Supply and demand: sink regulation of sugar accumulation in sugarcane.

Sugarcane (Saccharum spp. hybrids) accumulates sucrose to high concentrations and, as a result, has been the focus of extensive research into the biochemistry and physiology of sucrose accumulation. Despite this, the relationship between source leaf photosynthetic activity and sucrose accumulation in the culm sink is not well understood. The observations that photosynthetic activity declines during culm maturation in commercial cultivars and that high-sucrose-accumulating noble ancestral genotypes (Saccharum officinarum L.) photosynthesize at rates two-thirds of those of low-sucrose ancestors (Saccharum spontaneum L.) indicate that source-sink communication may play a pivotal role in determining sucrose yield. Although maturation of the culm results in a decreased demand for sucrose, recent evidence from partial leaf shading, defoliation, and transgenic studies indicates that sugarcane cultivars are capable of further increases in sugar content. Furthermore, sugarcane leaves appear to retain the capacity to increase the supply of assimilate to culm tissues under conditions of increased assimilate demand. The relationship between source and sink tissues in sugarcane should be viewed within a supply-demand paradigm; an often neglected conceptual approach in the study of this crop. Uncoupling of the signalling pathways that mediate negative feedback between source and sink tissues may result in improved leaf assimilation rates and, consequently, lead to increased sugarcane sucrose yields.

[1]  S. Huber,et al.  Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. , 1992, Plant physiology.

[2]  A. McCormick,et al.  Changes in photosynthetic rates and gene expression of leaves during a source-sink perturbation in sugarcane. , 2008, Annals of botany.

[3]  S. Smeekens,et al.  Genetic modification of photosynthesis with E. coli genes for trehalose synthesis. , 2004, Plant biotechnology journal.

[4]  J. Allison,et al.  Effect of specific leaf nitrogen content on photosynthesis of sugarcane , 1997 .

[5]  J. Sheen,et al.  Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[6]  G. Farquhar,et al.  Control analysis of photosynthetic CO2 fixation , 1990, Photosynthesis Research.

[7]  A. V. Van Dijken,et al.  Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P E H Minchin,et al.  New understanding on phloem physiology and possible consequences for modelling long-distance carbon transport. , 2005, The New phytologist.

[9]  M. Stitt,et al.  “Sink” regulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin-cycle enzymes and an increase of glycolytic enzymes , 1991, Planta.

[10]  C. Pollock,et al.  Photosynthesis and carbohydrate metabolism in detached leaves of Lolium temulentum L. , 1985 .

[11]  Sharon M. Brown,et al.  The anatomy of the pathway of sucrose unloading within the sugarcane stalk. , 2005, Functional plant biology : FPB.

[12]  C. E. Hartt,et al.  Factors affecting photosynthesis in sugar cane. , 1967 .

[13]  S. B. Milligan Intensive Sugarcane Production: Meeting the Challenges Beyond 2000. Proceedings of the Sugar 2000 Symposium, Brisbane, Australia, 20–23 August 199 , 1998 .

[14]  Steven A. Hill,et al.  Source metabolism dominates the control of source to sink carbon flux in tuberizing potato plants throughout the diurnal cycle and under a range of environmental conditions. , 2000 .

[15]  Luguang Wu,et al.  Doubled sugar content in sugarcane plants modified to produce a sucrose isomer. , 2007, Plant biotechnology journal.

[16]  M. Stitt,et al.  Regulation of the Expression of Rbcs and Other Photosynthetic Genes by Carbohydrates - a Mechanism for the Sink Regulation of Photosynthesis , 1993 .

[17]  R. Evert,et al.  Ultrastructure of and plasmodesmatal frequency in mature leaves of sugarcane , 1991, Planta.

[18]  J. Hofmeyr,et al.  Regulating the cellular economy of supply and demand , 2000, FEBS letters.

[19]  M. Stitt,et al.  An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: Changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves , 2004, Planta.

[20]  A. McCormick,et al.  Culm sucrose accumulation promotes physiological decline of mature leaves in ripening sugarcane , 2008 .

[21]  S. Mcfarlane,et al.  South African Sugarcane Research Institute: Embracing biotechnology for crop improvement research , 2008, Sugar Tech.

[22]  P. Eastmond,et al.  Is trehalose-6-phosphate a regulator of sugar metabolism in plants? , 2003, Journal of experimental botany.

[23]  W. Jakoby New Beer in an Old Bottle: Eduard Buchner and the Growth of Biochemical Knowledge. Edited by Athel Cornish-Bowden. Universitat de Valencia, Valencia, 1997, 252 pp. , 1999 .

[24]  F. Zimmermann,et al.  Overproduction of glycolytic enzymes in yeast , 1989, Yeast.

[25]  S. Smeekens,et al.  Photosynthesis, sugars and the regulation of gene expression. , 2000, Journal of experimental botany.

[26]  Hongmei Ma,et al.  Metabolic engineering of invertase activities in different subcellular compartments affects sucrose accumulation in sugarcane cells , 2000 .

[27]  M. Paul Trehalose 6-phosphate. , 2007, Current opinion in plant biology.

[28]  F. Botha,et al.  Sucrose metabolism in the culm of transgenic sugarcane with reduced soluble acid invertase activity , 2001 .

[29]  Alex G. Alexander,et al.  Sugarcane physiology: A comprehensive study of the Saccharum source-to-sink system , 1973 .

[30]  M. Stitt,et al.  Expression of a yeast‐derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. , 1990, The EMBO journal.

[31]  A. McCormick,et al.  Differential Expression of Genes in the Leaves of Sugarcane in Response to Sugar Accumulation , 2008, Tropical Plant Biology.

[32]  S. Gibson,et al.  Control of plant development and gene expression by sugar signaling. , 2005, Current opinion in plant biology.

[33]  M. Génard,et al.  Soluble sugars mediate sink feedback down-regulation of leaf photosynthesis in field-grown Coffea arabica. , 2006, Tree physiology.

[34]  F. Botha,et al.  Downregulation of neutral invertase activity in sugarcane cell suspension cultures leads to a reduction in respiration and growth and an increase in sucrose accumulation. , 2007, Functional plant biology : FPB.

[35]  A. McCormick,et al.  Sink strength regulates photosynthesis in sugarcane. , 2006, The New phytologist.

[36]  R. Giaquinta,et al.  Sucrose translocation and storage in the sugar beet. , 1979, Plant physiology.

[37]  J. Irvine Relations of Photosynthetic Rates and Leaf and Canopy Characters to Sugarcane Yield 1 , 1975 .

[38]  Paul H. Moore,et al.  Temporal and spatial regulation of sucrose accumulation in the sugarcane stem , 1995 .

[39]  Johann M Rohwer,et al.  Kinetic model of sucrose accumulation in maturing sugarcane culm tissue. , 2007, Phytochemistry.

[40]  Wolf B. Frommer,et al.  Phloem loading and unloading of sugars and amino acids , 2003 .

[41]  F. Botha,et al.  Increasing the utility of genomics in unravelling sucrose accumulation , 2005 .

[42]  T. Bull,et al.  The Evolutionary Significance of Sugar Accumulation in Saccharum , 1963 .

[43]  J. Allison,et al.  Effect of plant population on the production and distribution of dry matter in maize , 1969 .

[44]  B. E. Vaughan,et al.  Ethanol as Fuel: Energy, Carbon Dioxide Balances, and Ecological Footprint , 2005 .

[45]  W. Frommer,et al.  The Dual Function of Sugar Carriers: Transport and Sugar Sensing , 1999, Plant Cell.

[46]  L. Dendooven,et al.  Effects of Partial Defoliation on Sucrose Accumulation, Enzyme Activity and Agronomic Parameters in Sugar cane (Saccharum spp.) , 2004 .

[47]  A. Nose,et al.  Diurnal Changes in Photosynthesis in Sugarcane Leaves: I. Carbon dioxide exchange rate, photosynthetic enzyme activities and metabolite levels relating to the C4 pathway and the Calvin cycle , 2000 .

[48]  J. Ward,et al.  Sugarcane ShSUT1: analysis of sucrose transport activity and inhibition by sucralose. , 2006, Plant, cell & environment.

[49]  M. Talón,et al.  Regulation of photosynthesis through source: sink imbalance in citrus is mediated by carbohydrate content in leaves , 2002 .

[50]  R. Furbank,et al.  Effects of exogenous sucrose feeding on photosynthesis in the C3 plant tobacco and the C4 plant Flaveria bidentis , 1997 .

[51]  D. Fell Understanding the Control of Metabolism , 1996 .

[52]  A. McCormick,et al.  Regulation of photosynthesis by sugars in sugarcane leaves. , 2008, Journal of plant physiology.

[53]  F. Botha,et al.  Down-regulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in sugarcane enhances sucrose accumulation in immature internodes , 2008, Transgenic Research.

[54]  Phillip Jackson,et al.  Breeding for improved sugar content in sugarcane , 2005 .

[55]  M. Paul,et al.  Sink regulation of photosynthesis. , 2001, Journal of experimental botany.

[56]  R. Furbank,et al.  C4 Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco1 , 2003, Plant Physiology.

[57]  C. Grof,et al.  A modified assay method shows leaf sucrose-phosphate synthase activity is correlated with leaf sucrose content across a range of sugarcane varieties , 1998 .

[58]  R. Trethewey,et al.  The control of source to sink carbon flux during tuber development in potato. , 1998, The Plant journal : for cell and molecular biology.

[59]  S. Gibson,et al.  The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. , 2000, The Plant journal : for cell and molecular biology.

[60]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[61]  Prakash Lakshmanan,et al.  Sugarcane biotechnology: The challenges and opportunities , 2005, In Vitro Cellular & Developmental Biology - Plant.

[62]  Filip Rolland,et al.  Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling , 2003, Science.

[63]  J. Willenbrink,et al.  Sucrose accumulation in sweet sorghum stem internodes in relation to growth , 1996 .

[64]  M. Paul,et al.  Carbon metabolite feedback regulation of leaf photosynthesis and development. , 2003, Journal of experimental botany.

[65]  K. Glasziou Physiology of Sugar-Cane , 1961, Nature.

[66]  C. Grof,et al.  Sugarcane sucrose metabolism: scope for molecular manipulation , 2001 .

[67]  A. Rae,et al.  Sucrose partitioning between vascular bundles and storage parenchyma in the sugarcane stem: a potential role for the ShSUT1 sucrose transporter , 2005, Planta.

[68]  F. Rolland,et al.  Plant development: introducing trehalose metabolism. , 2007, Trends in plant science.

[69]  S. Baginsky,et al.  Identification of a Vacuolar Sucrose Transporter in Barley and Arabidopsis Mesophyll Cells by a Tonoplast Proteomic Approach1 , 2006, Plant Physiology.

[70]  A. Nose,et al.  Diurnal Changes in Photosynthesis in Sugarcane Leaves: II. Enzyme activities and metabolite levels relating to sucrose and starch metabolism , 2000 .

[71]  T. Bull,et al.  The Physiology of Sugar-Cane. IX.Factors Affecting Photosynthesis and Sugar Storage , 1967 .

[72]  P. Basu,et al.  Tuber sink modifies photosynthetic response in potato under water stress 1 Publication No. 1408, CPR , 1999 .

[73]  J. Sheen,et al.  Feedback control of gene expression , 1994, Photosynthesis Research.

[74]  A. Kruckeberg,et al.  Yeast sugar transporters. , 1993, Critical reviews in biochemistry and molecular biology.

[75]  J. Bailey,et al.  Fermentation pathway kinetics and metabolic flux control in suspended and immobilized Saccharomyces cerevisiae , 1990 .

[76]  T. Chiou,et al.  Sucrose is a signal molecule in assimilate partitioning. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Govindjee,et al.  Advances in Photosynthesis and Respiration: Focus on Plant Respiration , 2005, Photosynthesis Research.

[78]  N. Sauer,et al.  The Arabidopsis thaliana AtSUC2 Gene is Specifically Expressed in Companion Cells , 1996 .