollinators may depend on the pollen load (Stead and Moore, 1983). It has been suggested that advanced petal wilting and will discriminate between the ¯oral colour phases. Although changes in petal colour occur towards the end of ¯ower life abscission, following pollination, is mediated by endo- genous ethylene, although experimental evidence has been in at least 74 plant families (Weiss, 1991), an effect of pollination on petal colour has been described in only a reported for a few species only. Inhibitors of ethylene few species (Gori, 1983). Similarly, only a few studies synthesis or ethylene action prevented the effect of pollin- mention an effect of ethylene on ¯ower colour, for example ation on petal wilting in carnation (Nichols et al., 1983; in Petunia (Solanaceae; Gilissen, 1977), Cymbidium Larsen et al., 1995), orchids (O'Neill et al., 1993; Porat (Orchidaceae; Woltering and Somhorst, 1990) and et al., 1995) and Petunia (Hoekstra and Weges, 1986). In Lupinus (Fabaceae; Stead and Reid, 1990). In Cymbidium Digitalis (Stead and Moore, 1983) and Pelargonium (Hilioti and Lupinus, inhibitors of ethylene synthesis and ethylene et al., 2000), anti-ethylene compounds prevented the action prevented the colour change, indicating that the pollination effect on petal fall. Thus, although ethylene changes are produced by endogenous ethylene. seems to be involved in the production and/or the effect of Several ¯owers close permanently at the end of their the pollination signal, the nature of the agent that is lifespan. Pollination may hasten closure, e.g. in several transported from the stigma to the petals is still unclear, and orchids (Fitting, 1909). Earlier ¯ower closure in may differ between species. It has been suggested that the Phalaenopsis, following pollination, was prevented by signal transported is electrical in nature (Spanjers, 1977), or inhibitors of ethylene action and ethylene synthesis, that it is ACC, ethylene or other factors affecting ethylene indicating a role of endogenous ethylene (Porat et al., production or ethylene sensitivity (Porat et al., 1995; 1994). For correspondence. Fax: +31±317±475347, e-mail: w.g.vandoorn@ Ethylene treatment of ¯owers results in rapid petal ato.wag-ur.nl wilting or abscission, depending on the species. Petal ã 2002 Annals of Botany Company 376 van Doorn Ð Comparing the Effects of Ethylene Treatment and Pollination on Petals wilting has been found to be ethylene-sensitive or insensi- potted plants or at least ®ve ¯owers were used per chamber, tive, and these two categories were consistent within and two replicate chambers were used. Each species was families or subfamilies. Species in which pollination tested at least twice. Data on ¯ower closure and ¯ower advances petal wilting tended to belong to families in colour were collected from experiments performed on which most species showed ethylene-sensitive wilting. approx. 200 species (van Doorn, 2001). The present data Many other ¯owers exhibit petal fall, which is generally have thus been collected from the same plants as previously highly ethylene-sensitive. Petal fall is also generally con- published data on petal senescence and abscission. When sistent within families or subfamilies (Woltering and van comparing data on commercial species from different Doorn, 1988; van Doorn, 2001). These data, and reports on experiments, the cultivars used may have differed as the the effects of ethylene on petal colour and ¯ower closure, cultivar names were not always known. have led to speculation that the effects of pollination on ¯ower form and colour are generally mediated by endogenous ethylene (van Doorn, 1997). This suggestion Classi®cation of ethylene sensitivity has now been investigated further. A number of species that After ethylene treatment, the potted plants and ¯owers are known to terminate pollinator attractiveness rapidly were placed under controlled environmental conditions of following pollination were treated, whilst unpollinated, with 12 h ¯uorescent white light (15 mmol m±2 s±1) and 12 h exogenous ethylene. If the effects of pollination on ¯ower darkness, 60 % relative humidity and 20 6 1 °C. Changes in form and colour are indeed mediated by endogenous the perianth were determined daily. Ethylene sensitivity was ethylene then each of these ¯owers should be sensitive expressed as described previously (van Doorn, 2001). to exogenous ethylene and the symptoms of ethylene Effects were expressed as the percentage of the time taken treatment should be similar to the changes observed after for the symptoms to occur, compared with the controls. For pollination. example, a 100 % response indicates that clear symptoms A detailed comparison between the effects of ethylene occurred in all plants within 1 d of treatment. Similarly, a and pollination requires data on ¯ower colour and closure. 50 % response indicates that the symptoms occurred within Since there are limited data in the literature, ¯ower closure half the time taken by the controls. These percentages were and petal colour were studied here in approx. 200 species then grouped into ®ve classes as follows: class 0, no from 50 families. response (not sensitive); class 1, up to 33 % effect (low sensitivity); class 2, between 33 and 66 % effect (inter- mediate sensitivity); class 3, 66±99 % effect (high sensi- MATERIALS AND METHODS tivity); class 4, ethylene response already dramatic at the end of treatment (very high sensitivity). Plant material Potted plants were bought at a ¯ower auction at Aalsmeer (The Netherlands) or at retail outlets in Wageningen (The Taxonomic classi®cation Netherlands). The plants were well watered, and used for Plants were grouped into families according to the experiments on the day of purchase. Several other species classi®cation of the Angiosperm Phylogeny Group (APG, were obtained as cut parts, either from the Botanical Garden 1998), which is partially based on molecular techniques. of the Agricultural University in Wageningen, or from the Compared with older classi®cations such as that of ®eld. After severing, the ¯owering stems were immediately Heywood (1978), APG (1998) subtracts the basal-most placed in water. Stems were transported to the laboratory angiosperms from the dicotyledons, and calls the remaining within an hour of cutting, where they were used immedi- dicots `eudicotyledons'. Compared with the system of ately. Cut ¯owers from a few other species were bought at Heywood (1978), Dahlgren et al. (1985) separate the the Aalsmeer ¯ower auction. These were taken to the Alstroemeriaceae from the Amaryllidaceae and group laboratory (without water) within 3 h of purchase. The stems the Liliaceae in several families. APG (1998) largely of these ¯owers were recut under water and used for con®rmed the classi®cation of the monocotyledons pro- experimentation
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