Dataset Information

Diversity in forms of C4 in the genus Cleome (Cleomaceae).

ABSTRACT:

Background and aims

Cleomaceae is one of 19 angiosperm families in which C(4) photosynthesis has been reported. The aim of the study was to determine the type, and diversity, of structural and functional forms of C(4) in genus Cleome. Methods Plants of Cleome species were grown from seeds, and leaves were subjected to carbon isotope analysis, light and scanning electron microscopy, western blot analysis of proteins, and in situ immunolocalization for ribulose bisphosphate carboxylase oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC).

Key results

Three species with C(4)-type carbon isotope values occurring in separate lineages in the genus (Cleome angustifolia, C. gynandra and C. oxalidea) were shown to have features of C(4) photosynthesis in leaves and cotyledons. Immunolocalization studies show that PEPC is localized in mesophyll (M) cells and Rubisco is selectively localized in bundle sheath (BS) cells in leaves and cotyledons, characteristic of species with Kranz anatomy. Analyses of leaves for key photosynthetic enzymes show they have high expression of markers for the C(4) cycle (compared with the C(3)-C(4) intermediate C. paradoxa and the C(3) species C. africana). All three are biochemically NAD-malic enzyme sub-type, with higher granal development in BS than in M chloroplasts, characteristic of this biochemical sub-type. Cleome gynandra and C. oxalidea have atriplicoid-type Kranz anatomy with multiple simple Kranz units around individual veins. However, C. angustifolia anatomy is represented by a double layer of concentric chlorenchyma forming a single compound Kranz unit by surrounding all the vascular bundles and water storage cells.

Conclusions

NAD-malic enzyme-type C(4) photosynthesis evolved multiple times in the family Cleomaceae, twice with atriplicoid-type anatomy in compound leaves having flat, broad leaflets in the pantropical species C. gynandra and the Australian species C. oxalidea, and once by forming a single Kranz unit in compound leaves with semi-terete leaflets in the African species C. angustifolia. The leaf morphology of C. angustifolia, which is similar to that of the sister, C(3)-C(4) intermediate African species C. paradoxa, suggests adaptation of this lineage to arid environments, which is supported by biogeographical information.

SUBMITTER: Koteyeva NK

PROVIDER: S-EPMC3025737 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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Publications

Diversity in forms of C4 in the genus Cleome (Cleomaceae).

Koteyeva Nuria K NK Voznesenskaya Elena V EV Roalson Eric H EH Edwards Gerald E GE

Annals of botany 20101208 2

<h4>Background and aims</h4>Cleomaceae is one of 19 angiosperm families in which C(4) photosynthesis has been reported. The aim of the study was to determine the type, and diversity, of structural and functional forms of C(4) in genus Cleome. Methods Plants of Cleome species were grown from seeds, and leaves were subjected to carbon isotope analysis, light and scanning electron microscopy, western blot analysis of proteins, and in situ immunolocalization for ribulose bisphosphate carboxylase oxy ...[more]

PMID: 21147832

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Project description:In different lineages of C4 plants, the release of CO2 by decarboxylation of a C4 acid near rubisco is catalyzed by NADP-malic enzyme (ME) or NAD-ME, and the facultative use of phosphoenolpyruvate carboxykinase. The co-option of gene lineages during the evolution of C4-NADP-ME has been thoroughly investigated, whereas that of C4-NAD-ME has received less attention. In this work, we aimed at elucidating the mechanism of recruitment of NAD-ME for its function in the C4 pathway by focusing on the eudicot family Cleomaceae. We identified a duplication of NAD-ME in vascular plants that generated the two paralogs lineages: α- and β-NAD-ME. Both gene lineages were retained across seed plants, and their fixation was likely driven by a degenerative process of sub-functionalization, which resulted in a NAD-ME operating primarily as a heteromer of α- and β-subunits. We found most angiosperm genomes maintain a 1:1 β-NAD-ME/α-NAD-ME (β/α) relative gene dosage, but with some notable exceptions mainly due to additional duplications of β-NAD-ME subunits. For example, a significantly high proportion of species with C4-NAD-ME-type photosynthesis have a non-1:1 ratio of β/α. In the Brassicales, we found C4 species with a 2:1 ratio due to a β-NAD-ME duplication (β1 and β2); this was also observed in the C3 Tarenaya hassleriana and Brassica crops. In the independently evolved C4 species, Gynandropsis gynandra and Cleome angustifolia, all three genes were affected by C4 evolution with α- and β1-NAD-ME driven by adaptive selection. In particular, the β1-NAD-MEs possess many differentially substituted amino acids compared with other species and the β2-NAD-MEs of the same species. Five of these amino acids are identically substituted in β1-NAD-ME of G. gynandra and C. angustifolia, two of them were identified as positively selected. Using synteny analysis, we established that β-NAD-ME duplications were derived from ancient polyploidy events and that α-NAD-ME is in a unique syntenic context in both Cleomaceae and Brassicaceae. We discuss our hypotheses for the evolution of NAD-ME and its recruitment for C4 photosynthesis. We propose that gene duplications provided the basis for the recruitment of NAD-ME in C4 Cleomaceae and that all members of the NAD-ME gene family have been adapted to fit the C4-biochemistry. Also, one of the β-NAD-ME gene copies was independently co-opted for its function in the C4 pathway.

Dataset Information

Diversity in forms of C4 in the genus Cleome (Cleomaceae).

Background and aims

Key results

Conclusions

Publications

Diversity in forms of C4 in the genus Cleome (Cleomaceae).

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