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Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3-C4 intermediate in genus Portulaca L. (Portulacaceae).

Voznesenskaya EV, Koteyeva NK, Edwards GE, Ocampo G - J. Exp. Bot. (2010)

Bottom Line: Portulaca cryptopetala (clade Oleracea), an endemic species from central South America, was identified as a C(3)-C(4) based on its intermediate CO(2) compensation point and selective localization of glycine decarboxylase of the photorespiratory pathway in mitochondria of bundle sheath cells.The C(4) Portulaca species which were examined also have cotyledons with Kranz-type anatomy, while the stems of all species have C(3)-type photosynthetic cells.The results indicate that multiple structural and biochemical forms of C(4) photosynthesis evolved in genus Portulaca.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Anatomy and Morphology, V.L. Komarov Botanical Institute, Russian Academy of Sciences, Prof. Popov Street 2, 197376, St. Petersburg, Russia.

ABSTRACT
Portulacaceae is one of 19 families of terrestrial plants in which species having C(4) photosynthesis have been found. Representative species from major clades of the genus Portulaca were studied to characterize the forms of photosynthesis structurally and biochemically. The species P. amilis, P. grandiflora, P. molokiniensis, P. oleracea, P. pilosa, and P. umbraticola belong to the subgenus Portulaca and are C(4) plants based on leaf carbon isotope values, Kranz anatomy, and expression of key C(4) enzymes. Portulaca umbraticola, clade Umbraticola, is NADP-malic enzyme (NADP-ME)-type C(4) species, while P. oleracea and P. molokiniensis in clade Oleracea are NAD-ME-type C(4) species, all having different forms of Atriplicoid-type leaf anatomy. In clade Pilosa, P. amilis, P. grandiflora, and P. pilosa are NADP-ME-type C(4) species. They have Pilosoid-type anatomy in which Kranz tissues enclose peripheral vascular bundles with water storage in the centre of the leaf. Portulaca cf. bicolor, which belongs to subgenus Portulacella, is an NADP-ME C(4) species with Portulacelloid-type anatomy; it has well-developed Kranz chlorenchyma surrounding lateral veins distributed in one plane under the adaxial epidermis with water storage cells underneath. Portulaca cryptopetala (clade Oleracea), an endemic species from central South America, was identified as a C(3)-C(4) based on its intermediate CO(2) compensation point and selective localization of glycine decarboxylase of the photorespiratory pathway in mitochondria of bundle sheath cells. The C(4) Portulaca species which were examined also have cotyledons with Kranz-type anatomy, while the stems of all species have C(3)-type photosynthetic cells. The results indicate that multiple structural and biochemical forms of C(4) photosynthesis evolved in genus Portulaca.

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Light microscopy of leaf cross-sections, electron microscopy of bundle sheath (BS) cells and of chloroplasts and mitochondria in chlorenchyma cells in Portulaca species. (A–D) Portulaca umbraticola. (E–H) Portulaca oleracea. (I–L) Portulaca grandiflora. (M–P) Portulaca amilis. (Q–T) Portulaca cf. bicolor. (U–X) Portulaca cryptopetala. A, E, I, M, Q, U left panels: light microscopy. B, F, J, N, R, V: BS cells with centripetal positioning of organelles surrounding VBs. BS chloroplasts: (C, K, O, S) grana-deficient (G, W) with well-developed grana and numerous mitochondria. M chloroplasts: (D, L, P, T, X) with well-developed grana and (H) deficient in grana. BS, bundle sheath; H, hypoderm; M, mesophyll; VB, vascular bundle; WS, water storage tissue. Scale bars: 250 μm for A, E, I, M, Q, U; 20 μm for B, F, J, N, R; 100 μm for V; 1 μm for C, D, G, H, K, L, O, P, S, T, W, X.
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fig2: Light microscopy of leaf cross-sections, electron microscopy of bundle sheath (BS) cells and of chloroplasts and mitochondria in chlorenchyma cells in Portulaca species. (A–D) Portulaca umbraticola. (E–H) Portulaca oleracea. (I–L) Portulaca grandiflora. (M–P) Portulaca amilis. (Q–T) Portulaca cf. bicolor. (U–X) Portulaca cryptopetala. A, E, I, M, Q, U left panels: light microscopy. B, F, J, N, R, V: BS cells with centripetal positioning of organelles surrounding VBs. BS chloroplasts: (C, K, O, S) grana-deficient (G, W) with well-developed grana and numerous mitochondria. M chloroplasts: (D, L, P, T, X) with well-developed grana and (H) deficient in grana. BS, bundle sheath; H, hypoderm; M, mesophyll; VB, vascular bundle; WS, water storage tissue. Scale bars: 250 μm for A, E, I, M, Q, U; 20 μm for B, F, J, N, R; 100 μm for V; 1 μm for C, D, G, H, K, L, O, P, S, T, W, X.

Mentions: Study by light microscopy further shows differences in the distribution of minor VBs in leaves of the studied species and reveals additional features. In three of the species having flattened leaves, P. umbraticola, P. oleracea (Fig. 2A, E), and P. molokiniensis (not shown), the VBs are situated in the central part of the leaf, and delineated by one layer of hypoderm on the adaxial side and 1–2 layers of hypodermal cells on the abaxial side of the leaf. All lateral VBs are completely surrounded by specialized chlorenchyma layers, BS and M cells (Fig. 2A, E), while two chlorenchyma layers are present only on the adaxial side of the main veins (not shown). In these species, chloroplasts are located in a centripetal position in BS cells, and organelles have a similar concentration in all cells around the VBs (Fig. 2B, F). In P. umbraticola, BS chloroplasts are nearly agranal with only a few small grana (Fig. 2C), while M chloroplasts have well-developed grana (Fig. 2D). In contrast, BS cells in P. oleracea contain chloroplasts with well-developed grana and numerous large mitochondria (Fig. 2G), while M chloroplasts are grana deficient (Fig. 2H).


Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3-C4 intermediate in genus Portulaca L. (Portulacaceae).

Voznesenskaya EV, Koteyeva NK, Edwards GE, Ocampo G - J. Exp. Bot. (2010)

Light microscopy of leaf cross-sections, electron microscopy of bundle sheath (BS) cells and of chloroplasts and mitochondria in chlorenchyma cells in Portulaca species. (A–D) Portulaca umbraticola. (E–H) Portulaca oleracea. (I–L) Portulaca grandiflora. (M–P) Portulaca amilis. (Q–T) Portulaca cf. bicolor. (U–X) Portulaca cryptopetala. A, E, I, M, Q, U left panels: light microscopy. B, F, J, N, R, V: BS cells with centripetal positioning of organelles surrounding VBs. BS chloroplasts: (C, K, O, S) grana-deficient (G, W) with well-developed grana and numerous mitochondria. M chloroplasts: (D, L, P, T, X) with well-developed grana and (H) deficient in grana. BS, bundle sheath; H, hypoderm; M, mesophyll; VB, vascular bundle; WS, water storage tissue. Scale bars: 250 μm for A, E, I, M, Q, U; 20 μm for B, F, J, N, R; 100 μm for V; 1 μm for C, D, G, H, K, L, O, P, S, T, W, X.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
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fig2: Light microscopy of leaf cross-sections, electron microscopy of bundle sheath (BS) cells and of chloroplasts and mitochondria in chlorenchyma cells in Portulaca species. (A–D) Portulaca umbraticola. (E–H) Portulaca oleracea. (I–L) Portulaca grandiflora. (M–P) Portulaca amilis. (Q–T) Portulaca cf. bicolor. (U–X) Portulaca cryptopetala. A, E, I, M, Q, U left panels: light microscopy. B, F, J, N, R, V: BS cells with centripetal positioning of organelles surrounding VBs. BS chloroplasts: (C, K, O, S) grana-deficient (G, W) with well-developed grana and numerous mitochondria. M chloroplasts: (D, L, P, T, X) with well-developed grana and (H) deficient in grana. BS, bundle sheath; H, hypoderm; M, mesophyll; VB, vascular bundle; WS, water storage tissue. Scale bars: 250 μm for A, E, I, M, Q, U; 20 μm for B, F, J, N, R; 100 μm for V; 1 μm for C, D, G, H, K, L, O, P, S, T, W, X.
Mentions: Study by light microscopy further shows differences in the distribution of minor VBs in leaves of the studied species and reveals additional features. In three of the species having flattened leaves, P. umbraticola, P. oleracea (Fig. 2A, E), and P. molokiniensis (not shown), the VBs are situated in the central part of the leaf, and delineated by one layer of hypoderm on the adaxial side and 1–2 layers of hypodermal cells on the abaxial side of the leaf. All lateral VBs are completely surrounded by specialized chlorenchyma layers, BS and M cells (Fig. 2A, E), while two chlorenchyma layers are present only on the adaxial side of the main veins (not shown). In these species, chloroplasts are located in a centripetal position in BS cells, and organelles have a similar concentration in all cells around the VBs (Fig. 2B, F). In P. umbraticola, BS chloroplasts are nearly agranal with only a few small grana (Fig. 2C), while M chloroplasts have well-developed grana (Fig. 2D). In contrast, BS cells in P. oleracea contain chloroplasts with well-developed grana and numerous large mitochondria (Fig. 2G), while M chloroplasts are grana deficient (Fig. 2H).

Bottom Line: Portulaca cryptopetala (clade Oleracea), an endemic species from central South America, was identified as a C(3)-C(4) based on its intermediate CO(2) compensation point and selective localization of glycine decarboxylase of the photorespiratory pathway in mitochondria of bundle sheath cells.The C(4) Portulaca species which were examined also have cotyledons with Kranz-type anatomy, while the stems of all species have C(3)-type photosynthetic cells.The results indicate that multiple structural and biochemical forms of C(4) photosynthesis evolved in genus Portulaca.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Anatomy and Morphology, V.L. Komarov Botanical Institute, Russian Academy of Sciences, Prof. Popov Street 2, 197376, St. Petersburg, Russia.

ABSTRACT
Portulacaceae is one of 19 families of terrestrial plants in which species having C(4) photosynthesis have been found. Representative species from major clades of the genus Portulaca were studied to characterize the forms of photosynthesis structurally and biochemically. The species P. amilis, P. grandiflora, P. molokiniensis, P. oleracea, P. pilosa, and P. umbraticola belong to the subgenus Portulaca and are C(4) plants based on leaf carbon isotope values, Kranz anatomy, and expression of key C(4) enzymes. Portulaca umbraticola, clade Umbraticola, is NADP-malic enzyme (NADP-ME)-type C(4) species, while P. oleracea and P. molokiniensis in clade Oleracea are NAD-ME-type C(4) species, all having different forms of Atriplicoid-type leaf anatomy. In clade Pilosa, P. amilis, P. grandiflora, and P. pilosa are NADP-ME-type C(4) species. They have Pilosoid-type anatomy in which Kranz tissues enclose peripheral vascular bundles with water storage in the centre of the leaf. Portulaca cf. bicolor, which belongs to subgenus Portulacella, is an NADP-ME C(4) species with Portulacelloid-type anatomy; it has well-developed Kranz chlorenchyma surrounding lateral veins distributed in one plane under the adaxial epidermis with water storage cells underneath. Portulaca cryptopetala (clade Oleracea), an endemic species from central South America, was identified as a C(3)-C(4) based on its intermediate CO(2) compensation point and selective localization of glycine decarboxylase of the photorespiratory pathway in mitochondria of bundle sheath cells. The C(4) Portulaca species which were examined also have cotyledons with Kranz-type anatomy, while the stems of all species have C(3)-type photosynthetic cells. The results indicate that multiple structural and biochemical forms of C(4) photosynthesis evolved in genus Portulaca.

Show MeSH