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Environmental control of sepalness and petalness in perianth organs of waterlilies: a new Mosaic theory for the evolutionary origin of a differentiated perianth.

Warner KA, Rudall PJ, Frohlich MW - J. Exp. Bot. (2009)

Bottom Line: Our interpretation contradicts the unspoken rule that 'sepal' and 'petal' must refer to whole organs.We propose a novel theory (the Mosaic theory), in which the distinction between sepalness and petalness evolved early in angiosperm history, but these features were not fixed to particular organs and were primarily environmentally controlled.At a later stage in angiosperm evolution, sepaloid and petaloid characteristics became fixed to whole organs in specific whorls, thus reducing or removing the need for environmental control in favour of fixed developmental control.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.

ABSTRACT
The conventional concept of an 'undifferentiated perianth', implying that all perianth organs of a flower are alike, obscures the fact that individual perianth organs are sometimes differentiated into sepaloid and petaloid regions, as in the early-divergent angiosperms Nuphar, Nymphaea, and Schisandra. In the waterlilies Nuphar and Nymphaea, sepaloid regions closely coincide with regions of the perianth that were exposed when the flower was in bud, whereas petaloid regions occur in covered regions, suggesting that their development is at least partly controlled by the environment of the developing tepal. Green and colourful areas differ from each other in trichome density and presence of papillae, features that often distinguish sepals and petals. Field experiments to test whether artificial exposure can induce sepalness in the inner tepals showed that development of sepaloid patches is initiated by exposure, at least in the waterlily species examined. Although light is an important environmental cue, other important factors include an absence of surface contact. Our interpretation contradicts the unspoken rule that 'sepal' and 'petal' must refer to whole organs. We propose a novel theory (the Mosaic theory), in which the distinction between sepalness and petalness evolved early in angiosperm history, but these features were not fixed to particular organs and were primarily environmentally controlled. At a later stage in angiosperm evolution, sepaloid and petaloid characteristics became fixed to whole organs in specific whorls, thus reducing or removing the need for environmental control in favour of fixed developmental control.

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Experimental and non-experimental flower buds from Nuphar species. (A–D) Nuphar lutea untested flower buds. (A) Partially open bud (3 cm wide). (B) Mature bud (>3 cm wide), and (C) Individual tepals (from top left to right, tepals 1–5) showing exposed green (EG), covered green (CG), and covered non-green (CNG) areas of perianth. (D) Young inflorescence with pale yellow floral buds and surrounding young leaves. (E–G) Experimental flower bud of Nuphar advena (2.5 cm in width). Note the white-headed pin through the penducle which denotes the orientation of the bud in the photographs. (E) At the end of the test, the exposed area was dark green. (F) Bud with outermost tepal removed, displaying EE area. (G) Bud with EE tepal removed. The area of tepal directly beneath the experimentally light-exposed area is highlighted. (H–N) SEM images of tepals and flower buds of Nuphar lutea. (H–J) Tepal 3 from an untested bud (1.5 cm in width). (H) Abaxial exposed green patch. (I) Abaxial covered non-green patch. (J) Adaxial surface. (K) 0.1 cm wide bud. (l–M) 2.5 cm wide bud. Glands cover exposed (EG) patches and are present in covered green patches (CG). (N) Experimentally exposed tepal from Fig. 2A; boundary of experimentally exposed (EE) area marked with pinholes.
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fig2: Experimental and non-experimental flower buds from Nuphar species. (A–D) Nuphar lutea untested flower buds. (A) Partially open bud (3 cm wide). (B) Mature bud (>3 cm wide), and (C) Individual tepals (from top left to right, tepals 1–5) showing exposed green (EG), covered green (CG), and covered non-green (CNG) areas of perianth. (D) Young inflorescence with pale yellow floral buds and surrounding young leaves. (E–G) Experimental flower bud of Nuphar advena (2.5 cm in width). Note the white-headed pin through the penducle which denotes the orientation of the bud in the photographs. (E) At the end of the test, the exposed area was dark green. (F) Bud with outermost tepal removed, displaying EE area. (G) Bud with EE tepal removed. The area of tepal directly beneath the experimentally light-exposed area is highlighted. (H–N) SEM images of tepals and flower buds of Nuphar lutea. (H–J) Tepal 3 from an untested bud (1.5 cm in width). (H) Abaxial exposed green patch. (I) Abaxial covered non-green patch. (J) Adaxial surface. (K) 0.1 cm wide bud. (l–M) 2.5 cm wide bud. Glands cover exposed (EG) patches and are present in covered green patches (CG). (N) Experimentally exposed tepal from Fig. 2A; boundary of experimentally exposed (EE) area marked with pinholes.

Mentions: In all buds examined, the entire abaxial surface of the outermost tepal (tepal 1) was EG, whereas the inner four tepals (tepals 2–5) possessed EG, CG, and CNG patches (Fig. 2C). The position, shape, and size of the three patches varied between tepals of the same bud depending upon the arrnagement of their overlying tepals (see Supplementary Fig. S2 at JXB online). In mature buds, the green (EG and CG) and non-green (CNG) areas were morphologically distinct. All buds >0.5 cm in width had EG patches with glandular trichomes (hairs), domed epidermal cells, and chlorophyll (Fig. 2H). CG patches also possessed trichomes and chlorophyll, but epidermal cells were slightly less domed (Figs 2A, L, M, 3A–D). By contrast, CNG patches lacked glandular trichomes and the epidermal cells were relatively flat (Fig. 2I). The EG and CG patches had sharp boundaries which seem to follow the impressions left by the perianth organ that covered the tepal when the flower was in bud (Fig. 3B–D). Transverse sections of N. lutea and N. advena tepals show that EG patches also had a relatively thicker upper cuticle than the CNG areas. Stomata were present in all three areas.


Environmental control of sepalness and petalness in perianth organs of waterlilies: a new Mosaic theory for the evolutionary origin of a differentiated perianth.

Warner KA, Rudall PJ, Frohlich MW - J. Exp. Bot. (2009)

Experimental and non-experimental flower buds from Nuphar species. (A–D) Nuphar lutea untested flower buds. (A) Partially open bud (3 cm wide). (B) Mature bud (>3 cm wide), and (C) Individual tepals (from top left to right, tepals 1–5) showing exposed green (EG), covered green (CG), and covered non-green (CNG) areas of perianth. (D) Young inflorescence with pale yellow floral buds and surrounding young leaves. (E–G) Experimental flower bud of Nuphar advena (2.5 cm in width). Note the white-headed pin through the penducle which denotes the orientation of the bud in the photographs. (E) At the end of the test, the exposed area was dark green. (F) Bud with outermost tepal removed, displaying EE area. (G) Bud with EE tepal removed. The area of tepal directly beneath the experimentally light-exposed area is highlighted. (H–N) SEM images of tepals and flower buds of Nuphar lutea. (H–J) Tepal 3 from an untested bud (1.5 cm in width). (H) Abaxial exposed green patch. (I) Abaxial covered non-green patch. (J) Adaxial surface. (K) 0.1 cm wide bud. (l–M) 2.5 cm wide bud. Glands cover exposed (EG) patches and are present in covered green patches (CG). (N) Experimentally exposed tepal from Fig. 2A; boundary of experimentally exposed (EE) area marked with pinholes.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2724705&req=5

fig2: Experimental and non-experimental flower buds from Nuphar species. (A–D) Nuphar lutea untested flower buds. (A) Partially open bud (3 cm wide). (B) Mature bud (>3 cm wide), and (C) Individual tepals (from top left to right, tepals 1–5) showing exposed green (EG), covered green (CG), and covered non-green (CNG) areas of perianth. (D) Young inflorescence with pale yellow floral buds and surrounding young leaves. (E–G) Experimental flower bud of Nuphar advena (2.5 cm in width). Note the white-headed pin through the penducle which denotes the orientation of the bud in the photographs. (E) At the end of the test, the exposed area was dark green. (F) Bud with outermost tepal removed, displaying EE area. (G) Bud with EE tepal removed. The area of tepal directly beneath the experimentally light-exposed area is highlighted. (H–N) SEM images of tepals and flower buds of Nuphar lutea. (H–J) Tepal 3 from an untested bud (1.5 cm in width). (H) Abaxial exposed green patch. (I) Abaxial covered non-green patch. (J) Adaxial surface. (K) 0.1 cm wide bud. (l–M) 2.5 cm wide bud. Glands cover exposed (EG) patches and are present in covered green patches (CG). (N) Experimentally exposed tepal from Fig. 2A; boundary of experimentally exposed (EE) area marked with pinholes.
Mentions: In all buds examined, the entire abaxial surface of the outermost tepal (tepal 1) was EG, whereas the inner four tepals (tepals 2–5) possessed EG, CG, and CNG patches (Fig. 2C). The position, shape, and size of the three patches varied between tepals of the same bud depending upon the arrnagement of their overlying tepals (see Supplementary Fig. S2 at JXB online). In mature buds, the green (EG and CG) and non-green (CNG) areas were morphologically distinct. All buds >0.5 cm in width had EG patches with glandular trichomes (hairs), domed epidermal cells, and chlorophyll (Fig. 2H). CG patches also possessed trichomes and chlorophyll, but epidermal cells were slightly less domed (Figs 2A, L, M, 3A–D). By contrast, CNG patches lacked glandular trichomes and the epidermal cells were relatively flat (Fig. 2I). The EG and CG patches had sharp boundaries which seem to follow the impressions left by the perianth organ that covered the tepal when the flower was in bud (Fig. 3B–D). Transverse sections of N. lutea and N. advena tepals show that EG patches also had a relatively thicker upper cuticle than the CNG areas. Stomata were present in all three areas.

Bottom Line: Our interpretation contradicts the unspoken rule that 'sepal' and 'petal' must refer to whole organs.We propose a novel theory (the Mosaic theory), in which the distinction between sepalness and petalness evolved early in angiosperm history, but these features were not fixed to particular organs and were primarily environmentally controlled.At a later stage in angiosperm evolution, sepaloid and petaloid characteristics became fixed to whole organs in specific whorls, thus reducing or removing the need for environmental control in favour of fixed developmental control.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany, The Natural History Museum, Cromwell Road, London SW7 5BD, UK.

ABSTRACT
The conventional concept of an 'undifferentiated perianth', implying that all perianth organs of a flower are alike, obscures the fact that individual perianth organs are sometimes differentiated into sepaloid and petaloid regions, as in the early-divergent angiosperms Nuphar, Nymphaea, and Schisandra. In the waterlilies Nuphar and Nymphaea, sepaloid regions closely coincide with regions of the perianth that were exposed when the flower was in bud, whereas petaloid regions occur in covered regions, suggesting that their development is at least partly controlled by the environment of the developing tepal. Green and colourful areas differ from each other in trichome density and presence of papillae, features that often distinguish sepals and petals. Field experiments to test whether artificial exposure can induce sepalness in the inner tepals showed that development of sepaloid patches is initiated by exposure, at least in the waterlily species examined. Although light is an important environmental cue, other important factors include an absence of surface contact. Our interpretation contradicts the unspoken rule that 'sepal' and 'petal' must refer to whole organs. We propose a novel theory (the Mosaic theory), in which the distinction between sepalness and petalness evolved early in angiosperm history, but these features were not fixed to particular organs and were primarily environmentally controlled. At a later stage in angiosperm evolution, sepaloid and petaloid characteristics became fixed to whole organs in specific whorls, thus reducing or removing the need for environmental control in favour of fixed developmental control.

Show MeSH
Related in: MedlinePlus