Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
Shopping Cart: ( empty )
You are here: Home > Journals > FP > FP06278
RESEARCH ARTICLE
Contents Vol 34(3)

Photosynthetic responses of three C4 grasses of different metabolic subtypes to water deficit

Ana E. Carmo-Silva A B C D , Ana S. Soares A C , Jorge Marques da Silva A , Anabela Bernardes da Silva A , Alfred J. Keys B and Maria Celeste Arrabaça A
+ Author Affiliations
- Author Affiliations

A Centro de Engenharia Biológica and Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisbon, Portugal.

B Crop Performance and Improvement Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK.

C These authors contributed equally to this work.

D Corresponding author. Email: elizabete.carmo-silva@bbsrc.ac.uk

Functional Plant Biology 34(3) 204-213 https://doi.org/10.1071/FP06278
Submitted: 31 October 2006  Accepted: 29 January 2007   Published: 22 March 2007

Abstract

C4 plants are considered to be less sensitive to drought than C3 plants because of their CO2 concentrating mechanism. The C4 grasses, Paspalum dilatatum Poiret (NADP-ME), Cynodon dactylon (L.) Pers (NAD-ME) and Zoysia japonica Steudel (PEPCK) were compared in their response to water deficit imposed by the addition of polyethylene glycol to the nutrient solution in which they were grown. The effects of drought on leaf relative water content (RWC), net photosynthesis, stomatal conductance, carboxylating enzyme activities and chlorophyll a fluorescence were investigated. In C. dactylon the RWC was more sensitive, but the photosynthetic activity was less sensitive, to water deficit than in P. dilatatum and Z. japonica. The decrease of photosynthesis in P. dilatatum under water deficit was not closely related to the activities of the carboxylating enzymes or to chlorophyll a fluorescence. However, decreased activities of ribulose 1,5-bisphosphate carboxylase/oxygenase and phosphoenolpyruvate carboxylase, in addition to decreased stomatal conductance, may have contributed to the decrease of photosynthesis with drought in C. dactylon and Z. japonica. The different responses to water deficit are discussed in relation to the natural habitats of C4 grasses.

Additional keywords: C4 plants, drought, NADP-ME, NAD-ME, PEPCK.


Acknowledgements

This work was partially supported by ‘Programa de Desenvolvimento Educativo para Portugal’ (PRODEP III) and by ‘Federação Portuguesa de Golfe’. The authors thank Dr GL Lockett, Margot Forde Forage Germplasm Centre, New Zealand, for providing the seeds of P. dilatatum and Dr Daniel Ribeiro, Geodesenho, Portugal, for providing the seeds of C. dactylon and Z. japonica. The authors thank Ms Manuela Lucas of the Centro de Engenharia Biológica, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749–016 Lisbon, Portugal, for technical assistance; and Dr Stephen J Powers of the Biomathematics and Bioinformatics Division, Rothamsted Research, Harpenden, Herts., AL5 2JQ, UK, for advice on non-linear modelling. Note: Ana E. Carmo-Silva and Ana S. Soares have contributed equally to the work presented.


References


Bakrim N, Echevarria C, Cretin C, Arrio-Dupont M, Pierre JN, Vidal J, Chollet R, Gadal P (1992) Regulatory phosphorylation of sorghum leaf phosphoenolpyruvate carboxylase. Identification of the protein-serine kinase and some elements of the signal-transduction cascade. European Journal of Biochemistry 204, 821–830.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Beard JB (1982) ‘Turf management for golf courses.’ (Burgess Publishing: Minneapolis, MN)

Biehler K, Fock H (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiology 112, 265–272.
| PubMed |
open url image1

Brown RH (1999) Agronomic implication of C4 photosynthesis. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 173–211. (Academic Press: New York)

Catsky J (1960) Determination of water deficit in discs cut out from leaf blades. Biologia Plantarum 2, 76–77. open url image1

Chaves MM (1991) Effects of water deficits on carbon assimilation. Journal of Experimental Botany 42, 1–16.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought – from genes to the whole plant. Functional Plant Biology 30, 239–264.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Cornic G, Briantais J-M (1991) Partioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183, 178–184.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Du YC, Kawamitsu Y, Nose A, Hiyane S, Murayama S, Wasano K, Uchida Y (1996) Effects of water stress on carbon exchange rate and activities of photosynthetic enzymes in leaves of sugarcane (Saccharum sp.). Australian Journal of Plant Physiology 23, 719–726. open url image1

Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Annals of Botany 89, 183–189.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Foyer CH, Valadier A-H, Migge A, Becker TW (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiology 117, 283–292.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92. open url image1

Ghannoum O, von Caemerer S, Conroy JP (2002) The effect of drought on plant water use efficiency of nine NAD-ME and nine NADP-ME Australian C4 grasses. Functional Plant Biology 29, 1337–1348.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Ghannoum O, Conroy JP, Driscoll SP, Paul MJ, Foyer CH, Lawlor DW (2003) Nonstomatal limitations are responsible for drought-induced photosynthetic inhibition in four C4 grasses. New Phytologist 159, 599–608.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Hatch MD (1992) The making of the C4 pathway. In ‘Research in photosynthesis. Vol. III’. (Ed. M Murata) pp. 747–756. (Kluwer Academic Publishers: The Netherlands)

Hattersley PW (1992) C4 photosynthetic pathway variation in grasses (Poaceae): its significance for arid and semi-arid lands. In ‘Desertified grasslands: their biology and management’. (Ed. GP Chapman) pp. 181–212. (Academic Press: London)

Havaux M (1992) Stress tolerance of photosystem II in vivo. Antagonistic effects of water, heat, and photoinhibition stresses. Plant Physiology 100, 424–432.
| PubMed |
open url image1

Hewitt EJ (1966) ‘Sand and water culture methods.’ (Commonwealth Agricultural Bureau, Farnham Royal Buks: England)

Horton P , Bowyer JR (1990) Chlorophyll fluorescence transients. In ‘Methods in plant biochemistry. Vol. 4. Lipids, membranes and aspects of photobiology’. (Eds J Harwood, JR Bowyer) pp. 259–296. (Academic Press: New York)

Jagtap V, Bhargava S, Streb P, Feierabend J (1998) Comparative effect of water, heat and light on photosynthetic reactions in Sorghum bicolour (L.) Moench. Journal of Experimental Botany 49, 1715–1721.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta 376, 105–115.
| Crossref | PubMed |
open url image1

Lal A, Edwards E (1996) Analysis of inhibition of photosynthesis under water stress in the C4 species Amaranthus cruentus and Zea mays: electron transport, CO2 fixation and carboxylation capacity. Australian Journal of Plant Physiology 23, 403–412. open url image1

Lawlor DW (2002) Limitation to photosynthesis in water-stressed leaves: stomata vs. metabolism and the role of ATP. Annals of Botany 89, 871–885.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant, Cell & Environment 25, 275–294.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Long SP (1999) Environmental responses. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 215–249. (Academic Press: New York)

Long SP , Hällgren J-E (1985) Measurement of CO2 assimilation by plants in the field and in the laboratory. In ‘Techniques in bioproductivity and photosynthesis’. 2nd edn. (Eds J Coombs, DO Hall, SP Long, JMO Scullockpp) pp. 62–94. (Pergamon Press: Oxford)

Long SP , Hällgren J-E (1993) Measurement of CO2 assimilation by plants in the field and in the laboratory. In ‘Photosynthesis and production in a changing environment: a field and laboratory manual’. (Eds DO Hall, JMO Scurlock, HR Bolhàr-Nordenkampf, RC Leegood, SP Long) pp. 129–167. (Chapman & Hall: London)

Loreto F, Tricoli D, Di Marco G (1995) On the relationship between electron transport rate and photosynthesis in leaves of the C4 plant Sorghum bicolour exposed to water stress, temperature changes and carbon metabolism inhibition. Australian Journal of Plant Physiology 22, 885–892. open url image1

Lu C, Zhang J (1998) Effects of water stress on photosynthesis, chlorophyll fluorescence and photoinhibition in wheat plants. Australian Journal of Plant Physiology 25, 883–892. open url image1

Lu Z, Zhang J (1999) Effects of water stress on photosystem II photochemistry and its thermostability in wheat plants. Journal of Experimental Botany 50, 1199–1206.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Majumdar S, Ghosh S, Glick BR, Dumbroff EB (1991) Activities of chlorophyllase, phosphoenolpyruvate carboxylase and ribulose-1,5-bisphosphate carboxylase in the primary leaves of soybean during senescence and drought. Physiologia Plantarum 81, 473–480.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Maroco JP, Pereira JS, Chaves M (2000) Growth, photosynthesis and water-use efficiency of two C4 Sahelian grasses subjected to water deficits. Journal of Arid Environments 45, 119–137.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Marques da Silva J, Arrabaça MC (2004a) Photosynthesis in the water-stressed C4 grass Setaria sphacelata is mainly limited by stomata with both rapidly and slowly imposed water deficits. Physiologia Plantarum 121, 409–420.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Marques da Silva J, Arrabaça MC (2004b) Photosynthetic enzymes of the C4 grass Setaria sphacelata under water stress: a comparison between rapidly and slowly imposed water deficit. Photosynthetica 42, 43–47.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Money NP (1989) Osmotic pressure of aqueous polyethylene glycols – relationship between molecular weight and vapour pressure deficit. Plant Physiology 91, 766–769.
| PubMed |
open url image1

Mundree SG, Baker B, Mowla S, Peters S, Marais S , et al. (2002) Physiological and molecular insights into drought tolerance. African Journal of Biotechnology 1, 28–38. open url image1

Parry MAJ, Andralojc PJ, Parmar S, Keys AJ, Habash D, Paul MJ, Alred R, Quick WP, Servaites JC (1997) Regulation of Rubisco by inhibitors in the light. Plant, Cell & Environment 20, 528–534.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola J-M , et al. (1999) Climate and atmospheric history of the past 420 000 years from the Vostok ice core, Antarctica. Nature 399, 429–436.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Saccardy K, Cornic G, Brulfert J, Reyss A (1996) Effect of drought stress on net CO2 uptake by Zea leaves. Planta 199, 589–595.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Saccardy K, Pineau B, Roche O, Cornic G (1998) Photochemical efficiency of photosystem II and xanthophyll cycle components in Zea mays leaves exposed to water stress and high light. Photosynthesis Research 56, 57–66.
| 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 , Wedin DA , Li M (1999) The biogeography of C4 photosynthesis: patterns and controlling factors. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 313–373. (Academic Press: New York)

Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research 10, 51–62.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Slavík B (1974) ‘Methods of studying plant water relations. Ecological studies 9.’ (Springer-Verlag: Berlin)

Taub DR (2000) Climate and the US distribution of C4 grass subfamilies and decarboxylation variants of C4 photosynthesis. American Journal of Botany 87, 1211–1215.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tezara W, Mitchell V, Driscoll SP, Lawlor DW (1999) Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature 401, 914–917.
| Crossref | GoogleScholarGoogle Scholar | open url image1

von Caemmerer S, Farquhar GD (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376–387.
| Crossref | GoogleScholarGoogle Scholar | open url image1

Zhang SQ, Outlaw WH, Aghoram K (2001) Relationship between changes in guard cell abcisic-acid content and the other stress-related physiological parameters in intact plants. Journal of Experimental Botany 52, 301–308.
| Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhar JH (1996) ‘Biostatistical analysis.’ 3rd edn. (Prentice-Hall International, Inc.: New York)