‡Present address: Xiaojie Li, University of California at Davis/United States Department of Agriculture, Agriculture Research Service, 1636 East Alisal Street, Salinas, CA 93905, USA.
Taxonomy, anatomy and evolution of physical dormancy in seeds
Version of Record online: 18 JUL 2008
Plant Species Biology
Volume 15, Issue 2, pages 139–152, August 2000
How to Cite
Baskin, J. M., Baskin, C. C. and Li, X. (2000), Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology, 15: 139–152. doi: 10.1046/j.1442-1984.2000.00034.x
- Issue online: 18 JUL 2008
- Version of Record online: 18 JUL 2008
- fruit coat anatomy;
- physical dormancy;
- seed coat anatomy
- Top of page
- Taxonomic occurence of physical dormancy
- Future research needs
Physical dormancy (PY) is caused by a water-impermeable seed or fruit coat. It is known, or highly suspected, to occur in nine orders and 15 families of angiosperms (sensuAngiosperm Phylogeny Group 1998), 13 of which are core eudicots. The Zingiberales is the only monocot order, and Cannaceae (Canna) the only monocot family, in which PY is known to occur. Six of the nine orders, and 12 of the 15 families, in which PY occurs are rosids. Furthermore, six of the families belong to the Malvales. The water-impermeable palisade layer(s) of cells are located in the seed coats of 13 of the families, and in the fruit coats of Anacardiaceae and Nelumbonaceae. In all 15 families, a specialized structure is associated with the water-impermeable layer(s). The breaking of PY involves disruption or dislodgment of these structures, which act as environmental ‘signal detectors’ for germination. Representatives of the nine angiosperm orders in which PY occurs had evolved by the late Cretaceous or early Tertiary (Paleogene). Anatomical evidence for PY in fruits of the extinct species Rhus rooseae (Anacardiaceae, middle Eocene) suggests that PY had evolved by 43Ma, and probably much earlier. We have constructed a conceptual model for the evolution of PY, and of PY+ physiological dormancy (PD), within Anacardiaceae. The model begins in pre-Eocene times with an ancestral species that has large, pachychalazal, non-dormant (ND), recalcitrant seeds. By the middle Eocene, a derived species with relatively small, partial pachychalazal, orthodox seeds and a water-impermeable endocarp (thus PY) had evolved, and by the Oligocene, PD had been added to the seed (true seed + endocarp) dormancy mechanism. It is suggested that climatic drying (Eocene), followed by climatic cooling (Eocene–Oligocene transition), were the primary selective agents in the development of PY. An evolutionary connection between PY and recalcitrance is suggested by the relatively high concentration of these two character states in the rosids. Phylogenetic data and fossil evidence seem to support the PY(PY+PD) evolutionary sequence in Anacardiaceae, which also may have occured in Leguminosae.
- Top of page
- Taxonomic occurence of physical dormancy
- Future research needs
Seed dormancy caused by a water-impermeable seed (or fruit) coat is called physical dormancy (PY), and it develops during maturation drying of the seed (Van Staden et al. 1989; Baskin & Baskin 1998) or fruit (Li et al. 1999a). In seeds with PY, prevention of water uptake causes the seed to remain dormant until some factor(s) render the covering layer(s) permeable to water. In nature, these factors include high temperatures, widely fluctuating temperatures, fire, drying, freezing/thawing and passage through the digestive tracts of animals (Baskin & Baskin 1998).
Except for seeds of a few species in which the embryo also exhibits some degree of physiological dormancy (sensuNikolaeva 1969, 1977, 1999; Baskin & Baskin 1998), once the seed or fruit coat becomes permeable to water the seeds can germinate over a wide range of temperatures in both light and darkness. Furthermore, unlike seeds with physiological dormancy (PD) only, which may re-enter dormancy, that is, secondary dormancy, after primary dormancy is broken (Baskin & Baskin 1998), once the impermeable seed or fruit coat of seeds with PY becomes permeable it generally cannot revert to impermeability (Hamley 1932). Thus, the timing of the dormancy break in nature would appear to be a more critical event in the life history of plants with PY, than it is in those with PD. As such, to insure survival of species whose seeds have PY, the mechanism of PY-break must be fine-tuned to the environment in such a way that germination occurs only when and where chances for both establishment and eventual reproduction of the plant are maximized.
Various aspects of the biology of PY were reviewed in detail in Seeds: Ecology, biogeography, and evolution of dormancy and germination (Baskin & Baskin 1998). However, since completion of this book in July 1997, a considerable proportion of our library and laboratory research effort, including a PhD dissertation by the third author (Li 1999), has focused on the biology of PY. Thus, the purpose of this review is to present a more thorough synthesis of the taxonomic, anatomical and evolutionary aspects of PY in seeds (and fruits) than has been done heretofore.
Taxonomic occurence of physical dormancy
- Top of page
- Taxonomic occurence of physical dormancy
- Future research needs
Recognition of families and orders of plants in this paper is, for the most part, the same as that of the Angiosperm Phylogeny Group (1998). Baskin & Baskin (1998) listed 15 families (all angiosperms) with fully developed embryos at seed maturity for which evidence suggested that at least some species in them have PY: Anacardiaceae, Bombacaceae, Cannaceae, Cistaceae, Convolvulaceae (including Cuscutaceae), Curcurbitaceae, Geraniaceae, Leguminosae (including subfamilies Caesalpinioideae, Mimosoideae and Papilionoideae), Malvaceae, Musaceae, Nelumbonaceae, Rhamnaceae, Sapindaceae, Sterculiaceae and Tiliaceae. Of these, 13 are eudicots and only two, Cannaceae and Musaceae (both in Zingiberales), are monocots.
However, of the two monocot families, it now appears that only Cannaceae (Grootjen & Bouman 1988; Graven et al. 1997) has PY. Although mechanical scarification has been shown to enhance germination of Musa (Musaceae) seeds under suboptimal conditions (Stotzky et al. 1962), and the seed coat reported to be impermeable to water (e.g. Bhat et al. 1994), the seed coat, in fact, is not water-impermeable (Stotzky & Cox 1962). Furthermore, a water-impermeable layer of palisade cells (see following section) is not present in the Musaceae (Humphrey 1896; Graven et al. 1996).
Deleting Musaceae from the list of families with PY reduces the number from 15 to 14, and transferring three of the 15 families with PY (that is Bombacaceae, Sterculiaceae and Tiliaceae) to the Malvaceae (Angiosperm Phylogeny Group 1998) further reduces the number to 11. However, a recent detailed anatomical study of the chalazal region of species in ‘Cistaceae and related Malvanae’ by Nandi (1998) strongly suggests that Bixaceae, Cochlospermaceae, Dipterocarpaceae (subfamilies Monatoideae and Pakaraimoideae) and Sarcolaenaceae have water-impermeable seed coats. These four families bring the list of those with PY back to 15 (Table 1). All four families have an exotegmic palisade and a bixoid chalaza (Nandi 1998; see following section).
|Family||Seed type*||Specialized structure||Reference|
|Anacardiaceae†||Bent, investing||Carpellary micropyle||Li et al. 1999b|
|Bixaceae||Spatulate||Bixoid chalazal plug‡||Chopra & Kaur 1965; Corner 1976; Nandi 1998|
|Cannaceae||Linear-full||Imbibition lid||Grootjen & Bouman 1988; Boesewinkel & Bouman 1995|
|Cistaceae||Bent, spatulate||Bixoid chalazal plug‡||Thanos & Georghiou 1988; Corral et al. 1989; Nandi 1998|
|Cochlospermaceae||Spatulate||Bixoid chalazal plug‡||Corner 1976; Nandi 1998|
|Convolvulaceae||Folded, linear-full||Plug-like structure in micropylar region||Koller & Cohen 1959|
|Curcurbitaceae||Bent, investing, spatulate||?|
|Dipterocarpaceae||Folded, spatulate||Bixoid chalazal plug‡||Nandi 1998|
|Geraniaceae||Folded||Suberized ‘stopper’ (from nucellus)||Boesewinkel & Been 1979; Boesewinkel 1988|
|Caesalpinoideae||Folded, investing, spatulate||Hilar slit, lens||Jones & Geneve 1995; Bhattachary & Saha 1992; Lersten et al. 1992|
|Mimosoideae||Investing||Lens||Cavanagh 1980; Dell 1980; Hanna 1984; Lersten et al. 1992; Serrato-Valenti et al. 1995|
|Papilionoideae||Bent, investing||Lens||Hagon & Ballard 1970; Rolston 1978; Manning & Van Staden 1987a;|
|Malvaceae§||Bent, folded, investing, spatulate||Chalazal plug (from hypostase, at least in Tilia)||Christiansen & Moore 1959; Winter 1960; Egley et al. 1986; Nandi 1998;|
|Nelumbonaceae||Investing||Protuberance||Ohga 1926; Shaw 1929|
|Sapindaceae||Bent, folded, spatulate||?|
|Sarcolaenaceae||Folded||Bixoid chalazal plug‡||Capuron 1970; Nandi 1998|
As in the other families with PY, the embryos of Bixaceae, Cochlospermaceae, Dipterocarpaceae and Sarcolaenaceae are fully developed at seed maturity (Table 1). Seeds of Bixaceae have been shown to be water impermeable (Amaral et al. 1995), and this also appears to be true for those of Cochlospermum vitifolium (Cochlospermaceae) (Nandi 1998). Nandi found that dormancy in seeds of C. vitifolium could be broken best by mechanically scarifying the seed coat at the micropyle and incubating the seeds on blotting paper soaked with GA3. (Do seeds of this species have both PY and PD?) Furthermore, in contrast to the subfamilies Monotoideae and Pakaraimoideae, seeds of the other subfamily of Dipterocarpaceae, that is, Dipterocarpoideae, do not have the bixoid chalaza and most genera lack a palisade layer (Guerin 1911; Nandi 1998). In fact, a bixoid chalaza is not present in this subfamily and only a few genera in it have an exotegmic palisade (Nandi 1998). Seeds of Dipterocarpoideae (for example, Balanocarpus, Dipterocarpus, Hopea, Parashorea, Shorea and Vatica) are non-dormant, and those of many species are recalcitrant (Ashton 1982; Beniwal & Singh 1989; Baskin & Baskin 1998).
However, in spite of the presence of a bixoid chalazal region (Nandi 1998), it is not clear that Pakaraimaea dipterocarpacea seeds have PY or even any dormancy at all. Although a study of 22 seeds from a savanna woodland habitat of P. dipterocarpacea in Guyana showed low (2 seeds; 9%) germination after 2 weeks (Maguire & Ashton 1980), a second study of 50 seeds from a marginal Venezuelan woodland germinated to 86% (Maguire & Steyermark 1981). Although test conditions are not fully reported, these observations cast some doubt about seeds of P. dipterocarpacea having either PY or PD. However, the anatomy of the seed coat (Nandi 1998; also see Maguire & Ashton 1980) suggests that seeds should be impermeable to water. Therefore, for the time being, we include Dipterocarpaceae among the families with PY. Additional studies need to be done on Pakaraimaea, and the germination requirements need to be determined for species in subfamily Monotoideae.
Nandi (1998) discusses the apparent close relationship of Diegodendron (Diegodendraceae) to Bixa, but notes that the occurence of an exotegmic seed coat and a bixoid chalaza region remains to be determined. However, whatever the seed coat structure in Diegodendron humberti, the seeds are non-dormant: ‘La germination se fait immediatement après la chute des mericarpes . . .’ (Capuron 1965).
Several of the 15 families with species whose seeds have PY also have species with seeds that lack this type of dormancy. At least six also contain species that produce non-dormant seeds; these are Anacardiaceae, Dipterocarpaceae, Fabaceae, Malvaceae (including Bombacaceae, Sterculiaceae and Tiliaceae), Rhamnaceae and Sapindaceae (see Baskin & Baskin 1998). In addition, the following families contain one or more species whose seeds have both PY and PD: Anacardiaceae, Cucurbitaceae, Fabaceae, Geraniaceae, Malvaceae, Rhamnaceae and Sapindaceae. The Anacardiaceae and Rhamnaceae contain species whose seeds have PY, PD and (PY + PD), as well as ones that are ND. It seems that PY only may occur in Bixaceae, Cannaceae, Cistaceae, Cochlospermaceae (?), Convolvulaceae and Nelumbonaceae; and also in Malvaceae s. str. (excluding Bombacaceae, Sterculiaceae and Tiliaceae) (Baskin & Baskin 1998). We are not aware of any studies on seed germination in Sarcolaenaceae.
Undoubtedly, our list of 15 families with PY will be modified as research on seed dormancy and germination progress. Perhaps some families (for example, Dipterocarpaceae) will not stand the test of time, and it is possible that with further studies other families might be added. Based on seed coat anatomy (Netolitzky 1926; Corner 1976; Takhtajan 1988, 1992, 1996), we suggest that perhaps PY may occur in some member(s) of the following dicot families: Elaeagnaceae, Euphorbiaceae (subfamily Crotonoideae), Lardizabalaceae, Lauraceae (also see Nikolaeva 1999), Lecythidaceae, Melastomataceae, Neuradaceae (see Huber 1993; Nandi 1998), Passifloraceae, Polygalaceae, Staphyleaceae and Thymelaeaceae. Furthermore, water-impermeable seed coats also may occur in the Chloranthaceae, Illiciaceae, Myristicaceae, Schisandraceae and Winteraceae; in which case, these would be the only families, identified thus far, with both rudimentary embryos and PY.
Chenopodiaceae, Liliaceae, Poaceae and Solanaceae often are included in the list of plant families with PY (Crocker & Barton 1957; Nikolaeva 1969, 1977; Mayer & Poljakoff-Mayber 1989; Bewley & Black 1994; Werker 1997). In addition, Werker (1997) also included Rosaceae among families with PY. However, we have found no evidence that seeds of species in any of these five families have PY.
Seed (or fruit) coat anatomy and physical dormancy
In seeds of 13 of the 15 families, PY is caused by an impermeable layer(s) of the seed coat (Table 2). On the other hand, water uptake by the seed in the taxa of Anacardiaceae with PY is prevented by the palisade layers of the endocarp of the drupe (Li et al. 1999b) and in the Nelumbonaceae by the subepidermal palisade layer of the pericarp of the nut (Shaw 1929). The seed coat in these two families is not well developed (Shaw 1929; Corner 1976; von Teichman 1988, 1990), and its functional role is performed by the fruit coat.
|Family||Origin and characteristics of mechanical layer(s)|
|Anacardiaceae||Endocarp, which develops from inner epidermis of ovary wall; 3 innermost layers of a 4-layered endocarp are palisade-shaped; seed coat undifferentiated (that is, no mechanical layer sensuCorner 1976); with linea lucida (Wannan & Quinn 1990; Li et al. 1999c and references cited therein)|
|Bixaceae||Exotegmic palisade of lignified Malpighian cells (Dathan & Singh 1972; Corner 1976; Nandi 1998)|
|Cannaceae||Exotestal palisade of Malpighian cells; > 90% of seed coat formed from chalazal tissue and < 10% from integuments of ovule; with linea lucida (Takhtajan 1985; Grootjen & Bouman 1988; Graven et al. 1997)|
|Cistaceae||Exotegmic palisade of lignified Malpighian cells; with linea lucida (Dathan & Singh 1972; Corner 1976; Corral et al. 1989; Nandi 1998)|
|Cochlospermaceae||Exotegmic palisade of lignified Malpighian cells (Dathan & Singh 1972; Corner 1976; Nandi 1998)|
|Convolvulaceae*||Exotestal (but unitegmic) sensuCorner 1976; liginified palisade layer(s) developed from subdermal layer of integument; with linea lucida (Stripleng & Smith 1960; Bouman & Schier 1979)|
|Cucurbitaceae||Exotestal. Innermost sclerotic layer (of a three-layered exotesta developed from the outer epidermis) of thick-walled or lignified, radially elongated palisade-like cells, or of cuboidal-stellate cells (Singh 1964; Corner 1976; Takhtajan 1992)|
|Dipterocarpaceae†||Exotegmic palisade (Nandi 1998)|
|Geraniaceae||Endotestal/Exotegmic with sclerotized and crystal-containing cells of the inner epidermis of the outer integument and also sclerotized cells of the outer epidermis of the inner integument; with linea lucida (Boesewinkel & Been 1979; Boesewinkel 1988)|
|Leguminosae||Exotestal with palisade epidermal layer of thick-walled Malpighian cells; with linea lucida (Corner 1951, 1976; Takhtajan 1996)|
|Malvaceae‡||Exotegmic palisade of lignified Malpighian cells; with linea lucida (Reeves 1936a,b; Venkata Rao & Sambasiva Rao 1952; Venkata Rao 1953; Corner 1976; Mohana Rao 1976; Takhtajan 1992)|
|Nelumbonaceae||Pericarp with subdermal palisade of lignified and suberized Malpighian cells; with linea lucida (Ohga 1926; Shaw 1929; Takhtajan 1988)|
|Rhamnaceae||Exotegmic palisade; with linea lucida (Corner 1976; Keough & Bannister 1994)|
|Sarcolaenaceae||Exotegmic palisade (Capuron 1970; Nandi 1998)|
|Sapindaceae||Exotestal palisade of thick-walled (perhaps lignified) cells (in Koelreuteria); with linea lucida (Corner 1976)|
In addition, in some species of Leguminosae and in Malvaviscus drummondii (Malvaceae), that produce indehiscent fruits, the seed coat is not well developed, in which case the fruit coat mechanically protects the embryo. In Andira humilis (Leguminosae), an understory shrub in the Brazilian cerrados that produces a drupaceous fruit, the seed coat is differentiated very little (see fig. 45A, p. 96 in Werker 1997), and Rizzini states that ‘The main seed coat is the endocarp’ (Rizzini 1970). Removal or mechanical scarification of the endocarp promotes rapid germination of the seed. However, according to Rizzini, the endocarp is permeable to water, and dormancy is caused by a low oxygen supply to the embryo, due to low permeability of the endocarp to gases. However, Morrero (1949) reported that fresh seeds (apparently true seed + endocarp) of A. jamaicensis germinated to 100%. These results suggest that a survey is needed to determine whether the endocarp of drupe-producing taxa of Leguminosae is permeable to water, as occurs in the drupes of anacardiaceous taxa with the Anacardium-type, Rhoeae-Group A endocarp subtype (Wannan and Quinn 1990; Li et al. 1999a1999b1999c1999d–e). In M. drummondii, the seed coat is very thin and lacks a water-impermeable layer, and seeds ‘…are protected by thick, indehiscent, sclerified carpel walls’ (Reeves 1936a,b). Is the carpel wall of this species water-impermeable, and do the seeds have any PD?
Physical dormancy is associated with the main mechanical layer(s) (sensuCorner 1976) of the seed (or fruit) coat, which in most hardseeded species is a palisade of radially elongated cells (Table 2) that prevents passage of water to the embryo. It now seems clear that the palisade layer(s), and not the cuticle or some other layer(s) of the seed coat, is (are) responsible for water impermeability in seeds (Graaf & Van Staden 1983; Tran & Cavanagh 1984; Egley 1989; Werker 1997) and in fruits (Shaw 1929; Li et al. 1999b) of species with PY. However, the mere presence of a palisade layer, even if it is lignified, in the seed coat does not necessarily mean that the seed is impermeable to water. Corner (1976; also see Takhtajan 1988, 1991, 1992, 1996) describes various kinds of palisade layers in quite a few dicot families whose seeds are not known or suspected to have PY.
Thus, physical arrangement (how tightly packed) and chemical coatings/impregnates of cells in the palisade layer(s) undoubtedly is (are) important in determining whether passage of water into the seed is blocked. According to Corner (1951), ‘The hardness and impermeability of the dried testas [of seeds of Leguminosae] is caused mainly by the contraction of the walls of the palisade layer as the seed ripens.’ However, because water can infiltrate the cellulose fibrils in these cell walls, to be water impermeable the palisade cell walls must be coated or impregnated with (a) water-resistant substance(s) (Werker 1980/81), which may be waxes in association with the suberin-cutin matrix (Egley 1989). Egley (1989) also states that heavily lignified cell walls may make the palisade layer impermeable to water. According to Van Staden et al. (1989), resistance to water movement into the seeds of legumes is primarily due to water-impermeable substances in the outer ends of the palisade cells.
In seeds with bitegmic ovules, the outer integument gives rise to the testa (thus testal) and the inner integument to the tegmen (thus tegmic). Based on the layer(s) of mechanical cells, Corner (1976; also see Boesewinkel & Bouman 1984; Schmid 1986) classified seeds as exo-, meso- and endotestal and exo-, meso- and endotegmic. Exo-, meso- and endo- indicate the origin of the mechanical layer from the outer epidermis, middle layers and inner layer, respectively, of outer and inner integument. As pointed out by Schmid (1986), however, some seeds have two or more mechanical layers of different origin and can be described by appropriate hybrid terminology, for example endotestal/exotegmic seeds in Geraniaceae (Table 2). In most families that have unitegmic ovules, ‘. . . the integument differentiates in the exotestal manner . . .’, and seeds are called exotestal (Corner 1976; also see Schmid 1986). Thus, the water-impermeable layer(s) may be exotestal, exotegmic, endotestal/endotegmic (Geraniaceae), or, in Convolvulaceae, in which the ovule is unitegmic, exotestal with palisade developed from the subdermal layer of the single integument (Bouman & Schier 1979), and not from the outer hypodermal layer as Corner (1976) proposed (Table 2). In Anacardiaceae, the endocarp, which is the water-impermeable layer, develops from the inner epidermis of the ovary wall (Li et al. 1999c and references cited therein), and in Nelumbonaceae it originates from cells immediately below the epidermis of the pericarp (Shaw 1929).
Exotestal and endotestal seeds of angiosperms occur in the early Cretaceous of Portugal (Friis et al. 1999), with exotestal seeds being ‘especially abundant and diverse.’ Furthermore, the outer epidermis of the exotestal seed ‘. . . is often developed as a palisade layer’ (for example, see fig. 17 in Friis et al. 1999).
For seeds with PY to germinate, the water-impermeable layer(s) must become permeable, thereby allowing passage of water to the embryo. In Leguminosae, seeds become permeable after the lens (strophiole) (Table 1) is disrupted. Apparently, in most legume seeds, stress (for example via heating) causes disruption (pulling apart) of the relatively thin-walled cells of the lens. However, in some Leguminosae (subfamilies Caesalpinioideae and Mimosoideae) disruption also occurs via a pop-up lens (Dell 1980; Lersten et al. 1992), and in many taxa of these two subfamilies a lens may not be present. Gunn (1991) was able to locate a lens in only 49 of 151 genera of Caesalpinioideae and in only 33 of 66 genera of Mimosoideae (Gunn 1984). If a lens is not present, one wonders what is the route of water entry into the seeds and how they sense the environment?
In Cercis canadensis (Caesalpinioideae), neither Gunn (1991) nor Jones & Geneve (1995) discerned a lens, although the seed coat definitely is impermeable to water (Afanasiev 1944; Geneve 1991; Jones & Geneve 1995). The seed coat of this species contains a hilar slit, that is, the macrosclereid layer is interrupted, that possibly functions in the same way as the lens in other species in controlling water uptake (Jones & Geneve 1995).
Contrary to many reports, that the lens is the site of water entry into legume seeds following treatment (for example, Martin & Watt 1944; Cavanagh 1987), Egley (1979) found that covering the lens of hot water-pretreated seeds of the legume Crotalaria spectabilis with petroleum jelly did not prevent germination, implying that water uptake occurs in (a) region(s) of the seed coat other than the lens. In a recent paper, Morrison et al. (1998; also see Morrison et al. 1992) showed that dry-heating caused disruption of the seed coat only at the lens in some legumes; in others, an area on the seed coat, in addition to the lens region, was disrupted by dry heat. Seeds disrupted only at the lens had a thinner testa, thicker palisade layer and a thinner mesophyll layer (Morrison et al. 1998).
There is strong evidence that the lens is the weak point in the palisade layer of seeds of Leguminosae species with a lens: (i) seeds of the legumes Albizia lophantha (Dell 1980), Acacia kempeana (Hanna 1984) and Sesbania punicea (Manning & Van Staden 1987b) subjected to a boiling-water pretreatment imbibed water only at the lens; (ii) seeds of the legume Lupinus varius (≤8.5% moisture content) subjected to daily temperature fluctuations between 15 and 65°C became permeable to water only at the lens (Quinlivan 1968); (iii) seeds of the legume Astragalus cicer soaked in concentrated sulfuric acid became permeable only at the lens (Miklas et al. 1987) and (iv) seeds of the legumes Melilotus alba and M. officinalis overwintered outdoors in Iowa, USA, imbibed water only at the lens (Martin & Watt 1944). It follows, then, that the lens should function as the environmental ‘signal detector’ for the appropriate time and place for seeds to germinate. Van Staden et al. (1989) said it well: ‘Dry seeds maintain contact with ambient environmental events via the lens, which is sensitive to specific germination cues, including fluctuating temperatures and percussion.’
In addition to acting as an environmental ‘signal detector’, it seems that the lens may act as a regulator of the rate of water entry into the seed, thereby affecting seedling vigor (Van Staden et al. 1989). Seedlings of Sesbania punicea grown from seeds in which the lens was disrupted were more vigorous than those grown from seeds in which the lens region was excised mechanically. The rate of water entry was faster in seeds in the latter group, which resulted in lower seedling vigor, than in seeds in which the lens was merely disrupted (Manning & Van Staden 1987b).
Seed germination in most (all?) of the families with PY, except the Leguminosae, occurs only after a plug or lid that closes the discontinuity (‘water-gap’) in the water-impermeable layer(s) in the chalazal region is dislodged or disrupted, thereby creating a pore for entrance of water to the embryo. In Malvaceae, the so-called chalazal plug separates from the underlying subpalisade layer (Egley & Paul 1981; Egley et al. 1986; Egley 1989), and in Cannaceae the imbibition lid separates from the rupture layer (Grootjen & Bouman 1988). The subpalisade layer and the rupture layer occur only below the chalazal plug and imbibition lid, respectively, in seeds in these two families. Thus, a highly specialized anatomy that regulates dormancy and dormancy-break has evolved in Cannaceae and Malvaceae.
In Anacardiaceae, the endocarp of taxa with PY (that is, Anacardium-type, Rhoeae-Group A sensuWannan & Quinn 1990) consists of three water-impermeable palisade layers (from inside out): macrosclereids, osteosclereids and brachysclereids; and a fourth outer layer, the crystalliferous layer (Fig. 1). There is a discontinuity (which is the carpellary micropyle sensuLi et al. 1999b) in the macrosclereid layer. No discontinuity occurs in either the osteosclereid or the brachysclereid layer (Fig. 1), and these layers block the entrance of water to the carpellary micropyle in dormant seeds. Subjecting seeds (true seed + endocarp) of Rhus glabra to heat, for example, dipping them in boiling water (Li et al. 1999b) or subjecting them to fire (B. Mook et al., unpublished data) causes formation of a blister near the carpellary micropyle via uplifting of the osteosclereid and brachysclereid layers. During blister formation, a slit is formed in these layers, thereby creating an opening through which water passes to the seed (Fig. 1). On the other hand, seeds of R. aromatica soaked in concentrated sulfuric acid became permeable via the carpellary micropyle, because the osteosclereid and brachysclereid layers that block entrance of water to the carpellary micropyle were destroyed (Li et al. 1999b).
Evolutionary considerations of physical dormancy
Since PY is not known in gymnosperms (Baskin & Baskin 1998), this type of dormancy may be regarded as derived in the angiosperms. As discussed earlier, PY occurs in 15 families of angiosperms (sensuAngiosperm Phylogeny Group 1998), 14 of which are eudicots and one a commelinoid monocot. In addition, 13 of these are core eudicots, 12 are rosids, 11 are eurosids and six are Malvales (Fig. 2). All four families in the Malvales s. str. (that is, Bombacaceae, Malvaceae, Sterculiaceae and Tiliaceae) have PY.
The monogeneric monocot family Cannaceae is the only one of eight families in the Zingiberales (Kress 1990) that has a water-impermeable seed coat. The water-impermeable layer in the seed coat of Canna is an exotestal palisade of Malpighian cells (Table 2), and such a mechanical layer in the seed coat of monocots is rare (Grootjen & Bouman 1988; Graven et al. 1997). According to Grootjen & Bouman (1988), ‘The striking difference in ovule structure [that is, pachychalazal development of] and seed coat anatomy in Cannaceae and other Zingiberales families demonstrates that a particular set of characters can evolve quite independently.’
Fossil evidence shows that the nine orders in which the 15 families with PY are placed had evolved by the late Cretaceous or early Tertiary (Muller 1981, 1984; Taylor 1990; Magallon et al. 1999). Thus, it seems reasonable to propose that PY has been in existence for >100 Ma. However, we know of no study that shows seed coat anatomy of fossil seeds of families whose extant members have PY, and only one study that shows the anatomy of the endocarp in a family in which this layer is the one impermeable to water. A transverse section of the endocarp of the extinct species Rhus rooseae (Anacardiaceae, tribe Rhoeae) from the middle Eocene Clarno Nut Beds of Oregon, USA, is shown in Manchester (1994a). Its age is about 43 Ma. The three layers of endocarp cells that can be seen (crystalliferous layer not identified) seem to be identical, or nearly so, to the macrosclereid, brachysclereid and osteosclereid layers in extant Rhus species thus far examined (see Li et al. 1999c and references cited therein). Significantly, PY appears to occur throughout the genus Rhus (Li et al. 1999d,e and references cited therein). Therefore, it seems safe to conclude that PY had evolved by the middle Eocene and probably much earlier.
Evolution of physical dormancy in Anacardiaceae
Information is available on the relative level of evolutionary advancement of character states for each of several characters of seeds and fruits of Anacardiaceae. Thus, it is possible to construct a conceptual model of evolutionary trends in Anacardiaceae that led to the development of PY in seeds (true seed + endocarp) in this family. Character states considered here are: (i) recalcitrant (ancestral) versus orthodox (advanced) embryos; (ii) relatively large (ancestral) versus relatively small (advanced) seeds; (iii) pachychalazal (ancestral) versus partial pachychalazal (advanced) seeds and (iv) water-permeable (ancestral) versus water-impermeable (advanced) endocarps, and thus non-dormant (advanced) versus physically dormant seeds (advanced) (Corbineau et al. 1986; von Teichman & Robbertse 1986a; von Teichman et al. 1988; Wannan & Quinn 1990; von Teichman & van Wyk 1991, 1994; Pienaar & von Teichman 1998; Li et al. 1999a1999b1999c1999d–e).
The fossil record of the large-seeded, pachychalazal, recalcitrant tropical wet forest anacardiaceous genus Mangifera (Hou 1978; von Teichman et al. 1988), whose seeds are non-dormant (Corbineau et al. 1986), extends back to the Paleocene (Mehrotra et al. 1998). In addition, the Anacardium-type, Rhoeae-Group A endocarp in the tribe Rhoeae (sensuWannan & Quinn 1990), which initially is water impermeable (Li et al. 1999a,b,d,e), seems to have evolved by the middle Eocene (Manchester 1994a), by which time seasonally dry forests had developed in tropical and in temperate regions (Axelrod 1992; Graham 1999).
Using these observations, we constructed a conceptual model for the evolution of PY in seeds of Anacardiaceae (Fig. 3). We propose that the selective force for evolution of PY was climatic drying, resulting in seasonally dry forest habitats within the tropics/subtropics. In general, recalcitrance is not compatible with seasonally dry or xeric habitats; many (but not all, see von Teichman & van Wyk 1996) large-seeded, recalcitrant taxa are woody dicot plant species of moist tropical and subtropical forests (von Teichman & van Wyk 1991). Orthodoxy was selected for in embryos of certain taxa as they moved spatially or temporally into this type of habitat (see von Teichman & van Wyk 1991). Along with orthodox embryos, there was selective advantage to delay germination until the most favorable time of the year for seedling establishment and eventual reproduction of the plant. In seasonally dry tropical areas, the best time for germination would be at the beginning of a rainy season (Garwood 1982, 1983). Thus, PY, via a water-impermeable endocarp, evolved as a mechanism for delaying germination until the beginning of the next rainy season.
Support for an evolutionary connection between PY and recalcitrance comes from the fact that both of these seed character states are relatively highly concentrated in the rosids (Fig. 2). Thus: (i) 10 of the 19 orders of angiosperms with recalcitrant embryos are rosids; (ii) six of the 10 orders with recalcitrant embryos contain species with PY; (iii) 12 of the 15 families that contain species with PY are in six rosid orders with recalcitrant species and (iv) of the 15 families with PY, six are in the Malvales and two in the Sapindales, and both of these rosid orders contain recalcitrant species.
In addition to PY, PD also has been shown to occur in seeds of a few species in several plant families (Baskin & Baskin 1998), including Rhus aromatica and R. trilobata (but see Li et al. 1999d) of subgenus Lobadium (sensuYoung 1979) of the Anacardiaceae: tribe Rhoeae. Physiological dormancy does not occur in subgenus Rhus (sensuYoung 1979), in which R. copallina, R. glabra and R. typhina are placed. Baskin & Baskin (1998) reasoned that PD in seeds with (PY + PD) evolved after the seeds acquired PY, in response to climatic cooling. Thus, our model (Fig. 3) shows PD added to PY along one evolutionary pathway during the Eocene-Oligocene transition, a period of significant climatic cooling (Prothero 1994). The earliest fossil records of Cercis and Tilia, two other extant genera with (PY + PD) (see Baskin & Baskin 1998), are post middle Eocene: middle Miocene for Cercis (Owens et al. 1998) and late Eocene for Tilia (Manchester 1994b). A second line of evolution of seed dormancy, in which PD was not added to PY, continued unchanged through the Eocene-Oligocene climatic transition. Species with (PY + PD), as well as those with PY only, have persisted from the Paleogene to the present (Fig. 3).
Support for PD evolving after PY in Rhus, and thus in the Anacardiaceae, comes from heartwood flavonoid (Young 1979) and molecular phylogeny (Miller 1998) data, which show that subgenus Lobadium is more derived than subgenus Rhus. Furthermore, the fossil record of Rhus also seems to support this scenario. Macrofossils (leaflets) of Rhus nigricans (‘similar living species’ = R. typhina and the R. glabra-R. typhina complex in general) occur in the middle Eocene of the Green River flora of Utah and Wyoming, USA (MacGinitie 1969; also see Graham 1999), whereas the earliest report of macrofossils of Rhus (= Schmaltzia) vexans (‘analogous living species’ = R. trilobata) appears to be the latest Eocene-earliest Oligocene Florissant beds of Colorado, USA (MacGinitie 1953; also see Graham 1999).
However, not all species of Anacardiaceae that moved spatially or temporally into dry habitats lost their ancestral characters. An example is the monotypic Heeria argentea (Anacardiaceae: tribe Rhoeae), an endemic of the Cape Floristic Region of South Africa that usually is associated with sandstone outcrops in fynbos vegetation (von Teichman & van Wyk 1996). Seeds of Heeria are recalcitrant, pachychalazal, non-dormant and germinate hypogeally. Fruits of this species mature in late April and germinate at the beginning of the rainy season in late autumn (von Teichman & van Wyk 1996). Based on these ancestral character states, von Teichman & van Wyk (1996) suggest that H. argentea is a relict of a moist subtropical rainforest that once occured in southern Africa.
Wannan & Quinn (1990) recognized two distinct types of endocarp structure within the Anacardiaceae: the Spondias-type and the Anacardium-type. The Spondias-type occurs throughout the tribe Spondideae and the Anacardium-type occurs in the other four tribes: Anacardieae, Dobineeae, Rhoeae and Semecarpeae. However, the endocarps of Buchannia of tribe Anacardieae and of Campnosperma and Pentaspadon of the tribe Rhoeae are similar to the Spondias-type endocarp (Wannan & Quinn 1990). Furthermore, Wannan and Quinn defined three groups (subtypes) of endocarps (A, B and C) within the tribe Rhoeal, and von Teichman (1991, 1998) and von Teichman & van Wyk (1996) added a fourth one (Group D).
Fossil fruits of extinct Pentoperculum (Dracontomelon) minimus (tribe Spondideae) also have been collected from the middle Eocene Clarno Nut Beds of Oregon, USA (Manchester 1994a) and from the Eocene in England (Collinson 1983) and Hungary (Kovacs 1957). These fruits are quite similar to those of some extant genera of tribe Spondideae (Hill 1933, 1937). Opercula (germination lids) on the fossil fruits of Pentoperculum confirm that they belong to the tribe Spondideae.
Finally, fossil wood of the extinct species Tapirira clarnoensis (Anacardiaceae: tribe Spondideae), which is quite similar to that of extant species of the genus, also has been collected from the Clarno Nut Beds (Manchester 1977). This suggests that by the middle Eocene both the Anacardium-type endocarp, Rhoeae-Group A (Rhus) and the Spondias-type endocarp had evolved. Further, the endocarp of Tapirira differs from the typical Spondideae endocarp in that it does not have opercula (von Teichman 1990).
In addition to PY in Rhus, which is strongly indicated by the Anacardium-type, Rhoeae-Group A endocarp, there appears to have been at least two other seed (true seed + endocarp) dormancy/germination strategies of Anacardiaceae in the middle Eocene. The operculate fruits of Sclerocarya birrea ssp. caffra (tribe Spondideae) are physiologically dormant (von Teichman et al. 1986), and the nonoperculate fruits of Tapirira chimalapana are non-dormant, germinating easily in the laboratory (Wendt & Mitchell 1995). From these observations, we infer that seeds of the middle Eocene Pentoperculum had PD and that those of the middle Eocene Tapirira were non-dormant. They certainly did not have PY as the endocarp (which includes the operculum, sensuvon Teichman & Robbertse 1986b), did not restrict water uptake in Sclerocarya (von Teichman et al. 1986) and in Tapirira it is ‘relatively weakly developed’ compared to other members of the tribe Spondideae (von Teichman 1990). The mechanical layers in fruits of Spondideae are water-permeable, and the seed coats of Anacardiaceae are undifferentiated in that they lack a mechanical layer (Corner 1976).
Evolution of physical dormancy in Leguminosae
Van Staden et al. (1989) present a conceptual model for evolution of the control of water loss during the final stages of seed drying and of the evolution of PY in Leguminosae. Their model begins with a pleurogramless, tropical caesalpinioid ancestor in which the seed coat is permeable to water over its entire surface and the embryo is non-dormant. From this non-dormant ancestor with a water-permeable seed coat, there are two lines of evolution, both in response to increasing aridity. One line led to the development of the pleurogram and PY (in Caesalpinioideae and Mimosoideae) and the other to the development of the hilar value and PY (Papilionoideae). Van Staden et al. (1989) state that ‘Embryo dormancy [for example, in legumes with (PY + PD)] is a further strategy for controlling germination until environmental cues are experienced, which normally presage conditions for seedling survival.’ The combined dormancy (PY + PD), occurs in the genus Cercis in subfamily Caesalpinioideae (Baskin & Baskin 1998), and the oldest fossil evidence for this genus extends only to the middle Miocene (Owens et al. 1998), after climatic drying followed by climatic cooling in the early Tertiary that is Period. Thus, we suggest that PY and then (PY + PD) in Leguminosae also evolved in concert with climatic changes during the Paleogene.
Future research needs
- Top of page
- Taxonomic occurence of physical dormancy
- Future research needs
Much remains to be learned about the taxonomic occurence, anatomy (including ontogeny) and evolution of PY. We need answers to the following questions. (i) How accurate and complete is our list of families (Table 1, 2) that contain species with PY? In particular, we believe that a survey is needed of the taxonomic occurence of PY in moist tropical and subtropical areas of the world. (ii) Within which families is PY restricted to certain subfamilial groups, as seems to be the case, for example, within Anacardiaceae? (iii) If within-family taxonomic patterns are found for PY, are they related to the geography/climate of the biogeographic region of occurence (or origin) of the taxonomic group(s) in question? (iv) What are the specialized anatomical structures that serve as environmental signal detectors in seeds of Cucurbitaceae, Rhamnaceae and Sapindaceae (see Table 1)? (v) What is the environmental signal detector(s) in legume seeds that do not have a lens, and what is (are) the anatomical mechanism(s) for disruption of the seed coat? (vi) What is (are) the seed dormancy mechanism(s) in taxa of Leguminosae in which the seed coat does not contain a mechanical (that is, palisade) layer and the germination unit is an indehiscent fruit, such as a drupe or samara? Do the pericarps of these fruit-types in Leguminosae contain (a) water-impermeable layer(s) of palisade cells, such as occur in drupes of Rhus (Anacardiaceae) and in nuts of Nelumbo (Nelumbonaceae)? (vii) What are the anatomical mechanisms of physical dormancy-break in families other than the Anacardiaceae, Cannaceae, Leguminosae and Malvaceae, the only four families with PY in which the anatomy of dormancy-break seems to have been investigated in any detail? (viii) What physical/chemical characteristics of cells of the impermeable layer(s) of the seed and fruit coats are associated with dormancy induction (impermeability) and with dormancy break (permeability)? (ix) What biochemical pathways are involved in the development of impermeability? How are these physical/chemical changes controlled genetically at the molecular level? (x) Within a family or subfamilial group, how does the time of appearance of PY, based on seed or fruit coat anatomy, in the fossil record compare with the earliest reliable fossil records for that group? We need more information on the paleoanatomy of seed and fruit coats of extinct members of extant groups with PY. Answers to these questions will aid greatly in placing PY into a more secure phylogenetic/evolutionary context.
- Top of page
- Taxonomic occurence of physical dormancy
- Future research needs
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