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

Orchestration of transpiration, growth and carbohydrate dynamics in rice during a dry-down cycle

D. Luquet A C , A. Clément-Vidal A , D. Fabre A , D. This B , N. Sonderegger A and M. Dingkuhn A

A CIRAD, UPR 59, F-34398 Montpellier, France.

B CIRAD, UMR DAP, F-34398 Montpellier, France.

C Corresponding author. Email:

Functional Plant Biology 35(8) 689-704
Submitted: 12 February 2008  Accepted: 22 July 2008   Published: 19 September 2008


The regulation of carbohydrate metabolism and source–sink relationships among organs play a key role in plant adaptation to drought. This study aimed at characterising the dynamics of transpiration, development, growth and carbon metabolism, as well as the expression of invertase genes, in response to drought during a dry-down cycle. Three 1-month experiments were conducted in controlled environment using the rice genotype IR64 (Oryza sativa L., indica). Plant leaf relative transpiration and expansion rates decreased linearly when fraction of transpirable soil water (FTSW) dropped below 0.66 and 0.58, respectively. Hexose and starch concentration responses to FTSW in a given organ were generally linear and opposite: in source leaves, hexose concentration increased and starch decreased, and vice versa in sink leaves and roots. Sucrose remained constant in source leaves and increased slightly in sink leaves. Starch reserves built up during stress in sink organs were rapidly mobilised upon rewatering, indicating its involvement in a mechanism to ensure recovery. Expression of cell-wall and vacuolar invertase genes under stress increased in sink leaves, interpreted as a mechanism to maintain sink activity (cell wall) and osmotic adjustment (vacuolar). It is concluded that carbohydrate metabolism in sink organs under drought is highly regulated, and important for stress adaptation.


Allen RG , Pereira LS , Raes D , Smith M (1998) ‘Crop evapotranspiration – guidelines for computing crop water requirements – FAO irrigation and drainage paper 56.’ (FAO: Rome)

Araus JL Slafer JA Reynolds MP Roy C 2002 Plant breeding and drought in C3 cereals: what should we breed for? Annals of Botany 89 925 940 doi:10.1093/aob/mcf049

Black CC , Loboda T , Chen JQ , Sung SJS (1995) Can sucrose cleavage enzymes serve as markers for sink strenght and is sucrose a signal molecule during plant sink development. In ‘International symposium on sucrose metabolism’. pp. 49–64. (American Society of Plant Physiologists)

Bonfig KB Berger S Fatima T Gonzalez MC Roitsch T 2007 Metabolic control of seedling development by invertases. Functional Plant Biology 34 508 516 doi:10.1071/FP06206

Casadebaig P Debaeke P Lecoeur J 2008 Thresholds for leaf expansion and transpiration response to soil water deficit in a range of sunflower genotypes. European Journal of Agronomy 28 646 654 doi:10.1016/j.eja.2008.02.001

Chavez-Barcenas AT Valdez-Alarcon JJ Martynez-Trujillo M Chen L Xoconostle-Cazares B Lucas WJ Herrera-Estrella L 2000 Tissue-specific and developmental pattern of expression of the rice sps1 gene. Plant Physiology 124 641 653 doi:10.1104/pp.124.2.641

Cho JI Lee SK Ko S Kim HK Jun SH et al 2005 Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.). Plant Cell Reports 24 225 236 doi:10.1007/s00299-004-0910-z

Clerget B Gozé E Rattunde H Dingkuhn M Ney B 2007 Development- and growth-rate variability patterns of photoperiod-sensitive sorghums. Annals of Botany in press

Dingkuhn M Audebert A Jones MP Etienne K Sow A 1999 Control of stomatal conductance and leaf rolling in O. sativa and O. glaberrima upland rice. Field Crops Research 61 223 236

Dingkuhn M Luquet D Quilot B Reffye PD 2005 Environmental and genetic control of morphogenesis in crops: towards models simulating phenotypic plasticity. Australian Journal of Agricultural Research 56 1289 1302 doi:10.1071/AR05063

Dingkuhn M , Luquet D , Clément-Vidal A , Tambour L , Kim HK , Song YH (2007) Is plant growth driven by sink regulation? Implications for crop models, phenotyping approaches and ideotypes. In ‘Scale and complexity in plant systems research: gene–plant–crop relations’. (Eds PCSHJ Spiertz, HH van Laar) pp. 157–170. (Wageningen)

Fisher KS (2003) ‘Breeding rice for drought prone environment.’ (International Rice Research Institute: Los Baños, Philippines)

Foulkes MJ Sylvester-Bradley R Weightman R Snape JW 2007 Identifying physiological traits associated with improved drought resistance in winter wheat. Field Crops Research 103 11 24 doi:10.1016/j.fcr.2007.04.007

Foyer CH Valadier MH 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 doi:10.1104/pp.117.1.283

Hammer GL Kropff MJ Sinclair TR Porter JR 2002 Future contributions of crop modelling – from heuristics and supporting decision making to understanding genetic regulation and aiding crop improvement. European Journal of Agronomy 18 15 31 doi:10.1016/S1161-0301(02)00093-X

Heyer AG Raap M Schroeer B Marty B Willmitzer L 2004 Cellwall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. The Plant Journal 39 161 169 doi:10.1111/j.1365-313X.2004.02124.x

Ji X Van den Ende W Van Laere A Cheng S Bennett J 2005 a Structure, evolution, and expression of the two invertase gene families of rice. Journal of Molecular Evolution 60 615 634 doi:10.1007/s00239-004-0242-1

Ji X Raveendran M Oane R Ismail A Lafitte R Bruskiewich R Cheng SH Bennett J 2005 b Tissue-specific expression and drought responsiveness of cell-wall invertase genes of rice at flowering. Plant Molecular Biology 59 945 964 doi:10.1007/s11103-005-2415-8

Kim JY Mahé A Brangeon J Prioul JL 2000 A maize vacuolar invertase, IVR2, is induced by water stress. Organ/tissue specificity and diurnal modulation of expression. Plant Physiology 124 71 84 doi:10.1104/pp.124.1.71

Lecoeur J Sinclair TR 1996 Field pea transpiration and leaf growth in response to soil water deficits. Crop Science 36 331 335

Lecoeur J Guilioni L 1998 Rate of leaf production in response to soil water deficits in field pea. Field Crops Research 57 319 328

Leonardi S Piovani P Magnani F Menozzi P 2006 A simple general method to evaluate intra-specific transpiration parameters within and among seedling families. Oecologia 149 185 193 doi:10.1007/s00442-006-0427-y

Liu F 2004 Root signal controls pod growth in drought-stressed soybean during the critical, abortion-sensitive phase of pod development. Field Crops Research 85 159 166 doi:10.1016/S0378-4290(03)00164-3

Liu F Jensen CR Andersen MN 2004 a Drought stress effect on carbohydrate concentration in soybean leaves and pods during early reproductive development: its implicaton in altering pod set. Field Crops Research 86 1 13 doi:10.1016/S0378-4290(03)00165-5

Liu L Lafitte R Guan D 2004 b Wild Oryza species as potential sources of drought-adaptive traits. Euphytica 138 149 161 doi:10.1023/B:EUPH.0000046801.27042.14

Liu F Andersen MN Jacobsen SE Jensena CR 2005 a Stomatal control and water use efficiency of soybean (Glycine max L.Merr.) during progressive soil drying. Environmental and Experimental Botany 54 33 40 doi:10.1016/j.envexpbot.2004.05.002

Liu F Jensen CR Andersen MN 2005 b A review of drought adaptation in crop plants: changes in vegetative and reproductive physiology induced by ABA-based chemical signals. Australian Journal of Agricultural Research 56 1245 1252 doi:10.1071/AR05062

Livak KJ Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT. Methods 25 402 408 doi:10.1006/meth.2001.1262

Luquet D Zhang B Dingkuhn M Dexet A Clément-Vidal A 2005 Phenotypic plasticity of rice seedlings: case of phosphorus deficiency. Plant Production Science 8 145 151 doi:10.1626/pps.8.145

Luquet D Dingkuhn M Kim HK Tambour L Clément-Vidal A 2006 EcoMeristem, a model of morphogenesis and competition among sinks in rice. 1. Concept, validation and sensitivity analysis. Functional Plant Biology 33 309 323 doi:10.1071/FP05266

Masinde PW Stutzel H Agong SG Fricke A 2006 Plant growth, water relations and transpiration of two species of african nightshade (Solanum villosum Mill. ssp. Miniatum (Bernh. ex Willd.) edmonds and S. sarrachoides Sendtn.) under water-limited conditions. Scientia Horticulturae 110 7 15 doi:10.1016/j.scienta.2006.06.003

Mengel K Arneke WW 1982 Effect of potassium on the water potential, the pressure potential, the osmotic potential and cell elongation in leaves of Phaseolus vulgaris. Physiologia Plantarum 54 402 408 doi:10.1111/j.1399-3054.1982.tb00699.x

Pellegrino A Lebon E Voltz M Wery J 2005 Relationships between plant and soil water status in vine (Vitis vinifera L.). Plant and Soil 266 129 142 doi:10.1007/s11104-005-0874-y

Pelleschi S Rocher JP Prioul JL 1997 Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant, Cell & Environment 20 493 503 doi:10.1046/j.1365-3040.1997.d01-89.x

Pelleschi S Leonardi A Rocher JP Cornic D de Vienne D Thévenot C Prioul JL 2006 Analysis of the relationships between growth, photosynthesis and carbohydrate metabolism using quantitative trait loci (QTLs) in young maize plants subjected to water deprivation. Molecular Breeding 17 21 39

Ray DJ Sinclair TR 1997 Stomatal closure of maize hybrids in response to soil drying. Crop Science 37 803 807

Reymond M Muller B Leonardi A Charcosset A Tardieu F 2003 Combining quantitative trait loci analysis and an ecophysiological model to analyse the genetic variability of the responses of maize leaf growth to temperature and water deficit. Plant Physiology 131 664 675

Reymond M Muller B Tardieu F 2004 Dealing with the genotype × environment interaction via a modelling approach: a comparison of QTLs of maize leaf length or width with QTLs of model parameters. Journal of Experimental Botany 55 2461 2472 doi:10.1093/jxb/erh200

Rognoni S Teng S Arru L Smeekens SCM Perata P 2007 Sugar effects on early seedling development in Arabidopsis. Plant Growth Regulation 52 217 228 doi:10.1007/s10725-007-9193-z

Roitsch T Gonzales M 2004 Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9 606 613 doi:10.1016/j.tplants.2004.10.009

Roitsch T Ehne R Goetz M Hause B Hofmann M Krishna Sinha A 2000 Regulation and function of extracellular invertase from higher plants in relation to assimilate partitioning, stress responses and sugar signalling. Australian Journal of Plant Physiology 27 815 825

Rolland F Baena-Gonzalez E Sheen J 2006 Sugar sensing and signaling in plants: conserved and novel mechanisms. Annual Review of Plant Biology 57 675 709

Rouphael Y Colla G 2004 Modelling the transpiration of a greenhouse zucchini crop grown under a Mediterranean climate using the Penman–Monteith equation and its simplified version. Australian Journal of Agricultural Research 55 931 937 doi:10.1071/AR03247

Sherson SM Alford HL Forbes SM Wallace G Smith SM 2003 Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. Journal of Experimental Botany 54 525 531 doi:10.1093/jxb/erg055

Soltani A Ghassemi-Golenazi K Khooie FR Moghaddam M 1999 A simple model for chickpea growth and yield. Field Crops Research 62 213 224 doi:10.1016/S0378-4290(99)00017-9

Stitt M Gibon Y Lunn JE Piques M 2007 Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment. Functional Plant Biology 34 526 549 doi:10.1071/FP06249

Tardieu F Reymond M Hamard P Granier C Muller B 2000 Spatial distributions of expansion rate, cell division rate and cell size in maize leaves: a synthesis of the effects of soil water status, evaporative demand and temperature. Journal of Experimental Botany 51 1505 1514 doi:10.1093/jexbot/51.350.1505

Tardieu F Reymond M Muller B Granier C Simonneau T Sadok W Welcker C 2005 Linking physiological and genetic analyses of the control of leaf growth under changing environmental conditions. Australian Journal of Agricultural Research 56 937 946 doi:10.1071/AR05156

Travaglia C Cohen AC Reinoso H Castillo C Bottini R 2007 Exogenous abscisic acid increases carbohydrate accumulation and redistribution to the grains in wheat grown under field conditions of soil water restriction. Journal of Plant Growth Regulation 26 285 289 doi:10.1007/s00344-007-9018-3

Trouverie J Prioul JL 2006 Increasing leaf export and grain import capacities in maize plants under water stress. Functional Plant Biology 33 209 218 doi:10.1071/FP05206

Trouverie J Thévenot C Rocher JP Sotta B Prioul JL 2003 The role of abscisic acid in the response of a specific vacuolar invertase to water stress in the adult maize leaf. Journal of Experimental Botany 54 2177 2186 doi:10.1093/jxb/erg234

Turner NC 1996 Further progress in crop water relations. Advances in Agronomy 58 293 338 doi:10.1016/S0065-2113(08)60258-8

Vaughn MV Harrington GN Bush DR 2002 Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proceedings of the National Academy of Sciences of the United States of America 99 10876 10880 doi:10.1073/pnas.172198599

Waclawovsky AJ Loureiro ME Freitas RL Rocha CS Cano MAO Fontes EBP 2006 Evidence for the sucrose-binding protein role in carbohydrate metabolism and transport at early developmental stage. Physiologia Plantarum 128 391 404 doi:10.1111/j.1399-3054.2006.00751.x

Wingler A Purdy S MacLean JA Pourtau N 2006 The role of sugars in integrating environmental signals during the regulation of leaf senescence. Journal of Experimental Botany 57 391 399 doi:10.1093/jxb/eri279

Yang J Zhang J Wang Z Zhu Q Liu L 2002 Abscisic acid and cytokinins in the root exudates and leaves and their relationship to senescence and remobilization of carbon reserves in rice subjected to water stress during grain filling. Planta 215 645 652 doi:10.1007/s00425-002-0789-2

Yang J Zhang J Wang Z Zhu Q 2003 a Hormones in the grains in relation to sink strength and postanthesis development of spikelets in rice. Plant Growth Regulation 41 185 195 doi:10.1023/B:GROW.0000007503.95391.38

Yang J Zhang J Wang Z Zhu Q Liu L 2003 b Activities of enzymes involved in sucrose-to-starch metabolism in rice grain subjected to water stress during grain filling. Field Crops Research 81 69 81 doi:10.1016/S0378-4290(02)00214-9

Yang J Zhang J Wang Z Zhu Q Liu L 2004 Activities of fructan- and sucrose-metabolizing enzymes in wheat stems subjected to water stress during grain filling. Planta 220 331 343 doi:10.1007/s00425-004-1338-y

Export Citation Cited By (20)