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Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea.

Fukushima K, Fujita H, Yamaguchi T, Kawaguchi M, Tsukaya H, Hasebe M - Nat Commun (2015)

Bottom Line: Complex morphology is an evolutionary outcome of phenotypic diversification.However, how leaf development was altered during evolution remains unknown.These different growth patterns establish pitcher morphology.

View Article: PubMed Central - PubMed

Affiliation: 1] 1Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Okazaki 444-8585, Japan [2] National Institute for Basic Biology, Myodaiji-cho, Nishigonaka 38, Okazaki, Aichi 444-8585, Japan.

ABSTRACT
Complex morphology is an evolutionary outcome of phenotypic diversification. In some carnivorous plants, the ancestral planar leaf has been modified to form a pitcher shape. However, how leaf development was altered during evolution remains unknown. Here we show that the pitcher leaves of Sarracenia purpurea develop through cell division patterns of adaxial tissues that are distinct from those in bifacial and peltate leaves, subsequent to standard expression of adaxial and abaxial marker genes. Differences in the orientation of cell divisions in the adaxial domain cause bifacial growth in the distal region and adaxial ridge protrusion in the middle region. These different growth patterns establish pitcher morphology. A computer simulation suggests that the cell division plane is critical for the pitcher morphogenesis. Our results imply that tissue-specific changes in the orientation of cell division underlie the development of a morphologically complex leaf.

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Morphology of S. purpurea pitcher leaves.(a,b) External morphology of mature pitchers: adaxial view (a) and lateral dissected view (b). tu, tube; ke, keel; sh, sheath. Dissected planes corresponding to those in c and d are indicated. (c,d) Transverse sections of immature pitchers of ca. 20 mm in length, stained with toluidine blue (left). Schematics of vascular polarity (middle) and magnified views of vascular bundles (right) are indicated. Vascular polarity is shown by the positions of adaxial element xylem (blue) and abaxial element phloem (yellow). ph, phloem; xy, xylem. (e–i) Scanning electron micrographs of developing pitcher primordia of ca. 70 μm (e,f), 100 μm (g), 200 μm (h) and 400 μm (i) in length. Adaxial (e) and lateral (f) views of ca. 70-μm primordia are shown. The leaf margin and adaxial ridge are shown in green and pink, respectively, in the lower panel of g. Approximate positions of sections in Fig. 2a–c are indicated by arrows in e, h and i, respectively. SAM, shoot apical meristem. (j) A longitudinal section of a pitcher primordium of ca. 1 mm in length. The scanning electron micrographs and toluidine blue-stained sections represent three to ten leaf primordia. Scale bars, 100 μm.
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f1: Morphology of S. purpurea pitcher leaves.(a,b) External morphology of mature pitchers: adaxial view (a) and lateral dissected view (b). tu, tube; ke, keel; sh, sheath. Dissected planes corresponding to those in c and d are indicated. (c,d) Transverse sections of immature pitchers of ca. 20 mm in length, stained with toluidine blue (left). Schematics of vascular polarity (middle) and magnified views of vascular bundles (right) are indicated. Vascular polarity is shown by the positions of adaxial element xylem (blue) and abaxial element phloem (yellow). ph, phloem; xy, xylem. (e–i) Scanning electron micrographs of developing pitcher primordia of ca. 70 μm (e,f), 100 μm (g), 200 μm (h) and 400 μm (i) in length. Adaxial (e) and lateral (f) views of ca. 70-μm primordia are shown. The leaf margin and adaxial ridge are shown in green and pink, respectively, in the lower panel of g. Approximate positions of sections in Fig. 2a–c are indicated by arrows in e, h and i, respectively. SAM, shoot apical meristem. (j) A longitudinal section of a pitcher primordium of ca. 1 mm in length. The scanning electron micrographs and toluidine blue-stained sections represent three to ten leaf primordia. Scale bars, 100 μm.

Mentions: Mature pitcher leaves of S. purpurea are mainly composed of a tube, a keel and a sheath (Fig. 1a,b). In the tube, phloem bundles point towards the outer surface and xylem points towards the inner surface (Fig. 1c,d), indicating that this structure is bifacial, similar to the blades of conventional, planar leaves. In the keel, phloem bundles point towards the outer surface but xylem vessels face each other (Fig. 1d), indicating that the keel forms a distinct structure from the bifacial tube. We investigated the early development of S. purpurea pitcher leaves, using scanning electron microscopy. The adaxial surface of the incipient leaf primordium is flat (Fig. 1e,f), similar to that in conventional bifacial leaves31718. When a primordium becomes ~100 μm long, an adaxial ridge connecting both sides of a leaf margin appears in the middle of the primordium (Fig. 1g), which is similar to the ‘cross zone’ protrusions in peltate leaves of T. majus11 and pitcher leaves of D. californica15. In S. purpurea, the adaxial ridge develops into a keel (Fig. 1a,b). When the primordium reaches ~200 μm in length, it becomes obvious that the proximal and distal parts of the adaxial ridge will form a keel and the adaxial side of the tube, respectively (Fig. 1h). As a result of growth in the leaf margin and the adaxial ridge, a hollow structure develops in the distal part of the primordium (Fig. 1i) and the continued growth of these regions deepens the hollow to form a pitcher shape (Fig. 1j).


Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea.

Fukushima K, Fujita H, Yamaguchi T, Kawaguchi M, Tsukaya H, Hasebe M - Nat Commun (2015)

Morphology of S. purpurea pitcher leaves.(a,b) External morphology of mature pitchers: adaxial view (a) and lateral dissected view (b). tu, tube; ke, keel; sh, sheath. Dissected planes corresponding to those in c and d are indicated. (c,d) Transverse sections of immature pitchers of ca. 20 mm in length, stained with toluidine blue (left). Schematics of vascular polarity (middle) and magnified views of vascular bundles (right) are indicated. Vascular polarity is shown by the positions of adaxial element xylem (blue) and abaxial element phloem (yellow). ph, phloem; xy, xylem. (e–i) Scanning electron micrographs of developing pitcher primordia of ca. 70 μm (e,f), 100 μm (g), 200 μm (h) and 400 μm (i) in length. Adaxial (e) and lateral (f) views of ca. 70-μm primordia are shown. The leaf margin and adaxial ridge are shown in green and pink, respectively, in the lower panel of g. Approximate positions of sections in Fig. 2a–c are indicated by arrows in e, h and i, respectively. SAM, shoot apical meristem. (j) A longitudinal section of a pitcher primordium of ca. 1 mm in length. The scanning electron micrographs and toluidine blue-stained sections represent three to ten leaf primordia. Scale bars, 100 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4382701&req=5

f1: Morphology of S. purpurea pitcher leaves.(a,b) External morphology of mature pitchers: adaxial view (a) and lateral dissected view (b). tu, tube; ke, keel; sh, sheath. Dissected planes corresponding to those in c and d are indicated. (c,d) Transverse sections of immature pitchers of ca. 20 mm in length, stained with toluidine blue (left). Schematics of vascular polarity (middle) and magnified views of vascular bundles (right) are indicated. Vascular polarity is shown by the positions of adaxial element xylem (blue) and abaxial element phloem (yellow). ph, phloem; xy, xylem. (e–i) Scanning electron micrographs of developing pitcher primordia of ca. 70 μm (e,f), 100 μm (g), 200 μm (h) and 400 μm (i) in length. Adaxial (e) and lateral (f) views of ca. 70-μm primordia are shown. The leaf margin and adaxial ridge are shown in green and pink, respectively, in the lower panel of g. Approximate positions of sections in Fig. 2a–c are indicated by arrows in e, h and i, respectively. SAM, shoot apical meristem. (j) A longitudinal section of a pitcher primordium of ca. 1 mm in length. The scanning electron micrographs and toluidine blue-stained sections represent three to ten leaf primordia. Scale bars, 100 μm.
Mentions: Mature pitcher leaves of S. purpurea are mainly composed of a tube, a keel and a sheath (Fig. 1a,b). In the tube, phloem bundles point towards the outer surface and xylem points towards the inner surface (Fig. 1c,d), indicating that this structure is bifacial, similar to the blades of conventional, planar leaves. In the keel, phloem bundles point towards the outer surface but xylem vessels face each other (Fig. 1d), indicating that the keel forms a distinct structure from the bifacial tube. We investigated the early development of S. purpurea pitcher leaves, using scanning electron microscopy. The adaxial surface of the incipient leaf primordium is flat (Fig. 1e,f), similar to that in conventional bifacial leaves31718. When a primordium becomes ~100 μm long, an adaxial ridge connecting both sides of a leaf margin appears in the middle of the primordium (Fig. 1g), which is similar to the ‘cross zone’ protrusions in peltate leaves of T. majus11 and pitcher leaves of D. californica15. In S. purpurea, the adaxial ridge develops into a keel (Fig. 1a,b). When the primordium reaches ~200 μm in length, it becomes obvious that the proximal and distal parts of the adaxial ridge will form a keel and the adaxial side of the tube, respectively (Fig. 1h). As a result of growth in the leaf margin and the adaxial ridge, a hollow structure develops in the distal part of the primordium (Fig. 1i) and the continued growth of these regions deepens the hollow to form a pitcher shape (Fig. 1j).

Bottom Line: Complex morphology is an evolutionary outcome of phenotypic diversification.However, how leaf development was altered during evolution remains unknown.These different growth patterns establish pitcher morphology.

View Article: PubMed Central - PubMed

Affiliation: 1] 1Department of Basic Biology, School of Life Science, SOKENDAI (The Graduate University for Advanced Studies), Okazaki 444-8585, Japan [2] National Institute for Basic Biology, Myodaiji-cho, Nishigonaka 38, Okazaki, Aichi 444-8585, Japan.

ABSTRACT
Complex morphology is an evolutionary outcome of phenotypic diversification. In some carnivorous plants, the ancestral planar leaf has been modified to form a pitcher shape. However, how leaf development was altered during evolution remains unknown. Here we show that the pitcher leaves of Sarracenia purpurea develop through cell division patterns of adaxial tissues that are distinct from those in bifacial and peltate leaves, subsequent to standard expression of adaxial and abaxial marker genes. Differences in the orientation of cell divisions in the adaxial domain cause bifacial growth in the distal region and adaxial ridge protrusion in the middle region. These different growth patterns establish pitcher morphology. A computer simulation suggests that the cell division plane is critical for the pitcher morphogenesis. Our results imply that tissue-specific changes in the orientation of cell division underlie the development of a morphologically complex leaf.

Show MeSH
Related in: MedlinePlus