DCT4 - a new member of the dicarboxylate transporter family in C4 grasses

Malate transport shuttles atmospheric carbon into the Calvin-Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here we identify and characterize a previously unknown member of the DCT family, DCT4, in Sorghum bicolor. We show that SbDCT4 exchanges malate across membranes and its expression pattern is consistent with a role in malate transport during C4 photosynthesis. SbDCT4 is not syntenic to the characterized photosynthetic gene ZmDCT2, and an ortholog is not detectable in the maize reference genome. We found that the expression patterns of DCT family genes in the leaves of Z. mays, and S. bicolor varied by cell type. Our results suggest that sub-functionalization of members of the DCT family for the transport of malate into the bundle sheath (BS) plastids occurred during the process of independent recurrent evolution of C4 photosynthesis in grasses of the PACMAD clade. This study confirms the value of using both syntenic information and gene expression profiles to assign orthology in evolutionarily related genomes.

[1]  Rebecca L. Roston,et al.  Differentially Regulated Orthologs in Sorghum and the Subgenomes of Maize[OPEN] , 2017, Plant Cell.

[2]  James C. Schnable,et al.  Cross species selection scans identify components of C4 photosynthesis in the grasses , 2016, Journal of experimental botany.

[3]  E. Kellogg,et al.  The draft genome of the C3 panicoid grass species Dichanthelium oligosanthes , 2016, Genome Biology.

[4]  R. Dixon,et al.  Comparative cell-specific transcriptomics reveals differentiation of C4 photosynthesis pathways in switchgrass and other C4 lineages , 2016, Journal of experimental botany.

[5]  J. Gierse,et al.  Interactions of C4 Subtype Metabolic Activities and Transport in Maize Are Revealed through the Characterization of DCT2 Mutants[OPEN] , 2016, Plant Cell.

[6]  Haiyang Jiang,et al.  High level of microsynteny and purifying selection affect the evolution of WRKY family in Gramineae , 2016, Development Genes and Evolution.

[7]  S. Zhong,et al.  Identification of Photosynthesis-Associated C4 Candidate Genes through Comparative Leaf Gradient Transcriptome in Multiple Lineages of C3 and C4 Species , 2015, PloS one.

[8]  James C. Schnable,et al.  Phylogeny and photosynthesis of the grass tribe Paniceae. , 2015, American journal of botany.

[9]  Mark Stitt,et al.  Comparative analyses of C4 and C3 photosynthesis in developing leaves of maize and rice , 2014, Nature Biotechnology.

[10]  Yaqing Si,et al.  Developmental dynamics of Kranz cell transcriptional specificity in maize leaf reveals early onset of C4-related processes , 2014, Journal of experimental botany.

[11]  H. Woodfield,et al.  Evolutionary Convergence of Cell-Specific Gene Expression in Independent Lineages of C4 Grasses1[W][OPEN] , 2014, Plant Physiology.

[12]  A. Weber,et al.  Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis , 2014, Journal of experimental botany.

[13]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[14]  T. Brutnell,et al.  Engineering C4 photosynthetic regulatory networks. , 2012, Current opinion in biotechnology.

[15]  S. Shiu,et al.  Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. , 2012, The Plant journal : for cell and molecular biology.

[16]  Jian Wang,et al.  Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential , 2012, Nature Biotechnology.

[17]  Adam M. Szalkowski,et al.  Fast and robust multiple sequence alignment with phylogeny-aware gap placement , 2012, BMC Bioinformatics.

[18]  Uwe Scholz,et al.  Systems Analysis of a Maize Leaf Developmental Gradient Redefines the Current C4 Model and Provides Candidates for Regulation[W][OA] , 2011, Plant Cell.

[19]  N. Friedman,et al.  Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2011, Nature Biotechnology.

[20]  R. Furbank Evolution of the C(4) photosynthetic mechanism: are there really three C(4) acid decarboxylation types? , 2011, Journal of experimental botany.

[21]  A. Weber,et al.  The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism. , 2011, The Plant journal : for cell and molecular biology.

[22]  Brent S. Pedersen,et al.  Screening synteny blocks in pairwise genome comparisons through integer programming , 2011, BMC Bioinformatics.

[23]  Robert Turgeon,et al.  The developmental dynamics of the maize leaf transcriptome , 2010, Nature Genetics.

[24]  L. Clark,et al.  Phylogeny and a new tribal classification of the Panicoideae s.l. (Poaceae) based on plastid and nuclear sequence data and structural data. , 2010, American journal of botany.

[25]  A. Weber,et al.  Intracellular metabolite transporters in plants. , 2010, Molecular plant.

[26]  Sachin Kumar,et al.  Orthology between genomes of Brachypodium, wheat and rice , 2009, BMC Research Notes.

[27]  A. Weber,et al.  Comparative Proteomics of Chloroplast Envelopes from C3 and C4 Plants Reveals Specific Adaptations of the Plastid Envelope to C4 Photosynthesis and Candidate Proteins Required for Maintaining C4 Metabolite Fluxes1[W][OA] , 2008, Plant Physiology.

[28]  Robert S. Harris Improved Pairwise Alignmnet of Genomic DNA , 2007 .

[29]  John A. Hamilton,et al.  The TIGR Rice Genome Annotation Resource: improvements and new features , 2006, Nucleic Acids Res..

[30]  Peer Bork,et al.  PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments , 2006, Nucleic Acids Res..

[31]  Mark P. Simmons,et al.  How can third codon positions outperform first and second codon positions in phylogenetic inference? An empirical example from the seed plants. , 2006, Systematic biology.

[32]  R. Garcés,et al.  The sources of carbon and reducing power for fatty acid synthesis in the heterotrophic plastids of developing sunflower (Helianthus annuus L.) embryos. , 2005, Journal of experimental botany.

[33]  Elizabeth A. Kellogg,et al.  Primaclade - a flexible tool to find conserved PCR primers across multiple species , 2005, Bioinform..

[34]  T. Sugiyama,et al.  Differentiation of dicarboxylate transporters in mesophyll and bundle sheath chloroplasts of maize. , 2004, Plant & cell physiology.

[35]  S. Tabata,et al.  Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. , 2002, Plant & cell physiology.

[36]  J. Bennetzen Comparative Sequence Analysis of Plant Nuclear Genomes: Microcolinearity and Its Many Exceptions , 2000, Plant Cell.

[37]  J. Bennetzen,et al.  Colinearity and its exceptions in orthologous adh regions of maize and sorghum. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Chen,et al.  Phosphoenolpyruvate carboxykinase is involved in the decarboxylation of aspartate in the bundle sheath of maize , 1999, Plant physiology.

[39]  J. Bennetzen,et al.  Microcolinearity in sh2-homologous regions of the maize, rice, and sorghum genomes. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. Bennetzen,et al.  The unified grass genome: synergy in synteny. , 1997, Genome research.

[41]  K. Nishizawa,et al.  Substrate Recognition Domain of the Gal2 Galactose Transporter in Yeast Saccharomyces cerevisiae as Revealed by Chimeric Galactose-Glucose Transporters (*) , 1995, The Journal of Biological Chemistry.

[42]  M. Meisler,et al.  Phosphoenolpyruvate carboxykinase (GTP): characterization of the human PCK1 gene and localization distal to MODY on chromosome 20. , 1993, Genomics.

[43]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[44]  E. Karczmarewicz [Phosphoenolpyruvate carboxykinase]. , 1983, Postepy biochemii.

[45]  M. D. Hatch,et al.  Aspartate stimulation of malate decarboxylation in Zea mays bundle sheath cells: possible role in regulation of C4 photosynthesis. , 1979, Biochemical and biophysical research communications.

[46]  G. Edwards,et al.  C4 acid decarboxylation and CO2 donation to photosynthesis in bundle sheath strands and chloroplasts from species representing three groups of C4 plants. , 1977, Archives of biochemistry and biophysics.

[47]  M. Hatch The C4-pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C4-dicarboxylic acid , 1971 .

[48]  M. Hatch The C 4 -pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C 4 -dicarboxylic acid. , 1971, The Biochemical journal.

[49]  M. D. Hatch,et al.  Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. , 1966, The Biochemical journal.