Biol. Rev. (1998), 73, pp. 157–180 Printed in the United Kingdom # Cambridge Philosophical Society 157 Labile sex expression in plants

HELENA KORPELAINEN Department of Biosciences, Division of Genetics, P.O. Box 56, FIN-00014 University of Helsinki, Finland

(Received 27 February 1997; revised 12 September 1997; accepted 30 October 1997)

ABSTRACT

The range of environmental sex determination and sex changes throughout plant taxa from bryophytes and pteridophytes to spermatophytes is reviewed. Lability in sex expression occurs in many plant taxa but only in homosporous pteridophytes is labile sex the rule. Among angiosperms, labile sex appears to be more common among dioecious and monoecious plants than among hermaphrodites. However, hermaphrodites can control allocation to male and female functions by varying the relative emphasis on pollen and ovules. A majority of plants with labile sex expression are perennials, which indicates that flexibility in sex is more important for species with long life cycles. Environmental stress, caused by less-than-optimal light, nutrition, weather or water conditions, often favours maleness. The extreme lability in the sex expression of homosporous pteridophytes is suggested to be related primarily to the mating systems.

Key words: labile sex, adaptation, Bryophyta, Pteridophyta, Spermatophyta.

CONTENTS

I. Introduction ...... 157 II. Bryophyta...... 158 III. Pteridophyta...... 159 IV. Spermatophyta ...... 172 V. Conclusions...... 174 VI. References...... 174

I. INTRODUCTION the traditional morphological descriptions (Lloyd, 1980a). The functional gender of a plant estimates Sex expression is considered to have a strong the proportions of its genes which are transmitted environmental component when sex is determined through male or female gametes. Although estimates or changed at some point after fertilization. The of functional gender provide an ideal measure of the term sex expression refers here to male and female gender strategies of plants as sexual parents, they do individuals of dioecious plants, or to male and female not necessarily correspond with the actual success of flowers or gametangia of monoecious plants, or to a plant in leaving descendants through its male and hermaphrodism. Variation in the relative emphasis female gametes (Lloyd, 1980a). on pollen\sperm and ovules\eggs among mon- Why do various organisms then possess labile oecious or hermaphroditic plants is generally not systems instead of strictly genetic systems that included here. Sexually labile plants have the determine a fixed sex expression? Following the sex potential to have either male, female or both sex ratio model presented by Trivers & Willard (1973), organs, with some environmental feature deter- Charnov & Bull (1977) proposed a now classic mining which genes are switched on. However, such model to account for the adaptiveness of environ- simplified morphological descriptions of gender have mental sex determination in particular life histories. limitations. When analysing the adaptive signifi- They postulated that environmental sex determi- cance of gender variation, numerical estimates of the nation is favoured by natural selection when an relative capabilities of plants as male and female individual’s fitness as a male or female is strongly parents (functional gender) have advantages over influenced by environmental conditions and when 158 H. Korpelainen the individual has little control over which en- expressions within the same clone. Therefore, the sex vironment it will experience. The requirement for expression of sexually labile clonal plants is ramet- the evolution and maintenance of environmental sex specific and not genet-specific. determination is the ability to recognize an en- vironmental factor which differentially correlates with male or female fitness. Thus, labile sex II. BRYOPHYTA expression, through which an individual can increase its genetic contribution to future generations, is an Bryophytes are generally treated as a single division adaptation to certain life histories. including three classes: Anthocerotae (hornworts), Despite controversy over the adaptive significance Hepaticae (liverworts) and Musci (mosses). They of labile sex expression in plants (see Freeman, possess an alternation of generations in which the life Harper & Charnov, 1980; Lloyd & Bawa, 1984), sex cycle involves a free-living, haploid gametophyte changes appear generally advantageous and can be alternating with a reduced, dependent, diploid viewed as adaptations to patchy environments. sporophyte. Bryophytes are considered structurally However, some variation may result from the simple compared to vascular plants. Although inability of a plant to control its sex precisely in a bryophytes are homosporous, approximately 68% of complex environment. Such rare and irregular liverworts and 57% of mosses are dioecious (Wyatt inconstancies are hardly adaptive (Lloyd & Bawa, & Anderson, 1984; Wyatt, 1985). Hornworts are 1984). regarded as being approximately equally divided In the present paper, I review the range of between monoecious dioecious species (Longton & environmental sex determination and sex changes Schuster, 1983). In general, dioecy is considered to throughout plant taxa from bryophytes and pteri- be a primitive feature in bryophytes. The evolution dophytes to spermatophytes, and I explore the con- of monoecy has apparently occurred independently ditions that influence sex expression. Among labile in many lines (Longton & Schuster, 1983). Despite sex expressions, two categories can be distinguished. homospory, two ranges of spore sizes have been First, sex is influenced by the environment at some found in dioecious species (Chattopadhyay & point after fertilization. Sex then becomes fixed and Sharma, 1991). There is evidence that smaller spores is not amenable to further modification. Several give rise to male gametophytes and larger spores to studies have shown that such environmental effects females. Several species of dioecious bryophytes occur in a diverse range of animals (reviewed by possess distinguishable sex chromosomes (Anderson, Korpelainen, 1990). In plants, environmental effects 1980; Ramsay & Berrie, 1982; Chattopadhyay & on sex usually belong to the second category, Sharma, 1991). sequential hermaphrodism, in which sex is labile Although chromosomal sex determination is ex- during the reproductive lifespan. The choice of pected to result in a 1:1 production of male and gender can be made repeatedly or for a lifetime. In female spores, several investigations have detected animals, sequential hermaphrodism is a rare pheno- biased sex ratios in dioecious bryophytes (Wyatt & menon apparently because an early development of Anderson, 1984; Longton, 1990). Females outnum- fixed sexual differences enables an individual to ber males in most species that have been studied. better learn its sex role and become more successful Sterile gametophytes bearing neither male nor at mating and parenting. Despite the widespread female gametangia are also common in many occurrence of labile sex determination, the majority populations. Asexual methods of gametophyte re- of plants exhibit a fixed genetic sex expression, production are important in most mosses and in mostly hermaphrodism. The dioecious system with numerous hepatics (Longton & Schuster, 1983). It is separate male and female individuals is quite rare in also of minor importance in anthocerotes. Some plants, but is the rule in animals. bryophyte species have the ability to produce also Both genetic and environmental sex-determi- sporophytes asexually (Bopp, 1983). The rarity or nation mechanisms are sometimes found in closely the total absence of sporophyte production is usually related plant species, even within the same species. associated with the dioecious condition (Longton & Also, the degree of lability varies. In the case of Schuster, 1983). clonal growth, which is common among plants, Many monoecious bryophytes express temporal different parts of the clone (genet) may encounter variation in sex distribution (Anderson & Lemmon, different environmental conditions. If environment 1973, 1974; Longton & Miles, 1982; Shaw, 1991). influences sex expression, there may be varying sex In most cases, it is not known how such temporal Labile sex expression in plants 159 patterns in sex expression are controlled. However, b). The bisexual gametophytes of pteridophytes are there is some indication that environmental factors called hermaphrodites. Yet, a more appropriate have at least some effect (Table 1). In the mon- characterization would be monoecious, because the oecious species Tetraphis pellucida, sex expression antheridia and archegonia are produced in different is sensitive to density: male shoots dominate at locations on the same thallus. Unlike the other increased densities (Kimmerer, 1991). In some bryo- heterosporous pteridophytes, which are unisexual, phytes, the nutrient concentration of the medium the gametophytes of genus Platyzoma are partially can also influence sex differentiation (Selkirk, 1979). bisexual. The small spores produce male gameto- In the dioecious moss Bryum argenteum, maleness was phytes, and the large spores initially become female stimulated by auxin and gibberellin treatments, but but subsequently produce antheridia (Tryon, 1964). femaleness was stimulated by cytokinins (Bhatla & However, this pattern of sex expression is labile. Chopra, 1981). When the effects of some growth- Duckett & Pang (1985) have observed in Platyzoma relating substances on sex expression in the mainly microphyllum that subculturing of gametophyte frag- vegetative liverwort Riccia crystallina were studied, ments originating from either kind of spores resulted gibberellin and ethrel were found to enhance in males, females or hermaphrodites. The sex antheridial formation while auxin and glycocel were expression varies according to the type of the found to promote archegonial development (Chopra fragment rather than the kind of spore from which & Sood, 1973). Yet, some of the environmental the material is derived. In this case, the sex- effects might induce sexual reproduction in place of determining process has been transferred from the asexuality rather than influence the type of sex sporophyte to the gametophyte stage of the life cycle. expression. It can be assumed that the sex expression The sex expression of all homosporous pterido- of many monoecious bryophytes is labile and is phytes is labile. The choice between sex expressions influenced by the environment. However, there is a is determined by the age and size of the gametophyte considerable lack of experimental data on sex or by the presence of the gibberellin-like hormone determination in bryophytes. antheridiogen secreted by neighbouring gameto- phytes (Table 1). In schizaeaceous fern species and in some dryopterids, gibberellins have been found III. PTERIDOPHYTA to possess antheridiogenic properties (Schraudolf, 1962, 1966; Voeller, 1964a, b). In the absence of Pteridophytes, including ferns and fern allies, can be an antheridiogen, the most common sequence of classified as homosporous or heterosporous. They gametangial sex expression is male-hermaphrodite possess an alternation of generations in which the life (Klekowski, 1969a). The other possible sequences cycle involves a small, free-living, haploid gameto- are male–female–hermaphrodite, female–hermaph- phyte alternating with a large, independent, diploid rodite and male–hermaphrodite–female. In the sporophyte. Homosporous species, which form the genus Equisetum, gametophytes are initially male or majority of pteridophytes, produce spores of one size female. The females later produce antheridia, but while heterospores species produce spores of one size the males rarely produce archegonia (Duckett, while heterosporous species produce spores of two 1977). This result proves that there are no inherent size classes. Heterospory is restricted to the fern allies physiological differences between the spores in Isoetaceae and Selaginellaceae, to the aquatic ferns relation to gametophyte sex expression. Yet, most in the families Azollaceae, Marsileaceae and Salvini- gametophytes of homosporous pteridophytes finally aceae, and to the terrestrial fern genus Platyzoma develop as hermaphrodites, which produce egg- (Pteridaceae). Other heterosporous groups are forming archegonia, sperm-forming antheridia and known only from the fossil record. Heterosporous a well-defined meristem. Since the initial discovery forms are believed to have evolved from homo- by Do$ pp (1950) of an antheridiogen system con- sporous ancestors on several occasions (Haig & trolling sex expression in the gametophytes of Westoby, 1988). The smaller microspores and larger Pteridium aquilinum, the majority of homosporous megaspores of heterosporous species develop into pteridophytes tested have been found to produce haploid male and female gametophytes, respectively. and to respond to antheridiogen (for reviews, see This contrasts with homosporous species in which Voeller, 1964a;Na$f, Nakanishi & Endo, 1975). In spores of the same size may develop as haploid male, such populations, spores that germinate and develop female or hermaphroditic gametophytes (e.g. Smith, rapidly become hermaphrodites that secrete antheri- 1955; Klekowski & Lloyd, 1968; Klekowski, 1969a, diogen, while those that develop more slowly be- 160 H. Korpelainen . ! ); Singh & Roy b , a ) ) ) a a a means a change male , 1970 b , a K!L f (1956) f (1956) f (1959) pp (1950) $ $ $ $ (1969 (1977); Lloyd & Warne(1979); (1978); Masuyama Cousens (1979);(1994, Korpelainen 1995) Bhatla & Chopra (1981) Bhatla & Chopra (1981) Kimmerer (1991) Klekowski & Lloyd (1968); Klekowski Chopra & Sood (1973) Chopra & Sood (1973) Tryon & Vitale (1977) Voeller (1964 Na Voeller (1964 Na Voeller (1964 Na Do male; ! veg. Selkirk (1979) veg. Selkirk (1979) L!K L"K L!K L"K L" L"K L"K L"K L"K L!K L" L"K L"K L"K L"K L"K It is shown in parentheses whether the environmental effect . hermaphrodism \ The direction in which the emphasis in sex expression is altered is ). E ( ). female An asterisk indicates that the species is reported to have heteromorphic sex chromosomes ! . hermaphrodism or monoecy \ GRS (E): cytokinin Environmental factorGRS (E): gibberellin, ethrel Direction Reference monoecy or in manipulative experiments ! ) hermaphrodism Life history F \ ( female , male ! include exogenous treatments by hormones and other chemicals ) DioecyMonoecy PerennialHermaphrodism GRS (E): Perennial auxin, gibberellin Perennial Age, size (E) High density (F) (Vegetative) Perennial Low nutrition (E) Hermaphrodism PerennialHermaphrodism Antheridiogen absent (E) Perennial Antheridiogen absent (E) Hermaphrodism Perennial Antheridiogen absent (E) Main form of sexuality (Vegetative)(Vegetative) Perennial GRS (E): auxin, glycocel Perennial Low nutrition (E) Hermaphrodism Perennial Antheridiogen absent (F) HermaphrodismHermaphrodism Perennial Perennial Antheridiogen absent (E) Hermaphrodism Antheridiogen absent (E) Perennial Antheridiogen absent (E) Hermaphrodism Perennial Antheridiogen absent (E) GRS ( hermaphrodism or monoecy \ monoecy means a change female ! Environmental factors influencing sex expressing in plants virginica regulating substances male L!K rhenana fluitans gibbum - . ( . . . , punctilobula Bryum argenteum Tetraphis pellucida Homosporous species R Doodia media W Pteridium aquilinum Riccia crystallina R Asplenium pimpinellifolium Blechnum brasiliense B Woodwardia areolata Dennstaedtia Bryaceae Tetraphidaceae Species Ricciaceae Aspleniaceae Blechnaceae Dennstaedtiaceae Musci Pteridophyta Table 1. Growth Taxon Bryophyta Hepaticae female has been observed in natural conditions in the field shown Labile sex expression in plants 161 . (1975) et al f $ ) ) ) ) ) a a a a a . (1969) f (pers. obs.) in Na $ et al f (1956) pp (1959) f (1956) pp (1959, 1962) f (1965) f f (1956) f (1969) f (1959) f (1960) f (1969) $ $ $ $ $ $ $ $ $ $ $ Schneller (1979) Na Haufler & Ranker (1985) Haufler & Ranker (1985) Schneller (1981) Voeller (1964 Schraudolf (1966) Schneller (1981) Barker & Willmot (1985) Kirkpatrick & Soltis (1992) Do Na Do Voeller (1964 Na Schraudolf (1966) Klekowski & Lloyd (1968) Na Haufler & Gastony (1978) Na Voeller (1964 Na U. Na Na Duckett (1977) Hauke (1977) Voeller (1964 Na Na Chiou & Farrar (1997) Chiou & Farrar (1997) Chiou & Farrar (1997) Chiou & Farrar (1997) Chiou & Farrar (1997) Chiou & Farrar (1997) Voeller (1964 Chiou & Farrar (1997) L"K L"K L"K L"K L"K L"K L"K L%K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L%K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K Antheridiogen absent (E) Antheridiogen absent (E) Antheridiogen absent (E) Antheridiogen absent (E) GRS (E): gibberellin removed Antheridiogen absent (E) Antheridiogen absent (E) Antheridiogen absent (E) ? (E) GRS (E): gibberellin removed Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism Antheridiogen absent (E) Perennial Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism Antheridiogen absent (E) Perennial Antheridiogen absent (E) Hermaphrodism Perennial Antheridiogen absent (E) HermaphrodismHermaphrodism Perennial Perennial Antheridiogen absent (E) Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism Perennial Antheridiogen absent (E) Perennial Antheridiogen absent (E) Antheridiogen absent (E) HermaphrodismHermaphrodism Perennial Perennial Antheridiogen absent (E) Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism Antheridiogen absent (E) PerennialHermaphrodism Antheridiogen absent (E) Perennial Antheridiogen absent (E) HermaphrodismHermaphrodism Perennial Perennial Antheridiogen absent (E) Antheridiogen absent (E) HermaphrodismHermaphrodism PerennialHermaphrodism Perennial Antheridiogen absent (E) Perennial Antheridiogen absent (E) Hermaphrodism Antheridiogen absent (E) Hermaphrodism Perennial Perennial Antheridiogen absent (E) Hermaphrodism Antheridiogen absent (E) Hermaphrodism Perennial Perennial Antheridiogen absent (E) Antheridiogen absent (E) femina - sp. Dioecy Perennial ? (E) mas simense - - filix hirsutula thelypterioides robertianum tennesseensis tsus phyllitidis pellucidum ...... struthiopteris acrostichoides angustifolium heterophylla scolopendria Cystopteris protrusa Matteuccia Onoclea sensibilis Tectaria incisa Equisetum Aglaomorpha meyeniana Campyloneurum Athyrium filix A C Dryopteris affinis D Gymnocarpium dryopteris G Polystichum P Woodsia obtusa Nephrolepis cordifolia N C Lepisorus thunbergianus Microgramma Phlebodium aureum Phymatosorus Polypodium feei P Equisetaceae Polypodiaceae Dryopteridaceae Nephrolepidaceae 162 H. Korpelainen ) b ) ) ) ) ) ) ) ) , ) ) a a a a b b b b a b b pp (1959) pp (1959) pp (1959) pp (1959) pp (1959) f (1969) f (1959) $ $ $ $ $ $ $ Voeller (1964 Haufler & Gastony (1978) Haufler & Gastony (1978) Haufler & Gastony (1978) Haufler & Gastony (1978) Haufler & Gastony (1978) Warne & Lloyd (1981) Scott & Hickok (1987) Schedlbauer & Klekowski (1972) Do Voeller (1964 Ranker (1987) Do Do Do Whittier (1968) Do Voeller (1964 Tryon (1964) Duckett & Pang (1985) Voeller (1964 Voeller (1964 Na Voeller (1964 Voeller (1964 Voeller (1964 Na Schraudolf (1962, 1966) Voeller (1964 Haufler & Gastony (1978) Schraudolf (1962, 1966) Voeller (1964 Voeller (1964 Tryon & Vitale (1977) L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K Environmental factor Direction Reference Antheridiogen absent (E) Trauma (E) GRS (E): gibberellin removed GRS (E): gibberellin removed Antheridiogen absent (E) Antheridiogen absent (E) GRS (E): gibberellin removed Life history Hermaphrodism Perennial Antheridiogen absent (E) HermaphrodismHermaphrodism PerennialHermaphrodism Perennial Antheridiogen absent (E) Perennial Antheridiogen absent (E) Antheridiogen absent (E) Hermaphrodism Perennial GRS (E): gibberellin removed Main form of sexuality HermaphrodismHermaphrodism PerennialHermaphrodism Perennial Antheridiogen absent (E) Hermaphrodism Perennial Antheridiogen absent (E) (apogamy) Perennial Antheridiogen absent (E) Hermaphrodism Antheridiogen absent (E) Hermaphrodism Perennial Perennial Perennial Antheridiogen absent (E) Hermaphrodism Antheridiogen Antheridiogen absent absent (E) (E) Hermaphrodism PerennialHermaphrodism Perennial Antheridiogen absent (E) Perennial Antheridiogen absent (E) Hermaphrodism Antheridiogen absent (E) Hermaphrodism Perennial Perennial Antheridiogen absent (E) Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism Antheridiogen absent (E) PerennialHermaphrodism Age (E) PerennialHermaphrodism Antheridiogen absent (E) Perennial Antheridiogen absent (E) HermaphrodismHermaphrodism PerennialHermaphrodism Perennial GRS (E): gibberellin removed Perennial GRS (E): gibberellin removed Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism GRS (E): gibberellinHermaphrodism removed Perennial Perennial GRS (E): gibberellin removed Antheridiogen absent (F .) cont sinuata vellea palmata jaliscana hispida knoblochii pedata subpaleacea oblongifolia pastinacaria phyllitidis rotundifolia tomentosa richardii thalictroides viridis ...... pteridoides Hemionitis arifolia N N Pellaea glabella A Adiantum pedatum Bommeria ehrenbergiana B B B B Ceratopteris C C Cryptogramma crispa H Notholaena distans P Platyzoma microphyllum Pteris longifolia Anemia hirsuta A A A A A Lygodium heterodoxum Species Pteridaceae Schizaeaceae Table 1 ( Taxon Labile sex expression in plants 163 . . et al et al . (1980) et al ) ) b b , , . (1980) . (1980) . (1980) a a . (1981) . (1982) . (1970) et al et al et al et al et al et al f (1960) f (1956) ! $ (1980) obs.) in Freeman Freeman Freeman Freeman (1980) (1983) Na Schraudolf (1962) Voeller (1964 Voeller (1964 Na Pharis Lev-Yadun & Liphschitz (1987) Vasek (1966) Vasek (1966); Menninger (1967) cited in Freeman D. C. Freeman & E. D. McArthur (pers. Smith (1981) Chalupka (1984) Keen & Chadwick (1954) cited in Keen & Chadwick (1954) cited in Keen & Chadwick (1954) cited in Jones (1945) Barker Worsdell (1916) cited in Freman Hibbs & Fischer (1979) E. Iglisch cited inSakai Lloyd (1978) & cited Bawa in (1984) Sakai & Oden Amruthavalli (1978) Amruthavalli (1978) L"K L"K L"K L"K L"K L!K L%K L%K L!K L%K L"K L%K L%K L%K L%K L%K L!K L"K L"K L!K L!K L"K L!K L!K GRS (E): gibberellin removed GRS (E): gibberellin removed Drought (F) Freeman GRS (E): growth retardants Hermaphrodism Perennial Antheridiogen absent (E) Hermaphrodism PerennialHermaphrodism GRS (E): gibberellin removed Perennial Antheridiogen absent (E) MonoecyDioecyMonoecy Perennial AgeDioecy (F) Perennial Perennial ? ? (F) (F) Dioecy Perennial LowMonoecy temperature (E) Monoecy Perennial ?Dioecy (F) Perennial Perennial HighDioecy light intensity (F) GRS (E): gibberellin Dioecy Perennial ? (?) Perennial ?Dioecy (?) PerennialMonoecy ?Dioecy (?) Dioecy Perennial PerennialDioecy ? DroughtDioecy (F) (E) Perennial Trauma (E) PerennialMonoecy Perennial ? (F) Perennial Size (F) Size (F) Annual GRS (E): gibberellin Monoecy Perennial GRS (E): gibberellin cuspida media grandidentatum negundo pennsylvanicum rubrum saccharinum japonicum sempervirens osteosperma sylvestris ...... hexagonoptera L Mohria caffrorum Thelypteris C Juniperus australis J Cycas circinalis Ephedra viridis Pinus contorta P Taxus baccata T T Acer campestre A A A A A Coriandrium sativum Cupressus arizonica Thelypteridaceae Cycadaceae Ephedraceae Pinaceae Taxaceae Aceraceae Apiaceae Cupressaceae Angiospermae Spermatophyta Gymnospermae 164 H. Korpelainen , 1931) b . (1964) . (1964) et al et al Clark & Orton (1967) Atkinson (1898) Atkinson (1898) Pickett (1915) Schaffner (1922) Schaffner (1922) Policansky (1981, 1987) Bierzychudek (1982, 1984) Lovett Doust & CaversLovett (1982) Doust & CaversLovett (1982) Doust & CaversBierzychudek (1982) (1984) Bierzychudek (1984) Schaffner (1922) Schaffner (1922) Maekawa (1924) Thomson & Barrett (1981) Barrett (1984) Schlessman (1987, 1991) Sparnaaij Sparnaaij Williams & Thomas (1970) Berghoef & Bruinsma (1980) Matzke (1938) Schaffner (1921, 1925) Schaffner (1923 Borthwick & Scully (1954) Borthwick & Scully (1954) Borthwick & Scully (1954) Heslop-Harrison (1956) Thomas (1956) Atal (1959) L"K L"K L!K L!K L!K L!K L"K L"K L"K L"K L"K L!K L!K L!K L!K L"K L%K L%K L"K L!K L!K L"K L"K L"K L%K L%K L!K L!K L!K L"K L!K L!K Environmental factorTrauma (E) Drought (E) Drought (E) Low nutrition (E) Size (F) Size Direction (F) High light intensity Reference (E,F) High pH (E,F) Size (E,F) Previous seed production (E) Trauma (E) Low nutrition (E) ? (F) Trauma (E) High light intensity (E) Photoperiod (E) High light intensity (E) Short photoperiod (E) Low temperature (E) GRS (E): auxin Short photoperiod (E) GRS (E): gibberellin Life history Main form of sexuality DioecyDioecy Perennial Age (size) (E) Perennial High nutrition (E) DioecyDioecyMonoecy Perennial DroughtDioecy (E) Perennial Size PerennialMonoecy (E) ? (F) Perennial Size PerennialMonoecy (F) DroughtMonoecy (E) Perennial Perennial High nutrition (E) High nutrition (E) * Dioecy Annual ? (E) .) cont dracontium japonica semperflorens . . . Elaeis guineensis Ilex opaca Arisaema triphyllum A A Aralia hispida Panax trifolium Begonia franconis B Cannabis sativa Species Aquifoliaceae Araceae Araliaceae Begoniaceae Cannabaceae Arecaceae Table 1 ( Taxon Labile sex expression in plants 165 ) ) a a ) ) ) ) ) ) b b a a c c ) a . (1984) . (1984) . (1984) et al et al et al & Durand (1984) Harrison (1972) (1958) (1958) Chailakhyan & Khryanin (1978 Chailakhyan & Khryanin (1978 Galoch (1978) Chailakhyan (1979) Chailakhyan (1979) Mohan Ram & SettSarath (1979) & Mohan RamTournois (1979) (1911, 1912, 1914) Schaffner (1923 Heslop-Harrison (1963) cited in Durand De Jong & BruinsmaDe (1974 Jong & BruinsmaStout (1974 (1923) Murneek (1927) Murneek (1927) De Jong & BruinsmaDe (1974 Jong & BruinsmaDe (1974 Jong & BruinsmaDe (1974 Jong & Bruinsma (1974 Lange (1961) Lange (1961) Bocquet & Stroun (1960) cited in Heslop- Lyndon (1985) Frick & Cavers (1989) Correns (1928) Heslop-Harrison & Heslop-Harrison Heslop-Harrison & Heslop-Harrison Correns (1928) Webb (1979) Freeman Freeman Freeman Freeman & McArthur (1984) L"K L"K L!K L"K L!K L!K L!K L"K L%K L"K L"K L!K L%K L"K L"K L"K L"K L"K L!K L!K L!K L"K L!K L"K L"K L!K L%K L%K L!K L!K L!K L%K L%K GRS (E): auxin, cytokinin GRS (E): cytokinin GRS (E): gibberellin GRS (E): cytokinin GRS (E): gibberellin GRS (E): cobalt GRS (E): gibberellin, silver ? (E) GRS (E): gibberellin High nitrogen (E) Trauma (E) High nutrition (E) Mature leaves present (E) GRS (E): cytokinin, ethephon GRS (E): auxin, gibberellin Trauma (E) ? (E) Short photoperiod (E) Previous seed production (E) Low temperature (E) DioecyMonoecy PerennialMonoecy GRS (E): auxin Annual GRS Annual (E): cytokinin ? (E) DioecyHermaphrodism Perennial Perennial Short photoperiod High (E) temperature (E,F) Hermaphrodism Perennial GRS (E): auxin DioecyDioecyDioecy Perennial ? (E) PerennialDioecy ? (F) Perennial Drought (E) Perennial ? (E) * Dioecy Annual Short photoperiod (E) * Dioecy Perennial Parasites (E) * Dioecy Perennial ? (F) lupulus confertifolia spinosa otites pendula reomeri ...... Atriplex canescens Humulus japonicus H Cleome iberidella C Carica papaya Cerastium tomentosum Silene latifolia S S S Euonymus europaeus A Capparaceae Caricaceae Caryophyllaceae Celastraceae Chenopodiaceae 166 H. Korpelainen . ) ) b b et al ) . (1981) b . (1995) . (1952) . (1952) et al et al et al et al (1980) Freeman & McArthur (1984) Freeman & McArthur (1984) Freeman & McArthur (1984) Freeman & McArthur (1984) Takeno Freeman Thompson (1955) Thompson (1955) Thompson (1955) Chailakhyan & Khryanin (1978 Chailakhyan & Khryanin (1978 Chailakhyan (1979) Chailakhyan (1979) Jones (1947) Mann (1942) Jones (1947) Jones (1947) Correns (1928) Lloyd & Myall (1976) Lloyd (1980 Ikeno (1937) cited in Freeman Neidle (1939) Neidle (1939) Naylor (1941) Catarino (1964) Hall (1949) Hall (1949) Nitsch Nitsch Minina (1938) Brantley & Warren (1960) Brantley & Warren (1960) L!K L"K L"K L%K L%K L%K L%K L"K L!K L"K L"K L!K L"K L!K L"K L"K L"K L!K L"K L"K L%K L!K L!K L"K L"K L"K L!K L!K L!K L"K L"K L%K cytokinin GRS (E): gibberellin GRS (E): cytokinin Environmental factorLong photoperiod (E) High temperature (E) GRS Direction (E): abscisic acid, Reference auxin GRS (E): gibberellin Short photoperiod (E) High temperature (E) ? (F) Long photoperiod (E) Long photoperiod (E) Long photoperiod (E) Long photoperiod (E) High temperature (E) High nitrogen (E) Long photoperiod (E) Life history Monoecy Annual High nutrition (E) Main form of sexuality DioecyDioecyDioecyDioecyMonoecy PerennialMonoecy Perennial ? (E) Perennial ? (E) Perennial ? Perennial (E) ? Perennial Short (E) photoperiod (E) Drought (F) MonoecyMonoecy AnnualDioecy Annual Short photoperiodDioecy (E) Short photoperiod (E) PerennialMonoecy ? (F) Perennial ? (F) AnnualHermaphrodism Perennial High nitrogenMonoecy (E) GRS (E): cytokinin Annual High nitrogen (E) Dioecy Perennial ? (?) * Dioecy Annual High nitrogen (E) .) cont corrugata cuneata lentiformis tridentata trifida melo ...... C A A A A Salsola komarovii Sarcobatus vermiculatus Spinacia oleracea Ambrosia elatior A Cirsium arvense Cotula dendyi Xanthium pennsylvanicum Kalanchoe integra Cucumis anguria Petasites japonicus Species Composiate Crassulaceae Cucurbitaceae Table 1 ( Taxon Labile sex expression in plants 167 . et al . et al ) b , a . (1977) . (1977) . (1980) . (1992, 1993) . (1996) et al et al . (1969) . (1969) . (1969) . (1980) et al . (1952) . (1952) . (1952) . (1952) et al et al et al et al et al et al et al et al et al et al (1980) Gilbert (1988) (1980) Halevy & Rudich (1967) Rudich Tiedjens (1928) Tiedjens (1928) Tiedjens (1928) Minina (1938) Laibach & Kribben (1950 Friedlander Friedlander Owens Malepszy & Niemirowicz-Szczytt (1991) Malepszy & Niemirowicz-Szczytt (1991) Malepszy & Niemirowicz-Szczytt (1991) Nitsch Nitsch Wittwer & Hillyer (1954) Rudich Dzhaparidze (1963) cited in Freeman Condon & Gilbert (1988) Condon & Gilbert (1988) Condon & Gilbert (1988) Bose & Nitsch (1970) Bose & Nitsch (1970) Takahashi Hossain Joshi (1939) Condon & Gilbert (1988) Murawski (pers. obs.) in Condon & Yonemori Minina (1952) cited in Freeman Nitsch Nitsch Wittwer & Hillyer (1954) McMurray & Miller (1968) Rudich L"K L"K L!K L"K L"K L!K L"K L"K L!K L!K L"K L!K L%K L!K L!K L"K L"K L"K L"K L"K L"K L!K L"K L"K L"K L"K L!K L"K L%K L!K L!K L!K L"K L"K L"K gibberellin GRS (E): auxin, maleic gibberellin, growth retardants GRS (E): ethylene Short photoperiod (E) Trauma (E) Nutrition (E) GRS (E): auxin GRS (E): gibberellin GRS (E): ethylene inhibitor GRS (E): auxin, ethylene GRS (E): ethylene inhibitor, Parasites (E) High temperature hydrazide GRS (E): ethylene GRS (E): morphactin GRS (E): growth retardants GRS (E): abscisic acid, ethephon Drought (E) Long photoperiod (E) High temperature (E) GRS (E): auxin GRS (E): ethephon GRS (E): ethylene Monoecy Annual High nitrogen (E) Monoecy Annual GRS (E): methylene blue Dioecy Annual GRS (E): silver nitrate Monoecy Annual Long photoperiod (E) MonoecyMonoecyMonoecyMonoecy Perennial Perennial Size (E,F) Perennial SizeMonoecy (E,F) Annual Size (E,F) Monoecy GRS (E):Monoecy auxin, cytokinin, AnnualMonoecy GRS Perennial (E): cytokinin Perennial HighMonoecy nutrition (E) Perennial Size (E,F) Size (F) Perennial Previous seed production (E) makoyana spinulosa sativus sativa cylindrica warscewiczii ...... C C Momordia dioica Cucurbita pepo Gurania acuminata G G Luffa acutangula L Musa paradisiaca Spiguria triphylla S Diospyros kaki Ebenaceae 168 H. Korpelainen . . et al et al . . et al et al ) ) a b . (1987) et al . (1980) (1980) (1991) (1991) (1980) (1980) McArthur (pers. obs.) citedet in al Freeman (1980) (1972) (1957) Heslop-Harrison (1957) Dzhaparidze (1963) cited in Freeman Thomas (1956) Thomas (1956) Yampolsky (1919) Hamdi Louis (1989) Durand & Durand Durand & Durand Pannell (1997 Pannell (1997 Shifriss (1956) Dzhaparidze (1963) cited in Freeman Worsdell (1916) cited in Freeman Tothill & Knox (1968) K. T. Harper, D. C. Freeman & E. D. Fox & Harrison (1981) Minina (1952) cited in Freeman Meletti (1961) cited in Heslop-Harrison Schaffner (1927, 1930, 1935) Richey & Sprague (1932) Richey & Sprague (1932) Sabinin (1937) cited in Heslop-Harrison Minina (1938) Choudri and Krishan (1946) cited in Moore (1950) L"K L!K L!K L%K L!K L!K L"K L"K L"K L%K L!K L%K L!K L!K L"K L"K L"K L"K L"K L"K L"K L"K L"K L"K L!K Environmental factorHigh temperature (E) GRS (E): auxin GRS Direction (E): auxin Reference GRS (E): cytokinin Low density (E) High potassium (E) Drought (F) Long photoperiod (E) Short photoperiod (E) Low temperature (E) High nutrition (E) High nutrition (E) Short photoperiod (E) GRS (E): maleic hydrazide GRS (E): cytokinin High density (E) Life history Main form of sexuality DioecyMonoecy PerennialDioecy Age (size) (E) Annual Short photoperiod (E) Annual ? (E) DioecyMonoecyDioecy Perennial ? Perennial (?) LongHermaphrodism photoperiod (E) Perennial Annual ? (?) Drought (E) Monoecy Annual Short photoperiod (E) Monoecy Perennial ? (F) .) cont annua . Eucommia ulmoides Mercurialis ambigua M Buchloe dactyloides Heteropogon contortus Leucopoa kingii Triticum aestivum Zea mays Ricinus communis Species Eucommiaceae Euphorbiaceae Gramineae Table 1 ( Taxon Labile sex expression in plants 169 . . et al et al . (1981) . (1976) . (1980) et al et al et al (1980) (1980) Nickerson (1957) Nelson & Rossman (1958) Heslop-Harrison (1961) Moss & Heslop-Harrison (1968) Hansen Krishnamoorthy & Talukdar (1976) Rood & Pharis (1980) Cheng & Wright (1989) Tucker Freeman Benseler (1975) Bertin (1982) Rick & Hanna (1943) Lazarte & Garrison (1980) Dzhaparidze (1963) cited in Freeman Schaffner (1925) Dzhaparidze (1963) cited in Freeman Jaiswal & Kumar (1980) Davey & Gibson (1917) Lloyd (1981) Hartmann & Panetsos (1961) Gregg (1973, 1975) Gregg (1973) Gregg (1973) Dodson (1962) Gregg (1973) Dodson (1962) Gregg (1973) Zimmerman (1991) Zimmerman (1991) Gregg (1978) Gregg (1973, 1975) Gregg (1973) Dodson (1962) L"K L"K L"K L"K L"K L"K L"K L%K L!K L%K L"K L"K L!K L"K L%K L"K L"K L!K L%K L!K L!K L"K L!K L!K L!K L!K L!K L!K L"K L"K L"K L"K L"K L"K GRS (E): gibberellin Short photoperiod (E) Short photoperiod (E) GRS (E): gibberellin GRS (E): gibberellin Low light intensity (E) GRS (E): DPX-3778 Drought (F) GRS (E): cytokinin, gibberellin Trauma (E) ? (F) Low light intensity (E) Low light intensity (E) Size (E) Low light intensity (E) GRS (E): gibberellin MonoecyMonoecy PerennialMonoecy ? (F) Dioecy Perennial Perennial ? (F) HighDioecy light intensity (F) PerennialDioecy ? (E) PerennialDioecy Age (size) (E) PerennialDioecy ? (E) PerennialMonoecy GRS (E): ethrel PerennialDioecy DroughtDioecy (F) Perennial DroughtDioecy (E) PerennialDioecy Perennial LowDioecy light intensity (E) AgeDioecy (size) (E) Perennial LowDioecy light intensity (F) Perennial Perennial LowDioecy light intensity (F) Perennial LowDioecy light intensity (E) Low light intensity (E,F) Perennial Age (size) (E) Perennial Perennial Low light intensity (E) Low light intensity (F) nigra pavia macrocarpum macroglossum platyglossum ventricosum viridiflavum dianae lehmannii ...... Quercus gambelii Aesculus californica A Asparagus officinalis Castilloa elastica Morus alba M Myrica gale Olea europaea Catasetum expansum C C C C C Cycnoches densiflorum C C Fagaceae Hippocastanaceae Liliaceae Moraceae Myricaceae Oleaceae Orchidaceae 170 H. Korpelainen . et al . (1980) et al Freeman (1980) Gregg (1973) Gregg (1978) Gregg (1973, 1975) Dodson (1962) Stout (1919) Schaffner (1925, 1935) Schaffner (1925) Erlansson & Herman (1927) cited in Pauley & Mennel (1957) Stettler (1971) Heribert-Nilsson (1918) Heslop-Harrison (1924) Rainio (1927) Worsdell (1916) cited in Freeman Resende & Viana (1959) Solomon (1985) Solomon (1985) Solomon (1985) Solomon (1985) Solomon (1985) Solomon (1985) Diggle (1991) Hendrix & Trap (1981) Strasburger (1910) Schaffner (1935) Correns (1928) Iizuka & Hashizume (1968) Negi & Olmo (1966) L"K L"K L"K L"K L%K L%K L%K L%K L%K L%K L%K L"K L%K L%K L"K L!K L"K L!K L!K L!K L"K L!K L%K L%K L!K L%K L"K L"K Environmental factorLow light intensity (E) Direction Reference ? (F) Mites (E) ? (F) GRS (E): abscisic acidGRS cytokinin (E): gibberellin Low light intensity (E) High nutrition (E) Size (F) Life history Main form of sexuality DioecyDioecyDioecy PerennialHermaphrodism Perennial Low light Perennial intensity (E) AgeDioecy (size) ? (E) (E) PerennialDioecy Low light intensity (F) Perennial Perennial ?Dioecy (E) ? (E) Dioecy Perennial ? (F) HermaphrodismMonoecy Annual Perennial ? GRS (?) (E): gibberellin Perennial Drought (E) MonoecyHermaphrodism Biennial PerennialDioecy Trauma Previous (E) Monoecy fruit production (E) Dioecy Perennial PerennialDioecy ? ShortDioecy (F) photoperiod (E) Perennial ? (E) Perennial Perennial GRS (E): cytokinin GRS (E): cytokinin * Dioecy Perennial ? (?) .) .* Dioecy Perennial ? (E) cont dioicum vinifera stenodactylon warscewiczii trichocarpa aurita hirtum ...... C C Mormodes buccinator Plantago lanceolata Thalictrum dasycarpum T Populus tremuloides P Salix sp S Hyoscyamus niger Solanum carolinense S Pastinaca sativa Urtica dioica Urticastrum divaricatum Valeriana dioica Vitus thunbergii V Species Plantaginaceae Ranunculaceae Salicaceae Solanaceae Umbelliferae Urticaceae Valerianaceae Vitaceae Table 1 ( Taxon Labile sex expression in plants 171 come males under the influence of antheridiogen. Ceratopteris richardii (Scott & Hickok, 1987), Gymno- Variation in spore size has been observed even carpium dryopteris (Kirkpatrick & Soltis, 1992) and in among homosporous pteridophytes. Schedlbauer Hemionitis palmeta (Ranker, 1987), and in the fern (1976) observed in Ceratopteris thalictroides that vari- genum Cystopteris (Haufler & Ranker, 1985). Besides ation in spore size is correlated with variation in the influencing sex expression, antheridiogens also in- amount of stored nutrients, the time of spore duce dark germination in some ferns (Schneller, germination and subsequent rates of gametophyte 1988; Schneller, Haufler & Ranker, 1990; Chiou & development. The fastest-growing gametophytes Farrar, 1997). become hermaphroditic and influence the slower The extreme lability in sex expression in relation ones to become antheridial. Thus, variation in spore to antheridiogen production among homosporous size and consequent variation in developmental pteridophytes has several obviously adaptive conse- speed may relate to the sex-expression of the quences. First, antheridiogens play a role in con- gametophyte. On the other hand, in a study on the trolling the breeding system by promoting inter- genus Bommeria, Haufler & Gastony (1978) observed gametophytic matings and the maintenance of no bimodal distribution in spore size. genetic variation (Tryon & Vitale, 1977; Schneller, The homosporous fern Ceratopteris richardii has 1979; Haufler & Soltis, 1984). This may be been used as a model system for studying genetic and important for homosporous plants which possess environmental factors involved in sex determination. three types of matings in contrast to the two usual The gametophytic stage of the life cycle is easier to types: intergametophytic crossing (comparable to investigate and manipulate in ferns than in flowering outcrossing in seed plants), intergametophytic selfing plants, where the gametophyte is surrounded by the (comparable to selfing in seed plants) and intra- maternal sporophytic tissues of the flower. Banks, gametophytic selfing. Intragametophytic selfing pro- Webb & Hickok (1993) have shown in C. richardii duces a completely homozygous sporophyte in a that a gametophyte is responsive to antheridiogen single generation. Secondly, gametophytes carrying for only a brief period early in its development when archegonia may increase their fitness through the the spore wall cracks and the gametophyte is between secretion of antheridiogens by increasing the pool of one and four cells in size. Exposure to antheridiogen available males from which a mate may be chosen during this and subsequent stages of gametophyte (Willson, 1981). This aids intergametophytic mat- development is required for male development. If ings as well. Thirdly, antheridiogens may be im- antheridiogen is removed from the surrounding portant also for intra- and interspecific competition medium, the sexually undetermined or undifferen- (Schneller et al., 1990). Tall gametophytes are more tiated cells of the male gametophyte revert to likely to bear zygotes and support young sporo- hermaphrodism. Thus, the male expression is labile, phytes. By producing antheridiogens they inhibit the indicating that antheridiogen is necessary for both growth of potential competitors. Fourthly, the initiating and maintaining male expression. In response to antheridiogens may enhance the re- contrast, the hermaphroditic expression is stable productive success of small gametophytes by allow- once established and cannot be reversed by exposure ing for sex expression (maleness), which would not to antheridiogen. An application of abscisic acid occur via self-regulation (Hamilton & Lloyd, 1991). blocks the antheridiogen response in Ceratopteris spp. Approximately 10% of all pteridophyte species (Hickok, 1983; Eberle et al., 1995). Several muta- are agamosporous (Walker, 1984). In such species, tions that affect sex expression have been isolated there is no meiotic reduction in sporogenesis, and and characterized (Hickok, 1985; Banks, 1994; new sporophytes develop from the gametophyte Eberle et al., 1995; Eberle & Banks, 1996). These without fertilization (apogamy or apomixis). Still, mutations define at least some of the major regu- the gametophytes express sexuality and may produce latory genes involved in determining the sex of the suppressed archegonia and antheridia with func- Ceratopteris spp. gametophytes. tional, non-reduced sperm (Haufler & Gastony, There are several types of antheridiogens, with 1978; Gastony & Windham, 1989). They can some degree of taxonomic specificity. A given type of thereby act as male parents in crosses with the antheridiogen is effective in several species, and archegoniate gametophytes of sexually reproducing several types may be effective in particular species taxa. In three fern families, Grammitidaceae, (Voeller, 1964a;Na$fet al., 1975). Additionally, Hymenophyllaceae and Vittariaceae, the sporo- there is variation within populations in gametophyte phyte stage of the life cycle has been eliminated, and response to antheridiogens, as observed in the ferns the gametophytes reproduce vegetatively via gem- 172 H. Korpelainen mae (Farrar, 1985, 1990). Despite functional asexu- sexual). A difference between dioecious and other ality, such gametophytes produce gametangia as seed plants is that in dioecious species sex expression their likely ancestors with a more ordinary life cycle. is often not restricted to flowers but includes sexual dimorphism and secondary sexual characters in the morphology and phenology of the plant (e.g. Lloyd IV. SPERMATOPHYTA & Webb, 1977; Bullock & Bawa, 1981; Meagher & Antonovics, 1982; Longo, 1994). Despite the rela- Hermaphrodism is the most common and probably tively common occurrence of sexual dimorphism, the the original mode of reproduction in seed plants. sex of a plant can often be determined only at sexual Because species with unisexual flowers have evolved maturity. Even then, the potential presence of repeatedly from hermaphroditic progenitors, the rudiments of the opposite sex can lead to the wrong mechanisms controlling sex expression in seed plants conclusions. are diverse. Yampolsky & Yampolsky (1922) esti- Much evidence of environmental effects on sex has mated that only 4% of angiosperm species are been obtained from studies on commercially im- dioecious and 7% are monoecious. However, Lloyd portant species, such as maize and the cucurbit (1982) estimated that up to 10% of angiosperm species, which possess mainly monoecious sex ex- species may be dioecious. Dioecy is infrequent but pression. As seen in Table 1, a common factor widespread throughout the families of angiosperms. reversing sex expression in seed plants is exogenous In gymnosperms, dioecy is a more frequent con- treatment by hormones or other growth-regulating dition, approximately 25% of all species (Longo, substances. The effect of chemical treatments is 1994). An important question is then the extent to often the conversion of one sex to the other, rather which sex expression is constant. The reversion of sex than conversion to hermaphrodism. This suggests expression through chemical treatment or some that, at least in those cases, the floral primordia are other environmental factor would indicate lability in sexually bipotent and that sex determination genes the interaction between sex-determining genes and regulate alternative programs of sexuality, possibly physiology in such species. It seems that in many through a mechanism that modifies endogenous dioecious species sex is rigidly controlled by genetics, levels of hormones (Dellaporta & Calderon-Urrea, although only a few species possess sex chromosomes 1993, 1994). Plants have five classes of hormones: (Parker, 1990; Chattopadhyay & Sharma, 1991; auxins, gibberellins, abscisic acid, cytokinins and Grant et al., 1994). Sex chromosomes have evolved ethylene (Grant et al., 1994). Each type of hormone so recently that many dioecious species with sex is active in many plant functions. It has been chromosomes have hermaphroditic relatives without observed that the action of particular hormones in sex chromosomes in the same genus. Still, many feminizing or masculinizing flowers is species- dioecious seed plant species are known to change sex dependent. The same hormone can have completely or to express hermaphrodism or monoecy (Freeman opposite effects in different plants. For example, et al., 1980). Obviously, such species are not strictly gibberellic acid feminizes monoecious maize (Zea speaking dioecious. Lability in sex expression can mays) (Nickerson, 1957; Nelson & Rossman, 1958; sometimes lead to erroneous ideas about the mode of Hansen, Bellman & Sacher, 1976), but has the reproduction. For instance, the vines in the genera opposite effect on dioecious asparagus (Asparagus Gurania and Psiguria, which were long thought to be officinalis) (Lazarte & Garrison, 1980) and mon- dioecious, are actually monoecious (Condon & oecious cucumber (Cucumis sativus) (Malepszy & Gilbert, 1988). The confusion results from size- Niemirovicz-Szczytt, 1991). Cytokinins have a femin- related sex changes. izing effect on dioecious or subdioecious mercury The question of how labile or constant sex (Mercurialis annua), spinach (Spinacia oleracea), hemp expression is does not only relate to dioecious species (Cannabis sativa) and grapevine (Vitis vinifera) (Negi but also to monoecious and hermaphroditic plants, & Olmo, 1966; Galoch, 1978; Chailakhyan, 1979; and to plants expressing various intermediate forms Louis, 1989; Durand and Durand, 1991), while in of sexuality, such as gynomonoecy (female and asparagus females cytokinin treatment increases the hermaphrodite flowers on the same plant), andro- frequency of hermaphroditic flowers (Lazarte & monoecy (male and hermaphrodite flowers on the Garrison, 1980). Auxins have a masculinizing effect same plant), gynodioecy (male morph ambisexual in mercury (Hamdi, Teller & Louis, 1987; Louis, and female morph unisexual) and androdioecy 1989; Durand & Durand, 1991), but a feminizing (female morph ambisexual and male morph uni- effect in cucumber (Malepszy & Niemirovicz- Labile sex expression in plants 173

Szczytt, 1991). In some more strictly dioecious modification of sex expression in plants, see Heslop- species, such as white campion (Silene latifolia), Harrison, 1957). As shown in Table 1, the common hormone applications have little or no effect on the factors influencing sex expression in nature are sexuality of flowers (Dellaporta & Calderon-Urrea, photoperiod, light intensity, nutrition and tem- 1993). Monoecious Scots pine (Pinus sylvestris) ex- perature, all of which affect a plant’s nutritional presses seasonal and, to some extent, also genetic status either directly or indirectly. Other factors variation in the susceptibility to exogenous hormonal which do affect the sex expression of seed plants treatments. The spraying of branches with gib- include drought, trauma, parasite effects and pH. berellic acid in May and June significantly increased Less-than-optimal conditions often appear to favour male flowering, while July and August applications maleness. In plants in which sex expression is related resulted in a significant increase of female flowering to plant size (or age), males are usually smaller (or (Chalupka, 1984). younger) than females. Reproductive history may Yin & Quinn (1992) have suggested a model to influence sex as well. In the shrub Atriplex canescens,a explain the role of hormones in sex determination. prior heavy seed set is one of the stress factors under They assume that one hormone has male and female which females are more likely than male plants to receptors to inhibit one sex and induce the other change sex (Freeman, McArthur & Harper, 1984). independently. The range of hormone concentration Comparatively, the sex expression of the persimmon and the sensitivity levels of the receptors interact to tree Diospyros kaki is modified by the previous year’s regulate sex expression. The results of studies on fruit load and the nutritional status of the tree cucumber and maize support this model (Yin & (Yonemori, Kameda & Sugiura, 1992; Yonemori Quinn, 1992). The ratios of different hormones may et al., 1993). Apparently also in these cases, be more important than their absolute levels. hormones, which are known to be responsive to en- Chailakhyan (1979) has shown that in spinach and vironmental conditions, play important roles in sex hemp the ratio of cytokinin to gibberellic acid expression. controls sex expression. With cytokinin in excess, Some of the plants which express considerable plants generally produce female flowers. Molecular lability in sex expression are the epiphytic orchid studies on genes involved in flower development and Catasetum viridiflavum and species of the genus Atriplex. sex determination indicate that they have a role in In C. viridiflavum, gender is largely determined by hormone metabolism (Grant et al., 1994). Diggle light intensity (Zimmerman, 1991). Females occur (1991) has suggested that the lability of whole-plant most frequently in open canopies and males pre- sex is due to the labile sex expression of individual dominate in closed canopies. Smaller but significant flower buds, that is, the sex of a flower could be effects of plant size on sex expression have also been determined late in development, depending on the detected (Zimmerman, 1991). Males tend to be environment. Comparisons of floral development in small and females large while hermaphrodites are hermaphroditic and male buds of the andromonoe- intermediate in size. Hermaphroditic plants ob- cious Solanum hirtum showed that just 6–7 days before viously result from changes in sex expression within anthesis abnormalities occurred in the ovule de- and between years. Lability in the sex expression of velopment of male buds (Diggle, 1991). As a result, C. viridiflavum was confirmed experimentally: shaded fertilization could not take place in male buds. inflorescences were more frequently males than were Morphological evidence indicates that sex differenti- the unshaded inflorescences of plants of comparable ation of genetically determined male and female size (Zimmerman, 1991). individuals of dioecious asparagus consists of the In the genus Atriplex, up to 20% of individuals can selective abortion of the gynoecium or androecium alter their sex expression from one season to the next of initially hermaphrodite floral primordia (Bracale (McArthur & Freeman, 1982; Freeman & et al., 1991). Abortion occurs in pollen-mother cells McArthur, 1984; Freeman et al., 1984). These sex and anthers in females, and in megaspore-mother changes occurred in response to three stress factors, cells in males. The differential sexual development is an unusually cold winter, a drought and a prior accompanied by changes in the relative abundance heavy seed set. Under stress, females are significantly of auxins and cytokinins. more likely to change sex than are male individuals. Exogenous treatments by hormones and other In the genus Atriplex, changes from a unisexual to a growth-regulating substances are environmental fac- monoecious state appear to be more frequent than tors to which plants are not exposed in natural changes in the opposite direction. Although labile conditions (for an early review on experimental sex expression is common in Atriplex, a considerable 174 H. Korpelainen fraction of the population does not seem capable of species is less than 10% as well (Yampolsky & sex changes. Studies on the frequency of sex change Yampolsky, 1922). Therefore, lability in sex ex- in natural plant populations include the genera pression appears to be more common among Juniperus and Acer. Vasek (1966) reported 7n3% dioecious and monoecious species than among and 24n5% sex change in J. australis and J. osteo- hermaphrodites. However, hermaphrodites can con- sperma, respectively, and Hibbs & Fischer (1979) trol allocation to male and female function by found 10% sex change among plants of Acer varying the relative emphasis on pollen and ovules in pennsylvanicum. hermaphroditic flowers. Cannabis sativa, Silene latifolia and Spinacia oleracea (3) A great majority of angiosperms with labile are much-studied dioecious plant species with het- sex (78%) are perennials, which indicates that eromorphic sex chromosomes. Yet, they possess some flexibility in sex expression is more important for lability in sex expression (Table 1). The application species with long life cycles. of hormones as well as variable light conditions can (4) Observations of sex changes among gymno- induce sex reversal in C. sativa, while hormonal sperms are few and include both dioecious and treatments, nutrition and light influence sex ex- monoecious species. pression in S. oleracea.InSilene latifolia, exogenous (5) A requirement for adaptive lability in sex is to hormones have no effect but infection by the recognize an environmental factor which differen- basidiomycete Ustilago violacea can induce the ap- tially correlates with male or female fitness. The pearance of anthers in female flowers, thus trans- factor typically indicates stress as a result of less- forming them into hermaphroditic flowers. For the than-optimal light, nutrition, weather or water fungus genus Ustilago, this transformation is ad- conditions. Such environmental stress affects a vantageous since the teliospores of the fungus are plant’s nutritional status either directly or indirectly able to develop only in anthers (Lyndon, 1985). In and often favours maleness. greenhouse studies on S. latifolia, Frick & Cavers (6) Size may influence the ability of a plant to be (1989) have observed occasional hermaphroditic of a certain sex. When size affects sex expression, flowers among a majority of male flowers while they males are usually smaller than females. Environ- found no non-constant female plants. In field studies. mental cues influencing sex expression also include Frick & Cavers (1989) also observed sequential population density and mediation through other hermaphrodites, single plants that produced both individuals (antheridiogens secreted by neighbour- male and female flowers on separate branches, and ing fern gametophytes). both male and female plants cloned from single (7) I suggest that the extreme lability in the sex individuals. The lability in sex expression was not expression of homosporous pteridophytes relates consistent with regard to environment. When Frick primarily to their mating systems. A lack of flexibility & Cavers (1989) compared seeds from female plants in sex expression would potentially result in genetic to seeds from hermaphroditic but genetically male homozygosity (in the case of self-fertilization) or in a plants, those from male plants were less likely to poor ability to colonize (in the case of strict dioecy). germinate, and the resulting seedlings were less likely to survive to reproduction. V. REFERENCES

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