Seasonal effects on the relationship between photosynthesis and leaf carbohydrates in orange trees
Rafael V. Ribeiro A E , Eduardo C. Machado A , Gustavo Habermann B , Mauro G. Santos C and Ricardo F. Oliveira D
+ Author Affiliations
- Author Affiliations
A Laboratório de Fisiologia Vegetal ‘Coaracy M. Franco’, Centro de Pesquisa e Desenvolvimento em Ecofisiologia e Biofísica, Instituto Agronômico, IAC, PO Box 28, 13012-970, Campinas, SP, Brazil.
B Departamento de Botânica, Instituto de Biociências, Univ Estadual Paulista, UNESP, 13506-900, Rio Claro, SP, Brazil.
C Departamento de Botânica, Universidade Federal de Pernambuco, 50670-901, Recife, PE, Brazil.
D Departamento de Ciências Biológicas, Escola Superior de Agricultura ‘Luiz de Queiroz’, Universidade de São Paulo, PO Box 9, 13418-900, Piracicaba, SP, Brazil.
E Corresponding author. Email: rafael@iac.sp.gov.br
Functional Plant Biology 39(6) 471-480 https://doi.org/10.1071/FP11277
Submitted: 6 May 2011 Accepted: 26 March 2012 Published: 24 April 2012
Abstract
To understand the effect of summer and winter on the relationships between leaf carbohydrate and photosynthesis in citrus trees growing in subtropical conditions, ‘Valencia’ orange trees were subjected to external manipulation of their carbohydrate concentration by exposing them to darkness and evaluating the maximal photosynthetic capacity. In addition, the relationships between carbohydrate and photosynthesis in the citrus leaves were studied under natural conditions. Exposing the leaves to dark conditions decreased the carbohydrate concentration and increased photosynthesis in both seasons, which is in accordance with the current model of carbohydrate regulation. Significant negative correlations were found between total non-structural carbohydrates and photosynthesis in both seasons. However, non-reducing sugars were the most important carbohydrate that apparently regulated photosynthesis on a typical summer day, whereas starch was important on a typical winter day. As a novelty, photosynthesis stimulation by carbohydrate consumption was approximately three times higher during the summer, i.e. the growing season. Under subtropical conditions, citrus leaves exhibited relatively high photosynthesis and high carbohydrate levels on the summer day, as well as a high nocturnal consumption of starch and soluble sugars. A positive association was determined between photosynthesis and photoassimilate consumption/exportation, even in leaves showing a high carbohydrate concentration. This paper provides evidence that photosynthesis in citrus leaves is regulated by an increase in sink demand rather than by the absolute carbohydrate concentration in leaves.
Additional keywords: Citrus sinensis, gas exchange, growth, seasonality, source–sink.
References
Ainsworth EA, Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology 155, 64–69.| Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFagsLo%3D&md5=de9bc4de6ed8a590d531e54403f51e8aCAS |
Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170, 489–504.
| Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins.Crossref | GoogleScholarGoogle Scholar |
Bueno ACR, Prudente DA, Machado EC, Ribeiro RV (2011) Daily temperature amplitude affects the vegetative growth and carbon metabolism of orange trees in a rootstock-dependent manner. Journal of Plant Growth Regulation 30,
| Daily temperature amplitude affects the vegetative growth and carbon metabolism of orange trees in a rootstock-dependent manner.Crossref | GoogleScholarGoogle Scholar |
Bush DR (1999) Sugar transporters in plant biology. Current Opinion in Plant Biology 2, 187–191.
| Sugar transporters in plant biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1Cgs70%3D&md5=9c0f5c2dfc40ea86a91b82d0d9b12d05CAS |
Davies FS, Albrigo LG (1994) ‘Citrus.’ (CAB International: Wallingford, UK)
De Schepper V, Steppe K, Van Labeke MC, Lemeur R (2010) Detailed analysis of double girdling effects on stem diameter variations and sap flow in young oak trees. Environmental and Experimental Botany 68, 149–156.
| Detailed analysis of double girdling effects on stem diameter variations and sap flow in young oak trees.Crossref | GoogleScholarGoogle Scholar |
Dickson RE (1991) Assimilate distribution and storage. In ‘Physiology of trees’. (Ed. AS Raghavendra) pp. 51–85. (John Wiley & Sons: New York)
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.
Goldschmidt EE, Golomb A (1982) The carbohydrate balance of alternate-bearing citrus trees and the significance of reserves for flowering and fruiting. Journal of the American Society for Horticultural Science 107, 206–208.
Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiology 99, 1443–1448.
| Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtV2jt7o%3D&md5=efe9356fceb3db9778a463ad848f3c4cCAS |
Goldschmidt EE, Koch KE (1996) Citrus. In ‘Photoassimilate distribution in plants and crops: source-sink relationships’. (Eds E Zamski, AA Schaffer) pp. 797–823. (Marcel Dekker: New York)
Habermann G, Rodrigues JD (2009) Leaf gas exchange and fruit yield in sweet orange trees as affected by citrus variegated chlorosis and environmental conditions. Scientia Horticulturae 122, 69–76.
| Leaf gas exchange and fruit yield in sweet orange trees as affected by citrus variegated chlorosis and environmental conditions.Crossref | GoogleScholarGoogle Scholar |
Iglesias DJ, Lliso I, Tadeo FR, Talon M (2002) Regulation of photosynthesis through source-sink imbalance in citrus is mediated by carbohydrate content in leaves. Physiologia Plantarum 116, 563–572.
| Regulation of photosynthesis through source-sink imbalance in citrus is mediated by carbohydrate content in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xptlejtr0%3D&md5=ae86bb59c98d434d52b22a09c1c4aa0fCAS |
Kalt-Torres W, Keer PS, Usuda H, Huber SC (1987) Diurnal changes in maize leaf photosynthesis. 1. Carbon exchange rate, assimilate export rate, and enzyme activities. Plant Physiology 83, 283–288.
| Diurnal changes in maize leaf photosynthesis. 1. Carbon exchange rate, assimilate export rate, and enzyme activities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhtlGmsL4%3D&md5=322d8cb8e80d4df021869becd250171eCAS |
Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509–540.
| Carbohydrate-modulated gene expression in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgtrY%3D&md5=6827dc2ec0d449b0bc46a02e103db5e3CAS |
Li CY, Weiss D, Goldschmidt EE (2003) Effects of carbohydrate starvation on gene expression in citrus root. Planta 217, 11–20.
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochemical Society Transactions 11, 591–592.
McCormick AJ, Cramer MD, Watt DA (2006) Sink strength regulates photosynthesis in sugarcane. New Phytologist 171, 759–770.
| Sink strength regulates photosynthesis in sugarcane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVSku7%2FP&md5=66b1a38e084f4a75dc62c80526accac0CAS |
Nakano H, Muramatsu S, Makino A, Mae T (2000) Relationship between the suppression of photosynthesis and starch accumulation in the pod-removed bean. Australian Journal of Plant Physiology 27, 167–173.
Nebauer SG, Renau-Morata B, Guardiola JL, Molina R-V (2011) Photosynthesis down-regulation precedes carbohydrate accumulation under sink limitation in Citrus. Tree Physiology 31, 169–177.
| Photosynthesis down-regulation precedes carbohydrate accumulation under sink limitation in Citrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtlams7w%3D&md5=e480d2e097ce6e3025f482852477c77eCAS |
Paul MJ, Foyer CH (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 1383–1400.
| Sink regulation of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvVCmtLo%3D&md5=8b14f40a2c562d300532fad532b757b6CAS |
Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
| Carbon metabolite feedback regulation of leaf photosynthesis and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFKgtbY%3D&md5=516a54d108362e80a2d4603cfef2d7a7CAS |
Prado AKS, Machado EC, Medina CL, Machado DFSP, Mazzafera P (2007) Flowering and fruit set in ‘Valência’ orange trees under different crop load status and with and without irrigation. Bragantia 66, 173–182.
| Flowering and fruit set in ‘Valência’ orange trees under different crop load status and with and without irrigation.Crossref | GoogleScholarGoogle Scholar | [In Portuguese]
Ramos RA (2009) Thermal regime and source–sink relationship in young sweet orange plants: carbohydrate dynamics, photosynthesis and growth. Masters dissertation, Agronomic Institute. [In Portuguese]
Ramos RA, Ribeiro RV, Machado EC, Machado RS (2010) Seasonal variation in vegetative growth of Hamlin sweet orange grafted on Swingle citrumelo plants, in Limeira, São Paulo State. Acta Scientiarum Agronomy 32, 539–545. [In Portuguese]
Ribeiro RV, Machado EC (2007) Some aspects of citrus ecophysiology in subtropical climates: re-visiting photosynthesis under natural conditions. Brazilian Journal of Plant Physiology 19, 393–411.
| Some aspects of citrus ecophysiology in subtropical climates: re-visiting photosynthesis under natural conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1aju7c%3D&md5=91250fc06960d00de55acb027b380768CAS |
Ribeiro RV, Machado EC, Oliveira RF (2003) Early photosynthetic responses of sweet orange plants infected with Xylella fastidiosa. Physiological and Molecular Plant Pathology 62, 167–173.
| Early photosynthetic responses of sweet orange plants infected with Xylella fastidiosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvVSntLw%3D&md5=9ddab656fbf7c675faa1bda177db669bCAS |
Ribeiro RV, Machado EC, Oliveira RF (2006) Temperature response of photosynthesis and its interaction with light intensity in sweet orange leaf discs under non-photorespiratory condition. Ciência e Agrotecnologia 30, 670–678.
| Temperature response of photosynthesis and its interaction with light intensity in sweet orange leaf discs under non-photorespiratory condition.Crossref | GoogleScholarGoogle Scholar |
Ribeiro RV, Machado EC, Santos MG, Oliveira RF (2009a) Photosynthesis and water relations of well-watered orange plants as affected by winter and summer conditions. Photosynthetica 47, 215–222.
| Photosynthesis and water relations of well-watered orange plants as affected by winter and summer conditions.Crossref | GoogleScholarGoogle Scholar |
Ribeiro RV, Machado EC, Santos MG, Oliveira RF (2009b) Seasonal and diurnal changes in photosynthetic limitation of young sweet orange trees. Environmental and Experimental Botany 66, 203–211.
| Seasonal and diurnal changes in photosynthetic limitation of young sweet orange trees.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFCqs7s%3D&md5=f437386251dc1f474cca15544bbc7405CAS |
Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40, 13–29.
| Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships.Crossref | GoogleScholarGoogle Scholar |
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.
| Sugar sensing and signaling in plants: conserved and novel mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKht7k%3D&md5=97db2f75a5d37fb0115abcf497af4e3fCAS |
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
| Coordination of carbon supply and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrJ&md5=6ef45198ede904a8f335ac52f680c1e8CAS |
Somogyi M (1952) Notes on sugar determination. Journal of Biological Chemistry 195, 19–23.
Syvertsen JP (1994) Partial shoot removal increases net CO2 assimilation and alters water relations of Citrus seedlings. Tree Physiology 14, 497–508.
Syvertsen JP, Goñi C, Otero A (2003) Fruit load and canopy shading affect leaf characteristics and net gas exchange of ‘Spring’ navel orange trees. Tree Physiology 23, 899–906.
| Fruit load and canopy shading affect leaf characteristics and net gas exchange of ‘Spring’ navel orange trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3svntV2ntg%3D%3D&md5=34edd711734b3d868ab8ae5db2d33950CAS |
van Raij B, Cantarella H, Quaggio JA, Furlani AMC (1996) Recomendações de adubação e calagem para o Estado de São Paulo. Instituto Agronômico e Fundação IAC, Campinas.
Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochemical Journal 57, 508–514.
