title: C3-C4 intermediacy in grasses: organelle enrichment and distribution, glycine decarboxylase expression, and the rise of C2 photosynthesis.
abstract: Photorespiratory glycine shuttling and decarboxylation in bundle sheath (BS) cells exhibited by C2 species is proposed to be the evolutionary bridge to C4 photosynthesis in eudicots. To evaluate this in grasses, we compare anatomy, cellular localization of glycine decarboxylase (GDC), and photosynthetic physiology of a suspected C2 grass, Homolepis aturensis, with these traits in known C2 grasses, Neurachne minor and Steinchisma hians, and C3 S laxum that is sister to S hians We also use publicly available genome and RNA-sequencing data to examine the evolution of GDC subunits and enhance our understanding of the evolution of BS-specific GDC expression in C2 and C4 grasses. Our results confirm the identity of H aturensis as a C2 species; GDC is confined predominantly to the organelle-enriched BS cells in H aturensis and S hians and to mestome sheath cells of N minor Phylogenetic analyses and data obtained from immunodetection of the P-subunit of GDC are consistent with the hypothesis that the BS dominant levels of GDC in C2 and C4 species are due to changes in expression of a single GLDP gene in M and BS cells. All BS mitochondria and peroxisomes and most chloroplasts in H aturensis and S hians are situated centripetally in a pattern identical to C2 eudicots. In S laxum, which has C3-like gas exchange patterns, mitochondria and peroxisomes are positioned centripetally as they are in S hians This subcellular phenotype, also present in eudicots, is posited to initiate a facilitation cascade leading to C2 and C4 photosynthesis.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Ontario, ON M5S 3B2, Canada.
authors.forename: Roxana
authors.initials: R
authors.lastname: Khoshravesh
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Ontario, ON M5S 3B2, Canada.
authors.forename: Corey R
authors.initials: CR
authors.lastname: Stinson
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Ontario, ON M5S 3B2, Canada.
authors.forename: Matt
authors.initials: M
authors.lastname: Stata
authors.affiliation: Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.
authors.forename: Florian A
authors.initials: FA
authors.lastname: Busch
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Ontario, ON M5S 3B2, Canada.
authors.forename: Rowan F
authors.initials: RF
authors.lastname: Sage
authors.affiliation: School of Chemistry and Biochemistry, University of Western Australia, Crawley, WA 6009, Australia.
authors.forename: Martha
authors.initials: M
authors.lastname: Ludwig
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Ontario, ON M5S 3B2, Canada tammy.sage@utoronto.ca.
authors.forename: Tammy L
authors.initials: TL
authors.lastname: Sage
mesh_terms: D005075:Biological Evolution; D017343:Genes, Plant / Q000235:genetics / Q000502:physiology; D050841:Glycine Dehydrogenase (Decarboxylating) / Q000235:genetics / Q000378:metabolism*; D010788:Photosynthesis / Q000502:physiology*; D010802:Phylogeny; D018515:Plant Leaves / Q000033:anatomy & histology / Q000166:cytology / Q000502:physiology; D006109:Poaceae / Q000166:cytology / Q000201:enzymology / Q000378:metabolism / Q000502:physiology*; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism
chemical_list: D050841:Glycine Dehydrogenase (Decarboxylating); D012273:Ribulose-Bisphosphate Carboxylase
keywords: Arthropogoninae; C2 Kranz anatomy; C2 photosynthesis; Homolepis.; bundle sheath; glycine decarboxylase; grasses; mitochondria