Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Leaf anatomy, gas exchange and photosynthetic enzyme activity in Flaveria kochiana

Erika A. Sudderth A D , Riyadh M. Muhaidat B , Athena D. McKown B , Ferit Kocacinar C and Rowan F. Sage B
+ Author Affiliations
- Author Affiliations

A Department of Organismic and Evolutionary Biology, Harvard University, Biological Laboratories, 16 Divinity Ave., Cambridge, MA 02138 11, USA.

B Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, M5S1A1, Canada.

C Faculty of Forestry, Kahramanmaras Sutcu Imam University, 46100 Kahramanmaras, Turkey.

D Corresponding author. Email: sudderth@fas.harvard.edu

Functional Plant Biology 34(2) 118-129 https://doi.org/10.1071/FP06263
Submitted: 19 October 2006  Accepted: 4 December 2006   Published: 12 February 2007

Abstract

Flaveria (Asteraceae) is one of the few genera known to contain both C3 and C4 species, in addition to numerous biochemically-intermediate species. C3-C4 and C4-like intermediate photosynthesis have arisen more than once in different phylogenetic clades of Flaveria. Here, we characterise for the first time the photosynthetic pathway of the recently described species Flaveria kochiana B.L. Turner. We examined leaf anatomy, activity and localisation of key photosynthetic enzymes, and gas exchange characteristics and compared these trait values with those from related C4 and C4-like Flaveria species. F. kochiana has Kranz anatomy that is typical of other C4 Flaveria species. As in the other C4 lineages within the Flaveria genus, the primary decarboxylating enzyme is NADP-malic enzyme. Immunolocalisation of the major C4 cycle enzymes, PEP carboxylase and pyruvate, orthophosphate dikinase, were restricted to the mesophyll, while Rubisco was largely localised to the bundle sheath. Gas exchange analysis demonstrated that F. kochiana operates a fully functional C4 pathway with little sensitivity to ambient oxygen levels. The CO2 compensation point (2.2 µbar) was typical for C4 species, and the O2-response of the CO2 compensation point was the same as the C4 species F. trinervia. Notably, F. vaginata (B.L. Robinson & Greenman), a putative C4-like species that is the nearest relative of F. kochiana, had an identical response of the CO2 compensation point to O2. Furthermore, F. vaginata, exhibited a carbon isotope ratio (–15.4‰) similar to C4 species including F. australasica Hooker, F. trinervia Spreng. C. Mohr and the newly characterised F. kochiana. F. vaginata could be considered a C4 species, but additional studies are necessary to confirm this hypothesis. In addition, our results show that F. kochiana uses an efficient C4 cycle, with the highest initial slope of the A/Ci curve of any C4 Flaveria species.

Additional keywords: C4 photosynthesis, C3-C4 photosynthesis, C4 evolution, CO2 compensation point, Kranz anatomy.


Acknowledgements

The authors thank Dr Espinosa-García for generous assistance coordinating our research activities, Dr Louis Villaseñor for providing locality information and specimen identification, and Martín Paredes Flores and Isabelle Blanckaert for assistance with the collection of F. kochiana specimens. We also thank the Secretaría de Medio Ambiente y Recursos Naturales and the Secretaría de Relaciones Exteriors of Mexico for granting permission to collect F. kochiana specimens. We appreciate the experimental advice and helpful discussions of the manuscript provided by Dr Nancy G. Dengler and Dr Noel M. Holbrook, and suggested revisions from two anonymous reviewers. This work was supported by NSF DDIG (DEB-0407716) and the Deland Fund (EAS) and NSERC (ADM and RM).


References


Akhani H, Trimborn P, Ziegler H (1997) Photosynthetic pathways in chenopodiaceae from Africa, Asia and Europe with their ecological, phytogeographical and taxonomical importance. Plant Systematics and Evolution 206, 187–221.
Crossref | GoogleScholarGoogle Scholar | open url image1

Apel P, Maass I (1981) Photosynthesis in species of Flaveria: CO2 compensation concentration, O2 influence on photosynthetic gas-exchange and delta-C13 values in species of Flaveria (Asteraceae). Biochemie und Physiologie der Pflanzen 176, 396–399. open url image1

Bruhl JJ, Perry S (1995) Photosynthetic pathway-related ultrastructure of C3, C4 and C3-like C3-C4 intermediate sedges (Cyperaceae), with special reference to Eleocharis. Australian Journal of Plant Physiology 22, 521–530. open url image1

Bruhl JJ, Stone NE, Hattersley PW (1987) C4 acid decarboxylation enzymes and anatomy in sedges (Cyperaceae) – first record of NAD-malic enzyme species. Australian Journal of Plant Physiology 14, 719–728. open url image1

Chelle M (2005) Phylloclimate or the climate perceived by individual plant organs: what is it? How to model it? What for? New Phytologist 166, 781–790.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chen Z-H, Walker RP, Acheson RM, Leegood RC (2002) Phosphoenolpyruvate carboxykinase assayed at physiological concentrations of metal ions has a high affinity for CO2. Plant Physiology 128, 160–164.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cheng SH, Moore BD, Edwards GE, Ku MSB (1988) Photosynthesis in Flaveria brownii, a C4-like species. Leaf anatomy, characteristics of CO2 exchange, compartmentation of photosynthetic enzymes, and metabolism of 14CO2. Plant Physiology 87, 867–873.
PubMed |
open url image1

Dai ZY, Ku MSB, Edwards GE (1996) Oxygen sensitivity of photosynthesis and photorespiration in different photosynthetic types in the genus Flaveria. Planta 198, 563–571.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dengler NG, Dengler RE, Donnelly PM, Filosa MF (1995) Expression of the C4 pattern of photosynthetic enzyme accumulation during leaf development in Atriplex rosea (Chenopodiaceae). American Journal of Botany 82, 318–327.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dengler NG , Nelson AD (1999) Leaf structure and development in C4 plants. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 133–172. (Academic Press: San Diego)

Edwards GE , Ku MSB (1987) Biochemistry of C3-C4 intermediates. In ‘The biochemistry of plants’. (Eds PK Stumpf, EE Conn) pp. 275–325. (Academic Press: London)

Edwards GE , Walker JE (1983) ‘C3, C4: mechanisms, and cellular and environmental regulation, of photosynthesis.’ (Blackwell Scientific: Oxford)

Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthesis pathway variation. Annual Review of Ecology and Systematics 24, 411–439.
Crossref | GoogleScholarGoogle Scholar | open url image1

Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas-exchange to investigate CO2 diffusion in leaves of higher plants. Australian Journal of Plant Physiology 13, 281–292. open url image1

Farquhar GD (1983) On the nature of isotope discrimination in C4 species. Australian Journal of Plant Physiology 10, 205–226. open url image1

Hatch MD, Kagawa T (1974) NAD malic enzyme in leaves with C4-pathway photosynthesis and its role in C4 acid decarboxylation. Archives of Biochemistry and Biophysics 160, 346–349.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hatch MD, Tsuzuki M, Edwards GE (1982) Determination of NAD malic enzyme in leaves of C4 plants – effects of malate-dehydrogenase and other factors. Plant Physiology 69, 483–491.
PubMed |
open url image1

Henderson SA, von Caemmerer S, Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Australian Journal of Plant Physiology 19, 263–285. open url image1

Holaday AS, Lee KW, Chollet R (1984) C3-C4 intermediate species in the genus Flaveria – leaf anatomy, ultrastructure, and the effect of O2 on the CO2 compensation concentration. Planta 160, 25–32.
Crossref | GoogleScholarGoogle Scholar | open url image1

Instituto Nacional para el Federalismo y el Desarrollo Municipal O (2002) ‘Enciclopedia de los Municipios de México, Estado de Oaxaca, Santiago Juxtlahuaca.’

Kocacinar F , Sage RF (2005) Hydraulic properties of the xylem in plants of different photosynthetic pathways. In ‘Vascular transport in plants’. (Eds NM Holbrook, MA Zwieniecki) pp. 517–533. (Elsevier: Amsterdam)

Ku MSB, Wu JR, Dai ZY, Scott RA, Chu C, Edwards GE (1991) Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiology 96, 518–528.
PubMed |
open url image1

McKown AD, Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). American Journal of Botany in press , open url image1

McKown AD, Moncalvo JM, Dengler NG (2005) Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. American Journal of Botany 92, 1911–1928. open url image1

Monson RK (2003) Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164, S43–S54.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK, Moore BD, Ku MSB, Edwards GE (1986) Cofunction of C3 photosynthetic and C4 photosynthetic pathways in C3, C4 and C3-C4 intermediate Flaveria species. Planta 168, 493–502.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK, Moore DB (1989) On the significance of C3-C4 intermediate photosynthesis to the evolution of C4 photosynthesis. Plant, Cell and Environment 12, 689–699.
Crossref | GoogleScholarGoogle Scholar | open url image1

Monson RK , Rawsthorne S (2000) CO2 assimilation in C3-C4 intermediate plants. In ‘Photosynthesis: physiology and metabolism’. (Eds RC Leegood, TD Sharkey, S von Caemmerer) pp. 533–550. (Kluwer: Dordrecht)

Monson RK, Schuster WS, Ku MSB (1987) Photosynthesis in Flaveria brownii A.M. Powell. A C4-like C3-C4 intermediate. Plant Physiology 85, 1063–1067.
PubMed |
open url image1

Monson RK, Teeri JA, Ku MSB, Gurevitch J, Mets LJ, Dudley S (1988) Carbon-isotope discrimination by leaves of Flaveria species exhibiting different amounts of C3-cycle and C4-cycle co-function. Planta 174, 145–151.
Crossref | GoogleScholarGoogle Scholar | open url image1

Moore BD, Ku MSB, Edwards GE (1987) C4 photosynthesis and light-dependent accumulation of inorganic carbon in leaves of C3-C4 and C4 Flaveria species. Australian Journal of Plant Physiology 14, 657–668. open url image1

Moore BD, Ku MSB, Edwards GE (1989) Expression of C4-like photosynthesis in several species of Flaveria. Plant, Cell and Environment 12, 541–549.
Crossref | GoogleScholarGoogle Scholar | open url image1

Muhaidat R, Sage RF, Dengler NG (2007) Diversity of Kranz anatomy and biochemistry in C4 eudicots. American Journal of Botany in press , open url image1

Pittermann J, Sage RF (2000) Photosynthetic performance at low temperature of Bouteloua gracilis Lag., a high-altitude C4 grass from the Rocky Mountains, USA. Plant, Cell and Environment 23, 811–823.
Crossref | GoogleScholarGoogle Scholar | open url image1

Powell AM (1978) Systematics of Flaveria (Flaveriinae-Asteraceae). Annals of the Missouri Botanical Garden 65, 590–636.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pyankov VI, Gunin PD, Tsoog S, Black CC (2000) C4 plants in the vegetation of Mongolia: their natural occurrence and geographical distribution in relation to climate. Oecologia 123, 15–31.
Crossref | GoogleScholarGoogle Scholar | open url image1

Reiskind JB, Bowes G (1991) The role of phosphoenolpyruvate carboxykinase in a marine macroalga with C4-like photosynthetic characteristics. Proceedings of the National Academy of Sciences USA 88, 2883–2887.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sage RF (2001) Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biology 3, 202–213.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sage RF (2004) The evolution of C4 photosynthesis. New Phytologist 161, 341–370.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sage RF , Li MR , Monson RK (1999) The taxonomic distribution of C4 photosynthesis. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 551–584. (Academic Press: San Diego)

Smith BN, Powell AM (1984) C4-like F1-hybrid of C3 × C4 Flaveria species. Die Naturwissenschaften 71, 217–218.
Crossref | GoogleScholarGoogle Scholar | open url image1

Smith BN, Turner BL (1975) Distribution of Kranz syndrome among Asteraceae. American Journal of Botany 62, 541–545.
Crossref | GoogleScholarGoogle Scholar | open url image1

Turner BL (1995) A new species of Flaveria (Asteraceae, Helenieae) from Oaxaca, Mexico. Phytologia 78, 400–401. open url image1

Ueno O (1992) Immunogold localization of photosynthetic enzymes in leaves of Aristida latifolia, a unique C4 grass with a double chlorenchymatous bundle sheath. Physiologia Plantarum 85, 189–196.
Crossref | GoogleScholarGoogle Scholar | open url image1

Walker JE , Skehel JM , Buchanan SK (1995) Structural analysis of NADH: ubiquinone oxidoreductase from bovine heart mitochondria. In ‘Mitochondrial biogenesis and genetics. Part A’. pp. 14–34. (Academic Press: San Diego)

Winter K (1981) C4 plants of high biomass in arid regions of Asia: occurrence of C4 photosynthesis in Chenopodiaceae and Polygonaceae from the middle East and USSR. Oecologia 48, 100–106.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wintermans JF, Demots A (1965) Spectrophotometric characteristics of chlorophylls a and b and their pheophytins in ethanol. Biochimica et Biophysica Acta 109, 448–450.
PubMed |
open url image1









Appendix


Table 1.  The composition of reaction media used in the assays of photosynthetic enzyme activities in Flaveria kochiana and Flaveria trinervia leaves
Abbreviations: PEPC, PEP-carboxylase; NADP-ME, NADP-malic enzyme; NAD-ME, NAD-malic enzyme; PEP-CK, PEP-carboxykinase
A1