The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses
Oula Ghannoum A D , Matthew J. Paul B , Jane L. Ward C , Michael H. Beale C , Delia-Irina Corol C and Jann P. Conroy AA Centre for Plant and Food Science, University of Western Sydney, Locked Bag 1797, South Penrith DC, South Penrith, NSW 1797, Australia.
B Centre for Crop Genetic Improvement, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.
C National Centre for Plant and Microbial Metabolomics, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.
D Corresponding author. Email: o.ghannoum@uws.edu.au
Functional Plant Biology 35(3) 213-221 https://doi.org/10.1071/FP07256
Submitted: 31 October 2007 Accepted: 13 February 2008 Published: 23 April 2008
Abstract
Phosphorus (P) is an important determinant of plant productivity, particularly in the tropical grasslands of Australia, which contain both C3 and C4 species. Few studies have compared the responses of such species to P deficiency. Previous work led us to hypothesise that C3 photosynthesis and the three subtypes of C4 photosynthesis have different sensitivities to P deficiency. To examine their dynamic response to P deficiency in more detail, four taxonomically related tropical grasses (Panicum laxum (C3) and Panicum coloratum, Cenchrus ciliaris and Panicum maximum belonging to the C4 subtypes NAD-ME, NADP-ME and PCK, respectively) were grown under contrasting P supplies, including P withdrawal from the growing medium. Changes in photosynthesis and growth were compared with leaf carbohydrate contents and metabolic fingerprints obtained using high-resolution proton nuclear magnetic resonance (1H-NMR). The response of CO2 assimilation rates to leaf contents of inorganic phosphate ([Pi]) was linear in the C3 grass, but asymptotic for the three C4 grasses. Relative growth rate was affected most by low P in the C3 species and was correlated with the leaf content of glucose 6-phosphate more than with carbohydrates. Principal component analysis of the 1H-NMR spectra revealed distinctive profiles of carbohydrates and amino acids for the four species. Overall, the data showed that photosynthesis of the three C4 subtypes behaved similarly. Compared with the C3 counterpart, photosynthesis of the three C4 grasses had a higher P use efficiency and lower Pi requirement, and responded to a narrower range of [Pi]. Although each of the four grass species showed distinctive 1H-NMR fingerprints, there were no differences in response that could be attributed to the C4 subtypes.
Additional keyword: 1H-NMR metabolomics.
Acknowledgements
We thank Susanne von Caemmerer for critical reading of the manuscript. This research was supported by a Discovery Grant awarded to J. P. Conroy and M. J. Paul by the Australian Research Council, and an International Research Initiative Grant awarded to O. Ghannoum by the University of Western Sydney. Rothamsted Research receives grant-aided support from the Biotechnological and Biological Sciences Research Council of the United Kingdom.
Chollet R,
Vidal J, O’Leary MH
(1996) Phosphoenolpyruvate carboxylase: a ubiquitous highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 273–298.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fredeen AL,
Rao IM, Terry N
(1989) Influence of phosphorus nutrition on growth and carbon partitioning in Glycine max. Plant Physiology 89, 225–230.
| PubMed |
Ghannoum O, Conroy JP
(1998) Nitrogen deficiency precludes a growth response to CO2 enrichment in C3 and C4 Panicum grasses. Functional Plant Biology 25, 627–636.
| Crossref | GoogleScholarGoogle Scholar |
Ghannoum O, Conroy JP
(2007) Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses. Functional Plant Biology 34, 72–81.
| Crossref | GoogleScholarGoogle Scholar |
Ghannoum O,
Evans JR,
Chow WS,
Andrews TJ,
Conroy JP, von Caemmerer S
(2005) Faster Rubisco is the key to superior nitrogen-use efficiency in NADP-malic enzyme relative to NAD-malic enzyme C4 grasses. Plant Physiology 137, 638–650.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hatch MD
(1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81–106.
Iglesias AA,
Plaxton WC, Podesta FE
(1993) The role of inorganic phosphate in the regulation of C4 photosynthesis. Photosynthesis Research 35, 205–211.
| Crossref | GoogleScholarGoogle Scholar |
Khamis S,
Chaillou S, Lamaze T
(1990) CO2 assimilation and partitioning of carbon in maize plants deprived of orthophosphate. Journal of Experimental Botany 41, 1619–1625.
| Crossref | GoogleScholarGoogle Scholar |
Kondracka A, Rychter AM
(1997) The role of Pi recycling processes during photosynthesis in phosphate-deficient bean plants. Journal of Experimental Botany 48, 1461–1468.
| Crossref | GoogleScholarGoogle Scholar |
Krishnan P,
Kruger NJ, Ratcliffe RG
(2005) Metabolite fingerprinting and profiling in plants using NMR. Journal of Experimental Botany 56, 255–265.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lunn JE, Furbank RT
(1999) Sucrose biosynthesis in C4 plants. The New Phytologist 143, 221–237.
| Crossref | GoogleScholarGoogle Scholar |
Meyer RC,
Steinfath M,
Lisec J,
Becher M, Witucka-Wall H , et al.
(2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 104, 4759–4764.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Moing A,
Maucourt M,
Renaud C,
Gaudillère M, Brouquisse R , et al.
(2004) Quantitative metabolic profiling by 1-dimenional 1H-NMR analyses: application to plant genetics and functional genomics. Functional Plant Biology 31, 889–902.
| Crossref | GoogleScholarGoogle Scholar |
Murphy J, Riley JP
(1962) A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27, 31–36.
| Crossref | GoogleScholarGoogle Scholar |
Norman MJ
(1962) Response of native pasture to nitrogen and phosphate fertilizer at Katherine, N.T. Australian Journal of Experimental Agriculture and Animal Husbandry 2, 27–34.
| Crossref | GoogleScholarGoogle Scholar |
Paul MJ, Pellny TK
(2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pieters AJ,
Paul MJ, Lawlor DW
(2001) Low sink demand limits photosynthesis under Pi deficiency. Journal of Experimental Botany 52, 1083–1091.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rao IM,
Fredeen AL, Terry N
(1990) Leaf phosphate status, photosynthesis and carbon partitioning in sugar beet. III. Diurnal changes in carbon partitioning and carbon export. Plant Physiology 92, 29–36.
| PubMed |
Sage RF, McKown A
(2006) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? Journal of Experimental Botany 57, 307–317.
Schachtman DP,
Reid RJ, Ayling SM
(1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stitt M, Quick WP
(1989) Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiologia Plantarum 77, 633–641.
| Crossref | GoogleScholarGoogle Scholar |
Stitt M,
Lilley RM,
Gerhardt R, Heldt HW
(1989) Metabolite levels in specific cells and subcellular compartments of plant leaves. Methods in Enzymology 174, 518–552.
Usuda H, Shimogawara K
(1991a) Phosphate deficiency in maize. II. Enzyme activities. Plant & Cell Physiology 32, 1313–1317.
Usuda H, Shimogawara K
(1991b) Phosphate deficiency in maize. I. Leaf phosphate status, growth, photosynthesis and carbon partitioning. Plant & Cell Physiology 32, 497–504.
Ward JL,
Harris C,
Lewis J, Beale MH
(2003) Assessment of 1H NMR spectroscopy and multivariate analysis as a technique for metabolite fingerprinting of Arabidopsis thaliana. Phytochemistry 62, 949–957.
| Crossref | GoogleScholarGoogle Scholar | PubMed |