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0 Department of Botany, North Carolina State University, Raleigh, North Carolina 27695-7618 USA
Received for publication August 13, 1999. Accepted for publication January 3, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: apical meristem • commitment • Fabaceae • floral development • Glycine max • photoperiod • raceme • reversion • trifoliolate
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Levy and Dean, 1998
). This method can be particularly helpful in trying to identify the period of transition from the vegetative to the reproductive phase of development, as well as the specific timing of commitment to floral development. Floral commitment is influenced by the duration of exposure to an inductive stimulus (McDaniel, 1994
). Shifting plants from exposure to an inductive to noninductive stimulus during the transition period may be useful to determine whether floral commitment had already occurred. Resulting morphological abnormalities could identify those organs susceptible to changes in inductive stimuli, as well as those that are not.
Reversion of flowering occurs when production of vegetative structures is resumed in a meristem after floral development has been initiated (Battey and Lyndon, 1990; Lyndon, 1998
). It is possible for leaf production to resume at any time during flower initiation as long as the shoot apical meristem has not yet become completely determined for flower formation (Lyndon, 1990
). Reversion is a result of changes in inductive and noninductive stimuli that generate an initial, but insufficient, floral signal to maintain morphological floral development (Pouteau et al., 1997
). Stimuli capable of evoking a reversion event include manipulations in photoperiod (Biddulph, 1935
; Murneek, 1940
; Greulach, 1942
; Jacobs and Raghavan, 1962
; Kasperbauer, Gardner, and Loomis, 1962
; Bagnard, 1980
; Battey and Lyndon, 1986), temperature (Stokes and Verkerk, 1951
; King and Evans, 1969
), and chemical treatments (Lord and Eckard, 1987
; Marc and Hackett, 1991
; Donnison and Francis, 1994
).
Soybean is a preferential SD plant and its growth and development are sensitive to photoperiod length (Borthwick and Parker, 1938a
; Johnson, Borthwick, and Leffel, 1960
; Thomas and Raper, 1983
; Cregan and Hartwig, 1984
; Hadley et al., 1984
; Board and Settimi, 1988
; Kenworthy, Brown, and Thibou, 1989
; Wilkerson et al., 1989
). The determinate soybean (Glycine max [L.] Merrill cv. Ransom), which ceases vegetative activity when the apical meristem becomes an inflorescence, is induced to flower more rapidly under a SD photoperiod, whereas LD prolongs vegetative growth. According to Borthwick and Parker (1938b)
, exposing plants to LD photoperiods before bracteoles develop could prevent floral differentiation in Biloxi soybean (a more SD-sensitive cultivar). Thus, the critical point at which a soybean plant could be committed to flowering may be associated with the timing of bracteole development. It is possible, then, that if a floral photoperiodic stimulus was removed before bracteole development and replaced with a vegetative inducing photoperiodic stimulus, soybean plants may revert to vegetative growth. The morphological consequences of such a photoperiodic change and whether any floral organs would be initiated in the interim before the reestablishment of vegetative growth, however, have not been reported. Development of any aberrant floral or vegetative structures as a result of alterations in photoperiod would be readily identifiable and assisted by extant literature on the development of soybean apices and flowers, which has employed both light and scanning electron microscopy (LM and SEM, respectively) (Guard, 1931
; Sun, 1957
; Miksche, 1961
; Nougarède and Rondet, 1971
; Summerfield and Roberts, 1985
; Carlson and Lersten, 1987
; Lersten and Carlson, 1987
; Thomas and Kanchanapoom, 1991
; Crozier and Thomas, 1993
).
The objectives of this study were: (1) to describe with SEM the developmental and structural changes in the shoot apical meristem of soybean plants exposed to various SD and LD photoperiod combinations; and (2) to determine the timing of floral commitment.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Growth chambers were programmed for a day/night temperature regime of 26°/22°C with either a SD or a LD photoperiod. The SD photoperiod consisted of 9 h of high-intensity light from a combination of cool-white fluorescent and incandescent lamps at an input wattage ratio of 3:1. Photosynthetic photon flux density (PPFD) was 600–650 µmol·m -2·sec-1 (400–700 nm) and photomorphogenic irradiance (PI) was 11–13 W m2 (700–850 nm). The LD photoperiod consisted of the same high-intensity light period as the SD photoperiod, with an additional 3 h low-intensity light interruption from the incandescent lamps during the middle of the dark period with negligible PPFD of 40–50 µmol·m-2·sec-1 and PI of 10–12 W m2. Radiation was measured 95 cm below the lamps using a LI-COR 185 quantum/radiometer and sensors. The day temperature was coincident with the high-intensity light period. Seedlings were thinned to one plant per pot for uniformity, and plants were grown until pod set. Mature plants were harvested and measured to determine the average height of each experimental set and the number of main stem trifoliolate leaf nodes.
Experimental treatments
The day after emergence, experimental Day 1, cotyledons were vertical and closed. Preliminary experiments identified that plants were most sensitive to photoperiodic changes on Day 6. At this stage, the shoot apical meristem was initiating the buttress of the sixth leaf primordium. After 6 SD two sets of plants were transferred to LD conditions. They remained there for 4 d with four night interruptions. Note that previous studies have shown that under LD conditions the plastochron rate for G. max cv. Ransom is 2.0 d/leaf (Thomas and Kanchanapoom, 1991
), thereby 4-LD exposures would have provided time for the initiation of two leaf primordia under ordinary conditions. On Day 10, half of the plants transferred to LD were returned to SD conditions, while the other set of plants remained in LD conditions for the duration of the experiment. SD control (SDC) and LD control (LDC) plants were grown continuously under SD and LD photoperiods. The experiment was repeated four times. For morphological characteristics and SEM analysis six plants were sampled from each photoperiod at 2–3 d intervals for the duration of the study. Each respective photoperiod treatment was concluded when anthesis occurred in the terminal inflorescence.
Microscopy
Plant material was collected and dissected for SEM analysis from two replications of the experiment 3 times/wk at 2–3 d intervals. Six apices were sampled from each photoperiod treatment at each collection time. Shoot tips were fixed in formalin-acetic acid-alcohol (FAA), transferred to 95% ethanol with safranin O, then dissected in 95% ethanol and stored in 70% ethanol (Crozier and Thomas, 1993
; Ramírez-Domenech and Tucker, 1988
). Plant tissues were dehydrated in a graded ethanol series and critical-point dried in a Tousimis Samdri-PVT-3B with liquid CO2. Dried tissue was mounted on sonicated aluminum stubs with spot-o-glue and liquid colloidal silver. Shoot apical meristems were coated with 40 nm of gold palladium in a Hummer V sputter coater. SEM micrographs were taken on Polaroid Type 55 P/N film with a Phillips 505T scanning electron microscope at 15 kV and a spot size of 50.
Due to the structural complexity of the meristems identified in the SEM micrographs, schematic diagrams illustrating the developmental sequences of the various vegetative–reproductive and reproductive–vegetative transitions of these meristems were composed to assist in interpretation of the micrographs and are located in the Appendix. The number for each of the diagrams corresponds with the figure number of the respective SEM micrographs, and figure legends are applicable to the respective diagrams.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Each of the three floral meristems of the terminal inflorescence that were initiated by Day 10 continued to mature and exhibit different stages of development (Fig. 7). The youngest axillary meristem had initiated sepal and petal primordia, while the oldest flower primordium of the terminal raceme had initiated all five sepals. The second floral primordium of the terminal raceme had initiated bracteoles and an outer ridge of tissue, which indicated the beginning of sepal development. The third floral primordium of the raceme had begun to initiate bracteoles. No floral meristem was yet visible in the axil of the youngest, most recently initiated, floral bract of the raceme. The remaining meristematic tissue of the inflorescence apex either underwent further development to form another bract, which would subtend another floral primordium, or it remained as an undifferentiated apical residuum and later became a small protrusion of tissue that did not develop into a floral structure (Figs. 8, 9).
Floral development of the terminal raceme continued during Days 12 through 15 with each floral primordium progressively increasing the number of organ whorls for each flower (Figs. 8–11). Organogenesis was complete when the floral primordium had one whorl of five sepals, one whorl of five petals, two whorls of five stamens, and a solitary carpel (see Figs. 9–11).
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LD meristem development
Plants maintained under a continuous LD photoperiod initiated leaves in an alternate distichous manner for approximately the first 30 d of growth (Fig. 12), after which the pattern of trifoliolate leaf initiation began to change. The initiation of the next trifoliolate leaf shifted 
135° in a two-fifths phyllotactic pattern by Day 31 (Fig. 13). This was a common occurrence for the last three trifoliolate leaves initiated by the meristem by Day 45 (Fig. 14).
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SD–LD meristem development
SD–LD plants were initially grown under SD conditions and transferred at Day 6 to LD conditions. These plants then remained in a LD environment for the duration of the study. By Day 7, plants had made the transition to the reproductive phase as evidenced by the appearance of an undifferentiated meristem in the axil of the youngest trifoliolate leaf (Fig. 18). The first bract of the terminal inflorescence had also been initiated (Fig. 18). The terminal inflorescence meristem had initiated two bracts in the two-fifths floral phyllotaxy with floral apices in their axils by Day 8 (Fig. 19). Occasionally, bract-leaf intermediate structures would develop wherein the oldest bract was observed to possess side appendages resembling stipules (Fig. 19), that would often then fuse at the base later in development and elongate. The younger bracts, however, exhibited the more common morphology associated with floral bracts. Four bracts were initiated in the terminal raceme and the inflorescence meristem was developing by Day 11, similar to plants exposed to a continuous SD photoperiod (Fig. 20).
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80% of the population resumed initiation of trifoliolate leaf primordia beginning on Day 12. The remaining population of plants either developed as SD or LD plants, without producing any intermediate bracts. The number of additional trifoliolate leaves initiated also varied from plant to plant. In some plants only one trifoliolate leaf was produced (Fig. 23), while initiation of 2–3 trifoliolate leaves was more common (Figs. 21, 22). Initiation of these leaves occurred in the floral, two-fifths phyllotactic pattern. Thereafter, the meristem returned to an alternate distichous pattern of leaf initiation by Day 23 (Fig. 24). After a number of trifoliolate leaves were initiated, the phyllotactic arrangement of leaves began to shift again by Day 39 (Fig. 25). This was similar to meristem development in plants observed under continuous LD conditions. For example, in Fig. 26 three successively initiated trifoliolate leaves appear to have shifted orientation from alternate distichous to a two-fifths phyllotaxy. This consistently occurred for the last three trifoliolate leaves initiated. It was then evident that the terminal meristem had made the transition to reproductive growth by the appearance of a meristem in the axil of the most recently initiated trifoliolate leaf by Day 41 (Fig. 26). Once the terminal meristem had initiated a bract, it proceeded to initiate several more bracts, e.g., four by Day 49 (Fig. 27) and nine by Day 53 (Fig. 28). By Day 53, the meristem was still initiating bracts, and flowers were developing in the axils of these bracts (Fig. 28).
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25%), but continued to produce as many as seven bracts and develop as SDC plants (Fig. 35). The transition to the final floral phase of development occurred with the production of a meristem in the axil of the youngest trifoliolate leaf by Day 16 (Fig. 36). As in SDC plants, a final 3–4 bracts were initiated that subtended flowers of the terminal raceme by Day 17 (Fig. 37).
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Plant morphology
During their respective vegetative phases of development, SDC plants initiated 6–7 main stem trifoliolate leaves with a final main stem height of 83.5 ± 2.7 cm, while LDC plants initiated 20–22 trifoliolate leaves with a final height of 252.5 ± 17.5 cm. Anthesis occurred on Day 23 ± 1 for SDC plants and on Day 94 ± 7 for LDC plants.
SD–LD–SD and SD–LD plants matured and exhibited slightly different morphological characteristics than the SD and LD plants. SD–LD–SD plants first initiated 6–7 trifoliolate leaves, then 2–3 foliaceous bracts, followed by 1–2 trifoliolate leaves. These intermediate bracts were positioned as trifoliolate leaves on the main stem. A total of ten leaf-like organs were produced by most SD–LD–SD plants. These plants had a final height of 112 ± 5 cm and reached anthesis on Day 33 ± 1. SD–LD plants produced bracts that were positioned as trifoliolate leaves on the main stem. The plants first initiated 6–7 trifoliolate leaves, then 3–4 foliaceous bracts, followed by 10–12 trifoliolate leaves. They generally produced a total of 19–23 leaf-like organs on the main stem with a final height of 216.5 ± 15.7 cm. SD–LD plants reached anthesis on Day 79 ± 7. SD–LD–SD plants sometimes developed aberrant pods. Some aberrant flowers formed two carpels that produced a two-lobed pod, while other pods became curled and distorted.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), flowered faster under SD than LD photoperiods. A fourfold difference in the timing of anthesis occurred between SD and LD plants in this study (i.e., 23 ± 1 d vs. 94 ± 7 d, respectively). LD plants produced an average of 21 main stem trifoliolate nodes, while SD plants produced an average of seven main stem trifoliolate nodes. Heights of SD and LD main stems also exhibited threefold differences (i.e., 83.5 ± 2.7 cm vs. 252.5 ± 17.5 cm, respectively). SD–LD–SD plants resembled SD plants by mimicking their flowering time, height, and the number of trifoliolate leaves produced. The LD interruption caused SD–LD–SD plants to delay initiation of male and female reproductive organs by 6 d, produce three additional nodes, and grow slightly taller than SD plants. SD–LD growth was more similar to that of LD plants than to SD or SD–LD–SD plants. SD–LD plants became floral much later than SD plants (e.g., 79 ± 7 d vs. 23 ± 1 d, respectively), produced nearly the same number of main stem trifoliolate leaves as LD plants, and were taller than SD and SD–LD–SD plants. LD plants flowered last, produced the most trifoliolate leaves, and were the tallest.
The shoot apical meristem of SD–LD and SD–LD–SD plants exhibited reverted growth patterns under exposure to a noninductive photoperiod following a brief inductive photoperiod. SD–LD–SD and SD–LD plants were developing as SD plants when transferred to LD conditions; the terminal shoot apex had made the transition to the early floral phase of development and had begun initiating bracts in a two-fifths phyllotaxy. The initiation of bracts was interrupted when these plants were exposed to the night interruption of the LD photoperiod. Instead of continuing to initiate bracts with floral primordia in their axils, the meristem began to initiate trifoliolate leaves in the floral two-fifths phyllotaxy. With the resumption of growth and elongation of the main stem promoted by the LD photoperiod, the intermediate bracts appeared at maturity on the main stem in positions normally occupied by trifoliolate leaves. Some of these bracts were unusually shaped on SD–LD and SD–LD–SD plants. At maturity, bracts either consisted of a single triangular-shaped lobe, typical of a bract, or were tri-lobed with a larger center lobe (Fig. 19) (Crozier and Thomas, 1993
). Some intermediate bracts were fused like typical bracts, although they maintained a central structure resembling a trifoliolate leaf (Fig. 31). When mature, abnormal bracts elongated and become foliaceous. All trifoliolate leaves initiated after intermediate bracts on SD–LD and SD–LD–SD plants developed as normal trifoliolate leaves. The terminal racemes of some SD–LD–SD plants were elongated with visible internodes between each pod, and a small number of SD–LD–SD flowers produced aberrant pods that were fused or curled.
Photoperiodic sensitivity is most developed in leaves, and a critical threshold of an inductive stimulus must be reached for the floral program to permanently override vegetative development (Bernier, Kinet, and Sachs, 1981
). Floral promoting activity increases steadily under inductive conditions and triggers a series of events that leads the meristematic tissue to initiate floral structures (Meijer, Saedler, and Huijser, 1995
). The appearance of floral characteristics often occurs gradually, with possibly each characteristic having an individual activation threshold. Therefore, some floral characteristics may appear before others, and their presence may be more permanent than others.
When SD–LD–SD and SD–LD plants were transferred to a LD photoperiod on Day 6, they had begun to show early characteristics of floral development, but must have not reached their critical threshold for floral induction. Therefore, although meristems had entered the floral phase as a result of exposure to a SD photoperiod, they were not completely committed to floral development. Plants transferred to a LD photoperiod reverted to reinitiate vegetative structures. The production of trifoliolate leaves was stimulated, but at first occurred in the floral two-fifths phyllotaxy. This indicated that the program for the phyllotaxy shift required a lower inductive threshold, while the initiation of bracts apparently required a higher inductive threshold. Therefore, the floral phyllotaxy was established before commitment to the type of organ to be initiated was established. After exposure to 17 LD photoperiods, the pattern of trifoliolate leaf initiation was restored to the typical vegetative alternate distichous pattern in SD-LD plants (Fig. 24). This restoration did not occur in SD–LD–SD plants, which suggested that more than 4 LD were required to reinstitute a more complete vegetative developmental program.
Results from this study indicate that there is a short time frame wherein photoperiodic changes can affect floral development in soybean. The population of nonreverted plants, which were exposed to photoperiodic changes, was apparently insensitive to such changes. This may have been a result of slight physiological/developmental age differences in plants (even though when pots were thinned seedlings were selected for visible uniformity). Thus, plants that remained floral were possibly too "old" at the time of transfer to LD and plants that remained vegetative were too "young." Older plants must have received the critical threshold of the inductive stimulus by the time they were transferred to LD and did not revert to vegetative development in LD. These plants maintained bract development and did not initiate any additional trifoliolate leaves, even in a LD photoperiod. The level of inductive stimulus, however, was not sufficient to inhibit the elongation of internodes between the bracts of the terminal raceme. A small population of SD–LD and SD–LD–SD plants did not exhibit signs of floral onset after 6 SD and continued vegetative development. This indicated that meristems had not received a sufficient level of inductive stimulus to begin initial steps of floral development.
Morphological alterations have been documented in reversion studies induced by shifts in exposure to inductive and noninductive photoperiods. Leaves produced after floral development are often initiated in a floral phyllotaxy (Biddulph, 1935
; Greulach, 1942
; Battley and Lyndon 1984, 1986
). Floral bracts usually elongate and become foliaceous (Biddulph, 1935
; Greulach, 1942
). Unusual inflorescences have also been described. Flowers consisting of vegetative leaves have occurred (Murneek, 1940
; Kasperbauer, Gardner, and Loomis, 1962
; Lyndon, 1979
), as well as hybrid vegetative-floral organs (Greulach, 1942
; Battey and Lyndon, 1986). Lobes of anomalous bracts shared pigment qualities between green leaves and pink petals in Cosmos bipinnatus (Greulach, 1942
). Reverted Impatiens balsamina produced organs intermediate between leaves and petals containing pigments typical of each structure (Battey and Lyndon, 1986). Determination of these organs was not uniform, but rather individual areas of the organ were able to respond to the photoperiod and develop as petals or leaves. This observation indicated that differentiation and determination can occur at a cellular level (Battey and Lyndon, 1988) and that identities of cells of the apical meristem are dynamic and can change based on cellular communication (van der Schoot and Rinne, 1999
).
Successful morphological reversion studies have not been documented in Arabidopsis (Hempel et al., 1997
). The inability of Arabidopsis to revert between phases of vegetative and floral development seems to occur because complete floral commitment rapidly occurs 3 d before floral organs are initiated (Bradley et al., 1997
). Therefore, morphological alterations in floral organs would not be evident since reversion of flowering can only occur in species that initiate floral organs before complete commitment to flowering occurs. Plants developing a flowering bias, however, are able to maintain vegetative development if returned to noninductive conditions (Hempel et al., 1997
). The fate of an Arabidopsis primordium has also been shown to be modified by photoperiodic induction when a single flower has been initiated from a meristem that would ordinarily develop a paraclade (Hempel, Zambryski, and Feldman, 1998
). Investigations in species that commit to flowering after floral organ initiation may further define the genetic interactions occurring, and their dynamic nature, at the time period of meristem commitment to flowering (Pouteau et al., 1997
).
Clearly, changes in photoperiod are capable of a evoking a morphological response in soybeans. The plasticity of G. max (L.) Merrill cv. Ransom has been demonstrated by the changes in spatial and structural relationships between vegetative, floral, and reverted phases of development. These changes have included alterations in days to flowering, the number of trifoliolate leaves initiated, and position and type of organs initiated.
Reversion studies are useful in identifying the time period before complete commitment to flowering occurs in plants that commit during flower development. This methodology can also be used to identify organs most sensitive to changes in inductive stimuli. Glycine max (L.) Merrill cv. Ransom plants were susceptible to photoperiodic changes during the stage of bract production. This indicated that floral commitment occurred after floral development had already begun. The determination of organ initiation site in reverted soybeans, before the commitment of organ type, provided evidence that floral onset occurs as a summation of numerous individual steps. This observation may represent a very small or large step, but will only be distinguished when the developmental processes that occur at the shoot apical meristem of soybean plants are further characterized.
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FOOTNOTES |
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2 Current address: Washington Cooperative Fish and Wildlife Research Unit, School of Fisheries, Box 357980, University of Washington, Seattle, Washington 98195 USA.
3 Author for reprint requests (e-mail: jfthomas{at}unity.ncsu.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Battley, N. H., and R. F. Lyndon. 1984 Changes in apical growth and phyllotaxis on flowering and reversion in Impatiens balsamina L. Annals of Botany 54: 553–567
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———, and ———. 1988 Determination and differentiation of leaf and petal primordia in Impatiens balsamina. Annals of Botany 61: 9–16
———, and ———. 1990 Reversion of flowering. Botanical Review 56: 162–189
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