Source–Sink Relationships

Angela C Burnett, Brookhaven National Laboratory, Upton, New York, USA

Published online: May 2019

DOI: 10.1002/9780470015902.a0001304.pub2

Abstract

Life on earth depends on the growth and survival of plants. In order for plants to grow and develop effectively, coordination between sources and sinks is required. Source organs provide a net uptake of resources whilst sink organs have a net drawdown of resources. Molecular mechanisms regulate the relationship between sources and sinks. These molecular mechanisms include carbon‐ and nitrogen‐containing metabolites, plant hormones and genes. Sources and sinks for both carbon and nitrogen are key contributors to plant growth, and these regulate themselves and one another via feedback, feedforward and crosstalk mechanisms. Our understanding of the relationships between sources and sinks is increased by experimental manipulations of the source–sink balance. To bring about increases in crop growth and yield, a holistic view of sources and sinks must be developed, including the molecular mechanisms underpinning the relationships between them. Mathematical modelling can be an effective tool for providing this unified perspective.

Key Concepts

  • Sources have net uptake of a resource and sinks have net utilisation of a resource.
  • Plant growth is underpinned by sources and sinks.
  • Sources and sinks for both carbon and nitrogen are vital components of plant development.
  • Molecular mechanisms including metabolites, genes and phytohormones regulate the source–sink balance.
  • An understanding of source:sink relationships can help improve crop yield.

Keywords: carbon; growth; nitrogen; phytohormone; signalling; sink; source

Figure 1. Net sources and sinks for carbon (green) and nitrogen (blue), in a simplified plant system. Deepening colour illustrates the gradient for each element, indicated by the grey arrows. Sugars and amino acids are transported in the phloem.
Figure 2. Sources (a, b, c) and sinks (d, e, f) of three crop plants grown in the glasshouse at Brookhaven National Laboratory: Helianthus annuus (sunflower) leaves (a) and flower with developing seeds (d); Raphanus sativus (radish) leaves (b) and edible tuber (e); Curcubita pepe (courgette) leaves (c) and flowers with edible fruits (f). Photographs taken at Brookhaven National Laboratory by Angela C Burnett (a, b, c, e, f) and photograph courtesy of Erin O'Connor (d).
Figure 3. Schematic overview of nitrogen (N) transport processes and source–sink relationships at the whole‐plant level. N fluxes from soil to root to leaf to sinks involve short‐ and long‐distance transport of inorganic N (nitrate (NO3−), ammonium (NH4+) and di‐nitrogen (N2)) and organic N (amino acids (AA) and ureides (Ur)). The xylem and phloem connect sources with sinks and are essential for N mobilization. The smaller font size of xylem NH4+ and phloem NO3− refers to their lower concentration compared with other transported N compounds. Grey arrows indicate feedback controls exerted by source and sink on N uptake and partitioning, respectively. Tegeder and Masclaux‐Daubresse . Reproduced with permission of John Wiley and Sons.
Figure 4. A range of feedback mechanisms enables fine‐tuning of the balance between sources and sinks for carbon (green) and nitrogen (blue). These mechanisms include metabolites derived from carbon and nitrogen; genetic regulation; and control by phytohormones. Feedbacks operate at the tissue level (arrows 1–4 and 6–9) and at the whole‐plant level (arrows 5 and 10). White et al. . Reproduced with permission of Oxford University Press.
Figure 5. Trehalose 6‐phosphate (T6P), synthesized by trehalose phosphate synthase (TPS) and subsequently catalysed to trehalose by trehalose phosphate phosphatase (TPP), signals sucrose availability through the feast–famine protein kinase, SnRK1, which regulates genes involved in metabolism, growth and development. An intermediary factor (IF) is necessary for inhibition of SnRK1 by T6P (Zhang et al., ). Low T6P results in activation of genes for famine responses; high T6P results in activation of genes for feast responses. Decreases in T6P through genetic modification (Nuccio et al., ) and marker‐assisted selection (Kretzschmar et al., ), or increases in T6P through chemical intervention (Griffiths et al., ), have resulted in improved performance and large yield improvements in maize, rice and wheat. Paul et al. . Reproduced with permission of Oxford University Press.
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References

Acreche MM and Slafer GA (2009) Grain weight, radiation interception and use efficiency as affected by sink‐strength in Mediterranean wheats released from 1940 to 2005. Field Crops Research 110: 98–105.

Ainsworth EA, Davey PA, Hymus GJ, et al. (2003) Is stimulation of leaf photosynthesis by elevated carbon dioxide concentration maintained in the long term? A test with Lolium perenne grown for 10 years at two nitrogen fertilization levels under Free Air CO2 Enrichment (FACE). Plant, Cell & Environment 26: 705–714.

Ainsworth EA, Rogers A, Nelson R and Long SP (2004) Testing the ‘source‐sink’ hypothesis of down‐regulation of photosynthesis in elevated [CO2] in the field with single gene substitutions in Glycine max. Agricultural and Forest Meteorology 122: 85–94.

Ainsworth EA, Leakey ADB, Ort DR and Long SP (2008) FACE‐ing the facts: inconsistencies and interdependence among field, chamber and modeling studies of elevated [CO2] impacts on crop yield and food supply. New Phytologist 179: 5–9.

Ainsworth EA and Bush DR (2011) Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology 155: 64–69.

Álvaro F, Royo C, García del Moral LF and Villegas D (2008) Grain filling and dry matter translocation responses to source–sink modifications in a historical series of durum wheat. Crop Science 48: 1523–1523.

Aranjuelo I, Sanz-Sáez A, Jauregui I, et al. (2013) Harvest index, a parameter conditioning responsiveness of wheat plants to elevated CO2. Journal of Experimental Botany 64: 1879–1892.

Arp WJ (1991) Effects of source‐sink relations on photosynthetic acclimation to elevated CO2. Plant, Cell & Environment 14: 869–875.

Bryant J, Taylor G and Frehner M (1998) Photosynthetic acclimation to elevated CO2 is modified by source:sink balance in three component species of chalk grassland swards grown in a free air carbon dioxide enrichment (FACE) experiment. Plant, Cell and Environment 21: 159–168.

Burnett AC, Rogers A, Rees M and Osborne CP (2016) Carbon source‐sink limitations differ between two species with contrasting growth strategies. Plant, Cell & Environment 39: 2460–2472.

Burnett AC, Rogers A, Rees M and Osborne CP (2018) Nutrient sink limitation constrains growth in two barley species with contrasting growth strategies. Plant Direct 2.

von Caemmerer S and Farquhar GD (1984) Effects of partial defoliation, changes of irradiance during growth, short‐term water stress and growth at enhanced p(CO2) on the photosynthetic capacity of leaves of Phaseolus vulgaris L. Planta 160: 320–329.

Dijkshoorn W and Van Wijk A (1967) The sulphur requirements of plants as evidenced by the sulphur‐nitrogen ratio in the organic matter ‐ A review of published data. Plant and Soil 26: 129–157.

Ellis RJ (1979) The most abundant protein in the world. Trends in Biochemical Sciences 4: 241–244.

Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78: 9–19.

Eveland AL and Jackson DP (2012) Sugars, signalling, and plant development. Journal of Experimental Botany 63: 3367–3377.

Eyles A, Pinkard EA and Davies NW (2013) Whole‐plant‐ versus leaf‐level regulation of photosynthetic responses after partial defoliation in Eucalyptus globulus saplings. Journal of Experimental Botany 64: 1625–1636.

FAO, IFAD and WFP (2014) The State of Food Insecurity in the World. Strengthening the Enabling Environment for Food Security and Nutrition. FAO: Rome.

Farage P, McKee I and Long S (1998) Does a low nitrogen supply necessarily lead to acclimation of photosynthesis to elevated CO2? Plant Physiology 118: 573–580.

Geiger DR and Shieh W (1993) Sink strength: learning to measure, measuring to learn. Plant, Cell & Environment 16: 1017–1018.

Gigolashvili T and Kopriva S (2014) Transporters in plant sulfur metabolism. Frontiers in Plant Science 5: 442.

Griffiths CA, Sagar R, Geng Y, et al. (2016) Chemical intervention in plant sugar signalling increases yield and resilience. Nature 540: 574–578.

Hawkesford MJ (2000) Plant responses to sulphur deficiency and the genetic manipulation of sulphate transporters to improve S‐utilisation efficiency. Journal of Experimental Botany 51: 131–138.

Kinsman EA, Lewis C, Davies MS, et al. (1997) Elevated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata. Plant, Cell & Environment 20: 1309–1316.

Kretzschmar T, Pelayo MA, Trijatmiko KR, et al. (2015) A trehalose‐6‐phosphate phosphatase enhances anaerobic germination tolerance in rice. Nature Plants 1: 15124.

Lastdrager J, Hanson J and Smeekens S (2014) Sugar signals and the control of plant growth and development. Journal of Experimental Botany 65: 799–807.

Leakey ADB, Ainsworth EA, Bernacchi CJ, et al. (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. Journal of Experimental Botany 60: 2859–2876.

Liu Y, Ahn J‐E, Datta S, et al. (2005) Arabidopsis vegetative storage protein is an anti‐insect acid phosphatase. Plant Physiology 139: 1545–1556.

Long SP, Ainsworth EA, Leakey ADB, Nösberger J and Ort DR (2006) Food for thought: lower‐than‐expected crop yield stimulation with rising CO2 concentrations. Science 312: 1918–1921.

MacNeill GJ, Mehrpouyan S, Minow MAA, et al. (2017) Starch as a source, starch as a sink: the bifunctional role of starch in carbon allocation. Journal of Experimental Botany 68: 4433–4453.

Masle J (2000) The effects of elevated CO2 concentrations on cell division rates, growth patterns, and blade anatomy in young wheat plants are modulated by factors related to leaf position, vernalization, and genotype. Nature 122: 1399–1415.

McConnaughay KDM, Berntson GM and Bazzaz FA (1993) Limitations to CO2‐induced growth enhancement in pot studies. Oecologia 94: 550–557.

Müller‐Röber B, Sonnewald U and Willmitzer L (1992) Inhibition of the ADP‐glucose pyrophosphorylase in transgenic potatoes leads to sugarstoring tubers and influences tuber formation and expression of tuber storage protein genes. The EMBO Journal 11: 1229–1238.

Murray JD, Liu CW, Chen Y and Miller AJ (2017) Nitrogen sensing in legumes. Journal of Experimental Botany 68: 1919–1926.

Nuccio ML, Wu J, Mowers R, et al. (2015) Expression of trehalose‐6‐phosphate phosphatase in maize ears improves yield in well‐watered and drought conditions. Nature Biotechnology 33: 862–869.

Nunes C, O'Hara LE, Primavesi LF, et al. (2013) The trehalose 6‐phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiology 162: 1720–1732.

Pate J, Atkins C, White S, Rainbird R and Woo K (1980) Nitrogen nutrition and xylem transport of nitrogen in ureide‐producing grain legumes. Plant Physiology 65: 961–965.

Paul MJ, Oszvald M, Jesus C, Rajulu C and Griffiths CA (2017) Increasing crop yield and resilience with trehalose 6‐phosphate: targeting a feast‐famine mechanism in cereals for better source‐sink optimization. Journal of Experimental Botany 68: 4455–4462.

Perchlik M and Tegeder M (2018) Leaf amino acid supply affects photosynthetic and plant nitrogen use efficiency under nitrogen stress. Plant Physiology 178: 174–188.

Peterhansel C and Offermann S (2012) Re‐engineering of carbon fixation in plants ‐ challenges for plant biotechnology to improve yields in a high‐CO2 world. Current Opinion in Biotechnology 23: 204–208.

Pollock CJ and Cairns AJ (1991) Fructan metabolism in grasses and cereals. Annual Review of Plant Physiology and Plant Molecular Biology 42: 77–101.

Poorter H, Bühler J, van Dusschoten D, Climent J and Postma JA (2012) Pot size matters: a meta‐analysis of the effects of rooting volume on plant growth. Functional Plant Biology 39: 839–839.

Reekie EG, MacDougall G, Wong I and Hicklenton PR (1998) Effect of sink size on growth response to elevated atmospheric CO2 within the genus Brassica. Canadian Journal of Botany 76: 829–835.

Rogers A, Fischer B, Bryant J, et al. (1998) Acclimation of photosynthesis to elevated CO2 under low‐nitrogen nutrition is affected by the capacity for assimilate utilization. Perennial ryegrass under free‐air CO2 enrichment. Plant Physiology 118: 683–689.

Rogers A, Ainsworth EA and Leakey ADB (2009) Will elevated carbon dioxide concentration amplify the benefits of nitrogen fixation in legumes? Plant Physiology 151: 1009–1016.

Ruiz‐Vera UM, De Souza AP, Long SP and Ort DR (2017) The role of sink strength and nitrogen availability in the down‐regulation of photosynthetic capacity in field‐grown Nicotiana tabacum L. at elevated CO2 concentration. Frontiers in Plant Science 8: 998.

Sage RF, Pearcy RW and Seemann JR (1987) The nitrogen use efficiency of C3 and C4 plants: III. leaf nitrogen effects on the activity of carboxylating enzymes in Chenopodium album (L.) and Amaranthus retroflexus (L.). Plant Physiology 85: 355–359.

Schachtman D, Reid R and Ayling S (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiology 116: 447–453.

Scofield GN, Ruuska SA, Aoki N, et al. (2009) Starch storage in the stems of wheat plants: localization and temporal changes. Annals of Botany 103: 859–868.

Slewinski TL (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.

Smith AM and Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30: 1126–1149.

Sonnewald U and Fernie AR (2018) Next‐generation strategies for understanding and influencing source‐sink relations in crop plants. Current Opinion in Plant Biology 43: 63–70.

Stokes ME, Chattopadhyay A, Wilkins O, Nambara E and Campbell MM (2013) Interplay between sucrose and folate modulates auxin signalling in Arabidopsis. Plant Physiology 162: 1552–1565.

Sweetlove LJ, Nielsen J and Fernie AR (2017) Engineering central metabolism ‐ a grand challenge for plant biologists. The Plant Journal 90: 749–763.

Tegeder M and Masclaux‐Daubresse C (2017) Source and sink mechanisms of nitrogen transport and use. New Phytologist 217: 35–53.

Teng S, Rognoni S, Bentsink L and Smeekens S (2008) The Arabidopsis GSQ5/DOG1 Cvi allele is induced by the ABA‐mediated sugar signalling pathway, and enhances sugar sensitivity by stimulating ABI4 expression. The Plant Journal 55: 372–381.

Weichert N, Saalbach I, Weichert H, et al. (2010) Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiology 152: 698–710.

White AC, Rogers A, Rees M and Osborne CP (2016) How can we make plants grow faster? A source‐sink perspective on growth rate. Journal of Experimental Botany 67: 31–45.

Zhang Y, Primavesi LF, Jhurreea D, et al. (2009) Inhibition of SNF1‐related protein kinase1 activity and regulation of metabolic pathways by trehalose‐6‐phosphate. Plant Physiology 149: 1860–1871.

Zuther E, Hoermiller II and Heyer AG (2011) Evidence against sink limitation by the sucrose‐to‐starch route in potato plants expressing fructosyltransferases. Physiologia Plantarum 143: 115–125.

Further Reading

Chang T and Zhu X (2017) Source‐sink interaction: a century old concept under the light of modern molecular systems biology. Journal of Experimental Botany 68: 4417–4431.

Heldt H and Piechulla B (2011) Plant Biochemistry, 4th edn. Elsevier: New York.

Taiz L, Zeiger E, Møller IM and Murphy A (2014) Plant Physiology and Development, 6th edn. Sinauer Associates: Sunderland, MA.

Tegeder M and Masclaux‐Daubresse C (2017) Source and sink mechanisms of nitrogen transport and use. New Phytologist 217: 35–53.

White AC, Rogers A, Rees M and Osborne CP (2016) How can we make plants grow faster? A source‐sink perspective on growth rate. Journal of Experimental Botany 67: 31–45.

Related Sub-Topics:

Plant Development | Plant Genetics and Molecular Biology | Photosynthesis | Plant Responses to the Environment | Plant Nutrition | Crops and Plant Breeding
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Article Title: Source–Sink Relationships
 
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Burnett, Angela C(May 2019) Source–Sink Relationships. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001304.pub2]