title: Characterization of C₃--C₄ intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity.
abstract: Photosynthetic pathway characteristics were studied in nine species of Heliotropium (sensu lato, including Euploca), using assessments of leaf anatomy and ultrastructure, activities of PEP carboxylase and C₄ acid decarboxylases, and immunolocalization of ribulose 1·5-bisphosphate carboxylase/oxygenase (Rubisco) and the P-subunit of glycine decarboxylase (GDC). Heliotropium europaeum, Heliotropium calcicola and Heliotropium tenellum are C₃ plants, while Heliotropium texanum and Heliotropium polyphyllum are C₄ species. Heliotropium procumbens and Heliotropium karwinskyi are functionally C₃, but exhibit 'proto-Kranz' anatomy where bundle sheath (BS) cells are enlarged and mitochondria primarily occur along the centripetal (inner) wall of the BS cells; GDC is present throughout the leaf. Heliotropium convolvulaceum and Heliotropium greggii are C₃--C₄ intermediates, with Kranz-like enlargement of the BS cells, localization of mitochondria along the inner BS wall and a loss of GDC in the mesophyll (M) tissue. These C₃--C₄ species of Heliotropium probably shuttle photorespiratory glycine from the M to the BS tissue for decarboxylation. Heliotropium represents an important new model for studying C₄ evolution. Where existing models such as Flaveria emphasize diversification of C₃--C₄ intermediates, Heliotropium has numerous C₃ species expressing proto-Kranz traits that could represent a critical initial phase in the evolutionary origin of C₄ photosynthesis.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON M5S3B2, Canada.
authors.forename: Riyadh
authors.initials: R
authors.lastname: Muhaidat
authors.forename: Tammy L
authors.initials: TL
authors.lastname: Sage
authors.forename: Michael W
authors.initials: MW
authors.lastname: Frohlich
authors.forename: Nancy G
authors.initials: NG
authors.lastname: Dengler
authors.forename: Rowan F
authors.initials: RF
authors.lastname: Sage
mesh_terms: D005075:Biological Evolution; D002247:Carbon Isotopes / Q000032:analysis; D037142:Flaveria / Q000033:anatomy & histology* / Q000201:enzymology* / Q000378:metabolism; D050841:Glycine Dehydrogenase (Decarboxylating) / Q000378:metabolism; D028162:Heliotropium / Q000033:anatomy & histology* / Q000201:enzymology* / Q000378:metabolism; D008291:Malate Dehydrogenase / Q000378:metabolism; D010730:Phosphoenolpyruvate Carboxylase / Q000378:metabolism; D010788:Photosynthesis; D018515:Plant Leaves / Q000033:anatomy & histology / Q000201:enzymology* / Q000378:metabolism; D010940:Plant Proteins / Q000378:metabolism*; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism
chemical_list: D002247:Carbon Isotopes; D010940:Plant Proteins; D008291:Malate Dehydrogenase; C046446:malate dehydrogenase-(oxaloacetate-decarboxylating) (NAD+); C031917:malate dehydrogenase (oxaloacetate-decarboxylating) (NADP+); D050841:Glycine Dehydrogenase (Decarboxylating); D010730:Phosphoenolpyruvate Carboxylase; D012273:Ribulose-Bisphosphate Carboxylase