Annals of Botany 89: 375-383, 2002
© 2002 Annals of Botany Company
Does Ethylene Treatment Mimic the Effects of Pollination on Floral Lifespan and Attractiveness?
1Agrotechnological 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: 21 June 2001; Returned for revision: 10 November 2001; Accepted: 15 December 2001.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
In some species pollination may result in rapid changes in perianth colour and form (petal senescence and abscission, flower closure), rendering the flowers 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 flowers known to respond to pollination by rapid cessation of attractiveness were also exposed to ethylene: this produced the same effect as pollination, both on flower colour and form. Species that respond to pollination by changing flower 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.
Key words: Ethylene sensitivity, flower closure, flower longevity, petal abscission, petal colour, petal wilting, petal withering, petal senescence, pollination.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
Flowers are attractive to pollinators because they provide a source of food, and they advertise this by their form and colour. Petals of flowers that remain unpollinated eventually wither or abscise; this may be preceded by a change in colour or by flower closure. In some species pollination reportedly advances these changes in flower colour or form, but in other species it does not (Motten, 1986). Where pollination has an effect, the time course of the symptoms may depend on the pollen load (Stead and Moore, 1983).
It has been suggested that advanced petal wilting and abscission, following pollination, is mediated by endogenous ethylene, although experimental evidence has been reported for a few species only. Inhibitors of ethylene synthesis or ethylene action prevented the effect of pollination on petal wilting in carnation (Nichols et al., 1983; Larsen et al., 1995), orchids (O’Neill et al., 1993; Porat et al., 1995) and Petunia (Hoekstra and Weges, 1986). In Digitalis (Stead and Moore, 1983) and Pelargonium (Hilioti et al., 2000), anti-ethylene compounds prevented the pollination effect on petal fall. Thus, although ethylene seems to be involved in the production and/or the effect of the pollination signal, the nature of the agent that is transported from the stigma to the petals is still unclear, and may differ between species. It has been suggested that the signal transported is electrical in nature (Spanjers, 1977), or that it is ACC, ethylene or other factors affecting ethylene production or ethylene sensitivity (Porat et al., 1995; Woltering et al., 1995, 1997; Hilioti et al., 2000; Llop-Tous et al., 2000).
Many flowers change colour when their stigmas become non-receptive. This change coincides with the cessation of nectar production or pollen availability. Pollinators avoid flowers that no longer produce a reward, and this results in increased pollinator efficiency. Retention of the perianth beyond stigma receptivity (and pollen availability) is suggested to increase the plant’s longer-distance attractiveness to pollinators, whereas at close range the pollinators will discriminate between the floral colour phases. Although changes in petal colour occur towards the end of flower life in at least 74 plant families (Weiss, 1991), an effect of pollination on petal colour has been described in only a few species (Gori, 1983). Similarly, only a few studies mention an effect of ethylene on flower colour, for example in Petunia (Solanaceae; Gilissen, 1977), Cymbidium (Orchidaceae; Woltering and Somhorst, 1990) and Lupinus (Fabaceae; Stead and Reid, 1990). In Cymbidium and Lupinus, inhibitors of ethylene synthesis and ethylene action prevented the colour change, indicating that the changes are produced by endogenous ethylene.
Several flowers close permanently at the end of their lifespan. Pollination may hasten closure, e.g. in several orchids (Fitting, 1909). Earlier flower closure in Phalaenopsis, following pollination, was prevented by inhibitors of ethylene action and ethylene synthesis, indicating a role of endogenous ethylene (Porat et al., 1994).
Ethylene treatment of flowers results in rapid petal wilting or abscission, depending on the species. Petal wilting has been found to be ethylene-sensitive or insensitive, and these two categories were consistent within families or subfamilies. Species in which pollination advances petal wilting tended to belong to families in which most species showed ethylene-sensitive wilting. Many other flowers exhibit petal fall, which is generally highly ethylene-sensitive. Petal fall is also generally consistent within families or subfamilies (Woltering and van Doorn, 1988; van Doorn, 2001). These data, and reports on the effects of ethylene on petal colour and flower closure, have led to speculation that the effects of pollination on flower form and colour are generally mediated by endogenous ethylene (van Doorn, 1997). This suggestion has now been investigated further. A number of species that are known to terminate pollinator attractiveness rapidly following pollination were treated, whilst unpollinated, with exogenous ethylene. If the effects of pollination on flower form and colour are indeed mediated by endogenous ethylene then each of these flowers should be sensitive to exogenous ethylene and the symptoms of ethylene treatment should be similar to the changes observed after pollination.
A detailed comparison between the effects of ethylene and pollination requires data on flower colour and closure. Since there are limited data in the literature, flower closure and petal colour were studied here in approx. 200 species from 50 families.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
Plant material
Potted plants were bought at a flower auction at Aalsmeer (The Netherlands) 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. Stems were transported to the laboratory within an hour of cutting, where they were used immediately. Cut flowers from a few other species were bought at the Aalsmeer flower auction. These were taken to the laboratory (without water) within 3 h of purchase. The stems of these flowers were recut under water and used for experimentation the same day.
Ethylene treatment
Treatments were carried out as described previously (van Doorn, 2001). Briefly, ethylene was injected into closed 70 l stainless steel chambers held at 20 ± 1 °C, in darkness, exposing the plants or flowers to 3 (2·8–3·3) ppm for 24 h. Excess carbon dioxide was absorbed by 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 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. Data on flower closure and flower colour were collected from experiments performed on approx. 200 species (van Doorn, 2001). The present data have thus been collected from the same plants as previously published data on petal senescence and abscission. When comparing data on commercial species from different experiments, the cultivars used may have differed as the cultivar names were not always known.
Classification of ethylene sensitivity
After ethylene treatment, the 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 % relative humidity and 20 ± 1 °C. Changes in the perianth were determined daily. Ethylene sensitivity was expressed as described previously (van Doorn, 2001). 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 in all plants 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 into 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); class 4, ethylene response already dramatic at the end of 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’. Compared with the system of Heywood (1978), Dahlgren et al. (1985) separate the Alstroemeriaceae from the Amaryllidaceae and group the Liliaceae in several families. APG (1998) largely confirmed the classification of the monocotyledons proposed by Dahlgren et al. (1985). In the eudicotyledons, APG (1998) include the former Lobeliaceae in the Campanulaceae, and show that Saxifragaceae is a highly polyphyletic group. APG place the Ribesioideae subfamily of the Saxifragaceae (sensu Heywood) in a separate family, the Grossulariaceae. APG uses the synonyms Asteraceae for Compositae, Fabaceae for Leguminosae and Lamiaceae for Labiatae.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
Effects of ethylene on flower closure
Of the 200 species tested, ethylene treatment resulted in rapid flower closure in a few monocotyledonous species and in several eudicotyledonous plants (Table 1). In the monocotyledonous flowers tested, closure apparently did not occur throughout any of the families. Flower closure in Hemerocallis and Lachenalia occurred at the end of flower life (concomitant with wilting) and closure did not respond to ethylene, and in Cyrtanthus (Amaryllidaceae) ethylene had only a small effect. In several other monocotyledonous flowers, such as Bloomeria, Galtonia and some Orchidaceae, flower closure was clearly advanced by ethylene. In eudicotyledonous flowers, closure generally responded to ethylene. Rapid flower closure after ethylene treatment was observed in all species tested in the Aizoaceae, Convolvulaceae, Plumbaginaceae and Portulaceae. Rapid closure also occurred in a few species in the Campanulaceae, Crassulaceae and Gentianaceae. In contrast, no response was observed in Exacum affine (Gentianaceae), whilst in Sabatia (Gentianaceae) and Crassula (Crassulaceae) the response was only slightly ethylene-sensitive.
|
Effects of ethylene on petal colour
Following exposure of approx. 200 species to exogenous ethylene, colour changes in the perianth were observed in the Orchidaceae, but not in any other monocotyledonous flowers studied. Colour changes following exposure to ethylene were observed in a few eudicotyledonous families, such as the Boraginaceae (all generea tested), Caprifoliaceae (one genus) and Crassulaceae (two genera) (Table 2). A change in colour was usually followed by wilting/withering of the petals. Colour changes that occurred concomitantly with petal wilting have not been noted separately, as they may be due to the changes accompanying wilting, such as water loss.
|
Colour changes (prior to petal wilting or petal abscission) and flower closure generally occurred in different species, but two species tested, both in the Crassulaceae, showed both a colour change and flower closure. A similar finding was reported in some orchid species (Fitting, 1909).
Comparison of pollination and ethylene effects
Table 3 lists a number of species that are reported to show advanced petal wilting, petal abscission, a rapid colour change or flower closure following pollination. After treatment with ethylene the observed symptoms were the same as those following pollination. In all species studied the responses were highly ethylene-sensitive.
|
In Table 4 a comparison is made between reports in the literature on the effects of pollination in a genus, and the effects of ethylene treatment on species in the same genus. Several reports on the effects of pollination date from the 19th century (or even before) and species’ names may have changed since. Nomenclature has not been investigated in detail. In other cases the plants have not been identified at the species level. Table 4 shows that, even at the genus level, high consistency was found between the symptoms observed following pollination and the effects of ethylene treatment. Again, the symptoms were highly ethylene-sensitive. One exception was noted: in Pulmonaria officinalis a colour change has been observed following pollination (Süssenguth, 1936), but in the present experiments petal abscission following ethylene exposure was very rapid, apparently precluding a colour change.
|
Taxonomic comparison of the effects of ethylene treatment and pollination
Table 5 compares the families in which we investigated responses of petals to ethylene treatment with data regarding effects of pollination on floral attractiveness. Species known to respond to pollination by a change in flower form or colour are restricted to families that show similar changes after ethylene treatment. Table 5 also shows several families in which the flowers generally exhibit an ethylene-sensitive change in petal form or colour, whereas no incidence has been reported for similar pollination effects.
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
In many species, flower closure was sensitive to ethylene (Table 2). However, in some species ethylene had only a slight—or no—effect on closure. Interestingly, no effect of pollination on flower closure has been reported in these ethylene-insensitive species. A pollination effect on closure may therefore be absent in this group of species.
In the present experiments, flower closure was not observed in any of the families in which petals abscise. This is apparently due both to the experimental conditions and to the high sensitivity of petal abscission to exogenous ethylene: in many species the petals had already dropped by the end of the ethylene treatment, and in others the petals shattered within a day of treatment. Flower closure was observed in several families in which ethylene-sensitive petal wilting is found, and was absent from a number of (sub)families which show ethylene-insensitive petal wilting (e.g. Dipsacaceae, the Ericoideae subfamily in the Ericaceae, Fumariaceae, Primulaceae and Saxifragaceae). However, in some species in which petal wilting is ethylene-insensitive (such as Galtonia and Sempervivum), ethylene rapidly induced flower closure.
A colour change, after ethylene treatment, was generally ethylene-sensitive, but in one genus tested (Sedum) it was not. In Pulmonaria species the change from red to blue also occurs irrespective of pollination (Süssenguth, 1936; Oberrath et al., 1995), and ethylene was found to have no effect on colour (van Doorn, 2001). Thus, when it comes to petal colour, a relationship between the effects of ethylene and pollination seems possible, as is the case for flower closure. When the petals are insensitive to ethylene, pollination also seems to have no effect.
In our tests, colour changes preceded petal wilting (or wilting that occurred concomitantly with abscission), but did not precede petal abscission. This may be due to the experimental conditions, as discussed above for flower closure. Colour changes, after ethylene treatment, were found in the Orchidaceae, but were not observed in any other monocotyledon family tested. The species in these monocotyledonous families are ethylene-insensitive with regard to petal wilting. Only a few species in the eudicotyledons tested showed a colour change, although the eudicotyledons comprise many families in which petal wilting is generally ethylene-sensitive. In these tests we observed changes that were clear to the naked eye. Some species exhibit a small colour change in the nectar guides following pollination, which is often adequate to inform the pollinating insects (Gori, 1983). Other flowers may respond by a change in the ultraviolet range (Silberglied, 1979; Gori, 1983). Changes in the UV range and subtle colour changes in the visible part of the spectrum may also occur following ethylene treatment; these were not investigated in the present study.
In species where pollination has an effect on flower colour and form (time to petal wilting, petal abscission or floral closure), ethylene treatment produced the same visible symptoms as pollination, and induced these symptoms rapidly. Although only a limited number of species were tested, the results are consistent with the idea that the effect of pollination on perianth form and colour is generally mediated by endogenous ethylene (Table 3). This suggestion requires further testing, using ethylene inhibitors. The responses have also been tested on some representative species within the same genus (Table 4). The results show a good fit between pollination and ethylene effects and, although this evidence is weaker than that from a comparison of species, it does not contradict the hypothesis.
The literature shows some examples in which the responses found after pollination are somewhat different, at least in time, from the response found in unpollinated flowers. One example is Cyclamen, where the petals wilt and desiccate in unpollinated flowers, but following pollination the petals show rapid fall while still turgid. An abscission zone is apparently activated by ethylene, as a result of pollination, whereas in unpollinated flowers the abscission zone is not activated (Halevy et al., 1984). The eventual wilting of unpollinated Cyclamen flowers may be similar to that occurring in flowers in which petal wilting is ethylene-insensitive. Other examples are Potentilla argentea and P. nepalensis. Here the petals of unpollinated flowers reportedly remain turgid and finally fall, whereas those of pollinated flowers wilt rapidly and abscise immediately thereafter (Gärtner, 1844). Petal fall in unpollinated flowers may be due not to a well-regulated abscission process, but simply to tearing at the (usually small) petal base. This tearing occurs as a result of growth of the subtending tissue (Reiche, 1885; van Doorn and Stead, 1997). This process may also occur both in pollinated and unpollinated flowers. One would expect more instances of a such a discrepancy between these symptoms in pollinated and unpollinated flowers, but these have apparently not been reported by others, nor have they been found in our experiments (Woltering and van Doorn, 1988; van Doorn, 2001). Similarly, in some species flower closure or a change in colour may occur in pollinated flowers, due to increased ethylene production, whereas no such changes occur in unpollinated flowers.
Table 5 shows that species known to respond to pollination by a change in floral form or colour are restricted to families that exhibit similar changes after ethylene treatment. This relationship is substantiated by reports of a lack of a pollination effect on floral lifespan (for example in the Fumariaceae; Schemske et al., 1978). However, the effects of pollination reported to date, and those of ethylene, do not coincide, as there are many (sub)families in which changes in floral form and colour are ethylene-sensitive, while there are no reports of pollination affecting the timing of these floral changes in these groups. There may be several reasons for this discrepancy. First, the number of species in which pollination reportedly has an effect on flower form or colour is small compared with the number of species in which the petals are known to respond to ethylene. Thus, the effects of pollination may have received less attention. Secondly, there are biological reasons for the absence of a pollination effect. Generally, pollination does not affect flower form or colour in species in which the female phase precedes the male phase (protogynous flowers), as is the case in many families. Additionally, pollination tends not to shorten floral attractiveness in flowers that are short-lived, or in which the female phase is very short. Modulation of floral attractiveness apparently confers little benefit in these species. Many flowers, perhaps up to one-third of all conspicuous ones, last only a day or less (Ashman and Schoen 1976). Families that contain many short-lived flowers include the Commelinaceae, Convolvulaceae and Papaveraceae. Thirdly, the reason behind the evolution of ethylene-sensitivity in the perianth may not be to modulate floral attractiveness. Infection of petals by fungi, for example, generally results in ethylene production, which in turn leads to rapid petal abscission thus removing the infection.
The question as to the biological meaning of the lack of ethylene-sensitivity also remains unanswered. Flowers that do not respond to ethylene/pollination by changes in form and colour are relatively rare in the eudicotyledons. In contrast, numerous families in the monocotyledons exhibit neither ethylene-sensitivity nor show an effect of pollination on floral form and colour. Why this is so is unclear. Many aspects of floral biology vary among monocotyledons and eudicotyledons, such as the trait of petal abscission (almost exclusively ethylene-sensitive and almost exclusively found in eudicotyledons) vs. petal wilting (in monocotyledons and eudicotyledons). The reproductive strategy may also have a bearing on the difference in ethylene sensitivity of petals between monocotyledons and eudicotyledons. The former probably show more vegetative reproduction, by rhizomes, corms and bulbs. Retention of (turgid) pollinated flowers in a group of flowering stems enhances a plant’s long-distance attractiveness to pollinators (Gori, 1983). This may be a partial explanation for the virtual absence of pollination-induced changes in floral form and colour in the monocyledons. Insofar as ethylene-sensitivity in petals relates to pathogen removal or isolation, it is unclear why so many species (including almost all monocotyledons) do not have this capacity.
|
CONCLUSIONS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
The results lend support to the idea that pollination-induced changes in flower colour and floral form (due to flower closure, or to wilting or abscission of petals) are generally regulated by endogenous ethylene. The results also show a relationship between some physiological traits and taxonomy. The effects of ethylene on floral colour and floral closure are not consistent within families or subfamilies, unlike the previously reported effects of ethylene on petal senescence and abscission. In addition, the reported effects of ethylene and pollination on flower form and colour were found to coincide in some families but not in others.
|
ACKNOWLEDGEMENT |
|---|
I am grateful to Jan J. Bos (Department of Taxonomy, Wageningen Agricultural University) for permission to use flowers from the botanical garden and for relevant taxonomic literature.
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSLITERATURE CITED |
|---|
-
APG (The Angiosperm Phylogeny Group). 1998. An ordinal classification for the families of the flowering plants. Annals of the Missouri Botanical Garden 85: 531–553.[CrossRef][Web of Science]
Ashman TL, Schoen DJ. 1996. Floral longevity: fitness consequences and resource costs. In: Lloyd DG, Barrett SCH, eds. Floral biology. New York: Chapman and Hall, 112–139.
Dahlgren RMT, Clifford HT, Yeo PF. 1985. The families of the monocotyledons: structure, evolution and taxonomy. Berlin: Springer Verlag.
Fitting H. 1909. Die Beeinflussung der Orchideenblüten durch die Bestäubung und andere Umstände. Zeitschrift für Botanik 1: 1–86.
Gilissen LJW. 1977. Style-controlled wilting of the flower. Planta 133: 275–280.[CrossRef]
Gori DF. 1983. Post-pollination phenomena and adaptive floral changes. In: Jones CE, Little RJ, eds. Handbook of experimental pollination biology. New York: Van Nostrand Reinhold, 31–49.
Halevy AH, Whitehead CS, Kofranek AM. 1984. Does pollination induce corolla abscission of Cyclamen flowers by promoting ethylene production? Plant Physiology 75: 1090–1093.
Heywood VH. 1978. Flowering plants of the world. Oxford: Oxford University Press.
Hilioti Z, Richards C, Brown KM. 2000. Regulation of pollination-induced ethylene and its role in petal abscission of Pelargonium x hortorum. Physiologia Plantarum 109: 322–332.[CrossRef]
Hoekstra FA, Weges R. 1986. Lack of control by early pistillate ethylene of the accelerated wilting of Petunia hydrida flowers. Plant Physiology 80: 403–408.
Ichimura K, Goto R. 2000. Acceleration of senescence by pollination of cut ‘Asuka-no-nami’ Eustoma flowers. Journal of the Japanese Society for Horticultural Science 69: 166–170.
Larsen PB, Ashworth EN, Jones ML, Woodson WR. 1995. Pollination-induced ethylene in carnation: role of pollen tube growth and sexual compatibility. Plant Physiology 108: 1405–1412.[Abstract]
Llop-Tous I, Barry CS, Grierson D. 2000. Regulation of ethylene biosynthesis in response to pollination in tomato flowers. Plant Physiology 123: 971–978.
Motten AF. 1986. Pollination ecology in the spring wildflower community of a temperate deciduous forest. Ecological Monographs 56: 21–42.[CrossRef]
Nichols R, Bufler G, Mor Y, Fujino DW, Reid MS. 1983. Changes in ethylene and 1-aminocyclopropane-1-carboxylic acid content of pollinated carnation flowers. Journal of Plant Growth Regulation 2: 1–8.
Oberrath R, Zanke C, Böhning-Gaese K. 1995. Triggering and ecological significance of floral color change in lungwort (Pulmonaria spec.) Flora 190: 155–159.
O’Neill SD, Nadeau JA, Zhang XS, Bui AQ, Halevy AH. 1993. Interorgan regulation of ethylene biosynthetic genes by pollination. Plant Cell 5: 419–432.[Abstract]
Porat R, Borochov A, Halevy AH, O’Neill SD. 1994. Pollination-induced senescence of Phalaenopsis petals: The wilting process, ethylene production and sensitivity to ethylene. Plant Growth Regulation 15: 129–136.
Porat R, Halevy AH, Serek M, Borochov A. 1995. An increase in ethylene sensitivity following pollination is the initial event triggering an increase in ethylene production and enhanced senescence of Phalaenopsis orchid flowers. Physiologia Plantarum 93: 778–784.[CrossRef]
Reiche C. 1885. Über anatomische Veränderungen, welche in den Perianthkreisen der Blüten während der Entwicklung der Frucht vor sich gehen. Jahrbücher für wissenschaftliche Botanik 16: 638–687.
Schemske DW, Willson MF, Melampy MN, Miller LJ, Verner L, Schemske M, Best LB. 1978. Flowering ecology of some spring woodland herbs. Ecology 59: 351–366.[CrossRef]
Silberglied RE. 1979. Communication in the ultraviolet. Annual Reviews of Ecology and Systematics 10: 373–398.
Spanjers AW. 1977. Bioelectric potential changes in the style of Lilium longiflorum Thurb. after self and crosspollination from the stigma. Planta 153: 1–5.[CrossRef]
Stead AD, Moore KG. 1983. Studies on flower longevity in Digitalis. II. The role of ethylene in corolla abscission. Planta 157: 409–414.
Stead AD, Reid MS. 1990. The effect of pollination and ethylene on the colour change of the banner spot of Lupinus albifrons Bentham flowers. Annals of Botany 66: 655–663.
Süssenguth K. 1936. Über den Farbwechsel von Blüten. Berichte der Deutschen Botanischen Gesellschaft 54: 409–417.
van Doorn WG. 1997. Effects of pollination on floral attraction and longevity. Journal of Experimental Botany 48: 1615–1622.
van Doorn WG. 2001. Categories of petal senescence and abscission: a re-evaluation. Annals of Botany 87: 447–456.
van Doorn WG, Stead A. 1997. Abscission of flowers and floral parts. Journal of Experimental Botany 48: 821–837.
Webb CJ, Littleton J. 1987. Flower longevity and protandry in two species of Gentiana (Gentianaceae). Annals of the Missouri Botanical Garden 74: 51–57.[CrossRef]
Weiss MR. 1991. Floral colour changes as cues for pollinators. Nature 354: 227–229.[CrossRef]
Woltering EJ, van Doorn WG. 1988. Role of ethylene in senescence of petals – Morphological and taxonomical relationships. Journal of Experimental Botany 39: 1605–1616.
Woltering EJ, Somhorst D. 1990. Regulation of anthocyanin synthesis in Cymbidium flowers: effects of emasculation and ethylene. Journal of Plant Physiology 136: 295–299.
Woltering EJ, Somhorst D, van der Veer P. 1995. The role of ethylene in interorgan signalling during flower senescence. Plant Physiology 109: 1219–1225.[Abstract]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. J. Weber and C. Goodwillie Timing of self-compatibility, flower longevity, and potential for male outcross success in Leptosiphon jepsonii (Polemoniaceae) Am. J. Botany, August 1, 2007; 94(8): 1338 - 1343. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||