Regulation and recovery of sink strength in rice plants grown under changes in light intensity
Tanguy Lafarge A B E , Célia Seassau C , Meryll Martin D , Crisanta Bueno A , Anne Clément-Vidal B , Eva Schreck B and Delphine Luquet BA Crop and Environmental Sciences Division, International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines.
B Centre de Coopération Internationale en Recherche Agronomique pour le Développement, UPR AIVA, TA 70/01, Avenue Agropolis, 34398 Montpellier, France.
C INRA, UMR AGIR, Chemin de Borde Rouge, Auzeville, 31320 Castanet Tolosan, France.
D Université de Neuchatel, Faculté des Sciences, Institut de Biologie, Laboratoire de Physiologie Végétale, rue Emile Argand, 11/CP 158, 2009 Neuchatel, Switzerland.
E Corresponding author. Email: tanguy.lafarge@cirad.fr
Functional Plant Biology 37(5) 413-428 https://doi.org/10.1071/FP09137
Submitted: 4 June 2009 Accepted: 1 January 2010 Published: 30 April 2010
Abstract
The aim of this study was to characterise the sequence of traits that influence the response of rice morphogenesis to a shortage in carbohydrate supply and to its recovery. Plants were grown under 70% shading or full-light exposure for distinct periods during the vegetative and early reproductive phases in field and controlled environments. Lower organ vigour (i.e. higher specific leaf area and specific stem length), sugar concentration, tiller emergence and leaf elongation rate; higher leaf blade to sheath length ratio and preferential assimilate allocation to sink (elongating) leaves, were observed soon after the onset of shading. Organ vigour was affected before any appreciable effect on tiller emergence was noted. All the processes resumed after the shading removal, which coincided with a boost in sugar concentration; however, the extent of recovery in organ vigour and tillering depended on the growth stage at which shading was applied. It is concluded that crop response to changes in carbohydrate supply at the early stage favoured leaf area production by adjusting transient reserve levels and biomass allocation. Results of this study provide further insights into the role of soluble carbohydrates in plant and crop phenotypic plasticity and, thus, into the value of such processes in plant growth models.
Additional keywords: biomass partitioning, morphogenesis, regulation, shading, soluble sugar and starch, tillering.
Acknowledgements
We thank Nicole Sonderegger, Denis Fabre, Pedro Gapas, Rene Carandang, Luis Malabayabas, Victor Lubigan for the experimental setup in the field and in the growth chamber and plant process in the laboratory and Dr Bill Hardy for editing.
Andrieu B,
Hillier J, Birch C
(2006) Onset of sheath extension and duration of lamina extension are major determinants of the response of maize lamina length to plant density. Annals of Botany 98, 1005–1016.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ballaré CL, Casal JJ
(2000) Light signals perceived by crop and weed plants. Field Crops Research 67, 149–160.
| Crossref | GoogleScholarGoogle Scholar |
Beemster GTS, Masle J
(1996) Effects of soil resistance to root penetration on leaf expansion in wheat (Triticum aestivum L.): composition, number and size of epideraml cells in mature blades. Journal of Experimental Botany 47, 1651–1662.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Binder BM,
O’Malley RC,
Wang W,
Moore JM,
Parks BM,
Spalding EP, Bleecker AB
(2004)
Arabidopsis seedling growth response and recovery to ethylene: a kinetic analysis. Plant Physiology 136, 2913–2920.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Blum A
(1998) Improving wheat grain filling under stress by stem reserve mobilization. Euphytica 100, 77–83.
| Crossref | GoogleScholarGoogle Scholar |
Bonnett GD, Incoll LD
(1993) Effects on the stem of winter barley of manipulating the source and sink during grain filling. 1. Changes in accumulation and loss of mass from internodes. Journal of Experimental Botany 44, 75–82.
| Crossref | GoogleScholarGoogle Scholar |
Bruce TJA,
Matthes MC,
Nappier JA, Pickett J
(2007) Stressful ‘memories’ of plants: evidence and possible mechanisms. Plant Science 173, 603–608.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Caton BP,
Forin TC, Hill JE
(1997) Mechanisms of competition for light between rice (Oryza sativa) and redstem (Ammannia spp.). Weed Science 45, 269–275.
|
CAS |
Chenu K,
Chapman SC,
Hammer GL,
Mclean G,
Ben Haj Salah H, Tardieu F
(2008) Short-term responses of leaf growth rate to water deficit scale up to whole-plant and crop levels: an integrated modeling approach in maize. Plant, Cell & Environment 31, 378–391.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
De Lacerda CF,
Cambraia J,
Oliva MA, Ruiz HA
(2005) Changes in growth and in solute concentrations in sorghum leaves and roots during salt stress recovery. Environmental and Experimental Botany 54, 69–76.
| Crossref | GoogleScholarGoogle Scholar |
Dingkuhn M, Le Gal PY
(1996) Effect of drainage date on yield and dry matter partitioning in irrigated rice. Field Crops Research 46, 117–126.
| Crossref | GoogleScholarGoogle Scholar |
Dingkuhn M,
Johnson DE,
Sow A, Audebert AY
(1999) Relationship between upland rice canopy characteristics and weed competitiveness. Field Crops Research 61, 79–95.
| Crossref | GoogleScholarGoogle Scholar |
Dingkuhn M,
Luquet D,
Quilot B, de Reffye PD
(2005) Environmental and genetic control of morphogenesis in crops: towards models simulating phenotypic plasticity. Australian Journal of Agricultural Research 56, 1289–1302.
| Crossref | GoogleScholarGoogle Scholar |
Dingkuhn M,
Luquet D,
Kim HK,
Tambour L, Clément-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 |
CAS |
Fetene M, Beck E
(1993) Reversal of direction of photosynthate allocation in Urtica dioica L. contrasting leaf length. Annals of Botany 83, 423–429.
Fiorani F,
Beemster TSG,
Bultynck L, Lambers H
(2000) Can meristematic activity determine variation in leaf size and elongation rate among 4 Poa species? A kinematic study. Plant Physiology 124, 845–855.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Franklin KA
(2008) Shade avoidance. New Phytologist 179, 930–944.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gao LZ,
Jin ZQ, Li L
(1987) Photo-thermal models of rice growth duration for various varietal types in China. Agricultural and Forest Meteorology 39, 205–213.
| Crossref |
Gautier H,
Varlet-Grancher C, Hazard L
(1999) Tillering responses to the light environment and to defoliations in populations of perennial ryegrass (Lolium perenne L.) selected for contrasting leaf length. Annals of Botany 83, 423–429.
| Crossref |
Geigenberger P,
Muller-Rober B, Stitt M
(1999a) Contribution of adenosine 5′-diphosphoglucose pyrophosphorylase to the control of starch synthesis is decreased by water stress in growing potato tubers. Planta 209, 338–345.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Geigenberger P,
Reimholz R,
Deiting U,
Sonnewald U, Stitt M
(1999b) Decreased expression of sucrose phosphate synthase strongly inhibits the water stress-induced synthesis of sucrose in growing potato tubers. The Plant Journal 19, 119–129.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Geigenberger P,
Kolbe A, Tiessen A
(2005) Redox regulation of carbon storage and partitioning in response to light and sugars. Journal of Experimental Botany 56, 1469–1479.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Geiger DR,
Servaites JC, Fuchs MA
(2000) Role of starch in carbon translocation and partitioning at the plant level. Australian Journal of Plant Physiology 27, 571–582.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gibon Y,
Blaesing OE,
Hannemann J,
Carillo P,
Hohne M,
Hendriks JHM,
Palacios N,
Cross J,
Selbig J, Stitt M
(2004) A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. The Plant Cell 16, 3304–3325.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Granier C, Tardieu F
(1999) Leaf expansion and cell division are affected by reducing absorbed light before but not after the decline in cell division rate in sunflower leaf. Plant, Cell & Environment 22, 1365–1376.
| Crossref | GoogleScholarGoogle Scholar |
Haefele SM,
Johnson DE,
M’Bodj D,
Wopereis MCS, Miezan KM
(2004) Field screening of diverse rice genotypes for weed competitiveness in irrigated lowland ecosystems. Field Crops Research 88, 39–56.
| Crossref | GoogleScholarGoogle Scholar |
Hammer GL,
Carberry PS, Muchow RC
(1993) Modelling genotypic and environmental control of leaf area dynamics in grain sorghum. I. Whole-plant level. Field Crops Research 33, 293–310.
| Crossref | GoogleScholarGoogle Scholar |
Heuvelink E, Buiskool RPM
(1995) Influence of sink–source interaction on dry matter production in tomato. Annals of Botany 75, 381–389.
| Crossref | GoogleScholarGoogle Scholar |
Jamieson PD,
Brooking IR,
Porter JR, Wilson DR
(1995) Prediction of leaf appearance in wheat: a question of temperature. Field Crops Research 41, 35–44.
| Crossref | GoogleScholarGoogle Scholar |
Katsuhara M, Shibasaka M
(2000) Cell death and growth recovery of barley after transient salt stress. Journal of Plant Research 113, 239–243.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Kim HK,
Luquet D,
Hammer G,
Van Oosteroom E, Dingkuhn M
(2010) Regulation of tillering in sorghum: Environmental effects. Annals of Botany in press ,
| PubMed |
Kiniry JR
(1993) Non-structural carbohydrate utilization by wheat shaded during grain growth. Agronomy Journal 85, 844–849.
|
CAS |
Kirby EJM,
Appleyard M, Fellowes G
(1985) Leaf emergence and tillering in barley and wheat. Agronomie 5, 193–200.
| Crossref | GoogleScholarGoogle Scholar |
Kobata T,
Sugawara M, Takatu S
(2000) Shading during the early filling period does not affect potential grain dry matter increase in rice. Agronomy Journal 92, 411–417.
Kobayasi K,
Horie Y, Imaki T
(2002) Relationship between apical dome diameter at panicle initiation and the size of panicle components in rice grown under different nitrogen conditions during the vegetative stage. Plant Production Science 5, 3–7.
| Crossref | GoogleScholarGoogle Scholar |
Lafarge T, Hammer GL
(2002a) Predicting plant leaf area production: shoot assimilate accumulation and partitioning and leaf area ratio, are stable for a wide range of sorghum population density. Field Crops Research 77, 137–151.
| Crossref | GoogleScholarGoogle Scholar |
Lafarge T, Hammer GL
(2002b) Tillering in grain sorghum over a wide range of population densities: modelling dynamics of tiller fertility. Annals of Botany 90, 99–110.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lafarge T,
de Raïssac M, Tardieu F
(1998) Elongation rate of sorghum leaves has a common response to meristem temperature in diverse African and European environmental conditions. Field Crops Research 58, 69–79.
| Crossref | GoogleScholarGoogle Scholar |
Lafarge T,
Broad IJ, Hammer GL
(2002) Tillering in grain sorghum over a wide range of population densities: identification of a common hierarchy for tiller emergence, leaf area development and fertility. Annals of Botany 90, 87–98.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Lafitte HR, Travis RL
(1984) Photosynthesis and assimilate partitioning in closely related lines of rice exhibiting different sink: source relationships. Crop Science 24, 447–452.
Lee JH, Heuvelink E
(2003) Simulation of leaf area development based on dry matter partitioning and specific leaf area for cut chrysanthemum. Annals of Botany 91, 319–327.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Legros S,
Mialet-Serra I,
Caliman JP,
Siregar FA,
Clément-Vidal A,
Fabre D, Dingkuhn M
(2009) Role of transitory carbon reserves during adjustment to climate variability and source–sink imbalances in oil palm (Elaeis guineensis). Tree Physiology 29, 1199–1211.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Li F,
Bao W,
Wu N, You C
(2008) Growth, biomass partitioning and water-use efficiency of a leguminous schrub (Bauhinia faberi var. microphylla) in response to various water availabilities. New Forests 36, 53–65.
| Crossref | GoogleScholarGoogle Scholar |
Liu F,
Jensen CR, ersen MN
(2004) 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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Liu F,
Jensen CR, ersen MN
(2005) 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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
| Crossref | GoogleScholarGoogle Scholar |
Luquet D,
Clément-Vidal A,
This D,
Fabre D,
Sonderegger N, Dingkuhn M
(2008) Orchestration of transpiration, growth and carbohydrate dynamics in rice during a dry-down cycle. Functional Plant Biology 35, 689–704.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Miller BC,
Hill JE, Roberts SR
(1991) Plant population effects on growth and yield in water seeded rice. Agronomy Journal 83, 291–297.
Monaco TA,
Johnson DA, Creech JE
(2005) Morphological and physiological responses of the invasive weed Isatis tinctoria to contrasting light, soil-nitrogen and water. Weed Research 45, 460–466.
| Crossref | GoogleScholarGoogle Scholar |
Nelson DW, Sommers LE
(1980) Total nitrogen analysis of soil and plant tissues. Journal – Association of Official Analytical Chemists 63, 770–778.
|
CAS |
Nicholas PK,
Kemp PD, Barker DJ
(2004) Stress and recovery of hill pastures in the North Island of New Zealand. Grass and Forage Science 59, 250–263.
| Crossref | GoogleScholarGoogle Scholar |
Niinemets U
(2007) Photosynthesis and resource distribution through plant canopies. Plant, Cell & Environment 30, 1052–1071.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Okawa S,
Makino A, Mae T
(2003) Effects of irradiance on the partitioning of assimilated carbon during the early phase of grain filling in rice. Annals of Botany 92, 357–364.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ong CK, Marshall C
(1979) The growth and survival of severely-shaded tillers in Lolium perenne L. Annals of Botany 43, 147–155.
Peng S,
Garcia FV,
Gines HC,
Laza RC,
Samson MI,
Sanico AL,
Visperas RM, Cassman KG
(1996) Nitrogen use efficiency of irrigated tropical rice established by broadcast wet-seeding and transplanting. Nutrient Cycling in Agroecosystems 45, 123–134.
| Crossref | GoogleScholarGoogle Scholar |
Phillips I
(1975) Apical dominance. Annual Review of Plant Physiology 26, 341–367.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Poorter H, De Jong R
(1999) A comparison of specific leaf area, chemical composition and leaf construction costs of field plants from 15 habits differing in productivity. New Phytologist 143, 163–176.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Puijalon S, Bornette G
(2006) Phenotypic plasticity and mechanical stress: biomass partitioning and clonal growth of an aquatic plant species. American Journal of Botany 93, 1090–1099.
| Crossref | GoogleScholarGoogle Scholar |
Reymond M,
Muller B, Tardieu F
(2004) Dealing with the genotype x 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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schnier HF,
Dingkuhn M,
De Datta SK,
Mengel K, Faronilo JE
(1990a) Nitrogen fertilization of direct-seeded flooded vs. transplanted rice. I. Nitrogen uptake, photosynthesis, growth and yield. Crop Science 30, 1276–1284.
Schnier M,
Dingkuhn M,
de Datta SK,
Mengel K,
Wijanco E, Javellana C
(1990b) Nitrogen economy and canopy carbon dioxide assimilation of tropical lowland rice. Agronomy Journal 82, 451–459.
Shane MW,
Vos MD,
Roock SD, Lambers H
(2003) Shoot P status regulates cluster-root growth and citrate exudation in Lupinus albus grown with a derived root system. Plant, Cell & Environment 26, 265–273.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Tardieu F,
Granier C, Muller B
(1999) Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate? New Phytologist 143, 33–43.
| Crossref | GoogleScholarGoogle Scholar |
Wilson PJ,
Thompson K, Hodgson JG
(1999) Specific leaf area and dry matter content as alternative predictors of plant strategies. New Phytologist 143, 155–162.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wright SD, McConnaughay KDM
(2002) Interpreting phenotype plasticity: the importance of ontogeny. Plant Species Biology 17, 119–131.
| Crossref | GoogleScholarGoogle Scholar |
Yamamoto TD,
Kurokawa H,
Nitta Y, Yoshida T
(1995) Varietal differences of tillering response to shading and nitrogen levels in rice plant: comparison between high tillering semi dwarf indica and low tillering japonica. Nihon Sakumotsu Gakkai Kiji 64, 227–234.
Yang J,
Zhang J,
Wang Z,
Zhu Q, Wang W
(2001) Remobilization of carbon reserves in response to water deficit during grain filling of rice. Field Crops Research 71, 47–55.
| Crossref | GoogleScholarGoogle Scholar |
