Advertisement

Chapter 10 C4 Photosynthesis and Temperature

  • Rowan F. Sage
  • Ferit Kocacinar
  • David S. Kubien
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 32)

Summary

C4 plants perform poorly at low temperature, in contrast to C3 vegetation. As a consequence, low ­numbers of C4 species occur at high latitude, high elevation, and during cooler growing seasons. The mechanisms explaining the poor performance of C4 species in colder climates have not been clearly identified. Early physiological perspectives indicate that C4 species fail at low temperature due to either low quantum yield of the C4 relative to the C3 pathway, or enzyme lability in the C4 cycle, most notably at PEP regeneration by pyruvate-Pi dikinase (PPDK). Alternatively, recent phylogenetic surveys show that all C4 lineages originated from C3 ancestors adapted to warm climates, indicating the failure of most C4 species in colder environments could reflect prior heat adaptation within their respective evolutionary lineages. Numerous C4 species have independently evolved cold tolerance; these plants allow for examination of C4 photosynthesis at low temperature without complications from chilling injury. Relative to ecologically-similar C3 species, chilling-adapted C4 species have similar or slightly reduced photosynthetic capacities below 10°C and, after cold acclimation, show no chilling lability of PPDK, PEP carboxylase or other enzymes of the C4 cycle. Cold-adapted C4 species have enhanced photoprotective capacity at low ­temperature as indicated by greater levels of antioxidants and carotenoid pigments. Rubisco capacity is similar to gross CO2 assimilation rate below 20°C in cold-adapted C4 species, indicating it is an important limitation on C4 photosynthesis at cool temperature. Acclimation and adaptation of C4 species to the cold does not overcome the apparent Rubisco limitation. It is likely that a ceiling on carbon gain by insufficient Rubisco capacity at low temperature may be a leading trait that maladapts the C4 pathway to cold regions of the earth.

Keywords

Bundle Sheath Bundle Sheath Cell Thermal Optimum RuBP Regeneration Capacity Grass Flora 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

A

– Net CO2 assimilation rate;

Ci

– Intercellular partial pressure of CO2;

Ca

– Ambient partial pressure of CO2;

PEPC

– Phosphoenolpyruvate carboxylase;

PPDK

– Pyruvate orthophosphate dikinase;

Rubisco

– Ribulose-1,5-bisphosphate carboxylase/oxygenase.

Notes

Acknowledgments

The authors are grateful for support from their national funding agencies, the Canadian Natural Science and Engineering Council (NSERC) which funded RF Sage and DS Kubien, and The Scientific and Technological Research Council of ­Turkey (TÜBİTAK) grant no: 106O384 to F. Kocacinar. We also thank Ms. Debbie Tam for technical assistance with the the work that was originally generated by the authors.

References

  1. Ackerly DD, Coleman JS, Morse SR and Bazzaz FA (1992) CO2 and temperature effects on leaf-area production in two annual plant-species. Ecology 73: 1260–1269Google Scholar
  2. Ackerly DD (1999) Comparative plant ecology and the role of phylogenetic information. In: Press MC, Scholes JD and Barker MG (eds) Physiological Plant Ecology, pp 391–413. Blackwell, OxfordGoogle Scholar
  3. Akhani H, Trimborn P and Ziegler H (1997) Photosynthetic pathways in Chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Syst Evol 206: 187–221Google Scholar
  4. Auerswald K, Wittmer M, Mannel TT, Bai YF, Schaufele R and Schnyder H (2009) Large regional-scale variation in C3/C4 distribution pattern of Inner Mongolia steppe is revealed by grazer wool carbon isotope composition. ­Biogeosciences 6: 795–805Google Scholar
  5. Baker NR (2008) Chlorophyll fluorescence: a probe of ­photosynthesis in vivo. Annu Rev Plant Biol 59: 89–113PubMedGoogle Scholar
  6. Barkworth ME, Anderson LK, Capels KM, Long S and Biep MB (eds) (2007) Manual of Grasses for North America. Utah State University Press, Logan, UtahGoogle Scholar
  7. Batanouny KH, Stichler W and Ziegler H (1988) Photosynthetic pathways, distribution, and ecological characteristics of grass species in Egypt. Oecologia 75: 539–548Google Scholar
  8. Beale CV and Long SP (1995) Can perennial C4 grasses attain high efficiencies of radiant energy-conversion in cool climates. Plant Cell Environ 18: 641–650Google Scholar
  9. Beale CV, Bint DA and Long SP (1996) Leaf photosynthesis in the C4-grass Miscanthus x giganteus, growing in the cool temperate climate of southern England. J Exp Bot 47: 267–273Google Scholar
  10. Bernacchi CJ, Singsaas EL, Pimentel C, Portis AR and Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant Cell Environ 24: 253–259Google Scholar
  11. Bernacchi CJ, Pimentel C and Long SP (2003) In vivo ­temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant Cell Environ 26: 1419–1430Google Scholar
  12. Berry J and Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher-plants. Annu Rev Plant Physiol 31: 491–543Google Scholar
  13. Besnard G, Muasya AM, Russier F, Roalson EH, Salamin N and Christin P-A (2009) Phylogenomics of C4 photosynthesis in the sedges (Cyperaceae): Multiple appearances and genetic convergence. Mol Biol Evol 26:1909–1919PubMedGoogle Scholar
  14. Bird MI, Haberle SG and Chivas AR (1994) Effect of ­altitude on the carbon-isotope composition of forest and grassland soils from Papua-New-Guinea. Glob Biogeochem Cycles 8: 13–22Google Scholar
  15. Bird MI and Pousai P (1997) Variations of delta C13 in the surface soil organic carbon pool. Glob Biogeochem Cycles 11: 313–322Google Scholar
  16. Bixing S and Phillips SM (2006) Arundinella. In: Zhengyi W, Raven PH and Deyuan H (Eds) Flora of China – Poaceae, Vol 22, pp 563–570. Missouri Botanical Garden Press, St Louis, MOGoogle Scholar
  17. Bjorkman O, Pearcy RW and Nobs MW (1970) Photosynthetic characteristics. Carnegie Inst Yearbook 69:640–655Google Scholar
  18. Bjorkman O and Pearcy RW (1971) Effect of growth ­temperature on the temperature dependence of photosynthesis in vivo and on CO2 fixation by carboxydismutase in vitro in C3 and C4 species. Carnegie Inst Yearook 70: 511–520Google Scholar
  19. Bjorkman O, Pearcy RW, Mooney H and Harrison AT (1972) Photosynthetic adaptation to high-temperatures – field study in Death Valley, California. Science 175: 786–789PubMedGoogle Scholar
  20. Bjorkman O, Mahall B, Nobs M, Ward W, Nicholson F, and Mooney H (1974) An analysis of the temperature dependence of growth under controlled conditions. Carnegie Inst Yearbook 73:757–767Google Scholar
  21. Bjorkman O, Boynton J and Berry J (1976) Comparison of heat stability of photosynthesis, chloroplast membrane reactions, photosynthetic enzymes, and soluble protein in leaves of heat- adapted and cold-adapted C4 species. Carnegie Inst Yearbook 75: 400–407Google Scholar
  22. Bjorkman O, Boynton J and Berry J (1976) Comparison of heat stability of photosynthesis, chloroplast membrane reactions, photosynthetic enzymes, and soluble protein in leaves of heat- adapted and cold-adapted C4 species. ­Carnegie Inst Yearbook 75: 400–407Google Scholar
  23. Bjorkman O, Badger MR and Armond PA (1980) Responses and adaptation to high temperatures. In: Turner NC and Kramer PJ (eds) Adaptation of plants to water and high temperature stress, pp 233–249. Wiley, New YorkGoogle Scholar
  24. Black CC, Chen TM and Brown RH (1969) Biochemical basis for plant competition. Weed Sci 17: 338–344Google Scholar
  25. Black CC (1971) Ecological implications of dividing plants into groups with distinct photosynthetic productions capacities. Adv Ecol Res 7: 87–114Google Scholar
  26. Boom A, Mora G, Cleef AM and Hooghiemstra H (2001) High altitude C4 grasslands in the northern Andes: relicts from ­glacial conditions? Rev Palaeobot Palynol 115: 147–160PubMedGoogle Scholar
  27. Boutton TW, Harrison AT and Smith BN (1980) Distribution of biomass of species differing in photosynthetic pathway along an altitudinal transect in southeastern Wyoming grassland. Oecologia 45: 287–298Google Scholar
  28. Bowman WD and Turner L (1993) Photosynthetic sensitivity to temperature in populations of two C4 Bouteloua (Poaceae) species native to different altitudes. Am J Bot 80: 369–374Google Scholar
  29. Brako L and Zarucchi JL (1993) Catalogue of the Flowering Plants and Gymosperms of Peru. Missouri Botanical ­Garden Press, St Louis, MOGoogle Scholar
  30. Bunce JA (1982) Low humidity effects on photosynthesis in single leaves of C4 plants. Oecologia 54: 233–235Google Scholar
  31. Bunce JA (1983) Differential sensitivity to humidity of daily photosynthesis in the field in C3-species and C4-species. Oecologia 57: 262–265Google Scholar
  32. Burnell JN (1990) A comparative study of the cold sensi­tivity of pyruvate, Pi dikinase in Flaveria species. Plant Cell Physiol 31: 295–297Google Scholar
  33. Cabido M, Ateca N, Astegiano ME and Anton AM (1997) Distribution of C3 and C4 grasses along an altitudinal ­gradient in central Argentina. J Biogeog 24: 197–204Google Scholar
  34. Caldwell MM, White RS, Moore RT and Camp LB (1977a) Carbon balance, productivity, and water-use of cold-­winter desert shrub communities dominated by C3 and C4 species. Oecologia 29: 275–300Google Scholar
  35. Caldwell MM, Osmond CB and Nott DL (1977b) C4 pathway photosynthesis at low-temperature in cold-tolerant Atriplex species. Plant Physiol 60: 157–164PubMedGoogle Scholar
  36. Cavagnaro JB (1988) Distribution of C3 and C4 grasses at different altitudes in a temperate arid region of Argentina. Oecologia 76: 273–277Google Scholar
  37. Cen YP and Sage RF (2005) The regulation of rubisco activity in response to variation in temperature and atmospheric CO2 partial pressure in sweet potato. Plant Physiol 139: 979–990PubMedGoogle Scholar
  38. Chazdon RL (1978) Ecological aspects of the distribution of C4 grasses in selected habitats of Costa-Rica. Biotropica 10: 265–269Google Scholar
  39. Chinthapalli B, Murmu J and Raghavendra AS (2003)Dramatic difference in the responses of phosphoenolpyruvate carboxylase to temperature in leaves of C3 and C4 plants, J Exp Bot, 54: 707–714PubMedGoogle Scholar
  40. Christie EK and Detling JK (1982) Analysis of interference between C3 and C4 grasses in relation to temperature and soil-nitrogen supply. Ecology 63: 1277–1284Google Scholar
  41. Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V and Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18: 37–43PubMedGoogle Scholar
  42. Christin PA, Salamin N, Kellogg EA, Vicentini A and Besnard G (2009) Integrating phylogeny into studies of C4 variation in the rasses. Plant Physiol 149: 82–87PubMedGoogle Scholar
  43. Clements FE, Weaver JE and Hanson HC (1929) Plant ­Competition. Carnegie Institution, WashingtonGoogle Scholar
  44. Clifton-Brown JC, Long SP, Jorgensen U, Humphries SA, Schwarz KU and Schwarz H (2001) Miscanthus productivity. In: Jones MB and Walsh M (eds) Miscanthus for Energy and Fiber, pp 46–67. James & James, LondonGoogle Scholar
  45. Collatz GJ, Ribas-Carbo M and Berry JA (1992) Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Aust J Plant Physiol 19: 519–538Google Scholar
  46. Collatz GJ, Berry JA and Clark JS (1998) Effects of climate and atmospheric CO2 partial pressure on the global ­distribution of C4 grasses: present, past and future. ­Oecologia 114: 441–454Google Scholar
  47. Collins RP and Jones MB (1986a) The influence of climatic factors on the distribution of C4 species in Europe. Vegetatio 64: 121–129Google Scholar
  48. Collins RP and Jones MB (1986b) The seasonal pattern of growth and production of a temperate C4 species, Cyperus longus. J Exp Bot 37: 1823–1835Google Scholar
  49. Crafts-Brandner SJ and Salvucci ME (2002) Sensitivity of photosynthesis in a C4 plant, maize, to heat stress. Plant Physiol 129: 1773–1780PubMedGoogle Scholar
  50. Dai Z, Edwards Ge and Ku MSB (1992) Control of photosynthesis and stomatal conductance in Ricinus communis L. (castor bean) by leaf to air vapor pressure deficit. Plant Physiol 99: 1426–1434PubMedGoogle Scholar
  51. Dai ZY, Ku MSB and Edwards GE (1993) C4 photosynthesis - the CO2-concentrating mechanism and photorespiration. Plant Physiol 103: 83–90PubMedGoogle Scholar
  52. Dai Z, Ku MSB and Edwards GE (1996) Oxygen sensitivity of photosynthesis and photorespiration in different photosynthetic types in the genus Flaveria. Planta 198: 563–571.Google Scholar
  53. Dengler NG and Nelson T (1999) Leaf structure and development in C4 plants. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 133–172. Academic, San Diego, CAGoogle Scholar
  54. De Veau EJ and Burris JE (1989) Photorespiratory rates in wheat and maize as determined by O18 labeling. Plant Physiol 90: 500–511PubMedGoogle Scholar
  55. Dickinson CE and Dodd JL (1976) Phenological patterns in the shortgrass prairie. Am Midl Nat 96:367–378Google Scholar
  56. Doliner LH and Jolliffe PA (1979) Ecological evidence concerning the adaptive significance of the C4 dicarboxylic-acid pathway of photosynthesis. Oecologia 38: 23–34Google Scholar
  57. Du YC, Nose A and Wasano K (1999a) Effects of chilling temperature on photosynthetic rates, photosynthetic enzyme activities and metabolite levels in leaves of three sugarcane species. Plant Cell Environ 22: 317–324Google Scholar
  58. Du YC, Nose A and Wasano K (1999b) Thermal characteristics of C4 photosynthetic enzymes from leaves of three sugarcane species differing in cold sensitivity. Plant Cell Physiol 40: 298–304Google Scholar
  59. Dwyer SA, Ghannoum O, Nicotra A and Von Caemmerer S (2007) High temperature acclimation of C4 photosynthesis is linked to changes in photosynthetic biochemistry. Plant Cell Environ 30: 53–66PubMedGoogle Scholar
  60. Earnshaw MJ, Carver KA, Gunn TC, Kerenga K, Harvey V, Griffiths H and Broadmeadow MSJ (1990) Photosynthetic pathway, chilling tolerance and cell sap osmotic potential values of grasses along an altitudinal gradient in Papua New Guinea. Oecologia 84: 280–288Google Scholar
  61. Edwards EJ and Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proc Nat Acad Sci (USA) 107: 2532–2537.Google Scholar
  62. Edwards EJ, Still CJ and Donoghue MJ (2007) The ­relevance of phylogeny to studies of global change. Trends Ecol Evol 22: 243–249PubMedGoogle Scholar
  63. Edwards EJ and Still CJ (2008) Climate, phylogeny and the ecological distribution of C4 grasses. Ecol Lett 11: 266–276PubMedGoogle Scholar
  64. Edwards GE and Baker NR (1993) Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynth Res 32:89–102Google Scholar
  65. Edwards GE and Walker DA (1983) C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis. Blackwell Scientific, OxfordGoogle Scholar
  66. Ehleringer J and Bjorkman O (1977) Quantum yields for CO2 uptake in C3 and C4 plants - dependence on temperature, CO2 and O2 concentration. Plant Physiol 59: 86–90PubMedGoogle Scholar
  67. Ehleringer JR (1978) Implications of quantum yield differences on distributions of C3 and C4 grasses. Oecologia 31: 255–267Google Scholar
  68. Ehleringer J and Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 Plants. Plant Physiol 73: 555–559PubMedGoogle Scholar
  69. Ehleringer JR, Sage RF, Flanagan LB and Pearcy RW (1991) Climate change and the evolution of C4 photosynthesis. Trends Ecol Evol 6: 95–99PubMedGoogle Scholar
  70. Ehleringer JR and Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24: 411–439Google Scholar
  71. Ehleringer JR, Cerling TE and Helliker BR (1997) C4 photosynthesis, atmospheric CO2 and climate. Oecologia 112: 285–299Google Scholar
  72. Ehleringer JR (2005) The influence of atmospheric CO2, temperature and water on the abundance of C3/C4 taxa. In: Ehleringer JR, Cerling TE and Dearing MD (eds) A History of Atmospheric CO2 and its Effects on Plants, Animals and Ecosystems, pp 214–231. Springer, BerlinGoogle Scholar
  73. Ellis RP, Vogel JC and Fuls A (1980) Photosynthetic pathways and the geographical-distribution of grasses in Southwest Africa-Namibia. S Afr J Sci 76: 307–314Google Scholar
  74. Epstein HE, Lauenroth WK, Burke IC and Coffin DP (1996) Ecological responses of dominant grasses along two climatic gradients in the great plains of the United States. J Veg Sci 7: 777–788Google Scholar
  75. Epstein HE, Lauenroth WK, Burke IC and Coffin DP (1997) Productivity patterns of C3 and C4 functional types in the US Great Plains. Ecology 78: 722–731Google Scholar
  76. Evans LT and Bush MG (1985) Growth and development of channel millet (Echinochloa turneriana) in relation to its potential as a crop plant and compared with other ­Echinochloa millets, rice and wheat. Field Crops Res 12: 295–317Google Scholar
  77. Farage PK, Blowers D, Long SP and Baker NR (2006) Low growth temperatures modify the efficiency of light use by photosystem II for CO2 assimilation in leaves of two chilling-tolerant C4 species, Cyperus longus L. and ­Miscanthus x giganteus. Plant Cell Environ 29: 720–728PubMedGoogle Scholar
  78. Farquhar GD and von Caemmerer S (1982) Modeling of photosynthetic response to environmental conditions. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology II: Water Relations and ­Carbon Assimlation, Encyclopedia of Plant Physiology New Series, Vol 12B, pp 549–587. Springer-Verlag, BerlinGoogle Scholar
  79. Fladung M and Hesselbach J (1989) Effect of varying environments on photosynthetic parameters of C3, C3-C4 and C4 species of Panicum. Oecologia 79: 168–173Google Scholar
  80. Flint EP and Patterson DT (1983) Interference and temperature effects on growth in soybean (Glycine max) and associated C3 and C4 weeds. Weed Sci 31: 193–199Google Scholar
  81. Fryer MJ, Oxborough K, Martin B, Ort DR and Baker NR (1995) Factors associated with depression of photosynthetic quantum efficiency in maize at low growth temperature. Plant Physiol 108: 761–767PubMedGoogle Scholar
  82. Fryer MJ, Andrews JR, Oxborough K, Blowers DA and Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiol 116: 571–580PubMedGoogle Scholar
  83. Furbank RT and Badger MR (1982) Photosynthetic oxygen-exchange in attached leaves of C4 monocotyledons. Aust J Plant Physiol 9: 553–558Google Scholar
  84. Furbank RT and Badger MR (1983) Photorespiratory characteristics of isolated bundle sheath strands of C4 monocotyledons. Aust J Plant Physiol 10: 451–458Google Scholar
  85. Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S and Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Aust J Plant Physiol 24: 477–485Google Scholar
  86. Furbank RT, Jenkins CLD and Hatch MD (1990) C4 Photosynthesis - quantum requirement, C4 acid overcycling and Q-cycle involvement. Aust J Plant Physiol 17: 1–7Google Scholar
  87. Grise DJ (1997) Effects of Elevated CO2 and High Temperature on the Relative Growth Rates and Competitive Interactions Between a C3 (Chenopodium album) and a C4 (Amaranthus hybridus) Annual. PhD thesis. University of Georgia, Athens, GAGoogle Scholar
  88. Guo QF and Brown JH (1996) Temporal fluctuations and experimental effects in desert plant communities. Oecologia 107: 568–577Google Scholar
  89. Haldimann P (1996) Effects of changes in growth temperature on photosynthesis and carotenoid composition in Zea mays leaves. Physiol Plantarum 97: 554–562Google Scholar
  90. Haldimann P (1998) Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity. Plant Cell Environ 21: 200–208Google Scholar
  91. Hamel N and Simon JP (2000) Molecular forms and kinetic properties of phosphoenolpyruvate carboxylase from barnyard grass (Echinochloa crus-galli (L.) Beauv.:Poaceae). Can J Bot 78: 619–628Google Scholar
  92. Hatch MD (1979) Regulation of C4 photosynthesis - factors affecting cold-mediated inactivation and reactivation of pyruvate, pi-dikinase. Aust J Plant Physiol 6: 607–619Google Scholar
  93. Hattersley PW (1983) The distribution of C3 grasses and C4 grasses in Australia in relation to climate. Oecologia 57: 113–128Google Scholar
  94. Heaton EA, Dohleman FG and Long SP (2008) Meeting US biofuel goals with less land: the potential of Miscanthus. Glob Change Biol 14: 2000–2014Google Scholar
  95. Hendrickson L, Sharwood R, Ludwig M, Whitney SM, Badger MR and von Caemmerer S (2008) The effects of Rubisco activase on C4 photosynthesis and metabolism at high temperature. J Exp Bot 59: 1789–1798PubMedGoogle Scholar
  96. Henning JC and Brown RH (1986) Effects of irradiance and temperature on photosynthesis in C3, C4 and C3/C4 ­Panicum species. Photosynth Res 10: 101–112Google Scholar
  97. Hulten E and Fries M (1986) Atlas of North European Vascular Plants North of the Tropic of Cancer, volume I. Koeltz Scientific, Könisgstein, Germany.Google Scholar
  98. Ibrahim DG, Gilbert ME, Ripley BS and Osborne CP (2008) Seasonal differences in photosynthesis between the C3 and C4 subspecies of Alloteropsis semialata are offset by frost and drought. Plant Cell Environ 31: 1038–1050PubMedGoogle Scholar
  99. Ibrahim DG, Burke T, Ripley BS and Osborne CP (2009) A molecular phylogeny of the genus Alloteropsis (Panicoideae, Poaceae) suggests an evolutionary reversion from C4 to C3 photosynthesis. Ann Bot 103: 127–136PubMedGoogle Scholar
  100. Ishii R, Ohsugi R and Murata Y (1977) Effect of temperature on rates of photosynthesis, respiration and activity of RuDP carboxylase in barley, rice and maize leaves. Jpn J Crop Sci 46: 516–523Google Scholar
  101. Jones CA (1985) C4 Grasses and Cereals, Growth, Development and Stress Response. Wiley Interscience, New YorkGoogle Scholar
  102. Jones MB, Hannon GE and Coffey MD (1981) C4 Photosynthesis in Cyperus-longus L, a species occurring in temperate climates. Plant Cell Environ 4: 161–168Google Scholar
  103. Jordan DB and Ogren WL (1984) The CO2/O2 specificity of ribulose 1,5-bisphosphate carboxylase oxygenase – dependence on ribulosebisphosphate concentration, pH and temperature. Planta 161: 308–313Google Scholar
  104. Kamler AE (2004) C4 photosynthesis in a Mediterranean ­Climate: A Focus on Microhabitat and Competition. MSc. Thesis. San Francisco State University, San Francisco, CAGoogle Scholar
  105. Kanai R and Edwards GE (1999) The biochemistry of C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 49–87. Academic, San Diego, CAGoogle Scholar
  106. Kemp PR (1983) Phenological patterns of Chihuahuan desert plants in relation to the timing of water availability. J Ecol 71: 427–436Google Scholar
  107. Kemp PR and Williams GJ (1980) A physiological-basis for niche separation between Agropyron smithii (C3) and Bouteloua gracilis (C4). Ecology 61: 846–858Google Scholar
  108. Kingston-Smith AH, Harbinson J, Williams J and Foyer CH (1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiol 114:1039–1046PubMedGoogle Scholar
  109. Krall JP, Edwards GE and Andreo CS (1989) Protection of pyruvate, Pi dikinase from maize against cold lability by compatible solutes. Plant Physiol 89: 280–285PubMedGoogle Scholar
  110. Krall JP and Edwards GE (1993) PEP carboxylases from two C4 Species of Panicum with markedly different susceptibilities to cold inactivation. Plant Cell Physiol 34: 1–11Google Scholar
  111. Körner C (2003) Alpine Plant Life, Second Edition. Springer, BerlinGoogle Scholar
  112. Ku SB and Edwards GE (1975) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various types of C4 plants. IV. Enzymes of respiratory metabolism and energy utilizing enzymes of photosynthetic pathways. Z Pfanzenphysiol 77:16–32Google Scholar
  113. Ku SB and Edwards GE (1980) Oxygen inhibition of photosynthesis in the C4 species Amaranthus graecizans L. Planta 147: 277–282Google Scholar
  114. Kubien DS (2003) On the Performance of C4 Photosynthesis at Low Temperature and Its Relationship to the Ecology of C4 Plants in Cool Climates. PhD Thesis. University of Toronto, Toronto, Canada.Google Scholar
  115. Kubien DS and Sage RF (2003) C4 grasses in boreal fens: their occurrence in relation to microsite characteristics. Oecologia 137: 330–337PubMedGoogle Scholar
  116. Kubien DS, von Cammerer S, Furbank RT and Sage RF (2003) C4 photosynthesis at low temperature. A study using transgenic plants with reduced amounts of Rubisco. Plant Physiol 132: 1577–1585PubMedGoogle Scholar
  117. Kubien DS and Sage RF (2004a) Low-temperature photosynthetic performance of a C4 grass and a co-occurring C3 grass native to high latitudes. Plant Cell Environ 27: 907–916Google Scholar
  118. Kubien DS and Sage RF (2004b) Dynamic photo-inhibition and carbon gain in a C4 and a C3 grass native to high latitudes. Plant Cell Environ 27: 1424–1435Google Scholar
  119. Labate CA, Adcock MD and Leegood RC (1990) Effects of temperature on the regulation of photosynthetic carbon assimilation in leaves of maize and barley. Planta 181: 547–554Google Scholar
  120. Laisk A and Edwards GE (1997) CO2 and temperature-dependent induction in C4 photosynthesis: an approach to the hierarchy of rate-limiting processes. Aust J Plant Physiol 24: 505–516Google Scholar
  121. Laisk A and Edwards GE (1998) Oxygen and electron flow in C4 photosynthesis: Mehler reaction, photorespiration and CO2 concentration in the bundle sheath. Planta 205: 632–645Google Scholar
  122. Leegood RC and Edwards GE (1996) Carbon metabolism and photorespiration: temperature dependence in relation to other environmental factors. In: Baker NR (ed) Photosynthesis and the Environment, Vol 5, pp 191–121. ­Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  123. Leipner J, Fracheboud Y and Stamp P (1997) Acclimation by suboptimal growth temperature diminishes photooxidative damage in maize leaves. Plant Cell Environ 20: 366–372Google Scholar
  124. Li MR, Wedin DA and Tieszen LL (1999) C3 and C4 photosynthesis in Cyperus (Cyperaceae) in temperate eastern North America. Can J Bot 77: 209–218.Google Scholar
  125. Liu MZ and Osborne CP (2008) Leaf cold acclimation and freezing injury in C3 and C4 grasses of the Mongolian Plateau. J Exp Bot 59: 4161–4170PubMedGoogle Scholar
  126. Livingstone DA and Clayton WD (1980) An altitudinal cline in tropical African grass floras and its paleoecological significance. Quatern Res 13: 392–402Google Scholar
  127. Long SP (1983) C4 photosynthesis at low-temperatures. Plant Cell Environ 6: 345–363Google Scholar
  128. Long SP (1999) Environmental responses. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 215–249. Academic, San Diego, CAGoogle Scholar
  129. Long SP, Incoll LD and Woolhouse HW (1975) C4 photosynthesis in plants from cool temperate regions, with particular reference to Spartina townsendii. Nature 257: 622–624Google Scholar
  130. Long SP and Woolhouse HW (1978a) Responses of net photosynthesis to vapor-pressure deficit and CO2 concentration in Spartina townsendii (sensu lato), a C4 species from a cool temperate climate. J Exp Bot 29: 567–577Google Scholar
  131. Long SP and Woolhouse HW (1978b) Responses of net photosynthesis to light and temperature in Spartina townsendii (sensu-lato), a C4 species from a cool temperate climate. J Exp Bot 29: 803–814Google Scholar
  132. Loomis RS (1983) Productivity of agricultural ecosystems. In: Lange OL, Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology IV. Ecosystem Processes: Mineral Cycling, Productivity and Man’s Influence. Encyclopedia of Plant Physiology New Series, Vol 12D, pp 151–203. Springer-Verlag, BerlinGoogle Scholar
  133. Loreto F, Tricoli D and DiMarco G (1995) On the relationship between electron transport rate and photosynthesis in leaves of the C4 plant Sorghum bicolor exposed to water stress, temperature changes and carbon metabolism inhibition. Aust J Plant Physiol 22: 885–892Google Scholar
  134. Ludlow MM and Wilson GL (1971) Photosynthesis of ­Tropical Pasture Plants. I. Illuminance, carbon dioxide concentration, leaf temperature and leaf air-vapour pressure difference. Aust J Biol Sci 24:449–470Google Scholar
  135. Maroco JP, Ku MSB and Edwards GE (1997) Oxygen sensitivity of C4 photosynthesis: evidence from gas exchange and chlorophyll fluorescence with different C4 subtypes. Plant Cell Environ 20:1525–1533Google Scholar
  136. Marquez EJ, Rada F and Farinas MR (2006) Freezing tolerance in grasses along an altitudinal gradient in the ­Venezuelan Andes. Oecologia 150: 393–397PubMedGoogle Scholar
  137. Massacci A, Iannelli MA, Pietrini F and Loreto F (1995) The effect of growth at low-temperature on photosynthetic characteristics and mechanisms of photoprotection of maize leaves. J Exp Bot 46: 119–127Google Scholar
  138. Massad RS, Tuzet A and Bethenod O (2007) The effect of temperature on C4-type leaf photosynthesis parameters. Plant Cell Environ 30: 1191–1204PubMedGoogle Scholar
  139. Matsuba K, Imaizumi N, Kaneko S, Samejima M and Ohsugi R (1997) Photosynthetic responses to temperature of phosphoenolpyruvate carboxykinase type C4 species differing in cold sensitivity. Plant Cell Environ 20: 268–274Google Scholar
  140. McKown AD,Moncalvo JM,Dengler NG (2005)Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. Am J Bot 92:1911–1928PubMedGoogle Scholar
  141. Monson RK and Williams GJ (1982) A correlation between photosynthetic temperature adaptation and seasonal phenology patterns in the shortgrass prairie. Oecologia 54: 58–62Google Scholar
  142. Monson RK, Littlejohn RO and Williams GJ (1983) Photosynthetic adaptation to temperature in four species from the Colorado shortgrass steppe - a physiological model for coexistence. Oecologia 58: 43–51Google Scholar
  143. Muhaidat R, Sage RF and Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. Am J Bot 94: 362–381PubMedGoogle Scholar
  144. Mulroy TW and Rundel PW (1977) Annual plants – adaptations to desert environments. Bioscience 27: 109–114Google Scholar
  145. Murphy BP and Bowman D (2007) Seasonal water availability predicts the relative abundance of C3 and C4 grasses in Australia. Glob Ecol Biogeog 16: 160–169Google Scholar
  146. Naidu SL and Long SP (2004) Potential mechanisms of low-temperature tolerance of C4 photosynthesis in Miscanthus x giganteus: an in vivo analysis. Planta 220: 145–155PubMedGoogle Scholar
  147. Naidu SL, Moose SP, Al-Shoaibi AK, Raines CA and Long SP (2003) Cold tolerance of C4 photosynthesis in Miscanthus x giganteus: Adaptation in amounts and sequence of C4 photosynthetic enzymes. Plant Physiol 132: 1688–1697PubMedGoogle Scholar
  148. Nishimura N, Soga Y, Tsuda S, Saijoh Y, Mo W (1997) Altitudinal variation in the species composition of the main grasses in the Kirigamine subalpine grassland, central Japan. J Jpn Soc Grassland Sci 42:324–334Google Scholar
  149. Nord CA, Messersmith CG and Nalewaja JD (1999) Growth of Kochia scoparia, Salsola iberica, and Triticum aestivum varies with temperature. Weed Sci 47: 435–439Google Scholar
  150. Oberhuber W and Edwards GE (1993) Temperature-­dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiol 101: 507–512PubMedGoogle Scholar
  151. Ode DJ, Tieszen LL and Lerman JC (1980) The seasonal contribution of C3 and C4 plant-species to primary production in a mixed prairie. Ecology 61: 1304–1311Google Scholar
  152. Ohta S, Usami S, Ueki J, Kumashiro T, Komari T and Burnell JN (1997) Identification of the amino acid residues responsible for cold tolerance in Flaveria brownii pyruvate, orthophosphate dikinase. FEBS Lett 403: 5–9PubMedGoogle Scholar
  153. Ohta S, Ishida Y and Usami S (2004) Expression of cold-tolerant pyruvate, orthophosphate dikinase cDNA, and heterotetramer formation in transgenic maize plants. Transgenic Res 13: 475–485PubMedGoogle Scholar
  154. Ohta S, Ishida Y and Usami S (2006) High-level expression of cold-tolerant pyruvate, orthophosphate dikinase from a genomic clone with site-directed mutations in transgenic maize. Mol Breed 18: 29–38Google Scholar
  155. Osborne CP, Wythe EJ, Ibrahim DG, Gilbert ME and Ripley BS (2008) Low temperature effects on leaf physiology and survivorship in the C3 and C4 subspecies of Alloteropsis semialata. J Exp Bot 59: 1743–1754PubMedGoogle Scholar
  156. Osmond CB, Bjorkman O and Anderson DJ (1980). Physiological Processes in Plant Ecology: Toward a Synthesis with Atriplex. Springer, BerlinGoogle Scholar
  157. Osmond CB, Winter K and Ziegler H (1982) Functional significance of different pathways of CO2 fixation in photosynthesis. In: Lange OL Nobel PS, Osmond CB and Ziegler H (eds) Physiological Plant Ecology II: Water Relations and Carbon Assimilation, Encyclopedia of Plant Physiology New Series, Vol. 12B, pp 480–547. Springer-Verlag, BerlinGoogle Scholar
  158. Paruelo JM and Lauenroth WK (1996) Relative abundance of plant functional types in grasslands and shrublands of North America. Ecol Appl 6: 1212–1224Google Scholar
  159. Paruelo JM, Jobbagy EG, Sala OE, Lauenroth WK and Burke IC (1998) Functional and structural convergence of temperate grassland and shrubland ecosystems. Ecol Appl 8: 194–206Google Scholar
  160. Pearcy RW and Harrison AT (1974) Comparative photosynthetic and respiratory gas exchange characteristics of Atriplex lentiformis (Torr.) Wats. in coastal and desert habitats. Ecology 55: 1104–1111Google Scholar
  161. Pearcy RW (1977) Acclimation of photosynthetic and respiratory carbon-dioxide exchange to growth temperature in Atriplex lentiformis (Torr) Wats. Plant Physiol 59: 795–799PubMedGoogle Scholar
  162. Pearcy RW, Tumosa N and Williams K (1981) Relationships between growth, photosynthesis and competitive interactions for a C3 plant and a C4 Plant. Oecologia 48: 371–376Google Scholar
  163. Pearcy RW and Ehleringer J (1984) Comparative ecophysiology of C3 and C4 plants. Plant Cell Environ 7: 1–13Google Scholar
  164. Pittermann J and Sage RF (2000) Photosynthetic performance at low temperature of Bouteloua gracilis Lag., a high-altitude C4 grass from the Rocky Mountains, USA. Plant Cell Environ 23: 811–823Google Scholar
  165. Pittermann J and Sage RF (2001) The response of the high altitude C4 grass Muhlenbergia montana (Nutt.) AS Hitchc. to long- and short-term chilling. J Exp Bot 52: 829–838PubMedGoogle Scholar
  166. Postl WF and Bolhar-Nordenkampf (1993) ‘GASEX’: a program to study the influence of data variations on calculated rates of photosynthesis and transpiration. In: Hall DO, Scurlock JMO, Bolhar-Nordenkampf HR, Leegood RC and Long SP (eds) Photosynthesis and Production in a Changing Environment, A Field and Laboratory Manual, pp 448–455. Chapman & Hall, LondonGoogle Scholar
  167. Potvin C, Simon JP and Strain BR (1986) Effect of low-temperature on the photosynthetic metabolism of the C4 Grass Echinochloa crus-galli. Oecologia 69: 499–506Google Scholar
  168. Pyankov VI, Voznesenskaya EV, Kuzmin AN, Demidov ED, Vasilev AA and Dzyubenko OA (1992) C4 photosynthesis in alpine species of the Pamirs. Sov Plant Physiol 39: 421–430Google Scholar
  169. Pyankov VI (1993) C4 species of high-mountain deserts of eastern Pamir. Russ J Ecol 24: 156–160Google Scholar
  170. Pyankov VI and Vosnesenskaya E (1995) The occurrence and structural-biochemical features of the C4 alpine plants of the Pamir Mountains. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol IV, pp 805–808. Kluwer, Dordrecht, The NetherlandsGoogle Scholar
  171. Pyankov VI, Gunin PD, Tsoog S and Black CC (2000) C4 plants in the vegetation of Mongolia: their natural occurrence and geographical distribution in relation to climate. Oecologia 123: 15–31Google Scholar
  172. Raven PH, Evert RF and Eichorn SE (1999) Biology of Plants, sixth ed. Freemann/Worth, New YorkGoogle Scholar
  173. Rowley JA, Tunniclifee CG and Taylor AO (1975) Freezing sensitivity of leaf tissue of C4 grasses. Aust J Plant Physiol. 2: 447–451Google Scholar
  174. Rowley JA (1976) Development of freezing tolerance in leaves of C4 grasses. Aust J Plant Physiol 3:597–603.Google Scholar
  175. Rundel PW (1980) The ecological distribution of C4 and C3 grasses in the Hawaiian Islands. Oecologia 45: 354–359Google Scholar
  176. Sage RF, Pearcy RW and Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants. 3. Leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album L. and Amaranthus retroflexus L. Plant Physiol 85: 355–359PubMedGoogle Scholar
  177. Sage RF, Wedin DA, and Li M (1999) The biogeography of C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 313–373. Academic, San Diego, CAGoogle Scholar
  178. Sage RF and Pearcy RW (2000) The physiological ecology of C4 photosynthesis. In: Leegood RC, Sharkey TD and von Caemmerer S (eds) Photosynthesis: Physiology and Metabolism, pp 497–532. Kluwer, Dordrecht, The ­NetherlandsGoogle Scholar
  179. Sage RF (2002) Variation in the kcat of Rubisco in C3 and C4 plants and some implications for photosynthetic performance at high and low temperature. J Exp Bot 53: 609–620PubMedGoogle Scholar
  180. Sage RF and Sage TL (2002) Microsite characteristics of Muhlenbergia richardsonis (Trin.) Rydb., an alpine C4 grass from the White Mountains, California. Oecologia 132: 501–508Google Scholar
  181. Sage RF and Kubien DS (2003) Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants. Photosynth Res 77: 209–225PubMedGoogle Scholar
  182. Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161: 341–370Google Scholar
  183. Sage RF and McKown AD (2006) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? J Exp Bot 57: 303–317PubMedGoogle Scholar
  184. Sage RF and Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant Cell Environ 30: 1086–1106PubMedGoogle Scholar
  185. Sage RF, Sage TL, Pearcy RW and Borsch T (2007) The taxonomic distribution of C4 photosynthesis in Amaranthaceae sensu stricto. Am J Bot 94: 1992–2003PubMedGoogle Scholar
  186. Salisbury FB and Ross CW (1978) Plant Physiology, Second Edition. Wadsworth, Belmont, CAGoogle Scholar
  187. Salvucci ME and Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186PubMedGoogle Scholar
  188. Savitch LV, Ivanov AG, Gudynaite-Savitch L, Huner NPA and Simmonds J (2009) Effects of low temperature stress on excitation energy partitioning and photoprotection in Zea mays. Functional Plant Biology 36: 37–49Google Scholar
  189. Sayed OH and Mohamed MK (2000) Altitudinal changes in photosynthetic pathways of floristic elements in southern Sinai, Egypt. Photosynthetica 38: 367–372Google Scholar
  190. Schmitt and Edwards GE (1981) Photosynthetic capacity and nitrogen use efficiency of maize, wheat and rice: a comparison of C3 and C4 photosynthesis. J Exp Bot 32: 459–466Google Scholar
  191. Schuster WS and Monson RK (1990) An examination of the advantages of C3-C4 intermediate photosynthesis in warm environments. Plant Cell Environ 13: 903–912Google Scholar
  192. Schwarz AG and Redmann RE (1988) C4 grasses from the boreal forest region of northwestern Canada. Can J Bot 66: 2424–2430Google Scholar
  193. Schwarz AG and Reaney MJT (1989) Perennating structures and freezing tolerance of northern and southern-populations of C4 grasses. Bot Gaz 150: 239–246Google Scholar
  194. Sharkey TD (1988) Estimating the rate of photorespiration in leaves. Physiol Plant 73: 147–152Google Scholar
  195. Shenglian L, Shouliang C and Phillips SM (2006) Aristida. In: Zhengyi W, Raven PH and Deyuan H (eds) Flora of China – Poaceae, Vol 22, pp 453–455. Missouri Botanical Garden Press, St Louis, MOGoogle Scholar
  196. Shirahashi K, Hayakawa S and Sugiyama T (1978) Cold lability of pyruvate, ortho-phosphate dikinase in a maize leaf. Plant Physiol 62: 826–830PubMedGoogle Scholar
  197. Shouliang C, Bixing S, Phillips SM, and Renvoize SA (2006a) Tribe Andropogoneae. In: Zhengyi W, Raven PH and ­Deyuan H (eds), Flora of China – Poaceae, Vol 22, pp 570–651. Missouri Botanical Garden Press, St Louis, MOGoogle Scholar
  198. Shouliang C, Zhenlan W, Shenglian L, Bixing S, Phillips SM, and Peterson PM (2006b) Tribe Eragrostideae. In: Zhengyi W, Raven PH and Deyuan H (eds), Flora of China – Poaceae, Vol 22, pp 457–487. Missouri Botanical Garden Press, St Louis, MOGoogle Scholar
  199. Shouliang C, Phillips SM and Renvoize SA (2006c) Tribe Paniceae. In: Zhengyi W, Raven PH and Deyuan H (eds), Flora of China – Poaceae, Vol 22, pp 499–554. Missouri Botanical Garden Press, St Louis, MOGoogle Scholar
  200. Siebke K, von Caemmerer S, Badger M and Furbank RT (1997) Expressing an RbcS antisense gene in transgenic Flaveria bidentis leads to an increased quantum requirement for CO2 fixed in photosystems I and II. Plant Physiol 115: 1163–1174PubMedGoogle Scholar
  201. Simon JP and Hatch MD (1994) Temperature effects on the activation and inactivation of pyruvate, Pi dikinase in two populations of the C4 weed Echinochloa crus-galli (barnyard grass) from sites of contrasting climates. Aust J Plant Physiol 21: 463–473Google Scholar
  202. Simon JP (1996) Molecular forms and kinetic properties of pyruvate, Pi dikinase from two populations of barnyard grass (Echinochloa crus-galli) from sites of contrasting climates. Aust J Plant Physiol 23: 191–199Google Scholar
  203. Smith M and Wu Y (1994) Photosynthetic characteristics of the shade-adapted C4 grass Muhlenbergia sobolifera (Muhl) Trin - control of development of photorespiration by growth temperature. Plant Cell Environ 17: 763–769Google Scholar
  204. Still CJ, Berry JA, Collatz GJ and DeFries RS (2003) Global distribution of C3 and C4 vegetation: carbon cycle implications. Glob Biogeochemical Cycles 17: 1–14Google Scholar
  205. Stock WD, Chuba DK and Verboom GA (2004) Distribution of South African C3 and C4 species of Cyperaceae in relation to climate and phylogeny. Aust Ecol 29: 313–319Google Scholar
  206. Stowe LG and Teeri JA (1978) Geographic distribution of C4 species of Dicotyledonae in relation to climate. Am Nat 112: 609–623Google Scholar
  207. Sugiyama T and Boku K (1976) Differing sensitivity of pyruvate orthophosphate dikinase to low-temperature in maize cultivars. Plant Cell Physiol 17: 851–854Google Scholar
  208. Sugiyama T, Schmitt MR, Ku SB and Edwards GE (1979) Differences in cold lability of pyruvate, pi dikinase among C4 Species. Plant Cell Physio l20: 965–971Google Scholar
  209. Takeda T (1985) Studies on the ecology and geographical-distribution of C3 and C4 grasses. 3. Geographical distribution of C3 and C4 grasses in relation to climatic conditions in the Indian subcontinent. Jpn J Crop Sci 54:365–372Google Scholar
  210. Takeda T, Tanikawa T, Agata W and Hakoyama S (1985a) Studies on the ecology and geographic distribution of C3 and C4 grasses. 1. Taxonomic and geographical distribution of C3 and C4 grasses in Japan with special reference to climatic conditions. Jpn J Crop Sci 54: 54–64Google Scholar
  211. Takeda T and Hakoyama S (1985) Studies on the ecology and geographical-distribution of C3 and C4 grasses. 2. Geographical distribution of C3 and C4 grasses in Far-East and South East-Asia. Jpn J Crop Sci 54: 65–71Google Scholar
  212. Takeda T, Ueno O, Samejima M and Ohtani T (1985b) An investigation for the occurrence of C4 photosynthesis in the Cyperaceae from Australia. Bot Mag Tokyo 98: 393–411Google Scholar
  213. Taylor AO, Slack CR and McPherson HG (1974) Plants under climatic stress. 6. Chilling and light effects on photosynthetic enzymes of sorghum and maize. Plant Physiol 54: 696–701PubMedGoogle Scholar
  214. Teeri JA and Stowe LG (1976) Climatic patterns and distribution of C4 grasses in North-America. Oecologia 23: 1–12Google Scholar
  215. Tieszen LL and Detling JK (1983) Productivity of grassland and tundra. In: Lange OL, Nobel PS, Osmond CB and ­Ziegler H (eds) Physiological Plant Ecology IV: Ecosystem Processes, Productivity, and Man’s Influence. Encyclopedia of Plant Physiology New Series, Vol 12D, pp. 173–203. Springer-Verlag, BerlinGoogle Scholar
  216. Tieszen LL, Senyimba MM, Imbamba SK and Troughton JH (1979) Distribution of C3 grass and C4 grass and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37: 337–350Google Scholar
  217. Tieszen LL, Reed BC, Bliss NB, Wylie BK and DeJong DD (1997) NDVI, C3 and C4 production, and distributions in great plains grassland land cover classes. Ecol Appl 7: 59–78Google Scholar
  218. Trevanion SJ, Ashton AR and Furbank RT (1999) Antisense RNA inhibition of pyruvate, orthophosphate dikinase and NADP malate dehydrogenase in the C4 plant Flaveria bidentis: analysis of plants with a mosaic phenotype. Aust J Plant Physiol 26: 537–547Google Scholar
  219. Ueno O and Takeda T (1992) Photosynthetic pathways, ecological characteristics, and the geographical-distribution of the Cyperaceae in Japan. Oecologia 89: 195–203Google Scholar
  220. Ueno O, Yoshimura Y and Sentoku N (2005) Variation in the activity of some enzymes of photorespiratory metabolism in C4 grasses. Ann Bot 96: 863–869PubMedGoogle Scholar
  221. Usami S, Ohta S, Komari T and Burnell JN (1995) Cold stability of pyruvate, orthophosphate dikinase of Flaveria-Brownii. Plant Mol Biol 27: 969–980PubMedGoogle Scholar
  222. Usuda H, Ku MSB and Edwards GE (1984) Activation of NADP malate dehydrogenase, pyruvate,pi dikinase, and fructose 1,6-bisphosphatase in relation to photosynthetic rate in maize. Plant Physiol 76: 238–243PubMedGoogle Scholar
  223. Vicentini A, Barber JC, Aliscioni SS, Giussani LM and ­Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Change Biol 14: 2963–2977Google Scholar
  224. Vogel JC, Fuls A and Ellis RP (1978) Geographical distribution of Kranz grasses in South-Africa. S Afr J Sci 74: 209–215Google Scholar
  225. Volk RJ and Jackson WA (1972) Photorespiratory phenomena in maize – oxygen uptake, isotope discrimination, and carbon-dioxide efflux. Plant Physiol 49: 218–223PubMedGoogle Scholar
  226. von Caemmerer S and Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas-exchange of leaves. Planta 153: 376–387Google Scholar
  227. von Caemmerer S and Furbank RT (1999) Modeling C4 photosynthesis. In: Sage RF and Monson RK (eds) C4 Plant Biology, pp 173–211. Academic, San Diego, CAGoogle Scholar
  228. von Caemmerer S (2000). Biochemical Models of Leaf ­Photosynthesis. CSIRO, CollingwoodGoogle Scholar
  229. von B. Ruthsatz T and Hofmann U (1984) Die verbreitung von C4-Pflanzen in den semiariden Anden NW-Argentiniens, mit eine Beitrag zer Blattananatomie ausgewahlter Beispiele. Phytocoenologia 12:219–249Google Scholar
  230. von Fischer JC, Tieszen LL and Schimel DS (2008) Climate controls on C3 vs. C4 productivity in North American grasslands from carbon isotope composition of soil organic matter. Glob Change Biol 14: 1141–1155Google Scholar
  231. Vong N and Murata Y (1977) Studies on the physiological characteristics of C3 and C4 crop species. I. The effects of air temperature on the apparent photosynthesis, dark respiration, and nutrient absorption of some crops. Japanese J Crop Sci 46:45–52Google Scholar
  232. Vong NQ and Murata Y (1978) Studies on physiological characteristics of C3 and C4 crop species. 2. Effects of air temperature and solar-radiation on dry-matter production of some crops. Jpn J Crop Sci 47: 90–100Google Scholar
  233. Walker DJ, Romero O, de Hoyos A, Correal E (2008) Seasonal changes in cold tolerance, water relations and accumulation of cations and compatible solutes in Atriplex halimus L. Environ Exp Bot 64:217–224Google Scholar
  234. Wall DA (1993) Comparison of green foxtail (Setaria viridis) and wild oat (Avena fatua) growth, development, and competitiveness under three temperature regimes. Weed Sci 41: 369–378Google Scholar
  235. Wan CSM and Sage RF (2001) Climate and the distribution of C4 grasses along the Atlantic and Pacific coasts of North America. Can J Bot 79: 474–486Google Scholar
  236. Wang D, Naidu SL, Portis AR, Moose SP and Long SP (2008a) Can the cold tolerance of C4 photosynthesis in Miscanthus x giganteus relative to Zea mays be explained by differences in activities and thermal properties of Rubisco? J Exp Bot 59: 1779–1787PubMedGoogle Scholar
  237. Wang DF, Portis AR, Moose SP and Long SP (2008b) Cool C4 photosynthesis: pyruvate Pi dikinase expression and activity corresponds to the exceptional cold tolerance of carbon assimilation in Miscanthus x giganteus. Plant Physiol 148: 557–567PubMedGoogle Scholar
  238. Wang L, Lu HY, Wu NG, Chu D, Han JM, Wu YH, Wu HB and Gu ZY (2004) Discovery of C4 species at high altitude in Qinghai-Tibetan plateau. Chin Sci Bull 49: 1392–1396Google Scholar
  239. Wang RZ (2003) C4 plants in the vegetation of Tibet, China: their natural occurrence and altitude distribution pattern. Photosynthetica 41: 21–26Google Scholar
  240. Ward JK, Myers DA and Thomas RB (2008) Physiological and growth responses of C3 and C4 plants to reduced temperature when grown at low CO2 of the last ice age. J Int Plant Biol 50: 1388–1395Google Scholar
  241. Welsh SL (2003) Atriplex In: Flora of North America ­Committee (eds) Flora of North America North of Mexico, Vol 4, Magnoliophyta: Caryophyllidae, part 1, pp 322–381. Oxford University Press, OxfordGoogle Scholar
  242. Williams GJ (1974) Photosynthetic adaptation to temperature in C3 and C4 grasses – possible ecological role in shortgrass prairie. Plant Physiol 54: 709–711PubMedGoogle Scholar
  243. Wynn JG and Bird MI (2008) Environmental controls on the stable carbon isotopic composition of soil organic carbon: implications for modelling the distribution of C3 and C4 plants, Australia. Tellus Series B – Chem Phys Meteor 60: 604–621Google Scholar
  244. Yamazaki K and Sugiyama T (1984) Factor(s) protecting ­pyruvate ortho-phosphate dikinase of Panicum maximum against cold-inactivation. Plant Cell Physiol 25: 1319–1322Google Scholar
  245. Yoshimura Y, Kubota F and Ueno O (2004) Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase. Planta 220: 307–317PubMedGoogle Scholar
  246. Young HJ and Young TP (1983) Local distribution of C3 and C4 grasses in sites of overlap on Mount Kenya. Oecologia 58: 373–377Google Scholar
  247. Zacharias EH (2007) Evolutionary Studies in American Atripliceae (Chenopodiaceae). PhD thesis, University of California, Berkeley, CAGoogle Scholar
  248. Zuloaga FO and Morrone O (eds) (1999a) Catalago de las Plantes Vasculares de la Republica Argentina II. Acanthaceae-Euphorbiaceae (Dicotyledonae). Missouri Botanical Garden Press, St. Louis, MOGoogle Scholar
  249. Zuloaga FO and Morrone O (eds) (1999b) Catalago de las Plantes Vasculares de la Republica Argentina II. Fabaceae-Zygophyllaceae (Dicotyledonae). Missouri Botanical Garden Press, St. Louis, MOGoogle Scholar

Copyright information

© Springer Netherlands 2010

Authors and Affiliations

  • Rowan F. Sage
    • 1
  • Ferit Kocacinar
    • 2
  • David S. Kubien
    • 3
  1. 1.Department of Ecology and Evolutionary BiologyThe University of TorontoTorontoCanada
  2. 2.Faculty of ForestryKahramanmaras Sutcu Imam UniversityKahramanmarasTurkey
  3. 3.Department of BiologyUniversity of New BrunswickFrederictonCanada

Personalised recommendations