Journal Article

Diversity in forms of C<sub>4</sub> in the genus <i>Cleome</i> (Cleomaceae)

Nuria K. Koteyeva, Elena V. Voznesenskaya, Eric H. Roalson and Gerald E. Edwards

in Annals of Botany

Published on behalf of The Annals of Botany Company

Volume 107, issue 2, pages 269-283
Published in print February 2011 | ISSN: 0305-7364
Published online December 2010 | e-ISSN: 1095-8290 | DOI:
Diversity in forms of C4 in the genus Cleome (Cleomaceae)

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Background and Aims

Cleomaceae is one of 19 angiosperm families in which C4 photosynthesis has been reported. The aim of the study was to determine the type, and diversity, of structural and functional forms of C4 in genus Cleome.


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 C4-type carbon isotope values occurring in separate lineages in the genus (Cleome angustifolia, C. gynandra and C. oxalidea) were shown to have features of C4 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 C4 cycle (compared with the C3–C4 intermediate C. paradoxa and the C3 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.


NAD-malic enzyme-type C4 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, C3–C4 intermediate African species C. paradoxa, suggests adaptation of this lineage to arid environments, which is supported by biogeographical information.

Keywords: C3 plants; C4 plants; chloroplast ultrastructure; Cleome; Cleomaceae; immunolocalization; leaf anatomy; NAD-malic enzyme type; photosynthetic enzymes

Journal Article.  11278 words.  Illustrated.

Subjects: Ecology and Conservation ; Evolutionary Biology ; Plant Sciences and Forestry

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