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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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Nymphaea caerulea flower buds. (A–D) Tepals from a non-experimental flower bud. (A, B) Abaxial surface of covered entirely petaloid tepal. (C) Abaxial surface of exposed entirely sepaloid tepal. (D) Adaxial surfaces resemble abaxial surfaces of petaloid tepals (see Fig. 5A). (E, G) Experimental tepal. (E) Boundary of the experimentally exposed (EE) area marked with pinholes. Cells in EE area (right of pinholes) are relatively ill-defined compared with remaining covered area (left; Cov area). (F) Covered area. (G) EE area. (H) Abaxial surface of a leaf. Scales=100 μm.
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fig5: Nymphaea caerulea flower buds. (A–D) Tepals from a non-experimental flower bud. (A, B) Abaxial surface of covered entirely petaloid tepal. (C) Abaxial surface of exposed entirely sepaloid tepal. (D) Adaxial surfaces resemble abaxial surfaces of petaloid tepals (see Fig. 5A). (E, G) Experimental tepal. (E) Boundary of the experimentally exposed (EE) area marked with pinholes. Cells in EE area (right of pinholes) are relatively ill-defined compared with remaining covered area (left; Cov area). (F) Covered area. (G) EE area. (H) Abaxial surface of a leaf. Scales=100 μm.

Mentions: In buds longer than 3.5 cm, EGS patches of tepals 1–4 were dark green with dark purple irregular stripes or small blotches (Fig. 4D). EGS patches bore a striking resemblance to the leaf abaxial surface in this species (Fig. 5H). In contrast to many other Nymphaea species and cultivars (Fig. 4A) the CGS patches from tepals 2–4 of N. caerulea were light green and striped rather then petaloid (Fig. 4D). In young buds, the (future) EGS patches were orange/brown at the base with dark green tips. As the bud matured, chlorophyll development spread from the tip downwards, and dark purple stripes developed from the base upwards, until they both occurred over the entire EGS patches (see Supplementary Fig. S3 at JXB online).


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)

Nymphaea caerulea flower buds. (A–D) Tepals from a non-experimental flower bud. (A, B) Abaxial surface of covered entirely petaloid tepal. (C) Abaxial surface of exposed entirely sepaloid tepal. (D) Adaxial surfaces resemble abaxial surfaces of petaloid tepals (see Fig. 5A). (E, G) Experimental tepal. (E) Boundary of the experimentally exposed (EE) area marked with pinholes. Cells in EE area (right of pinholes) are relatively ill-defined compared with remaining covered area (left; Cov area). (F) Covered area. (G) EE area. (H) Abaxial surface of a leaf. Scales=100 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig5: Nymphaea caerulea flower buds. (A–D) Tepals from a non-experimental flower bud. (A, B) Abaxial surface of covered entirely petaloid tepal. (C) Abaxial surface of exposed entirely sepaloid tepal. (D) Adaxial surfaces resemble abaxial surfaces of petaloid tepals (see Fig. 5A). (E, G) Experimental tepal. (E) Boundary of the experimentally exposed (EE) area marked with pinholes. Cells in EE area (right of pinholes) are relatively ill-defined compared with remaining covered area (left; Cov area). (F) Covered area. (G) EE area. (H) Abaxial surface of a leaf. Scales=100 μm.
Mentions: In buds longer than 3.5 cm, EGS patches of tepals 1–4 were dark green with dark purple irregular stripes or small blotches (Fig. 4D). EGS patches bore a striking resemblance to the leaf abaxial surface in this species (Fig. 5H). In contrast to many other Nymphaea species and cultivars (Fig. 4A) the CGS patches from tepals 2–4 of N. caerulea were light green and striped rather then petaloid (Fig. 4D). In young buds, the (future) EGS patches were orange/brown at the base with dark green tips. As the bud matured, chlorophyll development spread from the tip downwards, and dark purple stripes developed from the base upwards, until they both occurred over the entire EGS patches (see Supplementary Fig. S3 at JXB online).

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