Skip to main content
Log in

Some aspects of the evolution of C4 photosynthesis

Einige Aspekte der Evolution des C4-Weges der Photosynthese

Некоторые аспекты эволюции C4-нути фотосинтеза

  • N. I. Vavilov — Symposium Zum 100. Geburtstag Von N.I. Vavilov Gatersleben, 8.–10. Dezember 1987
  • Published:
Die Kulturpflanze Aims and scope Submit manuscript

Summary

C4 photosynthesis occurs in at least 18 families of angiosperms. To our current knowledge it is lacking among the gymnosperms.

It seems to be appropriate assuming a polyphyletic origin of this syndrome of anatomical and metabolical traits during the course of angiosperm evolution, e. g. since the Cretaceaous period.

C4 photosynthesis per se is an adaptation of plants to hot and dry environments or in some cases to salinity.

Speculations about number and sequence of steps during the evolution of C4 species from ancestors with C3 photosynthesis should be based on careful comparisons of anatomical as well as biochemical features of related species with different photosynthetic pathways. Thinking about evolutionary problems with regard to C4 photosynthesis was much influenced by the discovery of C3–C4 intermediate species. These were thought to be on the way of evolution from C3 to C4 photosynthesis. Best investigated is the genusFlaveria (Asteraceae), which contains C3, C4 and C3–C4 intermediate species, respectively. Therefore a detailed description of the situation within this genus is given.

The genetic distance between C3 and C4 and the driving forces for selection of C4 genotypes in a given environment has to be elucidated by further investigations. Among those the analysis of hybrids between C3 and C4 species of the genusFlaveria may be a helpful approach.

Zusammenfassung

Vertreter des C4-Weges der Photosynthese sind von mindestens 18 Familien der Angiospermen bekannt. Innerhalb der Gymnospermen kommt dieser Photo-synthesetyp nicht vor.

Auf Grund der systematischen Verbreitung des C4-Syndroms muß ein poly-phyletischer Ursprung angenommen werden.

C4-Photosynthese ist eine Anpassung der Pflanzen an heiße und aride Bedingungen und in einigen Fällen an hohe Salzgehalte.

Abschätzungen über die Zahl und Sequenz der Mutationen während der Evolution von C4-Arten sollten basieren auf einem sorgfältigen Vergleich anatomischer und biochemischer Eigenschaften verwandter C3- und C4-Arten. Sie können allerdings nur einen groben Anhaltspunkt liefern.

C3-C4 intermediäre Arten können aufgefaßt werden als Zwischenglieder der Evolution von der C3- zur C4-Photosynthese. Arten der GattungFlaveria sind hier besonders gut untersuchte Beispiele.

Auch die Analyse von Hybriden zwischen C3- und C4-Arten vermag einen gewissen Aufschluß über die genetische Distanz zwischen Vertretern der beiden Photosynthesetypen zu geben.

Es werden einige Überlegungen über Mechanismen der Evolution des C4-Syndroms angestellt.

Краткое содержание

Иредставители C4-иути фотосинтеза известны, самое меньшее, у 18 семейств иокрытосеменных. Среди голосеменных этот тин фотосинтеза не существует.

На основе систематического распространения C4-синдрома, следует иредиоложить полифилетическое происхождение.

C4-фотосинтез является проявлением приснособления растений к жарким, сухим условиям и, в некоторых случаях, к высокой засоленности.

Оценки о числе и последовательности мутаций во время эволюции C4-видов должны основываться на тщательном сравнении анатомических и биохимических свойств подственных C3- и C4-видов. Однако, они могут иредоставить лишь грубую исходную точку.

C3–C4 промежуточные виды следует ионимать как промежуточные члены эволюции C3- и C4-фотосинтеза. Виды родаFlaveria представляют здесь особо хорошо изученные примеры.

Анализы гибридов между C3- и C4-видами могут также дать оиределенной объяснение о генетической дистанции между представителями обоих фотосинтетических типов.

Делаются некоторые размышления о механизме эволюции C4-снидрома.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature

  • Adams, C. A., F. Leung, andS. S. M. Sun, 1966: Molecular properties of phosphoenolpyruvate carboxylase from C3, C3–C4 intermediate and C4 Flaveria species. — Planta167, 218–225.

    Google Scholar 

  • Akin, D. E., andD. Burdick, 1977: Rumen microbial degradation of starch containing bundle sheath cells in warm seasons grasses. — Crop Sci.17, 529–533.

    Google Scholar 

  • ——, andW. R. Windham, 1983: Site and rate of tissue digestion in leaves of C3, C4 and C3 C4 intermediatePanicum species. — Crop Sci.23, 147–155.

    Google Scholar 

  • Apel, P., 1986: Intrageneric hybrids within the genusFlaveria Juss. (Asteraceae). — Kulturpflanze34, 177–184.

    Google Scholar 

  • ——, andM. Peisker, 1985: Beziehungen zwischen Kohlenstoff und Stickstoffmetabolismus bei Pflanzen — eine Übersicht über ausgewählte Aspekte. — Kulturpflanze33, 41–72.

    Google Scholar 

  • ——, andI. Maass, 1988: Photosynthetic properties ofFlaveria cronquistii, F. palmeri and hybrids between them. — Biochem. Physiol. Pflanzen183, 291–299.

    Google Scholar 

  • ——, andI. Maass, 1981: Photosynthesis in species ofFlaveria: CO2 compensation concentration, O2 influence on photosynthetic gas exchange andδ 13C values in species ofFlaveria (Asteraceae). — Biochem. Physiol. Pflanzen176, 396–399.

    Google Scholar 

  • ——, undM. Peisker, 1979: Pflanzenarten mit intermediärer Merkmalsausprägung in bezug auf den C3- und C4-pathway der Photosynthese. — Kulturpflanze27, 49–66.

    Google Scholar 

  • ——, undM. Peisker, 1978: CO3-Kompensationspunkt vonMoricandia arvensis (L.) DC bei Blättern unterschiedlicher Insertionshöhe und bei verschiedenen O2-Konzentrationen. — Biochem. Physiol. Pflanze172, 547–552.

    Google Scholar 

  • Bassüner, B., O. Keerberg, H. Bauwe, T. Pärnik, andH. Keerberg, 1984: Photosynthetic C metabolism in C3–C4 intermediate and C4 species ofFlaveria (Asteraceae). — Biochem. Physiol. Pflanzen179, 631–634.

    Google Scholar 

  • Bauwe, H., 1984: Photosynthetic enzyme activities and immunofluorescence studies on the localization of ribulose-1,5-biophosphate carboxylase oxygenase in leaves of C3, C4, and C3–C4 intermediate species ofFlaveria (Asteraceae). — Biochem. Physiol. Pflanzen179, 253–268.

    Google Scholar 

  • ——, 1987: Untersuchungen zur Evolution des C4-Weges der Photosynthese unter besonderer Berücksichtigung des Photosynthesestoffwechsels C3–C4-intermediärer Arten der GattungenMoricandia undFlaveria. — Diss. B, AdW der DDR, Berlin.

    Google Scholar 

  • ——, andP. Apel, 1979: Biochemical characterization ofMoricandia arvensis (L.) DC., a species with features intermediate between C3 and C4 photosynthesis, in comparison with the C3 speciesMoricandia foetida Bourg. — Biochem. Physiol. Pflanzen174, 251–254.

    Google Scholar 

  • ——, andR. Chollet, 1986: Kinetic properties of phosphoenolpyruvate carboxylase from C3, C4, and C3–C4 intermediate species ofFlaveria (Asteraceae). — Plant Physiol.82, 695–699.

    Google Scholar 

  • Björkman, O., 1976: Adaptive and genetic aspects of C4 photosynthesis. In: CO2 Metabolism and Plant Productivity (Eds.R. H. Burris andG. C. Black), pp. 287–309. — Univ. Park Press, Baltimore — London — Tokyo.

    Google Scholar 

  • Bolton, J. K., andR. H. Brown, 1980: Photosynthesis of grass species differing in carbon dioxide fixation pathways. V. Response ofPanicum maximum, Panicum milioides, and tall fescue (Festuca arundinacea) to nitrogen nutrition. — Plant Physiol.66, 97–100.

    Google Scholar 

  • Boutton, T. W., G. N. Cameron, andB. N. Smith, 1978: Insect herbivory on C3 and C4 grasses. — Oecologia36, 21–32.

    Google Scholar 

  • Brown, R. H., 1976: Characteristics related to photosynthesis and photorespiration ofPanicum milioides. In: CO2 Metabolism and Plant Productivity (Eds.R. H. Burris andC. C. Black) pp. 311–325. — University Park Press. Baltimore — London — Tokyo.

    Google Scholar 

  • ——, 1978: A difference in N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. — Crop Sci.18, 93–98.

    Google Scholar 

  • ——, 1985: Growth of C3 and C4 grasses under low N levels. — Crop Sci.25, 954–957.

    Google Scholar 

  • ——, andM. Deniro, 1986: Photosynthesis of F2 hybrids between C4 and C3–C4 species ofFlaveria. — Plant Physiol.82, 211–217.

    Google Scholar 

  • ——, andW. V. Brown, 1975: Photosynthetic characteristics ofPanicum milioides, a species with reduced photorespiration. — Crop Sci.15, 681–685.

    Google Scholar 

  • Caswell, H., andF. C. Reed, 1976: Plant herbivore interactions: The indigestibility of C4 bundle sheath cell by grasshoppers. — Oecologia26, 151–156.

    Google Scholar 

  • Cock, J. H., N. M. Riano, M. A. El-Sharkawy, Y. Lopez, andG. Bastidas, 1987: C3–C4 untermediate photosynthetic characteristics of cassava (Manihot esculenta Crantz) II. Initial products of14CO2 fixation. — Photosynth. Res.12, 237–241.

    Google Scholar 

  • Downton, W. J. S., 1975: The occurrence of C4 photosynthesis among plants. — Photosynthetica9, 96–105.

    Google Scholar 

  • Edwards, G., andD. Walker, 1983: C3, C4: Mechanism, and Cellular and Environmental Regulation of Photosynthesis. — Blackwell Sci. Publ., Oxford.

    Google Scholar 

  • El-Sharkawy, M. A., andJ. H. Cock, 1987: C3–C4 intermediate photosynthetic characteristics of cassava(Manihot esculenta Crantz) 1. Gas exchange. — Photosynthesis Res.12, 219–235.

    Google Scholar 

  • Gifford, R. M., andJ. I. L. Morison 1985: Photosynthesis, water use and growth of a C4 grass stand at high CO2 concentration. — Photosynthesis Res.7, 69–76.

    Google Scholar 

  • Goldstein, L. D., T. B. Ray, D. P. Kestler, B. C. Mayne, R. H. Brown, C. C. Black, 1976: Biochemical characterization ofPanicum species which are intermediate between C3 and C4 photosynthesis plant. — Plant Sci. Letters6, 85–90.

    Google Scholar 

  • Hattersley, P. W., andA. J. Browning, 1981: Occurrence of the suberized lamella in leaves of grasses of different photosynthetic type 1. In parenchymatous bundle sheath and PCR (‘Kranz’) sheaths. — Protoplasma109, 371–401.

    Google Scholar 

  • ——, andS. Perry, 1984: Occurrence of the suberized lamella in leaves of grasses of different photosynthetic type. II. In herbarium material. — Aust. J. Bot.32, 465–473.

    Google Scholar 

  • ——, andZ. Roksandic, 1983:δ 13C values of C3 and C4 species of australianNeurachne and its allies (Poaceae). — Austr. J. Bot.31, 317–321.

    Google Scholar 

  • Holaday, A. S., andR. Chollet, 1984: Photosynthetic photorespiratory characteristics of C3–C4 intermediate species. — Photosynthesis Res.5, 307–323.

    Google Scholar 

  • ——, andM. E. Doohan, 1985: Anatomical and enzyme studies of leaves of a C3 × C4 hybrid exhibiting reduced photorespiration. — Plant Sci.41, 31–39.

    Google Scholar 

  • Jones, C. A., 1985: C4 Grasses and Cereals. Growth, development and stress response. — John Wiley and Sons, New York.

    Google Scholar 

  • Kanai, R., andM. Kashiwagi, 1975:Panicum milioides, a Gramineae plant having Kranz leaf anatomy without C4-photosynthesis. — Plant and Cell Physiol.16, 669–679.

    Google Scholar 

  • Kennedy, R. A., andW. M. Laetsch, 1974: Plant species intermediate for C3, C4 photosynthesis. — Science184, 1087–1089.

    Google Scholar 

  • Krenzer, E. G., D. N. Moss andR. K. Crookston, 1975: Carbon dioxide compensation points of flowering plants. — Plant Physiol.56, 194–206.

    Google Scholar 

  • Ku, S. B., andG. E. Edwards, 1978: Photosynthetic efficiency ofPanicum hians andPanicum milioides in relation to C3 and C4 plants. — Plant and Cell Physiol.19, 665–675.

    Google Scholar 

  • Long, S. P., 1983: C4 photosynthesis at low temperature. — Plant, Cell and Environ.6, 345–363.

    Google Scholar 

  • Ludlow, M. M., 1985: Photosynthesis and dry matter production in C3 and C4 pasture plants with special emphasis in tropical C3 legumes and C4 grasses. — Aust. J. Plant Physiol.12, 557–572.

    Google Scholar 

  • Monson, R. K., B. D. Moore, M. S. B. Ku, andG. E. Edwards, 1986: Co-function of C3- and C4-photosynthetic pathways in C3, C4 and C3–C4 intermediate Flaveria species. — Planta168, 493–502.

    Google Scholar 

  • Nakamoto, H., M. S. B. Ku, andG. E. Edwards, 1983: Photosynthetic characteristics of C3–C4 intermediateFlaveria species II. Kinetic properties of phosphoenolpyruvate carboxylase from C3, C4 and C3–C4 intermediate species. — Plant and Cell Physiol.24, 1387–1393.

    Google Scholar 

  • Nambudiri, E. M. V., W. D. Tidwell, B. N. Smith, andN. P. Hebberd, 1978: A C4 plant from the Pliocene. — Nature276, 816–817.

    Google Scholar 

  • Oeschger, H., andB. Stauffer, 1986: Review of the history of atmospheric CO2 recorded in ice cores. In: The Changing Carbon Cycle—a global analysis. (Eds.J. R. Trabalka andD. E. Reichle), pp. 89–108. — Springer-Verlag, Berlin.

    Google Scholar 

  • Okuda, T., 1986: Effects of herbivores on the competition of C3 and C4 graminoids. — J. Sci. Hiroshima Univ., Ser. B, Div. 2 (Bot.)20, 1–27.

    Google Scholar 

  • Olson, J. M., andB. K. Pierson, 1986: Photosynthesis 3,5 thousand million years ago. — Photosynthesis Res.9, 251–259.

    Google Scholar 

  • Osmond, C. B., O. Björkman, andD. J. Anderson, 1980: Physiological Processes in Plant Ecology — Towards a Synthesis withAtriplex. — Springer-Verlag, Berlin.

    Google Scholar 

  • ——, andH. Ziegler, 1982: Functional significance of different pathways of CO2 fixation in photosynthesis. In: Encyclopedia of Plant Physiology (Eds.O. L. Lange, P. S. Nobel, C. B. Osmond andH. Ziegler). New Ser., vol.12B, Physiological Plant Ecology 11, pp. 479–547. — Springer-Verlag, Berlin.

    Google Scholar 

  • Patil, T. M., andB. A. Hedge, 1983: Pattern of starch distribution, carbon dioxide compensation concentration, and photochemical reduction of tetranitro tetrazolium blue inParthenium hysterophorus L. — Photosynthetica17, 64–68.

    Google Scholar 

  • Peisker, M., 1986: Models of carbon metabolism in C3–C4 intermediate plants as applied to the evolution of C4 photosynthesis. — Plant, Cell and Environment9, 627–635.

    Google Scholar 

  • Potvin, C., 1986: Differences in photosynthetic characteristics among northern and southern C4 plants. — Physiol. Plant,69, 659–664.

    Google Scholar 

  • Powell, A. M., 1978: Systematics ofFlaveria (Flaveriinae-Asteraceae). — Ann. Missouri Bot. Gard.65, 590–636.

    Google Scholar 

  • Raghavendra, A. S., 1980: Characteristics of plant species intermediate between C3 and C4 pathways of photosynthesis: their focus of mechanism and evolution of C4 syndrome. — Photosynthetica14, 271–283.

    Google Scholar 

  • ——, andV. S. R. Das, 1978: The occurrence of C4 photosynthesis: a supplementary list of C4 plants reported during late 1974-mid 1977. — Photosynthetica12, 200–208.

    Google Scholar 

  • Rajendrudu, G., J. S. R. Prasad, andV. S. M. Das, 1986: C3–C4 intermediate species inAlternanthera (Amaranthaceae): leaf anatomy, CO2 compensation point, net CO2 exchange and activities of photosynthetic enzymes. — Plant Physiol.80, 409–414.

    Google Scholar 

  • Rathnam-Chaguturu, C. K. M., 1981: C3–C4 intermediate species. — What's New in Plant Physiol.12, 21–24.

    Google Scholar 

  • Rathnam, C. K. M., andR. Chollet, 1980: Photosynthetic carbon metabolism in C4 plants and C3–C4 intermediate species. — Progr. Phytochem.6, 1–48.

    Google Scholar 

  • Rawsthorne, S., Ch. M. Hylton, A. M. Smith, andH. W. Woolhouse, 1988: Photo-respiratory metabolism and immunogold localization of photorespiratory enzymes in leaves of C3 and C3–C4 intermediate species ofMoricandia. — Planta, in press.

  • Reed, J. E., andR. Chollet, 1985: Immunofluorescent localization of phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase oxygenase protein in leaves of C3, C4, and C3–C4 intermediateFlaveria species. — Planta165, 439–445.

    Google Scholar 

  • Rumpho, M. E., M. S. B. Ku, S. H. Cheng, andG. E. Edwards, 1984: Photosynthetic characteristics of C3–C4 intermediateFlaveria species. — Plant Physiol.75, 993–996.

    Google Scholar 

  • Sabale, A. B., andJ. L. Bhosale, 1984: C3–C4 photosynthesis inBougainvillea cv. Mary Palmer. — Photosynthetica18, 84–89.

    Google Scholar 

  • Schmitt, M. R., andG. E. Edwards, 1981: Photosynthetic capacity and nitrogen use efficiency of maize, wheat and rice: A comparison between C3 and C4 photosynthesis. — J. Exp. Bot.32, 459–466.

    Google Scholar 

  • Stamp, P., 1984: Chilling tolerance of young plants demonstrated on the example of maize (Zea mays L.). — Suppl.7 to J. Agron. and Crop. Sci.

  • ——, 1987a: Seedling development of adapted and exotic maize genotypes at severe childling stress. — J. Exp. Bot.38, 1336–1342.

    Google Scholar 

  • ——, 1987b: The expression of photosynthetic traits during and following severe chilling stress of European and tropical maize genotypes. — Physiol. Plant.71, 73–76.

    Google Scholar 

  • ——, 1987c: Seedling development of maize genotypes at constant and at fluctuating temperatures. — J. Agron. and Crop. Sci.158, 289–293.

    Google Scholar 

  • Takeda, T., T. Tanikawa, W. Agata, andS. Hakoyama, 1985. Studies on the ecology and geographical distribution of C3 and C4 grasses. — Japan. J. Crop. Sci.54, 54–71.

    Google Scholar 

  • Teeri, J. A., andJ. G. Stowe, 1976: Climatic patterns and the distribution of C4 grasses in North America. — Oecologia23, 1–12.

    Google Scholar 

  • ter Hazeborg, E., andG. Geisler, 1983a: Das Wachstum von C3- und C4-Getreidearten in Abhängigkeit von der Stickstoffversorgung. — Z. Acker- und Pflanzenbau152, 116–124.

    Google Scholar 

  • ——, and ——, 1983b: Die Effizienz der Stickstoffassimilation von C3- und C4-Getreidearten in Abhängigkeit von der Stickstoffversorgung. — Z. Acker- und Pflanzenbau152, 300–309.

    Google Scholar 

  • Thomasson, J. R., M. E. Nelson, andR. J. Zakrzewski, 1986: A fossil grass (Gramineae: Chloridoideae) from the Miocene with Kranz anatomy. — Science233, 876–878.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Apel, P. Some aspects of the evolution of C4 photosynthesis. Die Kulturpflanze 36, 225–236 (1988). https://doi.org/10.1007/BF01986962

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01986962

Keywords

Navigation