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Categories of Petal Senescence and Abscission: A Re-evaluation
Annals of Botany 87: 447±456, 2001 doi:10.1006/anbo.2000.1357, available online at http://www.idealibrary.com on
Categories of Petal Senescence and Abscission: A Re-evaluation W. G .
VA N
DOORN
Agrotechnological Research Institute (ATO), Wageningen University and Research Centre, PO Box 17, 6700 AA Wageningen, The Netherlands Received: 17 May 2000
Returned for revision: 26 June 2000 Accepted: 11 December 2000
Published electronically: 15 February 2001
In a previous paper (Woltering and van Doorn, 1988, Journal of Experimental Botany 39: 1605±1616) we identi®ed three types of ¯ower life cessation: by petal wilting or withering, which was either ethylene-sensitive or insensitive, and by abscission of turgid petals, which was ethylene-sensitive. These categories tended to be consistent within families. Here we re-examine these relationships by testing a further 200 species, and a number of other families. As previously, ¯owering shoots were exposed to 3 ppm ethylene for 24 h at 20 8C, in darkness. Most monocotyledonous species tested showed ethylene-insensitive petal wilting, although ethylene-sensitive wilting occurred in the Alismataceae and Commelinaceae. Petals of the dicotyledonous species tested were generally sensitive to ethylene, except for a few groups showing wilting (Crassulaceae, Gentianaceae and Fumariaceae, and one subfamily in both the Ericaceae and Saxifragaceae). Petal abscission was generally ethylene-sensitive, but ethylene insensitivity was found in some Tulipa cultivars and three Saxifraga species. In most tulip cultivars tested, the petals wilted and then fell. It is concluded that (a) the response to ethylene is often consistent within either families or subfamilies; and (b) a fourth category, ethyleneinsensitive petal abscission, exists both in monocotyledons and dicotyledons. # 2001 Annals of Botany Company Key words: Ethylene sensitivity, ¯ower longevity, petal abscission, petal wilting, petal withering, petal senescence, taxonomic categories.
I N T RO D U C T I O N The life span of ¯owers is generally determined by the time to abscission of petals that are still turgid, or by the time to petal1 wilting or withering. In many species, the time to petal wilting or abscission is regulated by ethylene. We have previously found that high sensitivity to applied ethylene in petals coincides with a regulatory role of endogenous ethylene. We determined the ethylene-sensitivity of ¯owers of 93 species from a small number of families, and concluded that petal abscission is generally regulated by endogenous ethylene, as no species were found in which it was ethylene-insensitive. Petal abscission was consistent within families, for example in the Labiatea (Lamiaceae), Ranunculaceae and Rosaceae. Species in some other families, such as the Orchidaceae, predominantly showed ethylene-sensitive petal wilting2, whereas those in yet other families predominantly exhibited ethylene-insensitive wilting (Woltering and van Doorn, 1988). In our previous paper only a small number of monocotyledonous species was tested. A detailed report on morphological changes in ¯owers of numerous monocotyledonous species, at the end of their life, has since indicated a relationship with taxonomic category (McKenzie and Fax 31-317-475347, e-mail [email protected] For reasons of simplicity, all perianth parts (either in ¯owers having separate petals or in those with a corolla) as well as the tepals (of ¯owers with a perigon) will be termed petals, and both the perianth and the perigon will here be called perianth. 2 Petal wilting is considered to be a visible senescence symptom. Although petal fall is often thought to be a category of ¯ower senescence, senescence is usually de®ned as encompassing the processes leading to programmed cell death, which excludes abscission. 1
0305-7364/01/040447+10 $35.00/00
Lovell, 1992). These data generally con®rmed our conclusions, but were not accompanied by ethylene treatment, so the relationship with ethylene-sensitivity remained unclear. Furthermore, some of our preliminary experiments indicated that some ¯owers showed ethylene-insensitive petal abscission, and that in some families the response was consistent at the subfamily level. We therefore re-examined the conclusions drawn in our previous paper, testing a further 200 species, many from families not hitherto investigated. M AT E R I A L S A N D M E T H O D S Plant material Potted plants were bought at the ¯ower 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 ®eld. After severing, the ¯owering stems were immediately placed in water. Stems were transported in water to the laboratory, within 1 h of cutting, and were used immediately. Cut ¯owers from a few other species were bought at the Aalsmeer ¯ower auction. These were transported to the laboratory (without water) within 3 h of purchase. Stems of these ¯owers were recut under water and used for experimentation the same day. Ethylene treatment Treatments occurred in closed 70 l stainless steel chambers at 20 + 18C, in darkness, as described previously # 2001 Annals of Botany Company
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van DoornÐEthylene Eects on Petal Wilting and Abscission
(Woltering and van Doorn, 1988). In short, ethylene was injected into the chamber, exposing the plants or ¯owers to 3 (2.8±3.3) ppm for 24 h. Excess carbon dioxide was absorbed by calcium hydroxide (10 g) in the chamber. Ethylene and carbon dioxide partial pressures were checked regularly during the treatments, by extracting gas samples from the chamber and using gas chromatography. Control ¯owers were stored under identical conditions except that ethylene was removed using Ethysorb (aluminium oxide and potassium permanganate; Stay Fresh Ltd, London, UK). Ethylene concentrations were usually below the detection limit and remained below 0.01 ppm in all experiments, even when using potted plants. In each experiment at least three potted plants or at least ®ve ¯owers were used per chamber, and two replicate chambers were used. Each species was tested at least twice. A few species that have been tested previously (Woltering and van Doorn, 1988) were included, when a fuller range of species in a (sub)family was required or when inconsistencies were found between previous and present results. Classi®cation of ethylene sensitivity After ethylene treatment, the potted plants and ¯owers were placed under controlled environmental conditions of 12 h ¯uorescent white light (15 mmol m ÿ2 s ÿ1) and 12 h darkness, 60 % relative humidity (RH) and 20 + 18C. Perianth changes were determined daily. The eects were expressed as the percentage of the time taken for the symptoms to occur, compared to the controls. For example, a 50 % response indicates that the symptoms occurred within half the time they occurred in controls. These percentages were then grouped according to ®ve classes as follows: class 0, no response (insensitive); class 1, up to 33 % eect (low sensitivity); class 2, between 33 % and 66 % eect (intermediate sensitivity); class 3, 66±99 % eect (high sensitivity); and class 4, ethylene response already dramatic at the end of treatment (very high sensitivity). Taxonomic classi®cation Plants were grouped into families according to the classi®cation of Heywood (1978), which is similar to the classi®cation according to Tutin et al. (1964) used in our previous paper. Species in the Liliaceae are also classi®ed into families according to Dahlgren et al. (1985). These two classi®cations were used to enable direct comparison with the literature (Woltering and van Doorn, 1988; McKenzie and Lovell, 1992; van Doorn, 1997). The data are also compared with a more recent classi®cation, largely based on molecular systematic results (APG, 1998; Peter Endress, pers. comm., 2000). Time to petal abscission Tulip ¯owers were harvested at the commercial cutting stage (unopened buds) and treated with ethylene at that stage. In a few experiments, tulip ¯owers at various stages of opening and age were also used. The ¯owers were transported in water to the laboratory, and were used the
same day or were held overnight in water at 58C. Flowers were treated with ethylene as described above, with eight ¯owers per treatment. Flowers were individually placed in glass pots with deionized water at 208C, in the climatecontrolled room. The time to abscission of more than half of the petals was recorded. Experiments on each cultivar were performed twice. R E S U LT S Types of response and ethylene sensitivity After 24 h exposure to 3 ppm ethylene, petals of many species showed rapid wilting or abscission. The same symptoms were found, although later, in untreated ¯owers. In other ¯owers, mostly those exhibiting petal wilting, the ethylene treatment did not advance the senescence symptoms. Wilting, as de®ned here, includes turgor loss, liquid logging of the tissue (which results in translucency), and slow desiccation (withering). In most species whose ¯ower life span is terminated by petal wilting, the petals are eventually shed. Abscission is used here to indicate the fall of petals without concomitant wilting, hence in petals that seem, by visual inspection, turgid, and lack translucency. In some species, abscission occurs in petals that are only slightly wilted, i.e. in these ¯owers petal wilting and abscission concur (indicated by `wa' in Tables 1 and 2). The type of response to ethylene, and its sensitivity to ethylene is shown separately for monocotyledons (Table 1) and dicotyledons (Table 2). In many species petal wilting was hastened by ethylene, but in numerous others it was little or not aected by ethylene treatments (Tables 1 and 2). Petal abscission without prior wilting was generally highly sensitive to ethylene. Flowers in some tulip cultivars were an exception (Tables 3 and 4). In most Tulipa cultivars tested, the petals fell after the appearance of translucency, either solely at the distal margin or the whole petal. Translucency was mostly followed by turgor loss, and often by slight desiccation. In a few cultivars the distal petal margins rolled in or clearly desiccated prior to fall (Table 3). In all these cultivars, applied ethylene somewhat hastened the time to wilting (Table 3). In a few other cultivars the petals fell without prior symptoms of translucency, turgor loss, or desiccation. The time to abscission was unaected by the ethylene treatment (Table 4). In a few experiments, tulip ¯owers of these cultivars were treated with ethylene when already fully open or close to wilting and abscission. Ethylene did not hasten abscission in these tests (results not shown). Three Saxifraga species (S. apiculata, S. x arendsii and S. litacina) showed petal abscission concomitant with slight wilting (translucency). The time to petal abscission in these species was also ethylene-insensitive (Tables 2 and 4). Relationship with taxonomic groups In the monocotyledons tested, petal abscission without concomitant wilting was not observed, except in some tulip cultivars (see above). The wilting response was generally insensitive to applied ethylene (Table 1). Exceptions were
van DoornÐEthylene Eects on Petal Wilting and Abscission the species tested in the Alismataceae and the Commelinaceae, which showed ethylene-sensitive wilting. A few other examples of ethylene-sensitive petals were found within monocotyledonous families containing mostly species with ethylene-insensitive petal wilting, such as the Amaryllidaceae (Table 1). In the Iridaceae species tested, ethylenesensitive petals were observed in the SisyrinchieaeÐa tribe in the classi®cation of Heywood (1978)Ðwhile the other species tested were ethylene-insensitive (Table 1). The types of response to ethylene were slightly more consistent within monocotyledous families according to the classi®cation of Dahlgren et al. (1985) than the classi®cation of Heywood (1978). In the former classi®cation, the genus Alstroemeria and some related species, and many liliaceous species were placed in separate families. Among the liliaceous species, most exceptions with regard to ethylene-sensitivity and type of response occurred in the Liliaceae sensu Dahlgren et al. (1985), and the response was not uniform in this group (Table 1). In dicotyledonous ¯owers, the type of response and its ethylene sensitivity were also generally consistent with families according to Heywood (1978), although a number of exceptions were observed. The exceptions may, at least in some families, be consistent with lower taxonomic categories. In the Ericaceae and Saxifragaceae, for example, the response was apparently consistent with subfamilies (Table 2). Abscission without concomitant wilting was, in most dicotyledonous ¯owers tested, hastened by applied ethylene. Families, according to the classi®cation of Heywood (1978), in which the petals of all species studied abscised (without prior wilting symptoms) include the Acanthaceae, Boraginaceae, Caprifoliaceae, Cruciferae, Gesneriaceae, Oleaceae, Papaveraceae, Portulacaceae, Rubiaceae, Scrophulariaceae and Valerianaceae. Abscission without concomitant wilting also occurred in two subfamilies of both the Ericaceae and the Saxifragaceae. In the Primulaceae, all genera tested showed ethylene-sensitive abscission, but three Primula species tested exhibited petal wilting following ethylene exposure. In the classi®cation of Heywood (1978), the genus Primula belongs to the subfamily Primuleae, and the other Primulaceae tested to the subfamily Lysimachieae. In some families the petals of most species abscised while showing slight wilting symptoms (Solanaceae and Fumariaceae). In the Solanaceae this response was highly ethylene-sensitive, but in the Fumariaceae species tested it showed only intermediate sensitivity (Table 2). The ethylene-insensitivity of the response of three Saxifraga species (abscission after slight wilting) has been described in the previous paragraph. Petal wilting in a number of dicotyledonous families sensu Heywood (1978) was advanced by exogenous ethylene (Aizoaceae, Campanulaceae, Convolvulaceae, Dipsacaceae, Lobeliaceae, Plumbaginaceae and Portulacaceae). Ethylene-insensitive petal wilting was rare in the dicotyledonous plants tested. It was observed throughout the Crassulaceae and Gentianaceae, in the Ericoidieae subfamily of the Ericaceae, and in the Saxifragoideae subfamily of the Saxifragaceae.
449
Preliminary results on the Umbelliferae contrasted with conclusions drawn in our previous paper, where two species (Anethum graveolens and Conium maculatum) showed ethylene-insensitive wilting. This ®nding was corroborated here. However, several other species showed ethylenesensitive abscission (Anthriscus sylvestris, Apium graveolens, Coriandrum sativum and Heracleum sphondylium). The number of species tested to date is insucient to allow conclusions to be drawn about the correlation with taxonomic categories within the family (results not shown). Heywood (1978) distinguished three subfamilies in the Leguminosae: Mimosoideae, Caesalpinioideae and Papilionideae. These groups are often considered families in other classi®cations, such as that of Cronquist (1988). The former group generally contains ¯owers without conspicuous petals but with showy stamens. Mimosoideae and Caesalpinioideae have not been investigated. Preliminary results in the Papilionideae subfamily showed ethylene-insensitive wilting in the tribes Trifolieae (three Trifolium species) and Loteae (Lotus corniculatus and Dorycnium hirsutus), and ethylene-sensitive wilting in the tribes Galegeae (Astralagus galeniformis) and Genisteae (Genista lydia) (results not shown). Compared with the classi®cation of Heywood (1978), the results show a somewhat higher degree of consistency with families as classi®ed by the Angiosperm Phylogeny Group (APG, 1998) using a molecular systematic approach. According to this classi®cation, the Saxifragaceae are a highly polyphyletic group. Both Hydrangeoideae and Ribesoideae are considered separate families, Hydrangeaceae and Grossulariaceae, respectively. The responses to ethylene in the remaining Saxifragaceae species tested, classi®ed according to APG (1998), are rather uniform. Some of the relevant dierences between the classi®cation of Heywood (1978) and APG (1998) are shown in Table 5. APG (1998) places the Lobeliaceae in the Campanulaceae. Species in both groups tested showed the same response to ethylene. In the liliaceous species, APG (1998) generally agrees with the classi®cation of Dahlgren et al. (1985). As discussed above, this also renders the response to ethylene more consistent with family than in the classi®cation of Heywood (1978). APG (1998) places the Funkiaceae sensu Dahlgren in the Agavaceae, and the Uvulariaceae in the Colchicaceae. These changes still result in uniform families with regard to the response to ethylene in the species tested. DISCUSSION The present results con®rm our previous report that petal abscission is generally highly sensitive to applied ethylene (Woltering and van Doorn, 1988). However, it is now established that the time to abscission, occurring without prior wilting or withering, is ethylene-insensitive in a few species. In the previous paper we distinguished three categories of ¯ower life cessation: ethylene-sensitive or ethylene-insensitive petal wilting, and ethylene-sensitive petal abscission. We now de®ne a fourth category, that of ethylene-insensitive abscission. We found three tulip cultivars in which the petals fell without prior wilting, where ethylene had no eect on the time to abscission
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van DoornÐEthylene Eects on Petal Wilting and Abscission
T A B L E 1. Monocotyledons: response of the perianth to treatment with 3 ppm ethylene for 24 h in darkness at 208C Plant family (Tribe)
Species
Type of response
Response classi®cation
Agavaceae
Polianthes tuberosa Sansevieria sp.
w w
0 0
Alismataceae
Alisma parvi¯ora Baldellia ranunculoides Sagittaria lancifolia
w w w
4 4 4
Amaryllidaceae
Alstroemeria peregrina (r) Cyrtanthus purpureus Galanthus nivalis Hippeastrum x ackermannii Narcissus pseudonarcissus (r) Nerine bowdenii (r) Zephyranthes candida
wa w w w w w w
2±31 2 0 3 0 0 0
Cannaceae
Canna hybrid (3 cultivars)
w
0
Commelinaceae
Commelina sp. Tradescantia hybrid Zebrina pendula
w w w
4 4 3
Haemodoraceae
Anigozanthos spp. (3 species)
w
0
Chasmanthe aethiopica Crocus chrysanthus Gladiolus hybrid (r) Tritonia crocata Iris germanica Iris halophyta Iris sibirica Tigridia pavonia Crocosmia x crocosmii¯ora (r) Freesia hybrids (r) Ixia ¯exuosa Sisyrinchium angustifolium Sisyrinchium californicum Sisyrinchium laevigatum
w w w w w w w w wa w w w w w
0 0 0±1 0 0 0 0 0 1±2 0 0 4 4 4
Allium cernuum Brodiaea californica Bloomeria aurantiaca Nothoscordum aureum Triteleia laxa Tulbaghia violacea Asphodelus albus Asphodeline lutea Eremurus (hybrid) (r) Knipho®a (hybrid) (r) Colchicum autumnale Colchicum speciosum Gloriosa superba (r) Ornithoglossum parvi¯orum Sandersonia aurantiaca Convallaria majalis Liriope koreana Polygonatum odoratum Hosta lancifolia Hosta latifolia Hosta tardiana Hosta undulata Hemerocallis lilio-asphodelus Hemerocallis `Invictus' Hemerocallis `Mabel Fuller' Hemerocallis `Mrs. J. Tigert' Hemerocallis `Black Prince'
w w w w w w w w w w w w w w w w w w w w w w w w w w w
0 0 3 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Iridaceae (Croceae) (Gladioleae) (Irideae)
(Ixieae) (Sisyrinchieae)
Liliaceae [Alliaceae]
[Asphodelaceae]
[Colchicaceae]
[Convallariaceae] [Funkiaceae]
[Hemerocallidaceae]
Table continued over page
van DoornÐEthylene Eects on Petal Wilting and Abscission
451
T A B L E 1. Continued Plant family (Tribe) Liliaceae [Hyacinthaceae]
[Liliaceae]
[Uvulariaceae]
Species Camassia quamash Camassia leichtlinii Eucomis bicolor Galtonia candicans Galtonia sp. Hyacinthus orientalis Hyacinthoides non-scipta Lachenalia sp. Muscari armeniacum Ornithogalum thyrsoides (r) Erythronium americanum Lilium martagon Lilium hybrid (r) Brunello (Oriental hybrid) Montenegro (Oriental) Star Gazer (Aseatic hybrid) Woodru Memory (As.) Tulipa gesneriana (r) Tricyrtis latifolia
Type of response
Response classi®cation
w w w w w w w w w w wa wa
0 0 0 0 0 1±2 0 0 0±1 0 3 3
w w w w w or wa (most cultivars) a (some cultivars) w
1 0 2 0±1 1±2 (Table 3) 0 (Table 4) 0
1 The Alstroemeriaceae are a separate family in the system of Dahlgren et al. (1985). The perianth showed wilting or withering (w) or abscission (a). Wilting or withering also occurred concomitantly with abscission (wa). The time to the response is expressed in categories 0±4, de®ned in the text. Some ¯owers, indicated by `r', have also been tested previously (Woltering and van Doorn, 1988). Taxonomic classi®cation according to Heywood (1978) or, between square brackets, according to Dahlgren et al. (1985).
(Table 4). Absence of an eect of ethylene was also found when the ¯owers were treated at later stages of development. In roses, we previously observed that ethylene application did not aect abscission until the ¯owers were fully open and close to abscission (Woltering and van Doorn, 1988). In contrast, petal abscission in tulip ¯owers remained insensitive to ethylene even until shortly before they abscised. In tulip `Golden Apeldoorn', petal wilting generally preceded abscission. Although the time to wilting was slightly sensitive to ethylene (Table 3), we found that the time to petal abscission in this cultivar was also independent of ethylene treatment and not aected by ethylene inhibitors (Sexton et al., 2000). Three Saxifraga species also exhibited ethylene-insensitive abscission, which occurred concomitantly with slight liquid logging (Tables 2 and 4). Preliminary experiments with the Lilium hybrid `Montenegro' (belonging to the Oriental group of cultivars) also indicated ethylene-insensitive abscission, which occurred about 2 d after petal wilting (liquid logging and turgor loss; unpubl. res.). As in our previous work, the types of cessation of ¯ower life (and the sensitivity to ethylene) were generally consistent within plant families according to the classi®cation of Heywood (1978). However, it was observed here that in some families such consistency was apparent at the subfamily level, for example in the Ericaceae and Saxifragaceae. According to a more recent classi®cation (APG, 1998), the former Saxifragaceae are a polyphyletic group with Hydrangeaceae and Glossulariaceae ( formerly Ribesoideae) separate from Saxifragaceae. This would give consistency at the family level in the Saxifragaceae. According to the APG classi®cation, however, the consistency is still apparent at the subfamily level in the
Ericaceae. Such consistency at the subfamily level may also occur in the Iridaceae, but this conclusion is based on a rather small number of species tested in each of the tribes. The genus Sisyrinchium may be an exception, rather than the tribe Sisyrinchieae. Similarly, in the Primulaceae the genus Primula (subfamily Primuleae) may be an exception rather than the entire subfamily. More than a century ago, Reiche (1885) investigated the end of the natural perianth lifespan in ¯owers. His results are in close agreement with the present ®ndings. In the Boraginaceae, for example, petals fell in all 11 genera investigated. In the Ericaceae, two groups were found: one, comprising Azalea, Vaccinium and Pirola, showed petal abscission, and the other, including Calluna and Erica, exhibited petal wilting. In the Gentianaceae and several Leguminoseae, the corolla or petals were found to wilt. In the only Plumbaginaceae species tested (Armeria vulgaris), the petals wilted then were torn from the ¯ower by the growing fruit. In the Primulaceae, the general response was petal abscission, although in the genus Primula the petals wilted. Within the Solanaceae, the species investigated generally showed petal fall, sometimes with concomitant wilting. Similarly, McKenzie and Lovell (1992) observed the types of ¯ower life cessation in a large number of monocotyledons. They found numerous genera in which the petals wilted or withered and a relatively low number of genera in which the petals wilted and abscised almost concomitantly. No examples were found of ¯owers that showed petal abscission without prior wilting, a result that wasÐexcept for a few tulip cultivarsÐcon®rmed in our experiments. Although a number of exceptions were noted, a correlation was found between the types of symptoms and
452
van DoornÐEthylene Eects on Petal Wilting and Abscission T A B L E 2. Dicotyledons: response of the perianth to treatment with 3 ppm ethylene for 24 h darkness at 208C
Plant family (Subfamily)
Species
Type of response
Response classi®cation
Acanthaceae
Acanthus hungaricus Acanthus spinosus Crossandra sp. Thunbergia alata
a a a a
4 4 4 4
Aizoaceae
Carpathea pomeridiana Delospermum cooperi Delospermum lyndenburgensis Dorotheanthus bellidiformis Lithops dorothea Mesembryanthemum productus
w w w w w w
4 3 4 4 3 3
Boraginaceae
Borago ocinalis Brunnera macrophylla Buglossoides purpurocaerulea Echium plantagineum Lindolo®a stylosa Mertensia paniculata Omphalodes verna Pulmonaria ocinalis Symphytum cordatum Symphytum grandi¯orum Symphytum ottomanum
a a a a a a a a a a a
4 4 4 4 4 4 4 4 4 4 4
Campanulaceae
Campanula garganica Campanula glomerata Campanula pyramidalis (r) Edraianthus graminifolius Phyteuma scheuchzeri Trachelium caeruleum (r)
w w w w w w
4 3 4 3 2 3
Caprifoliaceae
Abelia schumanii Leicesteria formosa Lonicera x heckrottii `Gold¯ame' Sambucus nigra Viburnum henryi Viburnum lobophyllum Weigela ¯orida Weigela `Gustave Mallet'
a a a a a a w w
4 4 4 4 4 4 0 0
Convolvulaceae
Ipomoea alba Convolvulus arvensis Quamoclit coccinea
w w w
4 4 4
Crassulaceae
Crassula falcata Echeveria setosa KalanchoeÈ blossfeldiana Sedum hybrid Sedum spectabile Sedum spurium Sempervivum sp.
w w w w w w w
0 0 2 0 0 1 0
Cruciferae
Alliaria petiolata Arabis caucasia Brassica napus Cardamine pratensis Cheiranthus sp. Erysimum cuspidatum Lunaria rediviva Matthiola incana (r)
a a a a a a a w1
4 4 4 4 4 3 4 2
Dipsacaceae
Cephalaria alpina Cephalaria gigantea Scabiosa caucasia (r) Succisella in¯exa (r)
wa wa w w
2±3 2 2±3 3 Table continued over page
van DoornÐEthylene Eects on Petal Wilting and Abscission
453
T A B L E 2. Continued Plant family (Subfamily)
Type of response
Response classi®cation
Calluna vulgaris Erica gracilis Erica hiemalis Erica tetralix Pieris japonica Andromeda sp. Kalmia latifolia Rhododendron brachycarpum Rhododendron hybrid (several cvs) Gaultheria shallon Leucothoe axillaris Leucothoe walterii Vaccinium macrocarpon
w w w w w a a a a a a a a
0 0 0 0 0 3 4 4 4 3 3 3 4
Fumariaceae
Corydalis sp. Dicentra formosa Dicentra hybrid Fumaria sp.
wa wa wa wa
2 2 2 2
Gentianaceae
Exacum ane Gentiana dahurica Gentiana kochiana Gentiana sino-ornata Sabatia sp.
w w w w w
0 0 0 0 0
Gesneriaceae
Aeschynanthus sp. Columnea krakatau Columnea nesse Kohleria hybrid `Eriantha' Saintpaulia confusa Saintpaulia tongwensis Sinningia cardinalis Streptocarpus hybrid
a a a a a a a a
4 4 4 4 4 4 4 4
Lobeliaceae
Laurentia ¯uviatilis Lobelia cardinalis Lobelia siphylitica Monopsis sp.
w w w w
3 3 2±3 3
Oleaceae
Forsythia x intermedia Jasmium ocinale Ligustrum ovalifolium Syringa vulgaris
a a a a
4 4 4 4
Papaveraceae
Chelidonium majus Eschscholzia sp. Papaver rhoeas
a a a
4 4 4
Plumbaginaceae
Armeria maritima Armeria pseudoarmeria Ceratostigma plumbaginoides Limonium latifolium Plumbago auriculata
w w w w w
3 4 4 3 4
Portulacaceae
Claytonia sp. Lewisia cotyledon Portulaca grandi¯ora Portulaca umbraticola
w w w w
3 4 4 4
Primulaceae
Anagallis arvensis Cyclamen hybrid Lysimachia clethroides (r) Lysimachia punctata Primula denticulata Primula rosea `Grandi¯ora' Primula vialii
a a a a wa wa w
3 4 4 4 2±3 2±3 2
Ericaceae (Ericoideae)
(Rhododendroideae)
(Vaccinioideae)
Species
Table continued over page
454
van DoornÐEthylene Eects on Petal Wilting and Abscission T A B L E 2. Continued
Plant family (Subfamily)
Species
Rubiaceae
Asperula tinctoria Galium aparine Incarvillea delavayi Ixora hybrid Pentas lanceolata Rubia tinctorum
Saxifragaceae (Hydrangeoideae) (Ribesoideae) (Saxifragoideae)
Deutzia scabra `Macropetala' Deutzia schneideriana Ribes aureum Bergenia cordifolia Saxifraga apiculata `Gregor Mendel' Saxifraga x arendsii `Schneeteppich' Saxifraga litacina Tiarella cordifolia
Scrophulariaceae
Antirrhinum majus (r) Calceolaria sp. Gratiola ocinalis Phygelius sp. Penstemon cobaea Penstemon heterophyllus Penstemon serrulatus Torenia hybrid Veronica orchidea (r)
Solanaceae
Iochroma hybrid Lycopersicon esculentum Nicotiana tabacum Nierembergia sp. Petunia hybrid Solanum dulcamara
Valerianaceae
Centranthus ruber `Albus' Centranthus ruber `Coccineus' Patrinia gibbosa Valeriana ocinalis
Type of response
Response classi®cation
a a a a a a
3 3 4 3 4 3
a a a w wa wa wa w
4 4 3 0 0 0 0 0
a a a a a a a a a
3 4 3 3 4 4 3 4 4
wa wa wa wa wa w
3 4 4 3 4 3
a a a a
3 3 3 4
1 The early wilting in Matthiola incana cut ¯owers is apparently due to a vascular occlusion. The perianth showed wilting or withering (w) or abscission (a). Wilting or withering also occurred concomitantly with abscission (wa). The time to the response is expressed in categories 0±4, de®ned in the text. Some ¯owers, indicated by `r', have been tested previously (Woltering and van Doorn, 1988). Taxonomic classi®cation according to Heywood (1978).
the plant families, at least when using the classi®cation of Dahlgren et al. (1985). Most exceptions were found in the Iridaceae, where some genera showed petal wilting and others abscission concomitant with wilting. These results were largely con®rmed here. In Lilium martagon, petals fell just as they showed the very ®rst symptoms of wilting (translucency) (Table 1). In all cultivars of commercial cut lily ¯owers (both the Asiatic and Oriental type of cultivars), the present tests showed petal fall after symptoms such as liquid logging (translucency) and turgor loss. In the Oriental cultivars tested, the time between these wilting symptoms and petal fall was short (1±2 d), whereas in the Asiatic cultivars this span was as much as 5±6 d. This con®rms our previous work. McKenzie and Lovell (1992) interpreted our previous data on lily ¯owers as indicating no petal fall following wilting. We did, however, also observe petal abscission some days after wilting in all commercial lily cultivars previously studied. Most monocotyledonous families fall into one category, namely that of ¯owers showing ethylene-insensitive wilting. Exceptions include ethylene-sensitive wilting in the
Alismataceae and Commelinaceae, and in the previously investigated Orchidaceae. In contrast to monocotyledons, dicotyledonous ¯owers were generally sensitive to ethylene. One large family (Compositae) is an exception (Woltering and van Doorn, 1988), and in the present tests the petals in a few other groups, classi®ed as subfamilies, were also ethylene-insensitive. The majority of these dicotyledonous families tested exhibit petal abscission prior to any signs of wilting. In some species, petal fall may not be due to true abscission but to ovary growth. According to Reiche (1885) this occurs in several species of, for example, the Boraginaceae, Cucurbitaceae, Labiatae (Lamiaceae), Malvaceae, Plumbaginaceae and Solanaceae. If this claim is correct, a distinction should be made between groups in which petal fall is due to true abscission and those in which it is due to ovary growth. Ethylene treatment stimulates ovary growth, at least in some species (Nichols, 1971; Han et al., 1991). Ethylene-induced ovary growth may therefore advance the purported petal tearing. If ethylene-sensitive petal fall is recorded, it may thus be due, at least in some
van DoornÐEthylene Eects on Petal Wilting and Abscission T A B L E 3. Eects of applied ethylene (3 ppm for 24 h in darkness at 208C) on some Tulipa cultivars in which the perianth showed wilting (w) or wilting shortly followed by abscission (wa) Cultivar
Type of response
Abba Atilla Barcelona Bastogne Blenda Golden Apeldoorn Leen van der Mark Lucky Strike Lustige Witwe Monte Carlo Negrita Prominence Pink Impression Recreado White Dream Yokohama
w (sometimes w w w w w w (sometimes w w (sometimes w w w w (sometimes w w w
wa)
wa) wa)
wa)
Response classi®cation 1 1 1 1 1 1±2 1 2 1 1 1 1 2 1 1±2 1
455
species, to an ethylene eect on ovary development rather than on true petal abscission. In dicotyledonous plants, a further 20 families have now been studied that had not previously been investigated, increasing the total number of families tested, according to the classi®cations of Heywood (1978) and APG (1998), to 36. In the monocotyledons, depending on the classi®cation used, ®ve or more additional families have now been investigated. Nonetheless, the present experiments still include only a small number of genera from each of the families and subfamilies tested. It is concluded that the three types of the cessation of ¯ower life as de®ned earlier are, as a rule, consistent with families or subfamilies. A fourth category, ethyleneinsensitive petal abscission (without prior wilting) has also been observed. It occurred only in a few species, and was found both in monocotyledons and dicotyledons. AC K N OW L E D G E M E N T S
The time to the response is expressed in categories 0±4, de®ned in the text.
I am grateful to Rene Perik for growing some bulbous ¯owers, Delphine Raze and Laetitia Brunnevalle for
T A B L E 4. Eects of applied ethylene (3 ppm for 24 h in darkness at 208C) on three Tulipa cultivars in which the perianth abscised (a) without wilting symptoms, and in three Saxifraga species in which the petals fell concomitant with wilting (liquid logging) Time to abscission (d)
Type of response
Response classi®cation
Controls
Treated
a a a
0 0 0
9.3 + 1.1 7.9 + 0.7 11.0 + 1.3
9.4 + 0.8 7.9 + 1.0 10.5 + 1.0
Species
Cultivar
Tulipa gesneriana
Ad Rem Gander's Rhapsody Rosario
Saxifraga apiculata
Gregor Mendel
wa
0
5.2 + 1.5
5.9 + 1.4
Saxifraga x arendsii
Schneeteppich
wa
0
5.0 + 1.9
4.8 + 1.3
0
4.1 + 0.8
4.4 + 0.6
Saxifraga litacina
wa
Data on time to abscission are means + s.d. of ten ¯owers. Response is expressed in categories 0±4, de®ned in the text. The time to abscission (of more than half of the petals) was determined from the commercial harvesting stage (closed bud, in ¯owers placed individually in water at 208C, 65 % RH and 12 h white light (15 mmol m ÿ2 s ÿ1) and 12 h darkness.
T A B L E 5. Comparison of the taxonomic classi®cation of APG (1998) with that of Heywood (1978) and Dahlgren et al. (1985) Monocotyledons APG (1998) groups the liliaceous species into families similar to Dahlgren et al. except Funkiaceae, which are included in Agavaceae, and Uvulariaceae, which are included in Colchicaceae Eudicotyledons APG (1998) includes some species from the Caprifoliaceae, such as Sambucus and Viburnum, in Adoxaceae Lobeliaceae: included in Campanulaceae by APG Saxifragaceae: Hydrangeoideae a separate family (Hydrangeaceae) according to APG Ribesoideae a separate family (Grossulariaceae) according to APG Only a few changes, relevant to the present paper, are shown. In APG (1998) the basal-most angiosperms have been subtracted from the dicotyledons, and the remaining dicotyledons are called eudicotyledons. Data partially based on personal communication with Peter Endress (2000).
456
van DoornÐEthylene Eects on Petal Wilting and Abscission
carrying out repeat experiments, Dr Roy Sexton for critical discussions, and Dr Jan J. Bos (Department of Taxonomy, Wageningen University) for permission to harvest ¯owers in the botanical garden. L I T E R AT U R E C I T E D APG (The Angiosperm Phylogeny Group). 1998. An ordinal classi®cation for the families of the ¯owering plants. Annals of the Missouri Botanical Garden 85: 531±553. Cronquist A. 1988. The evolution and classi®cation of ¯owering plants. 2nd edn. New York: New York Botanical Garden. Dahlgren RMT, Cliord HT, Yeo PF. 1985. The families of the monocotyledons: structure, evolution and taxonomy. Berlin: Springer Verlag. Heywood VH. 1978. Flowering plants of the world. Oxford: Oxford University Press. Han S, Halevy AH, Reid MS. 1991. The role of ethylene and pollination in petal senescence and ovary growth of Brodiaea. Journal of the American Society for Horticultural Science 116: 68±72.
McKenzie RJ, Lovell PH. 1992. Flower senescence in monocotyledons: a taxonomic survey. New Zealand Journal of Crop and Horticultural Science 20: 67±71. Nichols R. 1971. Induction of ¯ower senescence and gynoecium development in the carnation (Dianthus caryophyllus) by ethylene and 2-chloroethylphosphonic acid. Journal of Horticultural Science 46: 323±332. Reiche C. 1885. UÈber anatomische VeraÈnderungen, welche in den Perianthkreisen der BluÈten waÈhrend der Entwickelung der Frucht vor sich gehen. JahrbuÈcher fuÈr wissenschaftliche Botanik 16: 638±687. Sexton R, Laird G, van Doorn WG. 2000. Lack of ethylene involvement in tulip tepal abscission. Physiologia Plantarum 108: 321±329. Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA. 1964. Flora Europaea, Volumes 1±5. Cambridge: Cambridge University Press. van Doorn WG. 1997. Eects of pollination on ¯oral attraction and longevity. Journal of Experimental Botany 48: 1615±1622. Woltering EJ, van Doorn WG. 1988. Role of ethylene in senescence of petalsÐmorphological and taxonomical relationships. Journal of Experimental Botany 39: 1605±1616.
Categories of Petal Senescence and Abscission: A Re-evaluation W. G .
VA N
DOORN
Agrotechnological Research Institute (ATO), Wageningen University and Research Centre, PO Box 17, 6700 AA Wageningen, The Netherlands Received: 17 May 2000
Returned for revision: 26 June 2000 Accepted: 11 December 2000
Published electronically: 15 February 2001
In a previous paper (Woltering and van Doorn, 1988, Journal of Experimental Botany 39: 1605±1616) we identi®ed three types of ¯ower life cessation: by petal wilting or withering, which was either ethylene-sensitive or insensitive, and by abscission of turgid petals, which was ethylene-sensitive. These categories tended to be consistent within families. Here we re-examine these relationships by testing a further 200 species, and a number of other families. As previously, ¯owering shoots were exposed to 3 ppm ethylene for 24 h at 20 8C, in darkness. Most monocotyledonous species tested showed ethylene-insensitive petal wilting, although ethylene-sensitive wilting occurred in the Alismataceae and Commelinaceae. Petals of the dicotyledonous species tested were generally sensitive to ethylene, except for a few groups showing wilting (Crassulaceae, Gentianaceae and Fumariaceae, and one subfamily in both the Ericaceae and Saxifragaceae). Petal abscission was generally ethylene-sensitive, but ethylene insensitivity was found in some Tulipa cultivars and three Saxifraga species. In most tulip cultivars tested, the petals wilted and then fell. It is concluded that (a) the response to ethylene is often consistent within either families or subfamilies; and (b) a fourth category, ethyleneinsensitive petal abscission, exists both in monocotyledons and dicotyledons. # 2001 Annals of Botany Company Key words: Ethylene sensitivity, ¯ower longevity, petal abscission, petal wilting, petal withering, petal senescence, taxonomic categories.
I N T RO D U C T I O N The life span of ¯owers is generally determined by the time to abscission of petals that are still turgid, or by the time to petal1 wilting or withering. In many species, the time to petal wilting or abscission is regulated by ethylene. We have previously found that high sensitivity to applied ethylene in petals coincides with a regulatory role of endogenous ethylene. We determined the ethylene-sensitivity of ¯owers of 93 species from a small number of families, and concluded that petal abscission is generally regulated by endogenous ethylene, as no species were found in which it was ethylene-insensitive. Petal abscission was consistent within families, for example in the Labiatea (Lamiaceae), Ranunculaceae and Rosaceae. Species in some other families, such as the Orchidaceae, predominantly showed ethylene-sensitive petal wilting2, whereas those in yet other families predominantly exhibited ethylene-insensitive wilting (Woltering and van Doorn, 1988). In our previous paper only a small number of monocotyledonous species was tested. A detailed report on morphological changes in ¯owers of numerous monocotyledonous species, at the end of their life, has since indicated a relationship with taxonomic category (McKenzie and Fax 31-317-475347, e-mail [email protected] For reasons of simplicity, all perianth parts (either in ¯owers having separate petals or in those with a corolla) as well as the tepals (of ¯owers with a perigon) will be termed petals, and both the perianth and the perigon will here be called perianth. 2 Petal wilting is considered to be a visible senescence symptom. Although petal fall is often thought to be a category of ¯ower senescence, senescence is usually de®ned as encompassing the processes leading to programmed cell death, which excludes abscission. 1
0305-7364/01/040447+10 $35.00/00
Lovell, 1992). These data generally con®rmed our conclusions, but were not accompanied by ethylene treatment, so the relationship with ethylene-sensitivity remained unclear. Furthermore, some of our preliminary experiments indicated that some ¯owers showed ethylene-insensitive petal abscission, and that in some families the response was consistent at the subfamily level. We therefore re-examined the conclusions drawn in our previous paper, testing a further 200 species, many from families not hitherto investigated. M AT E R I A L S A N D M E T H O D S Plant material Potted plants were bought at the ¯ower 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 ®eld. After severing, the ¯owering stems were immediately placed in water. Stems were transported in water to the laboratory, within 1 h of cutting, and were used immediately. Cut ¯owers from a few other species were bought at the Aalsmeer ¯ower auction. These were transported to the laboratory (without water) within 3 h of purchase. Stems of these ¯owers were recut under water and used for experimentation the same day. Ethylene treatment Treatments occurred in closed 70 l stainless steel chambers at 20 + 18C, in darkness, as described previously # 2001 Annals of Botany Company
448
van DoornÐEthylene Eects on Petal Wilting and Abscission
(Woltering and van Doorn, 1988). In short, ethylene was injected into the chamber, exposing the plants or ¯owers to 3 (2.8±3.3) ppm for 24 h. Excess carbon dioxide was absorbed by calcium hydroxide (10 g) in the chamber. Ethylene and carbon dioxide partial pressures were checked regularly during the treatments, by extracting gas samples from the chamber and using gas chromatography. Control ¯owers were stored under identical conditions except that ethylene was removed using Ethysorb (aluminium oxide and potassium permanganate; Stay Fresh Ltd, London, UK). Ethylene concentrations were usually below the detection limit and remained below 0.01 ppm in all experiments, even when using potted plants. In each experiment at least three potted plants or at least ®ve ¯owers were used per chamber, and two replicate chambers were used. Each species was tested at least twice. A few species that have been tested previously (Woltering and van Doorn, 1988) were included, when a fuller range of species in a (sub)family was required or when inconsistencies were found between previous and present results. Classi®cation of ethylene sensitivity After ethylene treatment, the potted plants and ¯owers were placed under controlled environmental conditions of 12 h ¯uorescent white light (15 mmol m ÿ2 s ÿ1) and 12 h darkness, 60 % relative humidity (RH) and 20 + 18C. Perianth changes were determined daily. The eects were expressed as the percentage of the time taken for the symptoms to occur, compared to the controls. For example, a 50 % response indicates that the symptoms occurred within half the time they occurred in controls. These percentages were then grouped according to ®ve classes as follows: class 0, no response (insensitive); class 1, up to 33 % eect (low sensitivity); class 2, between 33 % and 66 % eect (intermediate sensitivity); class 3, 66±99 % eect (high sensitivity); and class 4, ethylene response already dramatic at the end of treatment (very high sensitivity). Taxonomic classi®cation Plants were grouped into families according to the classi®cation of Heywood (1978), which is similar to the classi®cation according to Tutin et al. (1964) used in our previous paper. Species in the Liliaceae are also classi®ed into families according to Dahlgren et al. (1985). These two classi®cations were used to enable direct comparison with the literature (Woltering and van Doorn, 1988; McKenzie and Lovell, 1992; van Doorn, 1997). The data are also compared with a more recent classi®cation, largely based on molecular systematic results (APG, 1998; Peter Endress, pers. comm., 2000). Time to petal abscission Tulip ¯owers were harvested at the commercial cutting stage (unopened buds) and treated with ethylene at that stage. In a few experiments, tulip ¯owers at various stages of opening and age were also used. The ¯owers were transported in water to the laboratory, and were used the
same day or were held overnight in water at 58C. Flowers were treated with ethylene as described above, with eight ¯owers per treatment. Flowers were individually placed in glass pots with deionized water at 208C, in the climatecontrolled room. The time to abscission of more than half of the petals was recorded. Experiments on each cultivar were performed twice. R E S U LT S Types of response and ethylene sensitivity After 24 h exposure to 3 ppm ethylene, petals of many species showed rapid wilting or abscission. The same symptoms were found, although later, in untreated ¯owers. In other ¯owers, mostly those exhibiting petal wilting, the ethylene treatment did not advance the senescence symptoms. Wilting, as de®ned here, includes turgor loss, liquid logging of the tissue (which results in translucency), and slow desiccation (withering). In most species whose ¯ower life span is terminated by petal wilting, the petals are eventually shed. Abscission is used here to indicate the fall of petals without concomitant wilting, hence in petals that seem, by visual inspection, turgid, and lack translucency. In some species, abscission occurs in petals that are only slightly wilted, i.e. in these ¯owers petal wilting and abscission concur (indicated by `wa' in Tables 1 and 2). The type of response to ethylene, and its sensitivity to ethylene is shown separately for monocotyledons (Table 1) and dicotyledons (Table 2). In many species petal wilting was hastened by ethylene, but in numerous others it was little or not aected by ethylene treatments (Tables 1 and 2). Petal abscission without prior wilting was generally highly sensitive to ethylene. Flowers in some tulip cultivars were an exception (Tables 3 and 4). In most Tulipa cultivars tested, the petals fell after the appearance of translucency, either solely at the distal margin or the whole petal. Translucency was mostly followed by turgor loss, and often by slight desiccation. In a few cultivars the distal petal margins rolled in or clearly desiccated prior to fall (Table 3). In all these cultivars, applied ethylene somewhat hastened the time to wilting (Table 3). In a few other cultivars the petals fell without prior symptoms of translucency, turgor loss, or desiccation. The time to abscission was unaected by the ethylene treatment (Table 4). In a few experiments, tulip ¯owers of these cultivars were treated with ethylene when already fully open or close to wilting and abscission. Ethylene did not hasten abscission in these tests (results not shown). Three Saxifraga species (S. apiculata, S. x arendsii and S. litacina) showed petal abscission concomitant with slight wilting (translucency). The time to petal abscission in these species was also ethylene-insensitive (Tables 2 and 4). Relationship with taxonomic groups In the monocotyledons tested, petal abscission without concomitant wilting was not observed, except in some tulip cultivars (see above). The wilting response was generally insensitive to applied ethylene (Table 1). Exceptions were
van DoornÐEthylene Eects on Petal Wilting and Abscission the species tested in the Alismataceae and the Commelinaceae, which showed ethylene-sensitive wilting. A few other examples of ethylene-sensitive petals were found within monocotyledonous families containing mostly species with ethylene-insensitive petal wilting, such as the Amaryllidaceae (Table 1). In the Iridaceae species tested, ethylenesensitive petals were observed in the SisyrinchieaeÐa tribe in the classi®cation of Heywood (1978)Ðwhile the other species tested were ethylene-insensitive (Table 1). The types of response to ethylene were slightly more consistent within monocotyledous families according to the classi®cation of Dahlgren et al. (1985) than the classi®cation of Heywood (1978). In the former classi®cation, the genus Alstroemeria and some related species, and many liliaceous species were placed in separate families. Among the liliaceous species, most exceptions with regard to ethylene-sensitivity and type of response occurred in the Liliaceae sensu Dahlgren et al. (1985), and the response was not uniform in this group (Table 1). In dicotyledonous ¯owers, the type of response and its ethylene sensitivity were also generally consistent with families according to Heywood (1978), although a number of exceptions were observed. The exceptions may, at least in some families, be consistent with lower taxonomic categories. In the Ericaceae and Saxifragaceae, for example, the response was apparently consistent with subfamilies (Table 2). Abscission without concomitant wilting was, in most dicotyledonous ¯owers tested, hastened by applied ethylene. Families, according to the classi®cation of Heywood (1978), in which the petals of all species studied abscised (without prior wilting symptoms) include the Acanthaceae, Boraginaceae, Caprifoliaceae, Cruciferae, Gesneriaceae, Oleaceae, Papaveraceae, Portulacaceae, Rubiaceae, Scrophulariaceae and Valerianaceae. Abscission without concomitant wilting also occurred in two subfamilies of both the Ericaceae and the Saxifragaceae. In the Primulaceae, all genera tested showed ethylene-sensitive abscission, but three Primula species tested exhibited petal wilting following ethylene exposure. In the classi®cation of Heywood (1978), the genus Primula belongs to the subfamily Primuleae, and the other Primulaceae tested to the subfamily Lysimachieae. In some families the petals of most species abscised while showing slight wilting symptoms (Solanaceae and Fumariaceae). In the Solanaceae this response was highly ethylene-sensitive, but in the Fumariaceae species tested it showed only intermediate sensitivity (Table 2). The ethylene-insensitivity of the response of three Saxifraga species (abscission after slight wilting) has been described in the previous paragraph. Petal wilting in a number of dicotyledonous families sensu Heywood (1978) was advanced by exogenous ethylene (Aizoaceae, Campanulaceae, Convolvulaceae, Dipsacaceae, Lobeliaceae, Plumbaginaceae and Portulacaceae). Ethylene-insensitive petal wilting was rare in the dicotyledonous plants tested. It was observed throughout the Crassulaceae and Gentianaceae, in the Ericoidieae subfamily of the Ericaceae, and in the Saxifragoideae subfamily of the Saxifragaceae.
449
Preliminary results on the Umbelliferae contrasted with conclusions drawn in our previous paper, where two species (Anethum graveolens and Conium maculatum) showed ethylene-insensitive wilting. This ®nding was corroborated here. However, several other species showed ethylenesensitive abscission (Anthriscus sylvestris, Apium graveolens, Coriandrum sativum and Heracleum sphondylium). The number of species tested to date is insucient to allow conclusions to be drawn about the correlation with taxonomic categories within the family (results not shown). Heywood (1978) distinguished three subfamilies in the Leguminosae: Mimosoideae, Caesalpinioideae and Papilionideae. These groups are often considered families in other classi®cations, such as that of Cronquist (1988). The former group generally contains ¯owers without conspicuous petals but with showy stamens. Mimosoideae and Caesalpinioideae have not been investigated. Preliminary results in the Papilionideae subfamily showed ethylene-insensitive wilting in the tribes Trifolieae (three Trifolium species) and Loteae (Lotus corniculatus and Dorycnium hirsutus), and ethylene-sensitive wilting in the tribes Galegeae (Astralagus galeniformis) and Genisteae (Genista lydia) (results not shown). Compared with the classi®cation of Heywood (1978), the results show a somewhat higher degree of consistency with families as classi®ed by the Angiosperm Phylogeny Group (APG, 1998) using a molecular systematic approach. According to this classi®cation, the Saxifragaceae are a highly polyphyletic group. Both Hydrangeoideae and Ribesoideae are considered separate families, Hydrangeaceae and Grossulariaceae, respectively. The responses to ethylene in the remaining Saxifragaceae species tested, classi®ed according to APG (1998), are rather uniform. Some of the relevant dierences between the classi®cation of Heywood (1978) and APG (1998) are shown in Table 5. APG (1998) places the Lobeliaceae in the Campanulaceae. Species in both groups tested showed the same response to ethylene. In the liliaceous species, APG (1998) generally agrees with the classi®cation of Dahlgren et al. (1985). As discussed above, this also renders the response to ethylene more consistent with family than in the classi®cation of Heywood (1978). APG (1998) places the Funkiaceae sensu Dahlgren in the Agavaceae, and the Uvulariaceae in the Colchicaceae. These changes still result in uniform families with regard to the response to ethylene in the species tested. DISCUSSION The present results con®rm our previous report that petal abscission is generally highly sensitive to applied ethylene (Woltering and van Doorn, 1988). However, it is now established that the time to abscission, occurring without prior wilting or withering, is ethylene-insensitive in a few species. In the previous paper we distinguished three categories of ¯ower life cessation: ethylene-sensitive or ethylene-insensitive petal wilting, and ethylene-sensitive petal abscission. We now de®ne a fourth category, that of ethylene-insensitive abscission. We found three tulip cultivars in which the petals fell without prior wilting, where ethylene had no eect on the time to abscission
450
van DoornÐEthylene Eects on Petal Wilting and Abscission
T A B L E 1. Monocotyledons: response of the perianth to treatment with 3 ppm ethylene for 24 h in darkness at 208C Plant family (Tribe)
Species
Type of response
Response classi®cation
Agavaceae
Polianthes tuberosa Sansevieria sp.
w w
0 0
Alismataceae
Alisma parvi¯ora Baldellia ranunculoides Sagittaria lancifolia
w w w
4 4 4
Amaryllidaceae
Alstroemeria peregrina (r) Cyrtanthus purpureus Galanthus nivalis Hippeastrum x ackermannii Narcissus pseudonarcissus (r) Nerine bowdenii (r) Zephyranthes candida
wa w w w w w w
2±31 2 0 3 0 0 0
Cannaceae
Canna hybrid (3 cultivars)
w
0
Commelinaceae
Commelina sp. Tradescantia hybrid Zebrina pendula
w w w
4 4 3
Haemodoraceae
Anigozanthos spp. (3 species)
w
0
Chasmanthe aethiopica Crocus chrysanthus Gladiolus hybrid (r) Tritonia crocata Iris germanica Iris halophyta Iris sibirica Tigridia pavonia Crocosmia x crocosmii¯ora (r) Freesia hybrids (r) Ixia ¯exuosa Sisyrinchium angustifolium Sisyrinchium californicum Sisyrinchium laevigatum
w w w w w w w w wa w w w w w
0 0 0±1 0 0 0 0 0 1±2 0 0 4 4 4
Allium cernuum Brodiaea californica Bloomeria aurantiaca Nothoscordum aureum Triteleia laxa Tulbaghia violacea Asphodelus albus Asphodeline lutea Eremurus (hybrid) (r) Knipho®a (hybrid) (r) Colchicum autumnale Colchicum speciosum Gloriosa superba (r) Ornithoglossum parvi¯orum Sandersonia aurantiaca Convallaria majalis Liriope koreana Polygonatum odoratum Hosta lancifolia Hosta latifolia Hosta tardiana Hosta undulata Hemerocallis lilio-asphodelus Hemerocallis `Invictus' Hemerocallis `Mabel Fuller' Hemerocallis `Mrs. J. Tigert' Hemerocallis `Black Prince'
w w w w w w w w w w w w w w w w w w w w w w w w w w w
0 0 3 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Iridaceae (Croceae) (Gladioleae) (Irideae)
(Ixieae) (Sisyrinchieae)
Liliaceae [Alliaceae]
[Asphodelaceae]
[Colchicaceae]
[Convallariaceae] [Funkiaceae]
[Hemerocallidaceae]
Table continued over page
van DoornÐEthylene Eects on Petal Wilting and Abscission
451
T A B L E 1. Continued Plant family (Tribe) Liliaceae [Hyacinthaceae]
[Liliaceae]
[Uvulariaceae]
Species Camassia quamash Camassia leichtlinii Eucomis bicolor Galtonia candicans Galtonia sp. Hyacinthus orientalis Hyacinthoides non-scipta Lachenalia sp. Muscari armeniacum Ornithogalum thyrsoides (r) Erythronium americanum Lilium martagon Lilium hybrid (r) Brunello (Oriental hybrid) Montenegro (Oriental) Star Gazer (Aseatic hybrid) Woodru Memory (As.) Tulipa gesneriana (r) Tricyrtis latifolia
Type of response
Response classi®cation
w w w w w w w w w w wa wa
0 0 0 0 0 1±2 0 0 0±1 0 3 3
w w w w w or wa (most cultivars) a (some cultivars) w
1 0 2 0±1 1±2 (Table 3) 0 (Table 4) 0
1 The Alstroemeriaceae are a separate family in the system of Dahlgren et al. (1985). The perianth showed wilting or withering (w) or abscission (a). Wilting or withering also occurred concomitantly with abscission (wa). The time to the response is expressed in categories 0±4, de®ned in the text. Some ¯owers, indicated by `r', have also been tested previously (Woltering and van Doorn, 1988). Taxonomic classi®cation according to Heywood (1978) or, between square brackets, according to Dahlgren et al. (1985).
(Table 4). Absence of an eect of ethylene was also found when the ¯owers were treated at later stages of development. In roses, we previously observed that ethylene application did not aect abscission until the ¯owers were fully open and close to abscission (Woltering and van Doorn, 1988). In contrast, petal abscission in tulip ¯owers remained insensitive to ethylene even until shortly before they abscised. In tulip `Golden Apeldoorn', petal wilting generally preceded abscission. Although the time to wilting was slightly sensitive to ethylene (Table 3), we found that the time to petal abscission in this cultivar was also independent of ethylene treatment and not aected by ethylene inhibitors (Sexton et al., 2000). Three Saxifraga species also exhibited ethylene-insensitive abscission, which occurred concomitantly with slight liquid logging (Tables 2 and 4). Preliminary experiments with the Lilium hybrid `Montenegro' (belonging to the Oriental group of cultivars) also indicated ethylene-insensitive abscission, which occurred about 2 d after petal wilting (liquid logging and turgor loss; unpubl. res.). As in our previous work, the types of cessation of ¯ower life (and the sensitivity to ethylene) were generally consistent within plant families according to the classi®cation of Heywood (1978). However, it was observed here that in some families such consistency was apparent at the subfamily level, for example in the Ericaceae and Saxifragaceae. According to a more recent classi®cation (APG, 1998), the former Saxifragaceae are a polyphyletic group with Hydrangeaceae and Glossulariaceae ( formerly Ribesoideae) separate from Saxifragaceae. This would give consistency at the family level in the Saxifragaceae. According to the APG classi®cation, however, the consistency is still apparent at the subfamily level in the
Ericaceae. Such consistency at the subfamily level may also occur in the Iridaceae, but this conclusion is based on a rather small number of species tested in each of the tribes. The genus Sisyrinchium may be an exception, rather than the tribe Sisyrinchieae. Similarly, in the Primulaceae the genus Primula (subfamily Primuleae) may be an exception rather than the entire subfamily. More than a century ago, Reiche (1885) investigated the end of the natural perianth lifespan in ¯owers. His results are in close agreement with the present ®ndings. In the Boraginaceae, for example, petals fell in all 11 genera investigated. In the Ericaceae, two groups were found: one, comprising Azalea, Vaccinium and Pirola, showed petal abscission, and the other, including Calluna and Erica, exhibited petal wilting. In the Gentianaceae and several Leguminoseae, the corolla or petals were found to wilt. In the only Plumbaginaceae species tested (Armeria vulgaris), the petals wilted then were torn from the ¯ower by the growing fruit. In the Primulaceae, the general response was petal abscission, although in the genus Primula the petals wilted. Within the Solanaceae, the species investigated generally showed petal fall, sometimes with concomitant wilting. Similarly, McKenzie and Lovell (1992) observed the types of ¯ower life cessation in a large number of monocotyledons. They found numerous genera in which the petals wilted or withered and a relatively low number of genera in which the petals wilted and abscised almost concomitantly. No examples were found of ¯owers that showed petal abscission without prior wilting, a result that wasÐexcept for a few tulip cultivarsÐcon®rmed in our experiments. Although a number of exceptions were noted, a correlation was found between the types of symptoms and
452
van DoornÐEthylene Eects on Petal Wilting and Abscission T A B L E 2. Dicotyledons: response of the perianth to treatment with 3 ppm ethylene for 24 h darkness at 208C
Plant family (Subfamily)
Species
Type of response
Response classi®cation
Acanthaceae
Acanthus hungaricus Acanthus spinosus Crossandra sp. Thunbergia alata
a a a a
4 4 4 4
Aizoaceae
Carpathea pomeridiana Delospermum cooperi Delospermum lyndenburgensis Dorotheanthus bellidiformis Lithops dorothea Mesembryanthemum productus
w w w w w w
4 3 4 4 3 3
Boraginaceae
Borago ocinalis Brunnera macrophylla Buglossoides purpurocaerulea Echium plantagineum Lindolo®a stylosa Mertensia paniculata Omphalodes verna Pulmonaria ocinalis Symphytum cordatum Symphytum grandi¯orum Symphytum ottomanum
a a a a a a a a a a a
4 4 4 4 4 4 4 4 4 4 4
Campanulaceae
Campanula garganica Campanula glomerata Campanula pyramidalis (r) Edraianthus graminifolius Phyteuma scheuchzeri Trachelium caeruleum (r)
w w w w w w
4 3 4 3 2 3
Caprifoliaceae
Abelia schumanii Leicesteria formosa Lonicera x heckrottii `Gold¯ame' Sambucus nigra Viburnum henryi Viburnum lobophyllum Weigela ¯orida Weigela `Gustave Mallet'
a a a a a a w w
4 4 4 4 4 4 0 0
Convolvulaceae
Ipomoea alba Convolvulus arvensis Quamoclit coccinea
w w w
4 4 4
Crassulaceae
Crassula falcata Echeveria setosa KalanchoeÈ blossfeldiana Sedum hybrid Sedum spectabile Sedum spurium Sempervivum sp.
w w w w w w w
0 0 2 0 0 1 0
Cruciferae
Alliaria petiolata Arabis caucasia Brassica napus Cardamine pratensis Cheiranthus sp. Erysimum cuspidatum Lunaria rediviva Matthiola incana (r)
a a a a a a a w1
4 4 4 4 4 3 4 2
Dipsacaceae
Cephalaria alpina Cephalaria gigantea Scabiosa caucasia (r) Succisella in¯exa (r)
wa wa w w
2±3 2 2±3 3 Table continued over page
van DoornÐEthylene Eects on Petal Wilting and Abscission
453
T A B L E 2. Continued Plant family (Subfamily)
Type of response
Response classi®cation
Calluna vulgaris Erica gracilis Erica hiemalis Erica tetralix Pieris japonica Andromeda sp. Kalmia latifolia Rhododendron brachycarpum Rhododendron hybrid (several cvs) Gaultheria shallon Leucothoe axillaris Leucothoe walterii Vaccinium macrocarpon
w w w w w a a a a a a a a
0 0 0 0 0 3 4 4 4 3 3 3 4
Fumariaceae
Corydalis sp. Dicentra formosa Dicentra hybrid Fumaria sp.
wa wa wa wa
2 2 2 2
Gentianaceae
Exacum ane Gentiana dahurica Gentiana kochiana Gentiana sino-ornata Sabatia sp.
w w w w w
0 0 0 0 0
Gesneriaceae
Aeschynanthus sp. Columnea krakatau Columnea nesse Kohleria hybrid `Eriantha' Saintpaulia confusa Saintpaulia tongwensis Sinningia cardinalis Streptocarpus hybrid
a a a a a a a a
4 4 4 4 4 4 4 4
Lobeliaceae
Laurentia ¯uviatilis Lobelia cardinalis Lobelia siphylitica Monopsis sp.
w w w w
3 3 2±3 3
Oleaceae
Forsythia x intermedia Jasmium ocinale Ligustrum ovalifolium Syringa vulgaris
a a a a
4 4 4 4
Papaveraceae
Chelidonium majus Eschscholzia sp. Papaver rhoeas
a a a
4 4 4
Plumbaginaceae
Armeria maritima Armeria pseudoarmeria Ceratostigma plumbaginoides Limonium latifolium Plumbago auriculata
w w w w w
3 4 4 3 4
Portulacaceae
Claytonia sp. Lewisia cotyledon Portulaca grandi¯ora Portulaca umbraticola
w w w w
3 4 4 4
Primulaceae
Anagallis arvensis Cyclamen hybrid Lysimachia clethroides (r) Lysimachia punctata Primula denticulata Primula rosea `Grandi¯ora' Primula vialii
a a a a wa wa w
3 4 4 4 2±3 2±3 2
Ericaceae (Ericoideae)
(Rhododendroideae)
(Vaccinioideae)
Species
Table continued over page
454
van DoornÐEthylene Eects on Petal Wilting and Abscission T A B L E 2. Continued
Plant family (Subfamily)
Species
Rubiaceae
Asperula tinctoria Galium aparine Incarvillea delavayi Ixora hybrid Pentas lanceolata Rubia tinctorum
Saxifragaceae (Hydrangeoideae) (Ribesoideae) (Saxifragoideae)
Deutzia scabra `Macropetala' Deutzia schneideriana Ribes aureum Bergenia cordifolia Saxifraga apiculata `Gregor Mendel' Saxifraga x arendsii `Schneeteppich' Saxifraga litacina Tiarella cordifolia
Scrophulariaceae
Antirrhinum majus (r) Calceolaria sp. Gratiola ocinalis Phygelius sp. Penstemon cobaea Penstemon heterophyllus Penstemon serrulatus Torenia hybrid Veronica orchidea (r)
Solanaceae
Iochroma hybrid Lycopersicon esculentum Nicotiana tabacum Nierembergia sp. Petunia hybrid Solanum dulcamara
Valerianaceae
Centranthus ruber `Albus' Centranthus ruber `Coccineus' Patrinia gibbosa Valeriana ocinalis
Type of response
Response classi®cation
a a a a a a
3 3 4 3 4 3
a a a w wa wa wa w
4 4 3 0 0 0 0 0
a a a a a a a a a
3 4 3 3 4 4 3 4 4
wa wa wa wa wa w
3 4 4 3 4 3
a a a a
3 3 3 4
1 The early wilting in Matthiola incana cut ¯owers is apparently due to a vascular occlusion. The perianth showed wilting or withering (w) or abscission (a). Wilting or withering also occurred concomitantly with abscission (wa). The time to the response is expressed in categories 0±4, de®ned in the text. Some ¯owers, indicated by `r', have been tested previously (Woltering and van Doorn, 1988). Taxonomic classi®cation according to Heywood (1978).
the plant families, at least when using the classi®cation of Dahlgren et al. (1985). Most exceptions were found in the Iridaceae, where some genera showed petal wilting and others abscission concomitant with wilting. These results were largely con®rmed here. In Lilium martagon, petals fell just as they showed the very ®rst symptoms of wilting (translucency) (Table 1). In all cultivars of commercial cut lily ¯owers (both the Asiatic and Oriental type of cultivars), the present tests showed petal fall after symptoms such as liquid logging (translucency) and turgor loss. In the Oriental cultivars tested, the time between these wilting symptoms and petal fall was short (1±2 d), whereas in the Asiatic cultivars this span was as much as 5±6 d. This con®rms our previous work. McKenzie and Lovell (1992) interpreted our previous data on lily ¯owers as indicating no petal fall following wilting. We did, however, also observe petal abscission some days after wilting in all commercial lily cultivars previously studied. Most monocotyledonous families fall into one category, namely that of ¯owers showing ethylene-insensitive wilting. Exceptions include ethylene-sensitive wilting in the
Alismataceae and Commelinaceae, and in the previously investigated Orchidaceae. In contrast to monocotyledons, dicotyledonous ¯owers were generally sensitive to ethylene. One large family (Compositae) is an exception (Woltering and van Doorn, 1988), and in the present tests the petals in a few other groups, classi®ed as subfamilies, were also ethylene-insensitive. The majority of these dicotyledonous families tested exhibit petal abscission prior to any signs of wilting. In some species, petal fall may not be due to true abscission but to ovary growth. According to Reiche (1885) this occurs in several species of, for example, the Boraginaceae, Cucurbitaceae, Labiatae (Lamiaceae), Malvaceae, Plumbaginaceae and Solanaceae. If this claim is correct, a distinction should be made between groups in which petal fall is due to true abscission and those in which it is due to ovary growth. Ethylene treatment stimulates ovary growth, at least in some species (Nichols, 1971; Han et al., 1991). Ethylene-induced ovary growth may therefore advance the purported petal tearing. If ethylene-sensitive petal fall is recorded, it may thus be due, at least in some
van DoornÐEthylene Eects on Petal Wilting and Abscission T A B L E 3. Eects of applied ethylene (3 ppm for 24 h in darkness at 208C) on some Tulipa cultivars in which the perianth showed wilting (w) or wilting shortly followed by abscission (wa) Cultivar
Type of response
Abba Atilla Barcelona Bastogne Blenda Golden Apeldoorn Leen van der Mark Lucky Strike Lustige Witwe Monte Carlo Negrita Prominence Pink Impression Recreado White Dream Yokohama
w (sometimes w w w w w w (sometimes w w (sometimes w w w w (sometimes w w w
wa)
wa) wa)
wa)
Response classi®cation 1 1 1 1 1 1±2 1 2 1 1 1 1 2 1 1±2 1
455
species, to an ethylene eect on ovary development rather than on true petal abscission. In dicotyledonous plants, a further 20 families have now been studied that had not previously been investigated, increasing the total number of families tested, according to the classi®cations of Heywood (1978) and APG (1998), to 36. In the monocotyledons, depending on the classi®cation used, ®ve or more additional families have now been investigated. Nonetheless, the present experiments still include only a small number of genera from each of the families and subfamilies tested. It is concluded that the three types of the cessation of ¯ower life as de®ned earlier are, as a rule, consistent with families or subfamilies. A fourth category, ethyleneinsensitive petal abscission (without prior wilting) has also been observed. It occurred only in a few species, and was found both in monocotyledons and dicotyledons. AC K N OW L E D G E M E N T S
The time to the response is expressed in categories 0±4, de®ned in the text.
I am grateful to Rene Perik for growing some bulbous ¯owers, Delphine Raze and Laetitia Brunnevalle for
T A B L E 4. Eects of applied ethylene (3 ppm for 24 h in darkness at 208C) on three Tulipa cultivars in which the perianth abscised (a) without wilting symptoms, and in three Saxifraga species in which the petals fell concomitant with wilting (liquid logging) Time to abscission (d)
Type of response
Response classi®cation
Controls
Treated
a a a
0 0 0
9.3 + 1.1 7.9 + 0.7 11.0 + 1.3
9.4 + 0.8 7.9 + 1.0 10.5 + 1.0
Species
Cultivar
Tulipa gesneriana
Ad Rem Gander's Rhapsody Rosario
Saxifraga apiculata
Gregor Mendel
wa
0
5.2 + 1.5
5.9 + 1.4
Saxifraga x arendsii
Schneeteppich
wa
0
5.0 + 1.9
4.8 + 1.3
0
4.1 + 0.8
4.4 + 0.6
Saxifraga litacina
wa
Data on time to abscission are means + s.d. of ten ¯owers. Response is expressed in categories 0±4, de®ned in the text. The time to abscission (of more than half of the petals) was determined from the commercial harvesting stage (closed bud, in ¯owers placed individually in water at 208C, 65 % RH and 12 h white light (15 mmol m ÿ2 s ÿ1) and 12 h darkness.
T A B L E 5. Comparison of the taxonomic classi®cation of APG (1998) with that of Heywood (1978) and Dahlgren et al. (1985) Monocotyledons APG (1998) groups the liliaceous species into families similar to Dahlgren et al. except Funkiaceae, which are included in Agavaceae, and Uvulariaceae, which are included in Colchicaceae Eudicotyledons APG (1998) includes some species from the Caprifoliaceae, such as Sambucus and Viburnum, in Adoxaceae Lobeliaceae: included in Campanulaceae by APG Saxifragaceae: Hydrangeoideae a separate family (Hydrangeaceae) according to APG Ribesoideae a separate family (Grossulariaceae) according to APG Only a few changes, relevant to the present paper, are shown. In APG (1998) the basal-most angiosperms have been subtracted from the dicotyledons, and the remaining dicotyledons are called eudicotyledons. Data partially based on personal communication with Peter Endress (2000).
456
van DoornÐEthylene Eects on Petal Wilting and Abscission
carrying out repeat experiments, Dr Roy Sexton for critical discussions, and Dr Jan J. Bos (Department of Taxonomy, Wageningen University) for permission to harvest ¯owers in the botanical garden. L I T E R AT U R E C I T E D APG (The Angiosperm Phylogeny Group). 1998. An ordinal classi®cation for the families of the ¯owering plants. Annals of the Missouri Botanical Garden 85: 531±553. Cronquist A. 1988. The evolution and classi®cation of ¯owering plants. 2nd edn. New York: New York Botanical Garden. Dahlgren RMT, Cliord HT, Yeo PF. 1985. The families of the monocotyledons: structure, evolution and taxonomy. Berlin: Springer Verlag. Heywood VH. 1978. Flowering plants of the world. Oxford: Oxford University Press. Han S, Halevy AH, Reid MS. 1991. The role of ethylene and pollination in petal senescence and ovary growth of Brodiaea. Journal of the American Society for Horticultural Science 116: 68±72.
McKenzie RJ, Lovell PH. 1992. Flower senescence in monocotyledons: a taxonomic survey. New Zealand Journal of Crop and Horticultural Science 20: 67±71. Nichols R. 1971. Induction of ¯ower senescence and gynoecium development in the carnation (Dianthus caryophyllus) by ethylene and 2-chloroethylphosphonic acid. Journal of Horticultural Science 46: 323±332. Reiche C. 1885. UÈber anatomische VeraÈnderungen, welche in den Perianthkreisen der BluÈten waÈhrend der Entwickelung der Frucht vor sich gehen. JahrbuÈcher fuÈr wissenschaftliche Botanik 16: 638±687. Sexton R, Laird G, van Doorn WG. 2000. Lack of ethylene involvement in tulip tepal abscission. Physiologia Plantarum 108: 321±329. Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb DA. 1964. Flora Europaea, Volumes 1±5. Cambridge: Cambridge University Press. van Doorn WG. 1997. Eects of pollination on ¯oral attraction and longevity. Journal of Experimental Botany 48: 1615±1622. Woltering EJ, van Doorn WG. 1988. Role of ethylene in senescence of petalsÐmorphological and taxonomical relationships. Journal of Experimental Botany 39: 1605±1616.