title: Mesophyll cells of C4 plants have fewer chloroplasts than those of closely related C3 plants.
abstract: The evolution of C(4) photosynthesis from C(3) ancestors eliminates ribulose bisphosphate carboxylation in the mesophyll (M) cell chloroplast while activating phosphoenolpyruvate (PEP) carboxylation in the cytosol. These changes may lead to fewer chloroplasts and different chloroplast positioning within M cells. To evaluate these possibilities, we compared chloroplast number, size and position in M cells of closely related C(3), C(3) -C(4) intermediate and C(4) species from 12 lineages of C(4) evolution. All C(3) species had more chloroplasts per M cell area than their C(4) relatives in high-light growth conditions. C(3) species also had higher chloroplast coverage of the M cell periphery than C(4) species, particularly opposite intercellular air spaces. In M cells from 10 of the 12 C(4) lineages, a greater fraction of the chloroplast envelope was pulled away from the plasmalemma in the C(4) species than their C(3) relatives. C(3) -C(4) intermediate species generally exhibited similar patterns as their C(3) relatives. We interpret these results to reflect adaptive shifts that facilitate efficient C(4) function by enhancing diffusive access to the site of primary carbon fixation in the cytosol. Fewer chloroplasts in C(4) M cells would also reduce shading of the bundle sheath chloroplasts, which also generate energy required by C(4) photosynthesis.
authors.affiliation: Department of Ecology and Evolutionary Biology, The University of Toronto, Toronto, ON, Canada, M5S 3B2.
authors.forename: Matt
authors.initials: M
authors.lastname: Stata
authors.forename: Tammy L
authors.initials: TL
authors.lastname: Sage
authors.forename: Troy D
authors.initials: TD
authors.lastname: Rennie
authors.forename: Roxana
authors.initials: R
authors.lastname: Khoshravesh
authors.forename: Stefanie
authors.initials: S
authors.lastname: Sultmanis
authors.forename: Yannay
authors.initials: Y
authors.lastname: Khaikin
authors.forename: Martha
authors.initials: M
authors.lastname: Ludwig
authors.forename: Rowan F
authors.initials: RF
authors.lastname: Sage
mesh_terms: D005075:Biological Evolution; D002244:Carbon / Q000378:metabolism*; D002469:Cell Separation; D002736:Chloroplasts / Q000378:metabolism* / Q000648:ultrastructure; D019684:Magnoliopsida / Q000378:metabolism*; D058503:Mesophyll Cells / Q000166:cytology / Q000378:metabolism* / Q000648:ultrastructure; D013045:Species Specificity
chemical_list: D002244:Carbon
keywords: C3-C4 intermediate; C4 evolution; C4 photosynthesis; Kranz anatomy; mesophyll conductance