Download PDF
Plant Biol (Stuttg) 2006; 8(2): 253-259
DOI: 10.1055/s-2005-873050
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Evidence from Photosynthetic Characteristics for the Hybrid Origin of Diplotaxis muralis from a C3-C4 Intermediate and a C3 Species

O. Ueno1 , Y. Wada2 , M. Wakai2 , S. W. Bang2
  • 1Plant Physiology Department, National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
  • 2Faculty of Agriculture, Utsunomiya University, Minemachi 350, Utsunomiya 321-8505, Japan
Further Information

Publication History

Received: October 10, 2005

Accepted: November 14, 2005

Publication Date:
17 March 2006 (online)

   Permissions and Reprints

Abstract

Artificial hybridization studies have been carried out between plants with different photosynthetic types to study the genetic mechanism of photosynthetic types. However, there are only few reports describing the possibility of natural hybridization between plants with different photosynthetic types. A previous cytological and morphological study suggested that a cruciferous allotetraploid species, Diplotaxis muralis (L.) DC. (2n = 42), originated from natural hybridization between D. tenuifolia (L.) DC. (2n = 22) and D. viminea (L.) DC. (2n = 20). These putative parents have recently been reported to be a C3-C4 intermediate and a C3 species, respectively. If this hybridization occurred, D. muralis should have characteristics intermediate between those of the C3-C4 intermediate and C3 types. We compared leaf structures and photosynthetic characteristics of the three species. The bundle sheath (BS) cells in D. tenuifolia included many centripetally located chloroplasts and mitochondria, but those of D. viminea had only a few organelles. The BS cells in D. muralis displayed intermediate features between the putative parents. Glycine decarboxylase P protein was confined to the BS mitochondria in D. tenuifolia, but accumulated mainly in the mesophyll mitochondria in D. viminea. In D. muralis, it accumulated in both the BS and the mesophyll mitochondria. Values of CO2 compensation point and its response to changing light intensity were also intermediate between the putative parents. These data support the theory that D. muralis was created by natural hybridization between species with different photosynthetic types.

Key words

CO2 gas exchange - leaf anatomy - hybrid speciation - glycine decarboxylase - Diplotaxis muralis - C3-C4 intermediate species - C3 species

References

  • 1 Apel P.. Carbon metabolism type of Diplotaxis tenuifolia (L.) DC. (Brassicaceae).  Photosynthetica. (1996);  32 237-243
    PubMedGoogle Scholar
  • 2 Apel P., Bauwe H., Ohle H.. Hybrids between Brassica alboglabra and Moricandia arvensis and their photosynthetic properties.  Biochemische und Physiologie der Pflanzen. (1984);  179 793-797
    PubMedGoogle Scholar
  • 3 Apel P., Horstmann C., Pfeffer M.. The Moricandia syndrome in species of the Brassicaceae: evolutionary aspects.  Photosynthetica. (1997);  33 205-215
    CrossrefPubMedGoogle Scholar
  • 4 Bang S. W., Kaneko Y., Matsuzawa Y.. Production of intergeneric hybrids between Raphanus and Moricandia.  Plant Breeding. (1996);  115 385-390
    PubMedGoogle Scholar
  • 5 Bang S. W., Mizuno Y., Kaneko Y., Matsuzawa Y., Bang K. S.. Production of intergeneric hybrids between the C3-C4 intermediate species Diplotaxis tenuifolia (L.) DC. and Raphanus sativus L.  Breeding Science. (2003);  53 231-236
    CrossrefPubMedGoogle Scholar
  • 6 Björkman O.. Adaptive and genetic aspects of C4 photosynthesis. Burris, R. H. and Black, C. C., eds. CO2 Metabolism and Plant Productivity. Baltimore; University Park Press (1976): 287-309
    Google Scholar
  • 7 Brown R. H., Bouton J. H.. Physiology and genetics of interspecific hybrids between photosynthetic types.  Annual Review of Plant Physiology and Plant Molecular Biology. (1993);  44 435-456
    PubMedGoogle Scholar
  • 8 Douce R., Bourguignon J., Neuburger M., Rebeille F.. The glycine decarboxylase system: a fascinating complex.  Trends in Plant Science. (2001);  6 167-176
    CrossrefPubMedGoogle Scholar
  • 9 Douce R., Heldt H.-W.. Photorespiration. Leegood, R. C., Sharkey, T. D., and von Caemmerer, S., eds. Photosynthesis: Physiology and Metabolism. Dordrecht; Kluwer Academic Publishers (2000): 115-136
    Google Scholar
  • 10 Edwards G. E., Ku M. S. B.. Biochemistry of C3-C4 intermediates. Hatch, M. D. and Boardman, N. K., eds. The Biochemistry of Plants, Vol. 10: Photosynthesis. San Diego; Academic Press (1987): 275-325
    Google Scholar
  • 11 Ehleringer J. R., Monson R. K.. Evolutionary and ecological aspects of photosynthetic pathway variation.  Annual Review of Ecology and Systematics. (1993);  24 411-439
    CrossrefPubMedGoogle Scholar
  • 12 Ellis R. P.. The significance of the occurrence of both Kranz and non-Kranz leaf anatomy in the grass species Alloteropsis semialata.  South African Journal of Science. (1974);  70 169-173
    PubMedGoogle Scholar
  • 13 Ellstrand N. C., Whitkus R., Rieseberg L. H.. Distribution of spontaneous plant hybrids.  Proceedings of the National Academy of Sciences of the USA. (1996);  93 5090-5093
    CrossrefPubMedGoogle Scholar
  • 14 Harberd D. J., McArthur E. D.. The chromosome constitution of Diplotaxis muralis (L.) DC.  Watsonia. (1972);  9 131-135
    PubMedGoogle Scholar
  • 15 Hatch M. D.. C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure.  Biochimica et Biophysica Acta. (1987);  895 81-106
    PubMedGoogle Scholar
  • 16 Hattersley P. W., Watson L.. Diversification of photosynthesis. Chapman, G. P., ed. Grass Evolution and Domestication. Cambridge; Cambridge University Press (1992): 38-116
    Google Scholar
  • 17 Holaday A. S., Harrison A. T., Chollet R.. Photosynthetic/photorespiratory CO2 exchange characteristics of the C3-C4 intermediate species Moricandia arvensis.  Plant Science Letters. (1982);  27 181-189
    CrossrefPubMedGoogle Scholar
  • 18 Hunt S., Smith A. M., Woolhouse H. W.. Evidence for light-dependent system for reassimilation of photorespiratory CO2, which does not include a C4 cycle, in the C3-C4 intermediate species Moricandia arvensis.  Planta. (1987);  171 227-234
    CrossrefPubMedGoogle Scholar
  • 19 Hylton C. M., Rawsthorne S., Smith A. M., Jones A., Woolhouse H.W.. Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3-C4 intermediate species.  Planta. (1988);  175 452-459
    CrossrefPubMedGoogle Scholar
  • 20 Ku M. S. B., Wu J., Dai Z., Scott R. A., Chu C., Edwards G. E.. Photosynthetic and photorespiratory characteristics of Flaveria species.  Plant Physiology. (1991);  96 518-528
    PubMedGoogle Scholar
  • 21 Long R. W., Rhamstine E.L.. Evidence for the hybrid origin of Flaveria latifolia (Compositae).  Brittonia. (1968);  20 238-250
    PubMedGoogle Scholar
  • 22 McVetty P. B. E., Austin R. B., Morgan C. L.. A comparison of the growth, photosynthesis, stomatal conductance and water use efficiency of Moricandia and Brassica species.  Annals of Botany. (1989);  64 87-94
    PubMedGoogle Scholar
  • 23 Monson R. K., Moore B. D., Ku M. S. B., Edwards G. E.. Co-function of C3 and C4 photosynthetic pathways in C3, C4 and C3-C4 intermediate Flaveria species.  Planta. (1986);  168 493-502
    CrossrefPubMedGoogle Scholar
  • 24 Monson R. K., Rawsthorne S.. CO2 assimilation in C3-C4 intermediate plants. Leegood, R. C., Sharkey, T. D., and von Caemmerer, S., eds. Photosynthesis: Physiology and Metabolism. Dordrecht; Kluwer Academic Publishers (2000): 533-550
    Google Scholar
  • 25 Morgan C. L., Turner S. R., Rawsthorne S.. Coordination of the cell-specific distribution of the four subunits of glycine decarboxylase and of serine hydroxymethyltransferase in leaves of C3-C4 intermediate species from different genera.  Planta. (1993);  190 468-473
    PubMedGoogle Scholar
  • 26 Oliver D. J.. The glycine decarboxylase complex from plant mitochondria.  Annual Review of Plant Physiology and Plant Molecular Biology. (1994);  45 323-337
    CrossrefPubMedGoogle Scholar
  • 27 O'Neill C. M., Murata T., Morgan C. L., Mathias R. J.. Expression of the C3-C4 intermediate character in somatic hybrids between Brassica napus and the C3-C4 species Moricandia arvensis.  Theoretical and Applied Genetics. (1996);  93 1234-1241
    CrossrefPubMedGoogle Scholar
  • 28 Powell A. M.. Systematics of Flaveria (Flaveriinae - Asteraceae).  Annals of the Missouri Botanical Garden. (1978);  65 590-636
    PubMedGoogle Scholar
  • 29 Rawsthorne S., Morgan C. L., O'Neill C. M., Hylton C. M., Jones D. A., Frean M. L.. Cellular expression pattern of the glycine decarboxylase P protein in leaves of an intergeneric hybrid between the C3-C4 intermediate species Moricandia nitens and the C3 species Brassica napus.  Theoretical and Applied Genetics. (1998);  96 922-927
    CrossrefPubMedGoogle Scholar
  • 30 Rieseberg L. H.. Hybrid origins of plant species.  Annual Review of Ecology and Systematics. (1997);  28 359-389
    CrossrefPubMedGoogle Scholar
  • 31 Sage R. F.. Evolution of C4 photosynthesis.  New Phytologist. (2004);  161 341-370
    CrossrefPubMedGoogle Scholar
  • 32 Ueno O.. Immunogold localization of photosynthetic enzymes in leaves of Aristida latifolia, a unique C4 grass with a double chlorenchymatous bundle sheath.  Physiologia Plantarum. (1992);  85 189-196
    CrossrefPubMedGoogle Scholar
  • 33 Ueno O., Bang S. W., Wada Y., Kondo A., Ishihara K., Kaneko Y., Matsuzawa Y.. Structural and biochemical dissection of photorespiration in hybrids differing in genome constitution between Diplotaxis tenuifolia (C3-C4) and radish (C3).  Plant Physiology. (2003);  132 1550-1559
    CrossrefPubMedGoogle Scholar
  • 34 Ueno O., Bang S. W., Wada Y., Kobayashi N., Kaneko Y., Matsuzawa Y.. Inheritance of photosynthetic characteristics in reciprocal hybrids between Moricandia arvensis (C3-C4) and cabbage (C3).  Japanese Journal of Crop Science. (2005);  74 (Suppl. 2) 300-301
    PubMedGoogle Scholar
  • 35 Ueno O., Sentoku N.. Comparison of leaf structure and photosynthetic characteristics of C3 and C4 Alloteropsis semialata subspecies.  Plant, Cell and Environment. (2006);  29 DOI: 10.1111/j.1365-3040.2005.01418.x
    PubMedGoogle Scholar
  • 36 Willis L. C.. A Dictionary of the Flowering Plants and Ferns. Student edition. Cambridge; Cambridge University Press (1985)
    Google Scholar
  • 37 Wingler A., Lea P., Quick W. P., Leegood R. C.. Photorespiration: metabolic pathways and their role in stress protection.  Philosophical Transactions of the Royal Society of London, Series B. (2000);  355 1517-1529
    CrossrefPubMedGoogle Scholar
  • 38 Yan Z., Tian Z., Huang B., Huang R., Meng J.. Production of somatic hybrids between Brassica oleracea and the C3-C4 intermediate species Moricandia arvensis. .  Theoretical and Applied Genetics. (1999);  99 1281-1286
    CrossrefPubMedGoogle Scholar

O. Ueno

Plant Physiology Department
National Institute of Agrobiological Sciences

Tsukuba

Ibaraki 305-8602

Japan

Email: uenoos@nias.affrc.go.jp

Editor: R. C. Leegood

      >