Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density1[W][OA]

C4 photosynthesis has evolved in at least 66 lineages within the angiosperms and involves alterations to the biochemistry, cell biology, and development of leaves. The characteristic “Kranz” anatomy of most C4 leaves was discovered in the 1890s, but the genetic basis of these traits remains poorly defined. Oat × maize addition lines allow the effects of individual maize (Zea mays; C4) chromosomes to be investigated in an oat (Avena sativa; C3) genetic background. Here, we have determined the extent to which maize chromosomes can introduce C4 characteristics into oat and have associated any C4-like changes with specific maize chromosomes. While there is no indication of a simultaneous change to C4 biochemistry, leaf anatomy, and ultrastructure in any of the oat × maize addition lines, the C3 oat leaf can be modified at multiple levels. Maize genes encoding phosphoenolpyruvate carboxylase, pyruvate, orthophosphate dikinase, and the 2′-oxoglutarate/malate transporter are expressed in oat and generate transcripts of the correct size. Three maize chromosomes independently cause increases in vein density, and maize chromosome 3 results in larger bundle sheath cells with increased cell wall lipid deposition in oat leaves. These data provide proof of principle that aspects of C4 biology could be integrated into leaves of C3 crops.

[1]  Chun-jing Zou,et al.  Effects of elevated CO2, warming and precipitation change on plant growth, photosynthesis and peroxidation in dominant species from North China grassland , 2013, Planta.

[2]  R. Sage,et al.  Photorespiration and the evolution of C4 photosynthesis. , 2012, Annual review of plant biology.

[3]  Julian M Hibberd,et al.  Strategies for engineering a two-celled C(4) photosynthetic pathway into rice. , 2011, Journal of experimental botany.

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

[5]  Xinguang Zhu,et al.  Exploiting the engine of C(4) photosynthesis. , 2011, Journal of experimental botany.

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

[7]  U. Gowik,et al.  Evolution of C4 Photosynthesis—Looking for the Master Switch1 , 2010, Plant Physiology.

[8]  M. Lercher,et al.  An mRNA Blueprint for C4 Photosynthesis Derived from Comparative Transcriptomics of Closely Related C3 and C4 Species1[W][OA] , 2010, Plant Physiology.

[9]  A. Weber,et al.  Plastid transport and metabolism of C3 and C4 plants--comparative analysis and possible biotechnological exploitation. , 2010, Current opinion in plant biology.

[10]  R. Zhong,et al.  MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. , 2009, Plant & cell physiology.

[11]  Monica A. Schmidt,et al.  Suppression of soybean oleosin produces micro-oil bodies that aggregate into oil body/ER complexes. , 2008, Molecular plant.

[12]  R. Zhong,et al.  A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis , 2008, The Plant Cell Online.

[13]  M. Melis,et al.  Hydrophobic characterization of intracellular lipids in situ by Nile Red red/yellow emission ratio. , 2008, Micron.

[14]  R. Kowles,et al.  Expression of C4 photosynthetic enzymes in oat-maize chromosome addition lines , 2008 .

[15]  C. Peterson,et al.  Suberin lamellae of the onion root endodermis: their pattern of development and continuity , 2008 .

[16]  J. Langdale,et al.  Using C4 photosynthesis to increase the yield of rice-rationale and feasibility. , 2008, Current opinion in plant biology.

[17]  T. Köllner,et al.  Characterization of the Monoterpene Synthase Gene tps26, the Ortholog of a Gene Induced by Insect Herbivory in Maize1[W][OA] , 2008, Plant Physiology.

[18]  Chisato Masumoto,et al.  Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. , 2007, Journal of experimental botany.

[19]  J. Sullivan,et al.  Light and plastid signals regulate the expression of the pea plastocyanin gene through a common region at the 5' end of the coding region. , 2005, The Plant journal : for cell and molecular biology.

[20]  M. Matsuoka,et al.  Differential expression pattern of C4 bundle sheath expression genes in rice, a C3 plant. , 2005, Plant & cell physiology.

[21]  R. Jetter,et al.  Plant Cuticular Lipid Export Requires an ABC Transporter , 2004, Science.

[22]  A. Stec,et al.  Dissecting the maize genome by using chromosome addition and radiation hybrid lines. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G. Edwards,et al.  Development of biochemical specialization and organelle partitioning in the single-cell C4 system in leaves of Borszczowia aralocaspica (Chenopodiaceae). , 2003, American journal of botany.

[24]  R. Furbank,et al.  MOLECULAR ENGINEERING OF C4 PHOTOSYNTHESIS. , 2003, Annual review of plant physiology and plant molecular biology.

[25]  R. Häusler,et al.  An engineered phosphoenolpyruvate carboxylase redirects carbon and nitrogen flow in transgenic potato plants. , 2002, The Plant journal : for cell and molecular biology.

[26]  G. Edwards,et al.  Proof of C4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae). , 2002, The Plant journal : for cell and molecular biology.

[27]  R. Leegood.  C(4) photosynthesis: principles of CO(2) concentration and prospects for its introduction into C(3) plants. , 2002, Journal of experimental botany.

[28]  M. Matsuoka,et al.  Overexpression of C4 PEPC caused O2-insensitive photosynthesis in transgenic rice plants , 2002 .

[29]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[30]  M. Matsuoka,et al.  Significant Accumulation of C4-Specific Pyruvate, Orthophosphate Dikinase in a C3 Plant, Rice , 2001 .

[31]  A. Stec,et al.  A complete set of maize individual chromosome additions to the oat genome. , 2001, Plant physiology.

[32]  L. Smith,et al.  Tangled1: a microtubule binding protein required for the spatial control of cytokinesis in maize. , 2001, The Journal of cell biology.

[33]  F. Morel,et al.  Unicellular C4 photosynthesis in a marine diatom , 2000, Nature.

[34]  O. Riera-Lizarazu,et al.  Production and characterization of maize chromosome 9 radiation hybrids derived from an oat-maize addition line. , 2000, Genetics.

[35]  M. V. Lara,et al.  Induction of a C(4)-like mechanism of CO(2) fixation in Egeria densa, a submersed aquatic species. , 2000, Plant physiology.

[36]  K. Izui,et al.  cDNA cloning and characterization of maize phosphoenolpyruvate carboxykinase, a bundle sheath cell-specific enzyme , 1999, Plant Molecular Biology.

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

[38]  J. Langdale,et al.  BUNDLE SHEATH DEFECTIVE2, a Novel Protein Required for Post-Translational Regulation of the rbcL Gene of Maize , 1999, Plant Cell.

[39]  Smith,et al.  A functional calvin cycle is not indispensable for the light activation of C4 phosphoenolpyruvate carboxylase kinase and its target enzyme in the maize mutant bundle sheath defective2-mutable1 , 1998, Plant physiology.

[40]  J. Langdale,et al.  GOLDEN 2: A Novel Transcriptional Regulator of Cellular Differentiation in the Maize Leaf , 1998, Plant Cell.

[41]  T. V. Madsen,et al.  Evidence that inducible C4-type photosynthesis is a chloroplastic CO2 concentrating mechanism in Hydrilla a submersed monocot. , 1997 .

[42]  O. Riera-Lizarazu,et al.  Cytological and molecular characterization of oat x maize partial hybrids , 1996, Theoretical and Applied Genetics.

[43]  K. Pregitzer,et al.  Effects of elevated CO(2) and light availability on the photosynthetic light response of trees of contrasting shade tolerance. , 1996, Tree physiology.

[44]  K Nasmyth,et al.  Evolution of the cell cycle. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[45]  T. Sage,et al.  Structure, ultrastructure, and histochemistry of the pollen tube pathway in the milkweed Asclepias exaltata L. , 1995, Sexual Plant Reproduction.

[46]  C. Kidner,et al.  bundle sheath defective, a mutation that disrupts cellular differentiation in maize leaves , 1994 .

[47]  J. Langdale,et al.  Spatial regulation of photosynthetic development in C4 plants. , 1991, Trends in genetics : TIG.

[48]  J. Langdale,et al.  The argentia mutation delays normal development of photosynthetic cell-types in Zea mays. , 1987, Developmental biology.

[49]  P. Chomczyński,et al.  Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. , 1987, Analytical biochemistry.

[50]  S. Fowler,et al.  Application of Nile red, a fluorescent hydrophobic probe, for the detection of neutral lipid deposits in tissue sections: comparison with oil red O. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[51]  S. Fowler,et al.  Spectrofluorometric studies of the lipid probe, nile red. , 1985, Journal of lipid research.

[52]  S. Fowler,et al.  Nile red: a selective fluorescent stain for intracellular lipid droplets , 1985, The Journal of cell biology.

[53]  A. Feinberg,et al.  A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. , 1983, Analytical biochemistry.

[54]  D. Lewis,et al.  THE ACID INVERTASES OF THE DEVELOPING THIRD LEAF OF OAT. I. CHANGES IN ACTIVITY OF INVERTASE AND CONCENTRATIONS OF ETHANOL-SOLUBLE CARBOHYDRATES , 1981 .

[55]  D. Lewis,et al.  THE ACID INVERTASES OF THE DEVELOPING THIRD LEAF OF OAT , 1981 .

[56]  W. Brown.  Leaf Anatomy in Grass Systematics , 1958, Botanical Gazette.

[57]  M. Lercher,et al.  An mRNA Blueprint for C 4 Photosynthesis Derived from Comparative Transcriptomics of Closely Related C 3 and C 4 Species 1 [ W ] [ OA ] , 2010 .

[58]  G. Edwards,et al.  Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants , 2010 .

[59]  M. Holdsworth,et al.  Promoting Access to White Rose Research Papers Mutations in the Arabidopsis Peroxisomal Abc Transporter Comatose Allow Differentiation between Multiple Functions in Planta: Insights from an Allelic Series Isolation and Generation of New Cts Alleles Subcellular Localization Phenotypic Characterizatio , 2022 .

[60]  M. Matsuoka,et al.  Significant accumulation of C(4)-specific pyruvate, orthophosphate dikinase in a C(3) plant, rice. , 2001, Plant physiology.

[61]  R. Furbank,et al.  MOLECULAR ENGINEERING OF C 4 PHOTOSYNTHESIS , 2001 .

[62]  M. Matsuoka,et al.  High-level expression of maize phosphoenolpyruvate carboxylase in transgenic rice plants , 1999, Nature Biotechnology.

[63]  R. Monson,et al.  16 – The Taxonomic Distribution of C4 Photosynthesis , 1999 .

[64]  T. Nelson,et al.  5 – Leaf Structure and Development in C4 Plants , 1999 .

[65]  L. Técsi,et al.  Phosphoenolpyruvate Carboxykinase in C4 Plants: Its Role and Regulation , 1997 .

[66]  R. Monson,et al.  Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation , 1993 .

[67]  M. D. Hatch,et al.  C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure , 1987 .

[68]  S. Craig,et al.  Subdivision of C4-Pathway Species Based on Differing C4 Acid Decarboxylating Systems and Ultrastructural Features , 1975 .

[69]  D. Carr,et al.  A suberized layer in the cell walls of the bundle sheath of grasses. , 1970 .