Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses
Oula Ghannoum A B 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 Corresponding author. Email: o.ghannoum@uws.edu.au
Functional Plant Biology 34(1) 72-81 https://doi.org/10.1071/FP06253
Submitted: 10 October 2006 Accepted: 14 December 2006 Published: 19 January 2007
Abstract
This study compared the growth and photosynthetic responses of one C3 (Panicum laxum L.) and two C4 grasses (Panicum coloratum L. and Cenchrus ciliaris L.) to changes in soil phosphorus (P) nutrition. Plants were grown in potted soil amended with six different concentrations of P. One week before harvest, leaf elongation and photosynthetic rates and the contents of carbohydrate, P and inorganic phosphate (Pi) were measured. Five weeks after germination, plants were harvested to estimate biomass accumulation. At each soil P supply, leaf P contents were lower in the C3 (0.6–2.6 mmol P m–2) than in the two C4 grasses (0.8–4.1 mmol P m–2), and Pi constituted ~40–65% of total leaf P. The P deficiency reduced leaf growth, tillering and plant dry mass to a similar extent in all three grasses. In contrast, P deficiency suppressed photosynthetic rates to a greater extent in the C3 (50%) than the C4 grasses (25%). The foliar contents of non-structural carbohydrates were affected only slightly by soil P supply in all three species. Leaf mass per area decreased at low P in the two C4 grasses only, and biomass partitioning changed little with soil P supply. The percentage changes in assimilation rates and plant dry mass were linearly related in the C3 but not the C4 plants. Thus, P deficiency reduced growth in parallel with reductions of photosynthesis in the C3 grass, and independently of photosynthesis in the two C4 grasses. We propose that this may be related to a greater Pi requirement of C4 relative to C3 photosynthesis. Photosynthetic P use efficiency was greater and increased more with P deficiency in the C4 relative to the C3 species. The opposite was observed for whole-plant P-use efficiency. Hence, the greater P-use efficiency of C4 photosynthesis was not transferred to the whole-plant level, mainly as a result of the larger and constant leaf P fraction in the two C4 grasses.
Additional keyword: phosphorus use efficiency.
Acknowledgements
We thank Sylvia Rudmann and Jai Santosh for assistance with the harvests and P analysis. Thanks are also due to two anonymous reviewers whose critical comments greatly improved this manuscript. This research was supported by a Discovery grant awarded to JPC by the Australian Research Council.
Assuero SG,
Mollier A, Pellerin S
(2004) The decrease in growth of phosphorus-deficient maize leaves is related to lower cell production. Plant, Cell and Environment 27, 887–895.
| Crossref | GoogleScholarGoogle Scholar |
Brown RH
(1978) Difference in N use efficiency in C3 and C4 plants and its implications in adaptation and evolution. Crop Science 18, 93–98.
Chiera J,
Thomas J, Rufty T
(2002) Leaf initiation and development in soybean under phosphorus stress. Journal of Experimental Botany 53, 473–481.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Christie EK
(1975) A study of phosphorus nutrition and water supply on the early growth and survival of buffel grass grown on a sandy red earth from south-west Queensland. Australian Journal of Experimental Agriculture and Animal Husbandry 15, 239–249.
| Crossref | GoogleScholarGoogle Scholar |
Christie EK, Moorby J
(1975) Physiological responses of semiarid grasses: I. The influence of phosphorus supply on growth and phosphorus adsorption. Australian Journal of Agricultural Research 26, 423–436.
| Crossref | GoogleScholarGoogle Scholar |
Conroy JP,
Milham PJ,
Reed ML, Barlow EW
(1990) Increases in phosphorus requirements for CO2-enriched pine species. Plant Physiology 92, 977–982.
| PubMed |
Dingkuhn M,
Luquet D,
Kim HK,
Tambour L, Clement-Vidal A
(2006) EcoMeristem, a model of morphogenesis and competition among sinks in rice. 2. Simulating genotype responses to phosphorus deficiency. Functional Plant Biology 33, 325–337.
| Crossref | GoogleScholarGoogle Scholar |
Evans JR,
von Caemmerer S,
Setchell BA, Hudson GS
(1994) The relationship between CO2 transfer conductance and leaf anatomy in transgenic tobacco with a reduced content of Rubisco. Australian Journal of Plant Physiology 21, 475–495.
Foyer C, Spencer C
(1986) The relationship between phosphate status and photosynthesis in leaves. Effects on intercellular orthophosphate distribution, photosynthesis and assimilate partitioning. Planta 167, 369–375.
| Crossref | GoogleScholarGoogle Scholar |
Foyer C,
Walker D,
Spencer C, Mann B
(1982) Observations on the phosphate status and intercellular pH of intact cells, protoplasts and chloroplasts from photosynthetic tissue using phosphorus-31 nuclear magnetic resonance. The Biochemical Journal 202, 429–434.
| 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,
Evans JR,
Chow WS,
Andrews TJ,
Conroy JP, von Caemmerer S
(2005) Faster Rubisco is the key to superior nitrogen use efficiency in NADP-ME relative to NAD-ME C4 grasses. Plant Physiology 137, 638–650.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Güsewell S
(2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266.
| Crossref | GoogleScholarGoogle Scholar |
Halsted M, Lynch J
(1996) Phosphorus responses of C3 and C4 species. Journal of Experimental Botany 47, 497–505.
| Crossref |
Hatch MD
(1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochimica et Biophysica Acta 895, 81–106.
Hocking PJ, Meyer CP
(1991) Effects of CO2 enrichment and nitrogen stress on growth, and partitioning of dry matter and nitrogen in wheat and maize. Australian Journal of Plant Physiology 18, 339–356.
Hurry V,
Strand A,
Furbank R, Stitt M
(2000) The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants in Arabidopsis thaliana. The Plant Journal 24, 383–396.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
Jacob J, Lawlor DW
(1991) Stomatal and mesophyll limitations of photosynthesis in phosphate deficient sunflower, maize and wheat plants. Journal of Experimental Botany 42, 1003–1011.
| Crossref |
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 |
López-Bucio J,
Hernández-Abreu E,
Sánchez-Calderón L,
Nieto-Jacobo MF,
Simpson J, Herrera-Estrella L
(2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiology 129, 244–256.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McKeon GM,
Day KA,
Howden SM,
Mott JJ,
Orr DM,
Scattini WJ, Weston EJ
(1990) Northern Australian savannas: management for pastoral production. Journal of Biogeography 17, 355–372.
| 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 |
Nielsen TH,
Krapp A,
Röper-Schwarz U, Stitt M
(1998) The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant, Cell and Environment 21, 443–454.
| 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, Stitt M
(1993) Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant, Cell and Environment 16, 1047–1057.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Raghothama KG, Karthikeyan AS
(2005) Phosphate acquisition. Plant and Soil 274, 37–49.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Rogers GS,
Payne L,
Milham P, Conroy P
(1993) Nitrogen and phosphorus requirements of cotton and wheat under changing atmospheric CO2 concentrations. Plant and Soil 156, 231–234.
| Crossref | GoogleScholarGoogle Scholar |
Sage RF, McKown A
(2006) Is C4 photosynthesis less phenotypically plastic than C3 photosynthesis? Journal of Experimental Botany 57, 307–317.
Sage RF,
Pearcy RW, Seemann JR
(1987a) The nitrogen use efficiency of C3 and C4 plants. I. Leaf nitrogen, growth, and biomass partitioning in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 84, 954–958.
| PubMed |
Sage RF,
Pearcy RW, Seemann JR
(1987b) The nitrogen use efficiency of C3 and C4 plants. II. Leaf nitrogen effects on the gas exchange characteristics of Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 84, 959–963.
| PubMed |
Schachtman DP,
Reid RJ, Ayling SM
(1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116, 447–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schmitt MR, Edwards GE
(1981) Photosynthetic capacity and nitrogen use efficiency of maize, wheat, and rice: a comparison between C3 and C4 photosynthesis. Journal of Experimental Botany 32, 459–466.
| Crossref |
Silcock RG,
Noble A, Whalley RDB
(1976) Importance of phosphorus and nitrogen in the nutrition of grass seedlings growing in mulga soil. Australian Journal of Agricultural Research 27, 583–592.
| Crossref | GoogleScholarGoogle Scholar |
Usuda H, Shimogawara K
(1991) Phosphate deficiency in maize. I. Leaf phosphate status, growth, photosynthesis and carbon partitioning. Plant and Cell Physiology 32, 497–504.
Yemm EW, Willis AJ
(1954) The estimation of carbohydrates in plant extracts by anthrone. The Biochemical Journal 57, 508–514.
| PubMed |
