Genetics and Physiology of Sex Determination in Dioecious Plants

Fruits - vol . 40, n°11, 1985 - 739

Genetics and physiology of sex determination in dioecious plants.

S.M. LIONAKIS*

GENETIQUE ET PHYSIOLOGIE DE LA DETERMINATION DU SEXE CHEZ LES PLANTES DIOIQUES . S .M . LIONAKIS . Fruits, Nov. 1985, vol . 40, no 11, p . 739-743 .

RESUME - La base génétique de la détermination du sexe aussi bien que l'effet des facteurs climatiques des substances chimiques et des régulateurs d'accroissement à la manifestation du sexe chez les plantes dioïques sont mis en évidence .

INTRODUCTION cies in which some bisexual plants (hermaphrodite or monoecious) occur regularly in nature, is termed subdioe- The stamens and the carpels constitute the essential cious . organs of the flower in the sense that they are concerned with sporogenesis and the nurture of the gametophytes . Dioecism is rare but widespread among many separated The other structures of the flower must be regarded as families. According to YAMPOLSKY and YAMPOLSKY auxiliary in function . Flowers either contain both stamens (1922) only 5 % of the genera of the higher plants are and carpels or stamens alone and carpels alone . A species wholly dioecious, while about 75 % of the families contain is called bisexual if male and female flowers occur on the some dioecious species . same plant . Bisexual plants may be hermaphrodite when the two sexes are found in the saine flower, or monoe- Separation of the sexes on different plants is found in cious when the sexes are restricted to separate flowers on several important crop plants, including Cannabis satina, the same plant . Dioecious or unisexual is a species when Vitis vinifera, Asparagus officinalis, Humulus lupulus, the male (staminate) and female (carpellate or pistillate) Actinidia chinensis . flowers occur in individual plants . The step from dioecism to bisexuality is often a short one and in most cases dioe- GENETICS OF SEX DETERMINATION cism is not clear-cut . In many dioecious species bisexual types are found in nature often with a rather hight fre- The inheritance of dioecism was first demonstrated by quency. Such bisexual individual types of normally dioe- CORRENS at the beginning of this century . By crossing cious plant species are almost always fertile, whereas simi- dioecious and monoecious species of Bryonia he showed lar bisexual animals are sterile infersexes. A dioecious spe- that sexual dimorphism was inherited after the scheme of a Mendelian backcross, one sex (Heterogametic sex) produ- * - Institute of Subtropical Plants and Olive tree, Chania, Crete, cing two types of gametes-male determining and female Greece . determining-in equal proportions, whereas the other (homo- 740 - Fruits - vol . 40, n°11, 1985

TABLE 1 - Questionable or insufficiently established cases of heteromorphic sex chromosomes in plants (after WESTERGAARD, 1958).

Elodea canadensis Silene densiflora Elodea gigantee Cercidiphyllum japonicum Hydrilla verticillata Coccolus trilobus Trachycarpus excelsus Fragaria elatior Trachycarpus fortunei Zanthoxvlum piperitum Smilax spp . Daphniphyllum macropodum Dioscorea spp. Ilex serrata Sel ix spp . Acer negundo Populus spp . Picrassima quassioides Toisusu spp. Actinidia kolomikta Cudrania triloba Actinidia polygama Morus bombycis Eurreya japonica Urtica dioica Datisea cannabina Buckleya joan Valeriana dioica Phoradendron flavescens Trichosanthes cucumeroides Phoradendron villosum Trichosanthes japonica A triplex hymenelytra Trichosanthes dioica Spinacia tetrendra Trichosanthes multiloba Spinacia oleracea Coccinea indica Silene otites

TABLE 2 - Well-established cases of heteromorphic sex chromosomes in plants (after WESTERGAARD, 1958 and WILLIAMS, 1964) .

Species Chromosome number 2n Constitution d'Constitution

Cannabis sativa 20 XX XY Humulus lupulus 20 XX XY H. lupulus var . cordifolius 20 X1X1X2X2 X1Y1X2Y2 Humulus japonicus 169 17 d< XX X Y1Y2 Rumex sub-genus acetosella R. angiocarpus 14 XX XY R. tenuifolius 28 (XX)XX (XX)XY R. acetosella 42 (XXXX)XX (XXXX)XY R. graminifolius 56 (XXXXXX)XX (XXXXXX)XY Rumex sub-genus acetosa R. hastatulus 89 9d' XX XY1Y2 R. acetosa 149 15a XX XY1Y2 R. paucifolius 28 (XX)XX (XX)XY Melandrium album 22 XX XY Melandrium rubrum 22 XX XY Asparagus officinalis 20 XX XY or YY

TABLE 3 - A selected list of dioecious species in which heteromorphic sex chromosomes have not been found (after WILLIAMS, 1964).

Sedum rosea Aucuba japonica Thalictrum fendleri Bryonia dioica Mercurialis annua Carex grallatoria Mercurialis perennis Actinidia tuberculata Vitis vinifera Empetrum nigrum hermaphroditum Carica papaye Ecballium elaterium dioicum Fruits - vol . 40, n°11, 1985 - 741

gametic sex) produces only one type of gametes (after matelly equal proportions, an outbreeding mechanism of HESLOP-HARRISON, 1972). male sterility has become established in several species, which depends upon a cytoplasmic/genic interaction (LE- The discovery of sex chromosomes in higher plants WIS, 1941) . dates from 1923 when BLACKBURN, KIHARA and ONO, and WINGE independently reported the occurence The unisexual species differ from the bisexual ones of heteromorphic bivalents in Melandrium album, Rumex only by having developed a trigger mechanism which acetosa and Humulus spp . (BLACKBURN, 1923 ; WES- suppresses the potentialities of the opposite sex in males TERGAARD, 1958) . Sex chromosomes have since been and females . Most mutations in the sex genes of bisexual reported in many dioecious species of flowering plants, species will tend towards unisexuality, whereas most mu- but according to WESTERGAARD (1958) many of these tations in dioecious species will tend towards bisexuality . reports are not fully convincing . So the existence of hete- So the evolutionary process can be studied from two romorphic sex chromosomes is questionable or insufficien- angles, viz : The evolution from the bisexual to the uni- tly established in a number of species (Table 1) . sexual state, and the «backwards evolution» from dioecism to bisexuality (ALLEN, 1940) . Heteromorphic sex chromosomes have been well established, from cytological and genetical evidence, in some species (Table 2), while heteromorphic sex chromosomes PHYSIOLOGY OF SEX DETERMINATION have not been found in some other species (Table 3) . A substantial body of the litterature exists concerning The heterogametic form is the male in ail species of the control of flower morphogenesis, and in particular of Table 2 . Either male or female heterogamety has been sex expression by environmental, chemical and hormonal demonstrated genetically from breeding tests, but wi- influences in the dioecious species . thout sufficient cytological evidence, in many species of Table 1 and 3 . BORTHWICK and SCULLY (1954) have reported that female plants of Cannabis satina can produce male flowers For the localization of the sex-deciding genes, evidence under certain environmental conditions . This inversion has been provided from crosses between dioecious and in sex of Cannabis satina can be achieved by full intensity monoecious species, from subdioecious species and from of natural light, by short photoperiods and by low tempe- polyploids of dioecious species. The occurence of hete- rature during or immediately prior to photoperiodic in- romorphic sex chromosomes does not necessarily indicate duction . that ail the sex-deciding genes are located on them . The analysis of the sex determining mechanism has clearly An interaction of high temperature and short day- shown the existence of at least two types of trigger me- length on the variety «Blight Resistant savoy» of the chanisms. In the one type, typified by Rumex acetosella dioecious plant Spinacea oleracea results in the production and Melandrium album, the sex of individuals is decided of staminate flowers on pistillate plants (THOMPSON, entirely by the presence or absence of the Y-chromosome . 1955). In the other type, exemplified by Drosophila melanogaster and Rumex acetosa, the sex determining factor is the NEGI and OLMO (1970) observed the appearance of X-chromosome/autosome ratio and the Y-chromosome is functionally hermaphrodite flowers and seeded berries on inactive. The existence of a XO mechanism in plants is male vines of Vitis vinifera and they explained that as a not known with certainty (WESTERGAARD, 1958) . natural sex conversion from functionally male to functionally hermaphrodite flowers . The frequency of sex DARLINGTON (1958) has pointed out that efficient conversion varied markedly among inflorescences of the control of dioecism depends upon the absence of crossing sanie vine, among vines growing side by side and from over between blocks of sex determining genes, and this season Co season . leads, in some plants, to the development of heteromorphic sex chromosomes with the sex determining genes According HESLOP-HARRISON (1972), photoperiodism restricted to the differential segments . The differential itself was discovered in connection with an investigation segment of the Y-chromosome is totally precluded from of sex expression in two dioecious plants, Cannabis satina crossing over and because of the resulting loss in adaptive and Humulus japonicus by TOURNOIS in 1912. TOUR- efficiency the work of the Y-chromosome is often taken NOIS found that short days not only accelerated the by the autosomes . flowering of Humulus japonicus but also affected the sex of the plants and anomalus sex expression appeared in the There is probably no well established case where sex genetical male plants, many showing sex inversion or struc- determination in a strictly dioecious plant species is a tural intersexuality . This experiment with hop is of his- function of the interaction between nuclear genes and torical interest as the first true photoperiodic experiment . the cytoplasm . In the gynodioecious species, however, In male plants of Cannabis satina grown under short days, which comprice females and hermaphrodites in approxi- TOURNOIS observed an incidence of intersexuality ex- 742 - Fruits - vol . 40, n°11, 1985

ceeding 85 %. and hemps short day plants.

A conversion of genetically staminate plants of dioe- Formation of female flowers on male hemp plants by cious Vitis vinifera to functional hermaphrodites by the the application of morphactin IT 3456 [Methyl-2-Chloro- application of cytokinins has been reported by NEGI and 9-hydroxy fluorene-(9)-carboxylate] has been reported OLMO (1966, 1971), HASHIZUME and TIZUKA (1971) by MOHAN RAM and JAISWAL (1971) . and MOORE (1970) . OSTAPEMKO (1960) investigated the activity of oxi- HESLOP-HARRISON (1956) treated hemp with NAA dising enzymes in some dioecious plants . He found that and thereby induced female flowers on genetically male the polyphenoloxidase and peroxidase content in the plants and has suggested that auxins control sex according leaves of Cannabis sativa, Asparagus officinalis, Actinidia to an «optimum» curve, the optimum for staminate de- kolomikta, Hippophae thannoides and Ribes alpinum velopment being lower than for pistillate . differed greaty but was always higher in male than female plants . Infection of genetically females of Malandrium species by the fungus Ustilago violacea causes complete morpholo- Also HIRSCH et al ., (1977) have undertaken studies on gical sex inversion in the heavily infected parts of the in- the peroxidasic activity and isoperoxidases evolution of florescence . The development of the ovary is suppressed male and female Actinidia chinensis plants. They found and stamens develop . However the pollen is replaced by that the total soluble peroxidasic activity is suddenly the spores of the fungus (BAKER, 1947). GOLDSCHMIDT reduced in male and female flower buds just before flo- (1955) considers that these very specific morphogenetic wering, but it always remains higher in male flower buds effects of the fungal pathogen stroggly suggest that it than in female ones . Also they observed a striking diffe- interferes in some consistent way with the natural sex- rence between male and female flower buds, cdnnected determining mechanism of the flower, and one obvious with the existence of two anodic isoenzyme fractions found possibility is, that infection modifies the auxin metabo- only in male flower buds . lism in the differentiating flower primordia. The physiology of sex determination is not yet clearly WESTON (1960) has reported the induction of male understood . However it is generally agreed that all plants flowers on a female hop variety following treatment with have the potential to develop the sex organs of either sex a-(2-chlorophenythio) propionic acid, a compound with and that a trigger mechanism sets off one or other of two weak growth properties . He suggests that the change from possible chains of events, one leading to the development female to male induced in hops, instead of from male to of the female sex organs, the other of the male. female as in hemp, may result from hops being long-day

REFERENCES

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17 . OSTAPEMKO (V.I.). 1960. 20 . WESTON (E .W.). 1960. The activity of oxidising enzymes in some dioecious plants . Changes in sex in the hop caused by plant growth substances. Bot. Journal, 45, 114-161 . Nature, 188, 81.82 . 18. THOMPSON (A.E .). 1955 . 21 . WILLIAMS (W.). 1964 . Methods of producing first generation hybrid seed in spinach . Mechanisms of sex determination . Cornell Univ . Mem ., 336 . In : Genetical principles and plant breeding . 19. WESTERGAARD (M.). 1958 . Ed. W.O. James p . 235.260 . Blackwell Scient. Publ. Oxford . The mechanism of sex determination in dioecious flowering plants . 22 . YAMPOLSKY (C .) and YAMPOLSKY (H.) . 1922. Advances in Genetics, 9, 217-281 . Distribution of sex forms in the phanerogamic flora . Bibliotheca Genet., 3, 1-62 .