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2School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506-0225; and 4Department of Agronomy, University of Kentucky, Lexington, Kentucky 40546-0091
Received for publication May 11, 1998. Accepted for publication February 5, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 mo. However, they were similar in the timetable and pattern of fruit and seed development; it took 2 mo and 1.5 mo for flowers of Rhus aromatica and R. glabra, respectively, to develop into mature drupes. The single sigmoidal growth curve for increase in fruit size and in dry mass of these two species differs from the double-sigmoidal one described for typical commercial drupes such as peach and plum. Order of attainment of maximum size was fruit and endocarp (same time), seed coat, and embryo. By the time fruits turned red, the embryo had reached full size and become germinable; moisture content of seed plus endocarp had decreased to 40%. The endocarp was the last fruit component to reach physiological maturity, which coincided with development of its impermeability and a seed plus endocarp moisture content of <10%. At this time, 50, 37, and 13% of the dry mass of the drupe was allocated to the exocarp plus mesocarp unit, endocarp, and seed, respectively. The time course of fruit and seed development in these two species is much faster than that reported for other Anacardiaceae, including Rhus lancea, Protorhus, and Pistacia.
Key Words: Anacardiaceae • embryo germinability • endocarp impermeability • fruit development • mass allocation to fruit components • Rhus aromatica • Rhus glabra • seed development
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1971; Coombe, 1976
). Among the species that have received considerable attention are those with drupaceous fruits such as peach (Connors, 1919
; Lilleland, 1932
; Lott, 1932
), cherry (Tukey, 1934
), plum (Lilleland, 1934
), and apricot (Lilleland, 1930
). In these species, the endocarp is stony, but permeable to water, and the mesocarp is fleshy. Growth studies also have been done on drupes such as almond (Brooks, 1939
) and hackberry (Cowan et al., 1997
), in which the water-permeable endocarp is surrounded by a nonfleshy mesocarp. However, aside from studies on developmental anatomy in some species of Anacardiaceae native to southern Africa (von Teichman, 1987
, 1991b, 1993; von Teichman and Robbertse, 1986a
, b), little is known about fruit development in species with a water-impermeable endocarp.
Further, the relationship between attainment of embryo germinability and onset of endocarp impermeability has not been investigated. The impermeable endocarp of the germination unit (seed plus endocarp) of Anacardiaceae serves the same function as does the macrosclereid layer in the seed coat of hardseeded species of Convolvulaceae, Geraniaceae, Leguminosae, Malvaceae, and other plant families (Rolston, 1978
; Baskin and Baskin, 1998
). That is, the impermeable endocarp prevents water uptake by the embryo and, thus, is responsible for physical dormancy.
Rhus aromatica Ait. and R. glabra L. (Anacardiaceae) are dioecious shrubs with drupaceous fruits, in which the endocarp is impermeable to water at fruit maturity and is the only cause of physical dormancy (Heit, 1967
; Farmer, Lockley, and Cunningham, 1982
; Li et al., unpublished data). Rhus aromatica, the type species of subgenus Lobadium (Young, 1975
), mostly is distributed naturally in eastern United States and adjacent Canada, whereas R. glabra, of subgenus Rhus, occurs throughout the conterminous United States, north to southern Canada and south to northern Mexico (Barkley, 1937
; Little, 1977
). Rhus aromatica flowers in mid-spring and fruits in early summer, whereas R. glabra flowers in early summer and fruits in late summer. The variety of Rhus aromatica at our study site was Rhus aromatica var. aromatica (Gleason and Cronquist, 1991
).
Although there have been quite a few studies on the biology of some Rhus species (e.g., Boyd, 1943
, 1944; Brinkman, 1974
; Farmer, Lockley, and Cunningham, 1982
; Lovett Doust and Lovett Doust, 1988
; Facelli, 1993
), including three dissertations (Gilbert, 1959
; Lovell, 1964
; Smith, 1970
), virtually nothing is known about the pattern of fruit and seed development for any of the North American taxa. Thus, as part of a study on the comparative seed biology of R. aromatica and R. glabra we investigated the morphological and physiological changes that take place during fruit and seed development. More specifically, our primary objectives were to compare the (1) time course and pattern of fruit growth (size and mass) and of partitioning of dry mass to its components, and (2) time course of moisture content in relation to the development of endocarp impermeability and embryo germinability.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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20 km southeast of Lexington. Vegetation at the study site is the herb-shrub stage of old-field succession (Campbell, Ruch, and Meijer, 1995
). The soil is McAfee silty clay loam, 6–12% slopes, eroded phase (subgroup = Mollic Hapludalfs) (Sims et al., 1968
), and bedrock is Lexington Limestone (Middle Ordovician) (Black, 1967
). Mean annual precipitation (most of which is rainfall) at Lexington is 1141 mm and is fairly evenly distributed throughout the year. Mean annual temperature is 12.8°C, with a mean temperature of 0.8°C for the coldest month (January) and 24.4°C for the hottest month (July) (Hill, 1976
). Mean monthly maximum and minimum temperatures and precipitation recorded at Raven Run during the study period (1996–1997) are shown in Fig. 1. Nine clumps (
22 m2) of R. aromatica and three clumps ( 60 m2) of R. glabra plants were used in the study; clumps were separated by distances of 3–16 m, and each presumably was a distinct genotype.
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7.5 x 6.9 mm and 5.4 x 4.8 mm, respectively. A longitudinal section of a Rhus aromatica fruit at maturity prior to desiccation is shown in Fig. 2. A functional approach (von Teichman, 1989
, 1991b) is employed to define the various components of the pericarp. As such, the exocarp is the papery, relatively thin part of the pericarp in R. aromatica and in R. glabra that can be detached easily from the rest of the fruit, once the latter becomes desiccated. The endocarp is the stony inner part of the pericarp that encloses the seed. Between the exocarp and endocarp is the mesocarp, which easily can be detached from the endocarp and is united permanently with the exocarp in R. glabra. However, the mesocarp in R. aromatica is rather sticky and thus clings to the endocarp, and is separated spatially from the exocarp. In this study, the exocarp and mesocarp together are called pulp.
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Fifty fruits of each of the two species were collected randomly from the various clumps at maturity prior to desiccation, and their lengths and widths measured to the nearest 0.01 mm. Then, the pulp was removed from the fruit manually, and the lengths and widths of the endocarp, seed coat, and cotyledons were measured. Colors of these various fruit components also were recorded.
Time course and pattern of growth in length and width
Beginning at anthesis, lengths and widths of 50 flowers/fruits and of fruit components (endocarp, seed coat, and cotyledons) each of R. aromatica and R. glabra were collected weekly during the 1996 and 1997 growing seasons and measured to the nearest 0.01 mm under a dissecting microscope. On each collection date, five to seven infructescences were collected from each clump of each species. Flowers/fruits were removed from all infructescences and pooled. At the beginning (anthesis) and at the end of fruit development, there was only one size class. Fifty flowers/fruits were chosen randomly from the pool. Between anthesis and fruit maturity, fruits from all infructescences were pooled and sorted into four size classes. Fifty fruits were chosen randomly from the size class with the highest number of fruits. Fruits used in the following studies also were chosen using this procedure.
Time course and pattern of increase in dry mass
Masses (fresh and dry) also were determined for whole fruit, seed plus endocarp, and seed of R. aromatica and of R. glabra for each collection date. There were ten replications of ten fruits or of ten component units, i.e., each replicate consisted of ten whole fruits, ten seed plus endocarp units, or ten seeds. Mass data for pulp and endocarp were derived as follows:
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90°C until constant mass was reached (usually 3 d). All masses were determined to the nearest 0.01 mg and converted to mass per fruit, per seed plus endocarp unit, or per seed, prior to statistical analysis.
Time course and pattern of moisture content during development
Data collected in the mass growth study were used for calculating percentage moisture content (%MC), as shown below:
Development of embryo germinability
To determine when the embryo acquires the ability to germinate, four replicates of 15 embryos for each collection date were excised, placed on wet sand in petri dishes, and incubated under ambient laboratory temperature (22°–23°C) and light (cool-white flourescent for 10–12 h/d) conditions for 7 d, at which time the percentage of embryos that had germinated (i.e., radicle 
2 mm) was determined.
Development of endocarp impermeability
Time of onset of impermeability of the endocarp to water also was determined. The pulp (exocarp plus mesocarp) was manually removed from the fruit, and ten replications of 20 seed plus endocarp units each were kept on wet sand in petri dishes under ambient temperature and light conditions for 7 d. The percentage of seed plus endocarp units that had imbibed water was determined. An imbibed seed plus endocarp unit easily can be distinguished visually from a nonimbibed one. The former is considerably larger, and also lighter in color, than the latter.
Data analysis
For each species, a one-way (with collection date) ANOVA followed by Tukey's multiple comparison test (SAS, 1988
) was conducted for all measurements except mass and moisture content of pulp and endocarp. However, only length data are presented in this paper, since the pattern for width was exactly the same as that for length in both species. The square roots of all percentage data (i.e., moisture content, germination percentage, and imbibition percentage) were arcsine-transformed prior to statistical analyses.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2.0 and 1.5 mo, the initially inconspicuous ovary of R. aromatica and of R. glabra had developed into a mature, attractive drupe; drupes of R. aromatica are larger in size and in mass than those of R. glabra. Accordingly, the endocarp, seed coat, and cotyledons in R. aromatica are larger than those in R. glabra (Table 1). The pale creamy seed coat in both species is characterized by a dark saddle-like patch, which originates from the hypostase at the chalazal end of the ovule. The creamy-colored cotyledons of both R. aromatica and R. glabra are considerably flattened and bent.
General timetable of fruit and seed development
The time course of major developmental events for 1996 is shown in Table 2. In R. aromatica, the endocarp became physically separable from the rest of the fruit by 4 wk after anthesis (WAA hereafter), when the cotyledons were just beginning to appear (i.e., embryo at heart-shaped stage). By 5 WAA, the fruit reached its maximum size, and by 7 WAA the embryo had grown to its full length and width. This also was the time when most of the embryos attained the ability to germinate and the fruit turned ripe-red. After another week (8 WAA), physiological maturity was reached, which was 1 wk before the endocarp in the majority of fruits became impermeable to water. This developmental sequence was very similar in R. glabra, except for two minor differences. First, it took only 1 wk for the endocarp of R. glabra to become macrostructurally differentiated, as opposed to 4 wk in R. aromatica. Second, all other major developmental events occurred 1 wk sooner in R. glabra than the corresponding ones in R. aromatica, except physiological maturity, which was reached at the same time that fruits turned dark-red (ripe).
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Patterns of growth in length of fruit components in R. aromatica in 1996 and in 1997 are shown in Fig. 4. The whole fruit, endocarp, and seed coat reached mature size at the same time in both years. However, the embryo reached full size by 7 WAA in 1996 and by 9 WAA in 1997.
The fruit development pattern in R. glabra was exactly the same in 1996 and 1997 (Fig. 5). As stated above, the pericarp reached maximum size at 4 WAA; 1 and 2 wk later, the seed coat and embryo, respectively, also had grown to full size. Anthesis and thus all subsequent developmental events were 1 wk later in 1997 than in 1996.
Pattern of growth in dry mass
Growth curves
As in length growth, both R. aromatica and R. glabra showed a single sigmoidal growth curve for dry mass accumulation in whole fruit (Fig. 6a, c) and in seed plus endocarp (Fig. 6b, d). Growth rate was much higher in R. aromatica (Fig. 6a, b) than in R. glabra (Fig. 6c, d), as indicated by the much steeper slopes for R. aromatica. Mass increase of whole fruit in R. aromatica was faster, and maximum dry masses of both whole fruit and seed plus endocarp were greater in 1996 than in 1997. In contrast, the pattern of mass increase of R. glabra in 1996 and 1997 was identical.
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6–7% of the total dry mass had been allocated to the seed. However, these values increased to 22% in R. aromatica and to 16% in R. glabra at physiological maturity. By the time the endocarp became impermeable, 37% of the mass had been allocated to the endocarp in both R. aromatica and R. glabra. Pulp was the major allocation site, consisting of 50% of the total dry mass at maturity.
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82–84% at the time it became physically separable from the rest of the fruit to 10% when it became impermeable to water. However, before impermeability developed the pulp of the R. aromatica fruit had a higher moisture content than that of R. glabra. At that time, the fleshy part of the fruits of both species had a moisture content of 25%.
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60% to 40% in both species, the embryos changed from green to creamy in color and became germinable. However, endocarp impermeability did not develop until moisture content of seed plus endocarp dropped to below 20% in both species. It took 2 wk for the transition from permeability to impermeability of the endocarp in R. aromatica and 1 wk in R. glabra.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Lilleland, 1932
; Bollard, 1970
; Coombe, 1976
). In fact, Toldam-Andersen and Hansen (1997)
claimed that this double-sigmoidal growth pattern is characteristic of fruit growth in general. However, contrary to the shape of the growth curve of typical drupes of these commercial crops, that of R. aromatica and of R. glabra followed a single-sigmoidal pattern for increase in both size and mass, which is similar to what has been reported for some nondrupaceous fruits such as apple (Denne, 1960
), pear (Bain, 1961
), castor bean (Greenwood and Bewley, 1982
), and ash (Wagner, 1996
). Similar deviations from the double-sigmoidal growth curve also were observed in almond (Brooks, 1939
), date (Haas and Bliss, 1935
), and avocado (Schroeder, 1953
). Searching for an explanation for the single-sigmoidal pattern of growth, Bollard (1970)
pointed out that the almond has a dry leathery mesocarp vs. the fleshy ones of typical drupes; thus, the almond lacks a swelling stage. Although the mesocarps of R. aromatica and R. glabra are reasonably fleshy (moisture content of 45–89%) prior to maturation desiccation, they become dry (25% moisture content) after impermeability develops in the endocarp.
In both R. aromatica (Fig. 3a) and R. glabra (Fig. 3b), the temporal sequence of attainment of maximum size was fruit, seed coat, and embryo, which is similar to that of Fraxinus excelsior (Wagner, 1996
). This pattern of seed development lagging behind that of fruit development also has been reported in Rhus lancea (von Teichman and Robbertse, 1986b
) and in other genera (Copeland, 1961
; von Teichman and Robbertse, 1986a
; von Teichman, 1987
) of the Anacardiaceae. However, whereas the time lag between attainment of maximum size of pericarp and of seed in R. aromatica and R. glabra is only 1–2 wk, in other taxa of Anacardiaceae it is 5–20 wk (Grundwag, 1976
; von Teichman and Robbertse, 1986b
; von Teichman, 1991a
; Shuraki and Sedgley, 1996
).
Reproductive development of R. aromatica and R. glabra at the study site is separated by 2 mo. For example, the week after the endocarp of R. aromatica fruits became impermeable to water R. glabra was at peak anthesis (20 June–27 June in 1996 and 26 June–3 July in 1997). However, there are similarities in the timetable and in the pattern of the morphology and physiology of fruit and seed development in these two species.
The pericarp reached its maximum size (length) much earlier than it reached its maximum mass in both R. aromatica and R. glabra (6 vs. 9 wk in R. aromatica and 4 vs. 7 wk in R. glabra), whereas the embryo reached its maximal size and mass at the same time (i.e., 1 wk before impermeability developed) in both species (9 wk in R. aromatica and 6 wk in R. glabra). For both R. aromatica and R. glabra, the endocarp was the last fruit component to reach physiological maturity. These results are in contrast to those reported by Lilleland (1932)
, who showed that the stone of peach attained its maximum mass before either flesh or seed.
Allocation of fruit dry mass to the endocarp in both R. aromatica and R. glabra varied from 15% early in development to 37% at maturity (Fig. 7), which is much lower than that allocated to the mature endocarp in hackberry (Cowan et al., 1997
), but higher than that allocated to the mature endocarp in peach (Lilleland, 1932
).
Compared to 1996, size growth of the embryo in R. aromatica was delayed by 2 wk in 1997 (Fig. 4d), while in R. glabra it was the same in 1996 and 1997 (Fig. 5). Compared to R. glabra, there was a delay in increase in dry mass and in attainment of final mass of fruit and of seed plus endocarp in R. aromatica (Fig. 6). Further, whereas the time course of development of fruit and of seed plus endocarp in R. glabra was identical in 1996 and 1997, in R. aromatica there was a lag period of 1 wk in 1997 compared to 1996. This difference in the time course of growth in R. aromatica most likely is due to the variation in temperature and precipitation during the study period. Early summer 1997 was much cooler and wetter at the study site in 1997 than in 1996 (Fig. 1). For instance, mean monthly maximum temperature in both May and June was 5°C cooler in 1997 than in 1996, and precipitation in June 1997 was 245 mm, which is almost twice as much as that of June 1996 (125 mm). Presumably, the warm-dry conditions in late spring–early summer 1996 were more favorable for fruit growth and development than were the conditions in 1997. However, the cool, wet weather of 1997 did not continue for the rest of the summer, and thus did not affect R. glabra, except by delaying anthesis for 1 wk (26 June in 1996 and 3 July in 1997). In fact, moisture content data for fruit and for seed plus endocarp (Fig. 8) support this speculation. At similar developmental stages prior to the onset of endocarp impermeability, moisture content of whole fruit and of seed plus endocarp of R. aromatica was higher in 1997 than in 1996. On the contrary, no such difference was observed between these two years in R. glabra.
It took only 8–9 wk for the small flowers of R. aromatica and 6 wk for those of R. glabra to develop into conspicuous mature red fruits. These developmental periods are considerably shorter than those reported for other members of the Anacardiaceae, including R. lancea, a Southern African species (von Teichman and Robbertse, 1986b
; von Teichman, 1991a
), Protorhus (von Teichman, 1991b
), and Pistacia (Grundwag, 1976
), which take 13, 15, and 20 wk, respectively, for fruit development. In R. aromatica and R. glabra, the change in color of fruit from green to red coincided with color change of the embryo from green to creamy and its ability to germinate; soon afterwards, maturation desiccation resulted in endocarp impermeability to water.
In general, seed development and acquisition of the ability to germinate are associated with an overall loss of moisture (Adams and Rinne, 1980
), and this was absolutely true for R. aromatica (Fig. 9a) and R. glabra (Fig. 9b). Germinability of the embryo was coupled with a decrease in moisture content of the seed plus endocarp unit. Most embryos of both species attained the ability to germinate after the moisture content of the seed plus endocarp decreased to below 20%.
In both R. aromatica and R. glabra, development of endocarp impermeability was synchronized with attainment of physiological maturity, which was 1 wk after the dry mass of other components of the fruit had peaked. Thus, it seems that deposition of some chemical(s) in the endocarp may be coupled with desiccation, resulting in an increase in endocarp mass and in its impermeability to water. It would be interesting to investigate the effect of artificially decoupling the effects of these two factors on the development of endocarp impermeability, e.g., by collecting fruits immediately before the endocarp reaches physiological maturity and then artificially desiccating the seeds.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Bain, J. M. 1961 Some morphological, anatomical, and physiological changes in the pear fruit (Pyrus communis var. Williams Bon Chretien) during development and following harvest. Australian Journal of Botany 9: 99–123.
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Black, F. B. 1967 Geologic map of the Coletown quadrangle, East-central Kentucky. US Geological Survey Geological Quadrangle Map GQ-644.
Bollard, E. G. 1970 The physiology and nutrition of developing fruits. In A. C. Hulme [ed.], The biochemistry of fruits and their products, vol. 1, 387–425. Academic Press, London.
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———. 1944 An ecological study of four species of sumac in relation to development and growth on eroded soil. Transactions of the Kansas Academy of Science 47: 51–59.[CrossRef]
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———. 1971 The biochemistry of fruits and their products, vol. 2. Academic Press, London.
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———. 1932 Growth study of the Peach fruit. Proceedings of the American Society for Horticultural Science 29: 8–12.
———. 1934 Growth study of the plum fruit—the growth and changes in chemical composition of the climax plum. Proceedings of the American Society for Horticultural Science 30: 203–208.
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———. 1989 Reinterpretation of the pericarp of Rhus lancea (Anacardiaceae). South African Journal of Botany 55: 383–384.[ISI]
———. 1991a Ontogeny of the seed coat of Rhus lancea L. fil., and pachychalazy in the Anacardiaceae. Botanical Journal of the Linnean Society 107: 35–47.
———. 1991b Pericarp structure in Protorhus longifolia (Bernh.) Engl. (Anacardiaceae) and its taxonomic significance. Botanical Bulletin of Academia Sinica 32: 121–128.
———. 1993 Development and structure of the seed of Ozoroa paniculosa (Anacardiaceae) and taxonomic notes. Botanical Journal of the Linnean Society 111: 463–470.[CrossRef]
———, and P. J. Robbertse. 1986a Development and structure of the drupe in Sclerocarya birrea (Richard) Hochst. subsp. caffra Kokwaro (Anacardiaceae), with special reference to the pericarp and the operculum. Botanical Journal of the Linnean Society 92: 303–322.
———, and———. 1986b Development and structure of the pericarp and seed of Rhus lancea L. fil. (Anacardiaceae), with taxonomic notes. Botanical Journal of the Linnean Society 93: 291–306.
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 X. Li, J. M. Baskin, and C. C. Baskin Anatomy of two mechanisms of breaking physical dormancy by experimental treatments in seeds of two North American Rhus species (Anacardiaceae) Am. J. Botany, November 1, 1999; 86(11): 1505 - 1511. [Abstract] [Full Text] [PDF]
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), seed coat (
), and cotyledons (
) in Rhus aromatica (a) and in R. glabra (b) in 1996
) and in 1997 (•)
), and seed (
