Cold Tolerance of C4 photosynthesis in Miscanthus × giganteus: Adaptation in Amounts and Sequence of C4 Photosynthetic Enzymes1

Field-grown Miscanthus × giganteus maintains high photosynthetic quantum yields and biomass productivity in cool temperate climates. It is related to maize (Zea mays) and uses the same NADP-malic enzyme C4 pathway. This study tests the hypothesis that M. × giganteus, in contrast to maize, forms photosynthetically competent leaves at low temperatures with altered amounts of pyruvate orthophosphate dikinase (PPDK) and Rubisco or altered properties of PPDK. Both species were grown at 25°C/20°C or 14°C/11°C (day/night), and leaf photosynthesis was measured from 5°C to 38°C. Protein and steady-state transcript levels for Rubisco, PPDK, and phosphoenolpyruvate carboxylase were assessed and the sequence of C4-PPDK from M. × giganteus was compared with other C4 species. Low temperature growth had no effect on photosynthesis in M. × giganteus, but decreased rates by 80% at all measurement temperatures in maize. Amounts and expression of phosphoenolpyruvate carboxylase were affected little by growth temperature in either species. However, PPDK and Rubisco large subunit decreased >50% and >30%, respectively, in cold-grown maize, whereas these levels remained unaffected by temperature in M. × giganteus. Differences in protein content in maize were not explained by differences in steady-state transcript levels. Several different M. × giganteus C4-PPDK cDNA sequences were found, but putative translated protein sequences did not show conservation of amino acids contributing to cold stability in Flaveria brownii C4-PPDK. The maintenance of PPDK and Rubisco large subunit amounts in M. × giganteus is consistent with the hypothesis that these proteins are critical to maintaining high rates of C4 photosynthesis at low temperature.

[1]  J. Burnell,et al.  Cold stability of pyruvate, orthophosphate dikinase of Flaveria brownii , 1995, Plant Molecular Biology.

[2]  C. Foyer,et al.  Effect of Chilling on Carbon Assimilation, Enzyme Activation, and Photosynthetic Electron Transport in the Absence of Photoinhibition in Maize Leaves , 1997, Plant physiology.

[3]  R. Sage,et al.  The response of the high altitude C(4) grass Muhlenbergia montana (Nutt.) A.S. Hitchc. to long- and short-term chilling. , 2001, Journal of experimental botany.

[4]  S. Long,et al.  The effects of development at sub‐optimal growth temperatures on photosynthetic capacity and susceptibility to chilling‐dependent photoinhibition in Zea mays , 1992 .

[5]  D. Laurie,et al.  Microsatellites and RFLP probes from maize are efficient sources of molecular markers for the biomass energy crop Miscanthus , 2001, Theoretical and Applied Genetics.

[6]  G. Nie,et al.  Modifications to Thylakoid Composition during Development of Maize Leaves at Low Growth Temperatures. , 1991, Plant physiology.

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

[8]  I. Linde-Laursen,et al.  Cytogenetic Analysis of Miscanthus‘Giganteus’, an Interspecific Hybrid , 2004 .

[9]  A. Nose,et al.  Thermal Characteristics of C4 Photosynthetic Enzymes from Leaves of Three Sugarcane Species Differing in Cold Sensitivity , 1999 .

[10]  Trevor R. Hodkinson,et al.  Nomenclature of Miscanthus x giganteus (Poaceae) , 2001 .

[11]  J. Burnell,et al.  Identification of the amino acid residues responsible for cold tolerance in Flaveria brownii pyruvate,orthophosphate dikinase , 1997, FEBS letters.

[12]  R. Wise,et al.  The ultrastructure of chilling stress , 2000 .

[13]  T. Sugiyama,et al.  Purification, molecular, and catalytic properties of pyruvate phosphate dikinase from the maize leaf. , 1973, Biochemistry.

[14]  T. Sugiyama,et al.  Cold lability of pyruvate, orthophosphate dikinase in the maize leaf. , 1978, Plant physiology.

[15]  L. Schrader,et al.  Relationships between CO(2) Exchange Rates and Activities of Pyruvate,Pi Dikinase and Ribulose Bisphosphate Carboxylase, Chlorophyll Concentration, and Cell Volume in Maize Leaves. , 1985, Plant physiology.

[16]  N. Baker,et al.  Effects of ozone on the photosynthetic apparatus and leaf proteins during leaf development in wheat , 1993 .

[17]  G. Edwards,et al.  Differences in cold lability of pyruvate, Pi dikinase among C4 species , 1979 .

[18]  R. Sage Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature , 2002 .

[19]  S. Trevanion,et al.  Genetic Manipulation of Key Photosynthetic Enzymes in the C4 Plant Flaveria bidentis , 1997 .

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

[21]  N. Baker,et al.  Response of the photosynthetic apparatus in maize leaves grown at low temperature on transfer to normal growth temperature , 1995 .

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

[23]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[24]  J. Simon,et al.  Molecular forms and kinetic properties of phosphoenolpyruvate carboxylase from barnyard grass (Echinochloa crus-galli (L.) Beauv.: Poaceae) , 2000 .

[25]  B. Sobral,et al.  Phylogenetic analysis of chloroplast restriction enzyme site mutations in the Saccharinae Griseb. subtribe of the Andropogoneae Dumort. tribe , 1994, Theoretical and Applied Genetics.

[26]  M. Matsuoka The gene for pyruvate, orthophosphate dikinase in C4 plants: structure, regulation and evolution. , 1995, Plant & cell physiology.

[27]  S. Rodermel Subunit control of Rubisco biosynthesis – a relic of an endosymbiotic past? , 1999, Photosynthesis Research.

[28]  M. Matsuoka,et al.  Evolution and Expression of C4 Photosynthesis Genes , 1996, Plant physiology.

[29]  P. Miedema,et al.  The effects of low temperature on seedling growth of maize genotypes , 1987 .

[30]  T. Sugiyama,et al.  Correlation of the Activities of Phosphoenolpyruvate Carboxylase and Pyruvate,Orthophosphate Dikinase with Biomass in Maize Seedlings , 1983 .

[31]  Stephen P. Long,et al.  Can perennial C4 grasses attain high efficiencies of radiant energy conversion in cool climates , 1995 .

[32]  Stephen P. Long,et al.  Leaf photosynthesis in the C4-grass Miscanthus x giganteus, growing in the cool temperate climate of southern England , 1996 .

[33]  John A. yyGreaves Improving suboptimal temperature tolerance in maize- the search for variation , 1996 .

[34]  J. Sheen C4 GENE EXPRESSION. , 2003, Annual review of plant physiology and plant molecular biology.

[35]  R. Sage,et al.  Photosynthetic performance at low temperature of Bouteloua gracilis Lag., a high-altitude C4 grass from the Rocky Mountains, USA , 2000 .

[36]  S. Long,et al.  Analysis of Chill-Induced Depressions of Photosynthesis in Maize , 1990 .

[37]  J. Sheen C 4 GENE EXPRESSION , 1999 .

[38]  J. Sheen Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. , 1991, The Plant cell.

[39]  R. Wise Chilling-enhanced photooxidation: The production, action and study of reactive oxygen species produced during chilling in the light , 1995, Photosynthesis Research.

[40]  A. S. Raghavendra,et al.  Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants. , 2003, Journal of experimental botany.

[41]  O. Podhajcer,et al.  Bias in estimations of DNA content by competitive polymerase chain reaction. , 2000, Analytical biochemistry.

[42]  D. A. Ward,et al.  The temperature acclimation of photosynthetic responses to CO2 in Zea mays and its relationship to the activities of photosynthetic enzymes and the CO2-concentrating mechanism of C4 photosynthesis , 1987 .

[43]  C. Foyer,et al.  Acclimation of photosynthesis, H2O2 content and antioxidants in maize (Zea mays ) grown at sub-optimal temperatures , 1999 .

[44]  Carl J. Bernacchi,et al.  Improved temperature response functions for models of Rubisco‐limited photosynthesis , 2001 .

[45]  J. Greef,et al.  Syntaxonomy of Miscanthus x giganteus Greef et Deu , 1993 .

[46]  Ilia J Leitch,et al.  The use of dna sequencing (ITS and trnL-F), AFLP, and fluorescent in situ hybridization to study allopolyploid Miscanthus (Poaceae). , 2002, American journal of botany.

[47]  H. Kassemeyer,et al.  Characterization and Expression of Caffeoyl-Coenzyme A 3-O-Methyltransferase Proposed for the Induced Resistance Response of Vitis vinifera L , 1997, Plant physiology.

[48]  A. Nose,et al.  Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in leaves of three sugarcane species , 1999 .

[49]  Paul G. Falkowski,et al.  Photoinhibition of Photosynthesis in Nature , 1994 .

[50]  G. Edwards,et al.  Rates of Photosynthesis Relative to Activity of Photosynthetic Enzymes, Chlorophyll and Soluble Protein Content Among Ten C4 Species , 1984 .

[51]  Stephen P. Long,et al.  C4 photosynthesis at low temperatures , 1983 .