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Development and Morphology |
Indiana University, Department of Biology, Bloomington, Indiana 47405 USA
Received for publication March 15, 2001. Accepted for publication August 23, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Arabidopsis thaliana • evolutionary constraints • herkogamy • phenotypic plasticity • photomorphogenesis • phytochromes • pleiotropy, red : far-red light (R : FR)
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Levins, 1968
; Lively, 1986, 1998
). Whether adaptive or not, plasticity is expected to strongly affect phenotypic evolution by influencing the opportunity for selection (Bradshaw, 1965
; Sultan, 1987
; Schlichting and Pigliucci, 1999
). Developmental information at the genetic level can inform evolutionary studies of plasticity, because developmental mechanisms determine both the ability of an organism to perceive the environment and the breadth of ensuing phenotypic responses. For instance, plants possess photoreceptors that enable them to detect and respond to various aspects of light quality, such as ambient levels of ultraviolet, blue, and red wavelengths. In some cases, light quality is perceived in one organ and a signal transduced to a second organ where the phenotypic response occurs. Phenotypic responses to light quality can also occur in the organs where photoreceptor genes are expressed (e.g., Casal and Smith, 1988
; Ballaré, Scopel, and Sanchez, 1990
), such that a single organ acts as the locus of perception and response. Developmental studies examining how gene expression varies among organs (e.g., Somers and Quail, 1995a, b
) or across environments (e.g., Furuya, 1993
) can therefore suggest likely plasticity to the environment. Here, light-quality cues and individual photoreceptors (phytochromes) known to influence the expression of vegetative traits were tested for their effects on floral morphogenesis.
The phytochrome photoreceptor family in plants acts in perception of red light and has received increasing attention from evolutionary ecologists because the photoreceptors mediate demonstrably adaptive, morphological responses to competition. As light passes through a vegetative canopy, red wavelengths are absorbed while far-red are transmitted due to selective filtering by chlorophyll (Kasperbauer, 1971
; Holmes and Smith, 1977a, b
). Light reflected off neighboring plants exhibits a similar reduction in the ratio of red : far-red wavelengths (R : FR) (Ballaré, Scopel, and Sanchez, 1990
). Low R : FR resulting from foliar shading is therefore a reliable indicator of neighboring plants and future competition for sunlight (Smith, 1982
; Ballaré, Scopel, and Sanchez, 1990
; Schmitt and Wulff, 1993
). Phytochromes, which switch photoreversibly between R- and FR-absorbing forms (Quail, 1991
; Furuya, 1993
), perceive R : FR cues and stimulate stem elongation. Under crowded, competitive conditions, elongation responses increase access to sunlight (Weinig, 2000a
) and enhance fitness (Schmitt, McCormac, and Smith, 1995
; Dudley and Schmitt, 1996
; Weinig, 2000a
).
Although the importance of R : FR and phytochromes to vegetative morphogenesis and competitive interactions is well-documented, the influence on floral development has never been tested. Studies with Arabidopsis thaliana have characterized five phytochrome genes (PHYA–PHYE) (Sharrock and Quail, 1989
; Clack, Mathews, and Sharrock, 1994
; Whitelam and Devlin, 1997
). Phytochrome B is largely responsible for perceiving reductions in R : FR associated with neighbor proximity (Smith, 1982
; Ballaré, Scopel, and Sanchez, 1990
; Schmitt and Wulff, 1993
; Smith and Whitelam, 1997
) and stimulating elongation responses observed among crowded plants. Expression of genes encoding phytochrome B in leaves and stems is consistent with the role these organs play in perceiving light-quality cues associated with competition (Casal and Smith, 1988
; Ballaré, Scopel, and Sanchez, 1990
). However, all PHY genes are also active in flowers. PhytochromeA and PHYB are expressed in all floral organs other than petals (Somers and Quail, 1995a, b
). Both PHYD and PHYE are expressed in sepals, and the latter is further expressed in filament tips (Goosey, Palecanda, and Sharrock, 1997
). The loss of expression in petals and persistent expression in other, homologous organs is consistent with the hypothesis that PHY genes are functional in some floral parts. One possibility is that PHY genes have organ-specific effects in flowers, e.g., phytochrome B may influence filament but not petal elongation because it is expressed only in the former organ.
Genetic and environmental factors affecting floral morphogenesis are relevant to individual fitness because floral morphology influences both an individual's breeding system and reproductive assurance. Greater herkogamy, i.e., greater separation of the stigma and anthers, increases the level of outcross- relative to self-pollen deposited on the stigma and affects the paternity of resulting seed (Rick, 1950
; Carr, Fenster, and Dudash, 1997
; Karron et al., 1997
). Because seeds resulting from self- vs. cross-fertilization differ in quality, the effects of herkogamy on pollen deposition and seed paternity are selectively important. Decreased herkogamy may enhance reproductive success in environments where pollinator visitation is uncertain by increasing the deposition of self-pollen on the stigma (reviewed in Jain, 1976
; Lloyd, 1979
; Dole, 1992
). Depending on the species, other aspects of floral morphology such as degree of stigma and anther exsertion have equally strong fitness effects (Thomson and Stratton, 1985
; Campbell, Waser, and Price, 1994
; Conner and Sterling, 1995, 1996
). In light of the potential fitness consequences, it is important to test for plasticity of floral morphologies.
Growth-chamber and greenhouse experiments were performed to test the effects of R : FR and phytochromes on floral morphogenesis. The effect of R : FR on flowers was determined by exposing buds of wild-type A. thaliana and wild-type B. rapa to both high and low R : FR conditions, which are similar to sunlit and foliar-shade environments respectively. To test the role of individual phytochromes, floral morphogenesis of wild-type A. thaliana was compared with that of monogenic mutants deficient in phytochrome A, B, or D. In comparison to flowers that opened under high R : FR, flowers of wild-type A. thaliana and Brassica rapa plants opening under low R : FR exhibited significant differences in either petal, pistil, or filament lengths. Floral development also differed between wild-type individuals and phytochrome-deficient plants. These studies therefore provide the first evidence that R : FR and phytochromes affect floral morphogenesis (see Smith and Whitelam, 1997
; Smith, 2000
for review of known phytochrome effects), and flowers of plants in different shade environments may be more plastic than previously realized.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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for spectral analysis). Measurements of light conditions under the panels indicate that R : FR is reduced to 0.5 (Lee, 1985
; Weinig, 2000b, c
) and that irradiance is reduced to 40% of full sun (Weinig, 2000b, c
). High R : FR conditions were established through the use of neutral-shade cloths. The shade cloths reduce irradiance to 37% of full sun but leave light quality unchanged (Weinig 2000b, c
). Seeds of both A. thaliana (La-er ecotype) and B. rapa were planted in 6- and 10-cm pots, respectively, and 15–20 plants of each species were raised to maturity in the greenhouse. Flowering individuals were placed under the light treatments in the morning. Flower production was monitored, and only flowers that opened two mornings following the treatment application were collected for measurement. Because the potential for self-pollination was of interest, flowers were measured at the time of anther dehiscence. In B. rapa, flowers typically opened (i.e., petals were reflexed) prior to anther dehiscence. New flowers were checked every 30 min for anther dehiscence and were only collected once dehiscence had occurred. Dehiscence was observed to occur in buds of A. thaliana. Flowers were therefore collected immediately after the petals reflexed and measured under a dissecting microscope. Sepals and petals were removed, after which the two longest stamens and the pistil were removed from the receptacle and ovary, respectively. The size of each floral organ was measured using an ocular micrometer. Herkogamy was estimated as the difference between the pistil length and the average length of the two filaments rather than stamens because anther sacs collapsed to differing degrees following dehiscence. Floral responses observed in replicate experiments did not differ from those presented here.
Role of individual phytochromes
To determine the role of phytochromes in floral development, floral morphology of monogenic mutants deficient in either phytochrome A, B, or D (phyA, phyB, phyD) was compared with that of wild-type plants. All experiments with mutants used isogenic lines of A. thaliana Heynh, ecotype La-er, with mutant alleles phyA-201, phyB-1, and phyD-130 (Devlin et al., 1999
). A single ecotype was selected in order to control for the effects of genetic background.
Seeds of all genotypes were germinated and grown to maturity in growth chambers at Indiana University. Growth chambers were set to 12-h photoperiods and day/night temperatures of 24°/21°C. The growth chamber was illuminated using a combination of 15-W GE incandescent bulbs and Phillips TL370 fluorescent tubes. The combination of light sources created a red : far-red ratio of 3.5 and irradiance of 450 µmol·m–2·s–1. This R : FR ratio is substantially higher than sunlight, but results in both a comparable phytochrome photoequilibrium (proportion of total phytochrome in the active form) and similar phytochrome-mediated growth responses (Smith, 1982
). The irradiance is lower than that of full sunlight but is probably appropriate for a shade-tolerant plant such as A. thaliana. Moreover, physiological studies of phytochrome-mediated effects commonly use similar or lower irradiance levels, because a comparison is made between wild-type and mutant plants, not between irradiance treatments attempting to simulate natural conditions.
Floral measurements began once individuals within a genotype were flowering. One flower from 10–12 plants of each genotype was collected. Only flowers produced at nodes 6–12 on the main flowering inflorescence were used in order to control for position effects known to occur in A. thaliana (Diggle, 1997
). To ensure that flowers of similar age were compared, flower production was monitored on a daily basis, and only flowers that had opened in the preceding 24 h were used. In addition, flowers were measured within 1–3 h after the onset of the light period in the growth chamber to decrease variability in the duration of flower expansion. Flowers were dissected and measured as above. Floral responses observed in replicate experiments did not differ from those presented here.
All data were analyzed using the General Linear Model procedure of SPSS 8.0. Multivariate analyses of variance were performed to test the effect of genotype on floral characters including petal, pistil, and filament length. Planned contrasts were used to test for significant differences between the wild-type and phytochrome-deficient mutant individuals (wild type vs. phyA, wild type vs. phyB, and wild type vs. phyD individuals). ANCOVA (analyses of covariance) were subsequently conducted with petal size included as a covariate in order to test whether observed differences in pistil and filament length were proportionate to shifts in flower size. MANOVAs were carried out to test for light-treatment effects on floral characters.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Role of individual phytochromes
Floral morphologies of monogenic mutant individuals (phyA, phyB, and phyD) of A. thaliana differed significantly from those of wild-type plants. Mutants lacking phytochrome A had relatively smaller petals, shorter filaments, and shorter pistils than wild-type plants (Fig. 3). The phyB-deficient mutants had comparatively longer filaments than wild-type individuals, but did not differ from wild-type plants in petal and pistil lengths (Fig. 3). No differences were detected between mutants lacking phytochrome D and wild-type individuals. These results indicate that individual phytochromes can affect floral development. Notably, both phytochromes A and B are expressed in the floral parts studied here (Somers and Quail, 1995a, b
), whereas phytochrome D is not (Goosey, Palecanda, and Sharrock, 1997
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Ballaré, Scopel, and Sanchez, 1990
; Schmitt and Wulff, 1993
; Pigliucci and Schlichting, 1999
). This study provides the first evidence that both light quality (R : FR) and the phytochrome photoreceptor family influence floral morphogenesis. One possibility is that PHY genes affect floral organs where they are expressed. Alternatively, observed floral plasticity may be a consequence of gene action elsewhere in the plant; vegetative responses to R : FR may affect whole-plant growth such that floral phenotypes also change. Regardless of the exact mechanism of action, plasticity of floral morphologies to the external light environment may be more common in natural populations than previously realized. This plasticity may carry substantial fitness consequences, although its ecological relevance remains to be determined. The study also demonstrates how developmental studies provide valuable information regarding plant responses to the environment. The novel patterns of plasticity observed here were suggested by earlier physiological studies showing that phenotypic responses to R : FR can occur in organs where the photoreceptor genes are expressed (i.e., leaves and stems) (Casal and Smith, 1988
) and by developmental genetic studies localizing the expression of PHY genes to flowers (Somers and Quail, 1995a, b
; Goosey, Palecanda, and Sharrock, 1997
).
In A. thaliana and B. rapa, elongation of floral parts varied depending on R : FR conditions. Relative to A. thaliana plants experiencing high R : FR, individuals exposed to low R : FR typical of foliar-shade light had significantly smaller petals and shorter pistils. The observed decreases in petal and pistil lengths under low R : FR may reflect arrested development of flowers. Other studies have shown that plants experiencing low R : FR abscise more flowers and fruits than those grown under supplemental red light and correspondingly higher R : FR (Heindl and Brun, 1983
). A further alternative is that low R : FR influences pistil length by affecting the rate of anthesis and flower size, i.e., flowers may have opened more slowly under the low relative to high R : FR conditions and been smaller as a result (see discussion below regarding effects of phytochrome A). However, this alternative seems less likely because filament lengths were greater relative to flower size under low than under high R : FR. This increase in length seems unlikely if flower development was arrested. Flowers of B. rapa plants showed qualitatively similar responses to low R : FR.
The plasticity in floral morphogenesis observed here could affect reproductive assurance or the breeding system of some species. Decreases in pistil-filament separation, such as those observed in the selfing species A. thaliana, may increase levels of self-fertilization because the relative proximity of stigmas and anthers can affect both the deposition of self-pollen on the stigma and outcrossing rates (Rick, 1950
; Carr, Fenster, and Dudash, 1997
; Karron et al., 1997
). Although the magnitude of the responses observed in A. thaliana was small, increases in herkogamy of similar magnitude prevent self-pollination and fruit set in this species in the absence of an external pollination agent (N. Kane, Brown University, personal communication). Filament-stigma separation showed a fourfold increase in B. rapa. Although studies with other members of this genus suggest that herkogamy is selectively unimportant (Conner and Sterling, 1995
), analogous shifts in floral morphology could influence fitness in non-Brassicaceous species.
The observed morphogenic effect of phytochrome B in flowers is analogous to its effect in vegetative parts. Mutants deficient in phyB fail to perceive red light and therefore fail to suppress elongation in high R : FR environments (Chory et al., 1989
; Reed et al., 1993
; Johnson et al., 1994
; Whitelam and Devlin, 1997
). This failure results in constitutively elongated hypocotyls, stems, and petioles. Here, mutants lacking phyB had more elongated filaments than did wild-type plants. Direct effects of phytochrome B on filaments may explain the responses of wild-type plants to low R : FR; in these plants, filaments elongated independent of changes in flower size. The response could, however, reflect perception and signal transduction from another organ or an effect on whole-plant growth.
The mechanism by which phytochrome A affects floral morphogenesis is less clear. In general, the morphogenic responses mediated by phytochrome A in light-grown plants parallel those of phytochrome B, although the degree of the response is far less pronounced. Hypocotyl lengths are slightly longer in phyA-deficient relative to wild-type individuals among plants raised under diurnal light cycles (Johnson et al., 1994
). By analogy, longer petal, pistil, or filament lengths would be expected in phyA-deficient relative to wild-type individuals, but the opposite pattern was observed. The PHYA deletion may have a negative, pleiotropic effect such that overall flower size decreases. Alternatively, the absence of phytochrome A may slow the diurnal rate of anthesis, thereby diminishing petal, pistil, and filament lengths by reducing time available for floral growth prior to collection. Differences between phyA and wild-type plants in floral morphology are less pronounced when flowers are measured later after anthesis (data not shown), which is consistent with the hypothesis that flowers of phyA-deficient individuals have delayed development. In addition, differences in pistil and filament lengths observed between phyA and wild-type individuals were proportionate to flower size; differences between the genotypes in pistil and filament lengths were nonsignificant when petal size was included as a covariate in ANCOVA. Allometric differences in flower size could again result from variable duration of flower growth. Phytochrome A acts in the entrainment of diurnal rhythms (Somers, Devlin, and Kay, 1998
), mediates diurnal gene-expression patterns (Hauser, Cordonnier-Pratt, and Pratt, 1998
), and stimulates perception of critical daylength (Johnson et al., 1994
; Olsen et al., 1997
). This phytochrome might therefore regulate other diurnal aspects of the phenotype including timing of anthesis and may account for the smaller flower size of wild-type A. thaliana grown under low R : FR.
Differences between the phy-deficient and wild-type plants may indicate a role for phytochromes in floral morphogenesis under sunlit conditions. Phytochromes are synthesized in a form that absorbs red light, but the proteins shift photoreversibly to a far-red absorbing form when the ratio of red : far-red wavelengths is equivalent to or greater than that of full sun (Holmes and Smith, 1975
, 1977a
; Quail, 1991
). Thus, when seedlings emerge from the soil into sunlight, the total proportion of phytochrome in the far-red absorbing form increases. The resulting phytochrome photoequilibrium suppresses stem elongation and ensures that plants are short under noncompetitive, sunlit conditions. In some species, phytochromes may somewhat mediate normal petal, pistil, or filament elongation by a similar mechanism; R : FR perceived by floral organs is low in buds due to light absorption by the green sepals and increases after anthesis when plants are growing in open, sunlit conditions. However, many genes influence floral morphology (Lawton-Rauh, Alvarez-Buylla, and Purugganan, 2000
), and the role of phytochrome-mediated plasticity to R : FR in the natural environment remains to be tested.
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FOOTNOTES |
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2 Current address: Brown University, Department of Ecology and Evolutionary Biology, Box G-W, Providence, Rhode Island 02912 USA (tel: 401-863-2897, FAX: 401-863-2166, cweinig{at}brown.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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