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Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy.

ABSTRACT: In family Cleomaceae there are NAD-malic enzyme-type C4 species having different forms of leaf anatomy. Leaves of Cleome angustifolia have Glossocardioid-type anatomy with a single complex Kranz unit which surrounds all the veins, while C. gynandra has Atriplicoid anatomy with multiple Kranz units, each surrounding an individual vein. Biochemical and ultrastructural differentiation of mesophyll (M) and bundle sheath (BS) cells were studied along a developmental gradient, from the leaf base (youngest) to the tip (mature). Initially, there is cell-specific expression of certain photosynthetic enzymes, which subsequently increase along with structural differentiation. At the base of the leaf, following division of ground tissue to form M and BS cells which are structurally similar, there is selective localization of Rubisco and glycine decarboxylase to BS cells. Thus, a biochemical C3 default stage, with Rubisco expression in both cell types, does not occur. Additionally, phosphoenolpyruvate carboxylase (PEPC) is selectively expressed in M cells near the base. Surprisingly, in both species, an additional layer of spongy M cells on the abaxial side of the leaf has the same differentiation with PEPC, even though it is not in contact with BS cells. During development along the longitudinal gradient there is structural differentiation of the cells, chloroplasts, and mitochondria, resulting in complete formation of Kranz anatomy. In both species, development of the C4 system occurs similarly, irrespective of having very different types of Kranz anatomy, different ontogenetic origins of BS and M, and independent evolutionary origins of C4 photosynthesis.

SUBMITTER: Koteyeva NK

PROVIDER: S-EPMC4085953 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Background and aimsOttelia alismoides (Hydrocharitaceae) is a freshwater macrophyte that, unusually, possesses three different CO2-concentrating mechanisms. Here we describe its leaf anatomy and chloroplast ultrastructure, how these are altered by CO2 concentration and how they may underlie C4 photosynthesis.MethodsLight and transmission electron microscopy were used to study the anatomy of mature leaves of O. alismoides grown at high and low CO2 concentrations. Diel acid change and the activity of phosphoenolpyruvate carboxylase were measured to confirm that CAM activity and C4 photosynthesis were present.Key resultsWhen O. alismoides was grown at low CO2, the leaves performed both C4 and CAM photosynthesis whereas at high CO2 leaves used C4 photosynthesis. The leaf comprised an upper and lower layer of epidermal cells separated by a large air space occupying about 22 % of the leaf transverse-section area, and by mesophyll cells connecting the two epidermal layers. Kranz anatomy was absent. At low CO2, chloroplasts in the mesophyll cells were filled with starch even at the start of the photoperiod, while epidermal chloroplasts contained small starch grains. The number of chloroplasts in the epidermis was greater than in the mesophyll cells. At high CO2, the structure was unchanged but the thicknesses of the two epidermal layers, the air space, mesophyll and the transverse-section area of cells and air space were greater.ConclusionsLeaves of O. alismoides have epidermal and mesophyll cells that contain chloroplasts and large air spaces but lack Kranz anatomy. The high starch content of mesophyll cells suggests they may benefit from an internal source of CO2, for example via C4 metabolism, and are also sites of starch storage. The air spaces may help in the recycling of decarboxylated or respired CO2. The structural similarity of leaves at low and high CO2 is consistent with the constitutive nature of bicarbonate and C4 photosynthesis. There is sufficient structural diversity within the leaf of O. alismoides to support dual-cell C4 photosynthesis even though Kranz anatomy is absent.

Project description:Background and aimsCleomaceae 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 resultsThree 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.ConclusionsNAD-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.

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Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy.

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