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Plant function and evolutionary biology
RESEARCH ARTICLE

Physiological, anatomical and biochemical characterisation of photosynthetic types in genus Cleome (Cleomaceae)

Elena V. Voznesenskaya A , Nuria K. Koteyeva A , Simon D. X. Chuong B , Alexandra N. Ivanova A , João Barroca C , Lyndley A. Craven D and Gerald E. Edwards C E
+ Author Affiliations
- Author Affiliations

A Laboratory of Anatomy and Morphology, V. L. Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov Street 2, 197376, St Petersburg, Russia.

B Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada.

C School of Biological Sciences, Washington State University, Pullman, WA 99 164-4236, USA.

D Australian National Herbarium, Centre for Plant Biodiversity Research, GPO Box 1600, Canberra, ACT 2601, Australia.

E Corresponding author. Email: edwardsg@wsu.edu

F This paper originates from an International Symposium in Memory of Vincent R. Franceschi, Washington State University, Pullman, Washington, USA, June 2006.

Functional Plant Biology 34(4) 247-267 https://doi.org/10.1071/FP06287
Submitted: 4 November 2006  Accepted: 1 March 2007   Published: 19 April 2007

Abstract

C4 photosynthesis has evolved many times in 18 different families of land plants with great variation in leaf anatomy, ranging from various forms of Kranz anatomy to C4 photosynthesis occurring within a single type of photosynthetic cell. There has been little research on photosynthetic typing in the family Cleomaceae, in which only one C4 species has been identified, Cleome gynandra L. There is recent interest in selecting and developing a C4 species from the family Cleomaceae as a model C4 system, since it is the most closely related to Arabidopsis, a C3 model system (Brown et al. 2005). From screening more than 230 samples of Cleomaceae species, based on a measure of the carbon isotope composition (δ13C) in leaves, we have identified two additional C4 species, C. angustifolia Forssk. (Africa) and C. oxalidea F.Muell. (Australia). Several other species have δ13C values around –17‰ to –19‰, suggesting they are C4-like or intermediate species. Eight species of Cleome were selected for physiological, anatomical and biochemical analyses. These included C. gynandra, a NAD–malic enzyme (NAD–ME) type C4 species, C. paradoxa R.Br., a C3–C4 intermediate species, and 6 others which were characterised as C3 species. Cleome gynandra has C4 features based on low CO2 compensation point (Γ), C4 type δ13C values, Kranz-type leaf anatomy and bundle sheath (BS) ultrastructure, presence of C4 pathway enzymes, and selective immunolocalisation of Rubisco and phosphoenolpyruvate carboxylase. Cleome paradoxa was identified as a C3–C4 intermediate based on its intermediate Γ (27.5 μmol mol–1), ultrastructural features and selective localisation of glycine decarboxylase of the photorespiratory pathway in mitochondria of BS cells. The other six species are C3 plants based on Γ, δ13C values, non-Kranz leaf anatomy, and levels of C4 pathway enzymes (very low or absent) typical of C3 plants. The results indicate that this is an interesting family for studying the genetic basis for C4 photosynthesis and its evolution from C3 species.

Additional keywords: C3 plants, C4 plants, C3–C4 intermediate photosynthesis, chloroplast ultrastructure, immunolocalisation, NAD–ME type, photosynthetic enzymes.


Acknowledgements

The authors acknowledge support of this work by NSF Grants IBN-0131098 and IBN-0236959, NSF Isotope Facility Grant DBI-0116203, and partly by Civilian Research and Development Foundation grants RB1-2502-ST-03 and RUB1-2829-ST-06, and the Russian Foundation of Basic Research grant 05-04-49622. We are very grateful to Prof. H. Iltis for help with identification of plant material and suggestions on the manuscript. We thank Dr A. S. Raghavendra, University of Hyderabad, India, the National Plant Germplasm System, GRIN, and the following Botanical Gardens for providing seeds (Kew Royal Botanic Gardens, Prague, Kiev and Copenhagen Universities), and Herbariums of the Missouri Botanical Garden, Washington State University, the Komarov Botanical Institute, Kew Royal Botanic Gardens and Australian National Herbarium for providing plant samples for carbon isotope analysis. We also thank the Franceschi Microscopy and Imaging Center of Washington State University for use of their facilities and staff assistance and C. Cody for plant growth management.


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Appendix 1.  Carbon isotope composition of species of Cleome and some other representative species in the family Cleomaceae
For material from herbaria, the names listed are mainly according to names on the specimens sampled. In the case of plants grown in Washington State University greenhouse (WSUG), the names cited are according to identification of specimens and classification by Dr H. Iltis, University of Wisconsin, Madison (verifying names or correcting misidentifications). Under location, for the plants grown in WSUG the source of seeds and place of collection are indicated in parentheses. For source of herbarium specimens, CANB = Australian National Herbarium, Canberra, Australia; K = Royal Botanic Gardens Herbarium, Kew, UK; LE = Komarov Botanical Institute Herbarium, St Petersburg, Russia; MO = Missouri Botanical Garden Herbarium, St Louis, USA; WS = Washington State University Herbarium, Pullman, USA. SE values were usually less than ±0.1‰
A1A


Appendix 1 Cont.  Carbon isotope composition of species of Cleome and some other representative species in the family Cleomaceae
A1B


Appendix 1 Cont.  Carbon isotope composition of species of Cleome and some other representative species in the family Cleomaceae
A1C


Appendix 1 Cont.  Carbon isotope composition of species of Cleome and some other representative species in the family Cleomaceae
A1D