Bundle sheath and mesophyll cell differentiation in the C4 dicotyledon Atriplex rosea: quantitative ultrastructure

Abstract

In leaves of most C4 species, both bundle sheath and mesophyll cells are derived from ground meristem, yet at maturity differ in photosynthetic enzyme complement and in cell size, shape, and subcellular ultrastructure. This quantitative ultrastructural study of bundle sheath and mesophyll cell differentiation in Atriplex rosea shows that while developmental pathways of bundle sheath and meosphyll cells are generally coordinated, the timing of developmental divergence differs among individual characteristics. For instance, bundle sheath cells are larger, with more chloroplasts and more and larger mitochondria by 8 days after leaf emergence, while differential growth of mesophyll cell chloroplast peripheral reticulum and increase in thylakoids per granum in bundle sheath chloroplasts do not develop until after 12 days. Multigroup principal components analysis (M-PCA) of the data emphasizes that the greatest source of variation is overall size change as both cell types expand. M-PCA also identifies patterns of allometry within the data; for instance, mesophyll cell vacuoles and chloroplast peripheral reticulum undergo greater relative growth than do bundle sheath microbody area and number. The greater structural specialization of bundle sheath cells is reflected in higher growth rates from the time of divergence, but developmental change in both cell types continues until leaf expansion is complete. Most structural changes occur substantially after the stage of cell-specific expression of C4 enzymes. Key words: bundle sheath, mesophyll, C4 photosynthesis, leaf development, Atriplex rosea, multigroup principal components analysis.