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

Diversity and plasticity of C4 photosynthesis in Eleocharis (Cyperaceae)

Lesley R. Murphy A C , João Barroca A C , Vincent R. Franceschi A , Raymond Lee A , Eric H. Roalson A , Gerald E. Edwards A and Maurice S. B. Ku B D
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences and Center for Integrated Biotechnology, Washington State University, Pullman, WA 99164-4236, USA.

B Institute of Agricultural Biotechnology, National Chiayi University, Chiayi 60004, Taiwan.

C These authors contributed equally to this paper.

D Corresponding author. Email: mku@mail.ncyu.edu.tw

Functional Plant Biology 34(7) 571-580 https://doi.org/10.1071/FP06296
Submitted: 11 November 2006  Accepted: 29 March 2007   Published: 4 July 2007

Abstract

Eleocharis contains many amphibious species, and displays diversity of photosynthetic mechanism (C3, C4 or C3-C4 intermediates). A unique feature of Eleocharis is the plasticity in the photosynthetic mechanism of some species in response to the environment. In this study, we have examined the culm anatomy and photosynthetic property of several Eleocharis species grown terrestrially and the changes in the newly produced culms over a short period time frame after switching from terrestrial to submerged condition. Eleocharis baldwinii (Torrey) Chapman is C4-like in terrestrial habitat, exhibiting O2 inhibition of photosynthesis with Rubisco expressed in both mesophyll and bundle sheath cells and PEPC strictly in the mesophyll cells, but switches to C3-C4 intermediacy when submerged. In addition to Eleocharis vivipara Link type 1 (which switches from C4-like to C3), two other photosynthetic types examined in this study were shown to have different responses to growth in either terrestrial or submerged conditions. E. vivipara type 2 is a typical C4 plant in the terrestrial habitat, but becomes a C3-C4 intermediate under submerged conditions. Further, terrestrially, E. vivipara type 3 is a C3-C4 intermediate, but when submerged the δ13C value increases to –6.7‰, indicating its use of bicarbonate as a major carbon source. The submerged form of this plant exhibited about three times higher photosynthetic O2 evolution rate, compared to the C3 species Eleocharis erythropoda Steudel. These Eleocharis species possess different molecular switches for regulating C4 gene expression in response to environmental stimuli both between different species, and in E. vivipara among different populations. The apparent expression of a bicarbonate transport system by E. vivipara type 3 while submerged represents a unique adaptation to low CO2 availability.


Acknowledgements

We thank Chuck Cody for cultivation of plants in the greenhouse and Dr Elena Voznesenskaya for assistance with figure preparation. We also thank the staff of the Electron Microscopy Center at Washington State University for use of facilities and assistance. This work has been partially supported by NSF grants 0515975, IBN-0236959 and NSF Isotope Facility Grant DBI-0116203.


References


Agarie S, Kai M, Takatsuji H, Ueno O (1997) Expression of C3 and C4 photosynthetic characteristics in the amphibious plant Eleocharis vivipara: structure and analysis of the expression of isogenes of pyruvate, orthophosphate dikinase. Plant Molecular Biology 34, 363–369.
Crossref | GoogleScholarGoogle Scholar | PubMed | [accessed June 2007]. (The Board of Trustees of the Royal Botanic Gardens, Kew.)

Gutierrez M, Gracen VE, Edwards GE (1974) Biochemical and cytological relationships in C4 plants. Planta 119, 279–300.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hatch MD, Kagawa T, Graig S (1975) Subdivision of C4-pathway species based on C4 acid decarboxylating systems and ultrastructural features. Australian Journal of Plant Physiology 2, 111–128. open url image1

Knudson LL, Tibbitts TW, Edwards GE (1977) Measurement of ozone injury by determination of leaf chlorophyll concentration. Plant Physiology 60, 606–608.
PubMed |
open url image1

Ku MSB, Monson RK, Littlejohn RO, Nakamoto H, Fisher DB, Edwards GE (1983) Photosynthetic characteristics of C3-C4 intermediate Flaveria species. 1. Leaf anatomy, photosynthetic responses to O2 and CO2, and activities of key enzymes in the C3 and C4 pathways. Plant Physiology 71, 944–948.
PubMed |
open url image1

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

Laisk A, Loreto F (1996) Determining photosynthetic parameters from culm CO2 exchange and chlorophyll fluorescence. Plant Physiology 110, 903–912.
PubMed |
open url image1

Laisk A , Oja V (1998) ‘Dynamics of culm photosynthesis.’ (CSIRO Publishing: Melbourne)

Leonardos ED, Grodzinski B (2000) Photosynthesis, immediate export and carbon partitioning in source leaves of C3, C3-C4 intermediate, and C4 Panicum and Flaveria species at ambient and elevated CO2 levels. Plant, Cell & Environment 23, 839–851.
Crossref | GoogleScholarGoogle Scholar | open url image1

Levavassur G, Edwards GEE, Osmond CB, Ramus J (1991) Inorganic carbon limitation of photosynthesis in Ulva rotundata (Chlorophyta). Journal of Phycology 27, 667–672.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lieman-Hurwitz J, Rachmilevitch S, Mittler R, Marcus Y, Kaplan A (2003) Enhanced photosynthesis and growth of transgenic plants that express ictB, a gene involved in HCO3 – accumulation in cyanobacteria. Plant Biotechnology Journal 1, 43–50.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Magnin NC, Cooley BA, Reiskind JB, Bowes G (1997) Regulation and localization of key enzymes during the induction of Kranz-less, C4 -type photosynthesis in Hydrilla verticillata. Plant Physiology 115, 1681–1689.
PubMed |
open url image1

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

Muasya AM, Simpson DA, Chase MW, Culham A (1998) An assessment of suprageneric phylogeny in Cyperaceae using rbcL DNA sequences. Plant Systematics and Evolution 211, 257–271.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ohsugi R, Murata T (1986) Variations in the leaf anatomy among some C4 Panicum species. Annals of Botany 58, 443–453. open url image1

Ohsugi R, Murata T, Chonan N (1982) C4 syndrome of the species in the Dichotomiflorum group of the genus Panicum (Gramineae). Journal of Plant Research 95, 339–347.
Crossref | GoogleScholarGoogle Scholar | open url image1

Roalson EH, Friar EA (2000) Infrageneric classification of Eleocharis (Cyperaceae) revisited: evidence from the internal transcribed spacer (ITS) region of nuclear ribosomal DNA. Systematic Botany 25, 323–336.
Crossref | GoogleScholarGoogle Scholar | open url image1

Robe WE, Griffiths H (2000) Physiological and photosynthetic plasticity in the amphibious, freshwater plant, Littorella uniflora, during the transition from aquatic to dry terrestrial environments. Plant, Cell & Environment 23, 1041–1054.
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 , Li M , 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)

Soros CL, Dengler NG (2001) Ontogenetic derivation and cell differentiation in photosynthetic tissues of C3 and C4 Cyperaceae. American Journal of Botany 88, 992–1005.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Takeda T, Ueno O, Samejima M, Ohtani T (1985) An investigation for the occurrence of C4 photosynthesis in the Cyperaceae from Australia. Botanical Magazine-Tokyo 98, 393–411.
Crossref | GoogleScholarGoogle Scholar | open url image1

Uchino A, Samejima M, Ishii R, Ueno O (1995) Photosynthetic carbon metabolism in an amphibious sedge, Eleocharis balwinii (Torr.) Chapman: modified expression of C4 characteristics under submerged aquatic conditions. Plant & Cell Physiology 36, 229–238. open url image1

Uchino A, Sentoku N, Nemoto K, Ishii R, Samejima M, Matsuoka M (1998) C4-type gene expression is not directly dependent on Kranz anatomy in an amphibious sedge Eleocharis vivipara Link. The Plant Journal 14, 565–572.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ueno O (1996a) Immunocytochemical localization of enzymes involved in the C3 and C4 pathways in the photosynthetic cells of an amphibious sedge, Eleocharis vivipara. Planta 199, 394–403. open url image1

Ueno O (1996b) Structural characterization of photosynthetic cells in an amphibious sedge, Eleocharis vivipara, in relation to C3 and C4 metabolism. Planta 199, 382–393. open url image1

Ueno O (1998) Induction of Kranz anatomy and C4-like biochemical characteristics in a submerged amphibious plant by abscisic acid. The Plant Cell 10, 571–583.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ueno O (2001) Environmental regulation of C3 and C4 differentiation in the amphibious sedge Eleocharis vivipara. Plant Physiology 127, 1524–1532.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ueno O (2004) Environmental regulation of photosynthetic metabolism in the amphibious sedge Eleocharis baldwinii and comparisons with related species. Plant, Cell & Environment 27, 627–639.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ueno O, Samejima M (1989) Structural features of NAD-malic enzyme type C4 Eleocharis: an additional report of C4 acid decarboxylation types of the Cyperaceae. Botanical Magazine-Tokyo 102, 393–402.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ueno O, Wakayama M (2004) Cellular expression of C3 and C4 photosynthetic enzymes in the amphibious sedge Eleocharis retroflexa ssp. chaetaria. Journal of Plant Research 117, 433–441.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ueno O, Samejima M, Koyama T (1989) Distribution and evolution of C4 syndrome in Eleocharis, a sedge group inhabiting wet and aquatic environments, based on culm anatomy and carbon isotope ratios. Annals of Botany 64, 425–438. open url image1

Ueno O, Takeda T, Murata T (1986) C4 acid decarboxylating enzyme activities of C4 species possessing different Kranz anatomical types in the Cyperaceae. Photosynthetica 20, 111–116. open url image1

Ueno O, Samejima M, Muto S, Miyachi S (1988) Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. Proceedings of the National Academy of Sciences USA 85, 6733–6737.
Crossref | GoogleScholarGoogle Scholar | open url image1