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

Diurnal variation in gas exchange and nonstructural carbohydrates throughout sugarcane development

Amanda P. De Souza A B , Adriana Grandis A , Bruna C. Arenque-Musa A and Marcos S. Buckeridge A C
+ Author Affiliations
- Author Affiliations

A Laboratory of Plant Physiological Ecology, Department of Botany, Institute of Biosciences, University of São Paulo, São Paulo, 05508-090, SP, Brazil.

B Current address: Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, 61801, IL, USA.

C Corresponding author. Email: msbuck@usp.br

Functional Plant Biology - https://doi.org/10.1071/FP17268
Submitted: 18 June 2017  Accepted: 10 February 2018   Published online: 27 March 2018

Abstract

Photosynthesis and growth are dependent on environmental conditions and plant developmental stages. However, it is still not clear how the environment and development influence the diurnal dynamics of nonstructural carbohydrates production and how they affect growth. This is particularly the case of C4 plants such as sugarcane (Saccharum spp.). Aiming to understand the dynamics of leaf gas exchange and nonstructural carbohydrates accumulation in different organs during diurnal cycles across the developmental stages, we evaluated these parameters in sugarcane plants in a 12-month field experiment. Our results show that during the first 3 months of development, light and vapour pressure deficit (VPD) were the primary drivers of photosynthesis, stomatal conductance and growth. After 6 months, in addition to light and VPD, drought, carbohydrate accumulation and the mechanisms possibly associated with water status maintenance were also likely to play a role in gas exchange and growth regulation. Carbohydrates vary throughout the day in all organs until Month 9, consistent with their use for growth during the night. At 12 months, sucrose is accumulated in all organs and starch had accumulated in leaves without any diurnal variation. Understanding of how photosynthesis and the dynamics of carbohydrates are controlled might lead to strategies that could increase sugarcane’s biomass production.

Additional keywords: carbohydrate metabolism, carbon partitioning, growth regulation, Saccharum, sugar accumulation, sugar sensing.


References

Ball-Coelho B, Sampaio E, Tiessen H, Stewart J (1992) Root dynamics in plant and ratoon crops of sugar cane. Plant and Soil 142, 297–305.
Root dynamics in plant and ratoon crops of sugar cane.CrossRef |

Barbour M, Buckley T (2007) The stomatal response to evaporative demand persists at night in Ricinus communis plants with high nocturnal conductance. Plant, Cell & Environment 30, 711–721.
The stomatal response to evaporative demand persists at night in Ricinus communis plants with high nocturnal conductance.CrossRef |

Bucci S, Scholz F, Goldstein G, Meinzer F, Hinojosa J, Hoffman W, Franco A (2004) Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species. Tree Physiology 24, 1119–1127.
Processes preventing nocturnal equilibration between leaf and soil water potential in tropical savanna woody species.CrossRef |

Buckley TN (2005) The control of stomata by water balance. New Phytologist 168, 275–292.
The control of stomata by water balance.CrossRef | 1:CAS:528:DC%2BD2MXht1Smu7bI&md5=8dec8bd01b0164854ebe3869649a9388CAS |

Caird M, Richards J, Donovan L (2007) Nighttime stomatal conductance and transpiration in C3 and C4 plants. Plant Physiology 143, 4–10.
Nighttime stomatal conductance and transpiration in C3 and C4 plants.CrossRef | 1:CAS:528:DC%2BD2sXpt1Ohtw%3D%3D&md5=b4042533da3b7b9e2a8d00a240a85f62CAS |

Castro P (1999) Maturadores químicos em cana-de-açúcar. In ‘Anais da IV semana da cana-de-açúcar de Piracicaba’ Comissão Organizadora, Piracicaba. pp. 12–16.

De Souza AP, Arundale RA, Dohleman FG, Long SP, Buckeridge MS (2013) Will the exceptional productivity of Miscanthus × giganteus increase further under rising atmospheric CO2? Agricultural and Forest Meteorology 171–172, 82–92.
Will the exceptional productivity of Miscanthus × giganteus increase further under rising atmospheric CO2?CrossRef |

De Souza AP, Grandis A, Leite DCC, Buckeridge MS (2014) Sugarcane as a bioenergy source: history, performance, and perspectives for second-generation bioethanol. BioEnergy Research 7, 24–35.
Sugarcane as a bioenergy source: history, performance, and perspectives for second-generation bioethanol.CrossRef |

De Souza AP, Cocuron JC, Garcia AC, Alonso AP, Buckeridge MS (2015) Changes in whole-plant metabolism during the grain-filling stage in sorghum grown under elevated CO2 and drought. Plant Physiology 169, 1755–1765.

Du Y-C, Nose A, Kondo A, Wasano K (2000a) 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. Plant Production Science 3, 3–8.
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.CrossRef |

Du Y-C, Nose A, Kondo A, Wasano K (2000b) Diurnal changes in photosynthesis in sugarcane leaves: II. Enzyme activities and metabolite levels relating to sucrose and starch metabolism. Plant Production Science 3, 9–16.
Diurnal changes in photosynthesis in sugarcane leaves: II. Enzyme activities and metabolite levels relating to sucrose and starch metabolism.CrossRef |

Fischer R, Edmeades G (2010) Breeding and cereal yield progress. Crop Science 50, S85–S98.
Breeding and cereal yield progress.CrossRef |

Genty B, Briantais J-M, Baker N (1989) The relationship between the quantum yield of photosynthesis electron transport rate and quanching of clhorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
The relationship between the quantum yield of photosynthesis electron transport rate and quanching of clhorophyll fluorescence.CrossRef | 1:CAS:528:DyaL1MXhsFWntL4%3D&md5=9d9e270bbaccee4721105a2ded548bc0CAS |

Glover J (1968) The behavior of the root-system of sugarcane at and after harvest. In ’Proceedings of the South African Sugar Technologists’ Association. Vol. 42’. pp. 133–135.

Inman-Bamber N, Jackson P, Hewitt M (2011) Sucrose accumulation in sugarcane stalks does not limit photosynthesis and biomass production. Crop and Pasture Science 62, 848–858.
Sucrose accumulation in sugarcane stalks does not limit photosynthesis and biomass production.CrossRef | 1:CAS:528:DC%2BC3MXhsFKrsb3M&md5=89f29532a9507cf4c4c5c533551c9538CAS |

Jaiswal D, De Souza A, Larsen S, LeBauer D, Miguez F, Sparovek G, Bollero G, Buckeridge M, Long S (2017) Brazilian sugarcane ethanol as an expandable green alternative to crude oil use. Nature Climate Change 169, 1755–1765.
Brazilian sugarcane ethanol as an expandable green alternative to crude oil use.CrossRef |

Koch K (1996) Carbohydrate-modulated gene expression in plants. Annual Review of Plant Biology 47, 509–540.
Carbohydrate-modulated gene expression in plants.CrossRef | 1:CAS:528:DyaK28XjtlWgtrY%3D&md5=e9a94cfbebbeb597bdd0dcb5eb3c5d41CAS |

Landell M, Bressiani J (2008) Melhoramento genético, caracterização e manejo varietal. In ‘Cana-de-açúcar’. (Eds L Dinardo-Miranda, A Vasconcelos, M Landell.) pp. 101–155. (Instituto Agronômico: Campinas, SP)

Leegood R, Walker R (1999) Regulation of the C4 pathway. In ‘C4 plant biology.’ (Eds R Sage, R Monson.) pp. 89–131. (Academic Press: San Diego, CA)

Lobo AKM, Martins MO, Lima Neto EC, Ribeiro RV, Silveira JAG (2015) Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity. Journal of Plant Physiology 179, 113–121.
Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of Rubisco abundance and activity.CrossRef | 1:CAS:528:DC%2BC2MXlslCltbw%3D&md5=583c2df57c562a1040ffd190159577b9CAS |

Marks C, Lechowicz M (2007) The ecological and functional correlates of nocturnal transpiration. Tree Physiology 27, 577–584.
The ecological and functional correlates of nocturnal transpiration.CrossRef |

McBee GG, Miller FR (1982) Carbohydrates in sorghum culms as influenced by cultivars, spacing, and maturity over a diurnal period. Crop Science 22, 381–385.
Carbohydrates in sorghum culms as influenced by cultivars, spacing, and maturity over a diurnal period.CrossRef |

McCormick A, Cramer M, Watt D (2006) Sink strength regulates photosynthesis in sugarcane. New Phytologist 171, 759–770.
Sink strength regulates photosynthesis in sugarcane.CrossRef | 1:CAS:528:DC%2BD28XhtVSku7%2FP&md5=f13b25a53daff8ae9209f8cdbcb6faadCAS |

McCormick A, Cramer M, Watt D (2008a) Culm sucrose accumulation promotes physiological decline of mature leaves in ripening sugarcane. Field Crops Research 108, 250–258.
Culm sucrose accumulation promotes physiological decline of mature leaves in ripening sugarcane.CrossRef |

McCormick A, Cramer M, Watt D (2008b) Regulation of photosynthesis by sugars in sugarcane leaves. Journal of Plant Physiology 165, 1817–1829.
Regulation of photosynthesis by sugars in sugarcane leaves.CrossRef | 1:CAS:528:DC%2BD1cXhsVKgurbL&md5=9ea8f98237c8a4f01c0ec01b7e82127fCAS |

Molinari H, Marur C, Daros E, Campos M, Carvalho J, Filho J, Pereira L, Vieira L (2007) Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress. Physiologia Plantarum 130, 218–229.
Evaluation of the stress-inducible production of proline in transgenic sugarcane (Saccharum spp.): osmotic adjustment, chlorophyll fluorescence and oxidative stress.CrossRef | 1:CAS:528:DC%2BD2sXmslOhtLw%3D&md5=a574e80665decea2a840a32e5db1ee9cCAS |

Moore P (1995) Temporal and spatial regulation of sucrose metabolism in the sugarcane stem. Functional Plant Biology 22, 661–679.

Mott K, Peak D (2013) Testing a vapour-phase model of stomatal responses to humidity. Plant, Cell & Environment 36, 936–944.
Testing a vapour-phase model of stomatal responses to humidity.CrossRef | 1:CAS:528:DC%2BC3sXlsFyquro%3D&md5=0ab9656a6c39936e9ab266238ead0b7eCAS |

Nozue K, Maloof J (2006) Diurnal regulation of plant growth. Plant, Cell & Environment 29, 396–408.
Diurnal regulation of plant growth.CrossRef | 1:CAS:528:DC%2BD28Xktlyltrk%3D&md5=f162f4e3831549130261ee2940d966edCAS |

O’Neill PM, Shanahan J, Schepers J (2006) Use of chlorophyll fluorescence assessments to differentiate corn hybrid response to variable water conditions. Crop Science 46, 681–687.
Use of chlorophyll fluorescence assessments to differentiate corn hybrid response to variable water conditions.CrossRef | 1:CAS:528:DC%2BD28XjtV2ktr4%3D&md5=88474c69c2f8a8a1e93cfbaca2159674CAS |

Oren R, Sperry J, Ewers B, Pataki D, Phillips N, Megonigal J (2001) Sensitivity of mean canopy stomatal conductance to vapor pressure deficit in flooded Taxodium distichum L. forest: hydraulic and non-hydraulic effect. Oecologia 126, 21–29.
Sensitivity of mean canopy stomatal conductance to vapor pressure deficit in flooded Taxodium distichum L. forest: hydraulic and non-hydraulic effect.CrossRef | 1:STN:280:DC%2BC1cnhsFymsg%3D%3D&md5=5b691d2f99e18b3c1923ebe955517a44CAS |

Otto R, Trivelin PCO, Franco HCJ, Faroni CE, Vitti AC (2009) Root system distribution of sugar cane as related to nitrogen fertilization, evaluated by two methods: monolith and probes. Revista Brasileira de Ciência do Solo 33, 601–611.
Root system distribution of sugar cane as related to nitrogen fertilization, evaluated by two methods: monolith and probes.CrossRef | 1:CAS:528:DC%2BD1MXpvFOrtLo%3D&md5=1c136b046acb2b9f11e4e9b020a57e0eCAS |

Paul M, Foyer C (2001) Sink regulation of photosynthesis. Journal of Experimental Botany 52, 1383–1400.
Sink regulation of photosynthesis.CrossRef | 1:CAS:528:DC%2BD3MXlvVCmtLo%3D&md5=a9a5ebf320fc8a0e15b2cdff8e062f05CAS |

Paul M, Pellny T (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 | 1:CAS:528:DC%2BD3sXhsFKgtbY%3D&md5=d7b7e0d264985a11847ec5c8ad4a6046CAS |

R Core Team (2013) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)

Rae A, Grof C, Casu R, Bonnett G (2005) Sucrose accumulation in the sugarcane stem: pathways and control points for transport and compartmentation. Field Crops Research 92, 159–168.

Ribeiro RV, Machado EC, Magalhães Filho JR, Lobo AKM, Martins MO, Silveira JAG, Yin X, Struik PC (2017) Increased sink strength offsets the inhibitory effect of sucrose on sugarcane photosynthesis. Journal of Plant Physiology 208, 61–69.
Increased sink strength offsets the inhibitory effect of sucrose on sugarcane photosynthesis.CrossRef | 1:CAS:528:DC%2BC28XhvV2iu7bK&md5=c08d821ffee48cf8ec6351b48ca7a159CAS |

Robinson-Beers K, Evert R (1991) Ultrastructure of and plasmodesmatal frequency in mature leaves of sugarcane. Planta 184, 291–306.

Slewinski T (2012) Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production. Journal of Experimental Botany 63, 4647–4670.
Non-structural carbohydrate partitioning in grass stems: a target to increase yield stability, stress tolerance, and biofuel production.CrossRef | 1:CAS:528:DC%2BC38Xht1Kjsb7J&md5=9cfd02ab781db7b6e565c31c74785cffCAS |

Slewinski T, Braun D (2010) Current perspectives on the regulation of whole-plant carbohydrate partitioning. Plant Science 178, 341–349.
Current perspectives on the regulation of whole-plant carbohydrate partitioning.CrossRef | 1:CAS:528:DC%2BC3cXjt1Ghsbw%3D&md5=054604ea9587e2e2dde295045b1d0600CAS |

Smith A, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
Coordination of carbon supply and plant growth.CrossRef | 1:CAS:528:DC%2BD2sXhtVeiurrJ&md5=f92f7101da15c29f13f3bc588f25c523CAS |

Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell & Environment 14, 741–762.
Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells.CrossRef | 1:CAS:528:DyaK38XhsVyisbY%3D&md5=6538ba021b69c9be28e5ef1e30de4839CAS |

Sulpice R, Flis A, Ivakov A, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn J, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Molecular Plant 7, 137–155.
Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods.CrossRef | 1:CAS:528:DC%2BC2cXisFOqtg%3D%3D&md5=1c9bd6907491556164dd3ae520707b39CAS |

Turgeon R (1991) Symplastic phloem loading and the sink-source transition in leaves: a model. In ‘Recent advances in phloem transport and assimilate compartmentation’. (Eds J Bonnemain, S Delrot, W Lucas, J Dainty.) pp. 18–22. (Ouest Editions: Nantes, France)

Usuda H, Kalttorres W, Kerr PS, Huber SC (1987) Diurnal changes in maize leaf photosynthesis. 2. Levels of metabolic intermediates of sucrose synthesis and the regulatory metabolite fructose 2,6-bisphosphate. Plant Physiology 83, 289–293.
Diurnal changes in maize leaf photosynthesis. 2. Levels of metabolic intermediates of sucrose synthesis and the regulatory metabolite fructose 2,6-bisphosphate.CrossRef | 1:CAS:528:DyaL2sXhtlGmsL8%3D&md5=9d67c2d84794da5ffa8582d9cdef350bCAS |

Van Bel AJ (1993) Strategies of phloem loading. Annual Review of Plant Physiology and Plant Molecular Biology 44, 253–281.
Strategies of phloem loading.CrossRef | 1:CAS:528:DyaK3sXlsFKisb0%3D&md5=ce9684bec639911a696bc02612828bffCAS |

Waclawovsky A, Sato P, Lembke C, Moore P, Souza G (2010) Sugarcane for bioenergy production: an assessment of yield and regulation of sucrose content. Plant Biotechnology Journal 8, 263–276.
Sugarcane for bioenergy production: an assessment of yield and regulation of sucrose content.CrossRef | 1:CAS:528:DC%2BC3cXks1Clu78%3D&md5=ed1331c0ad99c21b45c8fb5dce3bbf85CAS |

Walter A, Schurr W (2005) Dynamics of leaf and root growth: endogenous control versus environmental impact. Annals of Botany 95, 891–900.
Dynamics of leaf and root growth: endogenous control versus environmental impact.CrossRef |

Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2016) ‘gplots: various R programming tools for plotting data. R package version 3.0.1, CRAN’. Available at: https://cran.r-project.org/web/packages/gplots/index.html [Verified 18 February 2017]

Weise S, van Wijk KJ, Sharkey T (2011) The role of transitory starch in C3, CAM, and C4 metabolism and opportunities for engineering leaf starch accumulation. Journal of Experimental Botany 62, 3109–3118.

Welbaum G, Meinzer F (1990) Compartmentation of solutes and water in developing sugarcane stalk tissue. Plant Physiology 93, 1147–1153.
Compartmentation of solutes and water in developing sugarcane stalk tissue.CrossRef | 1:CAS:528:DyaK3cXlt12ntrY%3D&md5=ebdad0ee34d3994482763de1e7a97d70CAS |

White L (1973) Carbohydrate reserves of grasses: a review. Journal of Range Management 26, 13–18.
Carbohydrate reserves of grasses: a review.CrossRef | 1:CAS:528:DyaE3sXhtVyitL4%3D&md5=acdb113878a7953011758bfa99fd64b3CAS |



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