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Reproduction and Gene Flow in the Genus Quercus L

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Reproduction and Gene Flow in the Genus Quercus L Review article Reproduction and gene flow in the genus Quercus L A Ducousso H Michaud R Lumaret 1 INRA, BP 45, 33611 Gazinet-Cestas; 2 CEFE/CNRS, BP 5051, 34033 Montpellier Cedex, France Summary — In this paper we review the characteristics of the floral biology, life cycle and breeding system in the genus Quercus. The species of this genus are self-incompatible and have very long life spans. The focus of our review is on the effects of gene flow on the structuration of genetic varia- tion in these species. We have examined the influence of gene flow in 2 ways: 1) by measuring the physical dispersal of pollen, seed and vegetative organs; and 2) by using nuclear and cytoplasmic markers to estimate genetic parameters (Fis, Nm). These approaches have shown that nuclear (iso- zyme markers) as well as cytoplasmic (chloroplastic DNA) gene flow is usually high, so that very low interspecific differentiation occurs. However, intraspecific differentiation is higher for the cytoplasmic DNA than for the nuclear isozyme markers. floral biology / life cycle / breeding system / gene flow / oak Résumé — Système de reproduction et flux de gènes chez les espèces du genre Quercus. Les caractéristiques de la biologie florale, du cycle de vie et du système de reproduction ont été analysées pour les espèces du genre Quercus. Ces espèces sont auto-incompatibles et à très lon- gue durée de vie. Les effets des flux de gènes sur la structuration de la variabilité génétique ont aussi été étudiés de 2 manières. D’une part, grâce aux mesures de la dispersion du pollen, des graines et des organes végétatifs, et, d’autre part, en utilisant des paramètres génétiques (Fis, Nm) obtenus à partir des marqueurs nucléaires et cytoplasmiques. Il apparaît que les flux géniques nu- cléaires (isozymes) et cytoplasmiques (ADN chloroplastique) sont en général importants, d’où une faible différenciation interspécifique. Néanmoins la différenciation intraspécifique est plus forte lors- qu’elle est estimée à partir des marqueurs cytoplasmiques que lorsqu’elle l’est à partir des mar- queurs nucléaires. biologie florale / cycle de vie / système de reproduction / flux de gènes / chêne INTRODUCTION Staminate flowers Male flowers are grouped in catkins which Plant populations show a significant in the axils of either the inner bud amount of organization in the genetic vari- develop scales or the first leaves, in the lower part ation they contain (Wright, 1951). Such or- of the branches in the same ganization is significantly influenced by produced Staminate inflorescences are initiat- joint action of mutation, migration, selec- year. ed in late spring, flowers develop in early tion and genetic drift. In this context, gene summer and meiosis occurs in the follow- flow among plant populations may repre- ing spring, giving rise to binucleate pollen sent a significant factor influencing the grains immediately prior to the emergence maintenance of genetic organization in of catkins (Sharp and Chisman, 1961; plant species populations (Slatkin, 1987). Stairs, 1964; Tucovic and Jovanovic, 1970; Gene flow is generally considered to be Hagman, 1975; Bonnet-Masimbert, 1978; both small enough to permit substantial lo- Merkle et al, 1980). For a given tree, if cal genetic differentiation (Levin and Kerst- weather conditions are suitable, catkin and to introduce er, 1974), large enough growth is achieved 1-2 weeks after bud variability into widely separated popula- opening, and pollination is completed in 2- tions and Hamrick, This (Loveless 1984). 4 days (Sharp and Chisman, 1961; Stairs, is in particularly important outbreeding, 1964; Vogt, 1969; Lumaret et al, 1991). In perennial and iteroparous species, such deciduous oaks, leaf expansion ceases as forest trees. during the release of pollen, which allows In the present paper, the influences of freer movement of pollen (Sharp and Chis- the mating system and factors operating man, 1961). on gene flow at different stages of the life are reviewed in various of cycle species Pistillate flowers the genus Quercus. Female flowers appear in the axils of leaves in the same REPRODUCTIVE SYSTEM produced year. They are produced on a short stalk and become visible a few days after the emergence of the male catkins and Floral biology (Sharp Sprague, 1967). Inflorescence primordia are difficult to distinguish from lateral bud primordia Species of the genus Quercus (the oaks) before late summer, hence the exact time are predominantly monoecious with dis- of the initiation of pistillate inflorescences tinct male and female flowers borne on 2 is difficult to determine. As hermaphrodite types of inflorescences; very occasionally flowers are known to occur occasionally, they bear hermaphroditic flowers or inflo- Bonnet-Masimbert (1978) has hypothe- rescences (Scaramuzzi, 1958; Stairs, sized that their initiation may occur in late 1964; Tucker, 1972; Bonnet-Masimbert, spring, when the staminate inflorescences 1978; Tucker et al, 1980). The characteris- develop. Female flowers develop in late tics of male and female flowers are sum- winter or early spring (Bonnet-Masimbert, marized below. 1978; Merkle et al, 1980). Each flower is included in a cupule, which is regarded as fertilized ovule either suppresses the homologous to a third-order inflorescence growth of the other fertilized ovules or pre- branch (Brett, 1964; McDonald, 1979). vents their fertilization. After fertilization, During elongation of the stalk, 3-5 styles the acorns mature within about 3 months, emerge from the cupule and become red- then fall (Sharp, 1958; Corti, 1959). Each dish and sticky when receptive (Corti, year, even when a good acorn crop oc- 1959; Sharp and Sprague, 1967; Rushton, curs, a large amount (70% or more) of fruit 1977). Stigma receptivity for a single flow- abscisses (Williamson, 1966; Feret et al, er may last up to 6 d and 10-14 d for the 1982). inflorescence as a whole pistillate (Pjatni- The occurrence of a period of stigma re- ski, 1947; in Rushton, 1977). Stigma re- ceptivity longer than the period of pollen for a tree was found to be ceptivity given production for an individual tree may diver- 15 in Q ilex L et roughly days (Lumaret al, sify the number of potential partners for a 1991). In annual acorns, eg in the white given tree (Lumaret et al, 1991). oaks section of the genus, meiosis and fer- tilization of ovules occur 1 or 2 months af- ter pollen deposition. In biennial acorns, eg Life cycle in most of the American red oak section, the delay is about 13-15 months (Helmq- vist, 1953; Arena, 1958; Sharp, 1958; Cor- Life span and vegetative multiplication ti, 1959; Stairs, 1964; Brown and Mogen- Several which sen, 1972). In several species, such as Q species possess vegetative coccifera L and Q suber L, annual and bi- multiplication produce rejuvenated stems from root crown, trunk or rhizomes, so that ennial, or even intermediate acorns, occur it becomes to ascertain the on distinct individual trees (Corti, 1955; Bi- impossible age of a individual. It is, nevertheless, anco and Schirone, 1985). One embryo given that such oaks are sac is usually initiated per spore and this likely long-lived species 1950; Muller, exam- develops in the nucellus. Rare cases of (Stebbins, 1951). For Q ilicifolia and Q polyembryony, due to the development of ple, Wangenh hinckleyi Muller have short-lived stems yr more than 1 embryo sac per nucellus, or to (20-30 and 7-9 yr but re- the occurrence of 2 nucelli per ovule, have respectively) they mainly via been reported (Helmqvist, 1953; Corti, produce sprouts (Muller, 1951; Wolgast and This for 1959; Stairs, 1964). At fertilization, the pol- Zeide, 1983). capacity stump be in and, len tube enters the ovule through the sprouting may present juveniles with the of the micropyle (Helmqvist, 1953) after which 1 although decreasing age trunk, may enable oaks to maintain their of the 6 ovules in the ovary develops into a populations even in the absence of acorn seed. This ovular dominance occurs during early embryo growth (Stairs, 1964). Mo- production (Muller, 1951; Jones, 1959; Neilson and Wullstein, 1980; Andersson, gensen (1975) reported that 4 types of 1991). abortive ovules occur in Q gambelii Nutt, with an average of 2.7 ovules per ovary that do not develop into seed due to lack of Age and reproduction fertilization. In other cases, ovule abortion was due to zygote or embryo failure, or the The age of first acorn production varies absence of an embryo sac or the occur- with the species, but also with latitude, life rence of an empty one. For these reasons, span, tree density (a low density favors Mogensen (1975) proposed that the first earlier reproductive maturity) and site (Sharp, 1958; Jones, 1959; Shaw, 1974). same stand to be greater than stand-to- The age of first reproduction also occurs stand or site-to-site variation. Many other earlier for trees in coppiced sites than similar examples have been reported (eg those from seed origin, and range from 3 Jones, 1959; Feret et al, 1982; Hunter and growing seasons old for the short-lived Van Doren, 1982; Forester, 1990; Hails sprouts of Q ilicifolia (Wolgast and Stout, and Crawley, 1991). 1977b) to 30-45 years for the long-lived For interannual variation, Forester species Q petraea (Matt) Liebl (Jones, (1990) and Hails and Crawley (1991) have 1959). Acorn yield is often correlated with observed that fruit set in Q robur L is main- tree decreases size, although, fecundity ly a characteristic of individual trees. Simi- with increasing diameter (Sharp, 1958; larly, Sharp (1958) has reported that, in Iketake et al, 1988). white oaks, each tree is fairly consistent in acorn production, at least in years of good Sex allocation acorn crops. In addition, for Q ilicifolia indi- viduals transplanted to a common site, in- As oaks are monoecious, individual trees dividuals of different origins were not found may show biased reproductive effort favor- to have the same productivity (Wolgast, ing one or the other of the sexes.
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