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

Source and sink activity of Holcus lanatus in response to absolute and relative supply of nitrogen and phosphorus

Shuqiong Wang https://orcid.org/0000-0002-9088-238X A B , Jerry van Dijk A , Hugo J. de Boer A and Martin J. Wassen A
+ Author Affiliations
- Author Affiliations

A Environmental Sciences, Copernicus Institute of Sustainable Development, Utrecht University, Princetonlaan 8a, PO Box 80115, 3508 TC Utrecht, the Netherlands.

B Corresponding author. Email: s.wang@uu.nl

Functional Plant Biology 48(5) 493-502 https://doi.org/10.1071/FP20118
Submitted: 29 April 2020  Accepted: 10 December 2020   Published: 18 January 2021

Abstract

Mineral nutrients influence photosynthesis and tissue formation; a shift from nitrogen (N)-limited to phosphorus (P)-limited growth induced by high N deposition may change plant growth in terms of physiology and morphology. This experiment showed that absolute and relative N and P supply affected net photosynthesis (source activity) and biomass formation (sink activity), and the relationship between source and sink activities of Holcus lanatus L. under various nutrient treatments. H. lanatus was grown at three N:P ratios (5, 15, 45) with two absolute supply levels of N and P. Between N:P 5 at low level and N:P 45 at high level, and between N:P 45 at low level and N:P 5 at high level, there was a nine-fold difference in N and P supply. Maximum light-saturated net photosynthesis rate (Amax), specific leaf area (SLA), leaf area, and shoot and root biomass were determined during and after the growth process. Amax was minimal at N:P 5 and increased only with increasing absolute N supply. Neither SLA nor leaf area were affected by N:P; increasing absolute P supply significantly increased leaf area. Shoot and root biomass were minimal at N:P 45 and increased dramatically with increasing absolute P supply. Plant biomass was not correlated with Amax. Our results highlight that H. lanatus growth is predominantly controlled by P supply and to a lesser extent by N, whereas net photosynthesis exerted no apparent control on growth under these sink-limited growth conditions. Our findings contribute to understanding of plant growth under sink-limited conditions.

Keywords: biomass, grassland, greenhouse experiment, Holcus lanatus L., low relative nutrient supply, net photosynthesis, N:P supply ratio.


References

Adam P, Stricker P, Anderson DJ (1989) Species‐richness and soil phosphorus in plant communities in coastal New South Wales. Australian Journal of Ecology 14, 189–198.
Species‐richness and soil phosphorus in plant communities in coastal New South Wales.Crossref | GoogleScholarGoogle Scholar |

Aerts R, Bobbink R (1999) The impact of atmospheric nitrogen deposition on vegetation processes in terrestrial, non-forest ecosystems. In ‘The impact of nitrogen deposition on natural and semi-natural ecosystems’. (Ed. S. J. Langan.) pp. 85–122. (Kluwer Academic Publishers: Dordrecht, The Netherlands.)

Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1–67.
The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns.Crossref | GoogleScholarGoogle Scholar |

Andrews M, Sprent JI, Raven JA, Eady PE (1999) Relationships between shoot to root ratio, growth and leaf soluble protein concentration of Pisum sativum, Phaseolus vulgaris and Triticum aestivum under different nutrient deficiencies. Plant, Cell & Environment 22, 949–958.
Relationships between shoot to root ratio, growth and leaf soluble protein concentration of Pisum sativum, Phaseolus vulgaris and Triticum aestivum under different nutrient deficiencies.Crossref | GoogleScholarGoogle Scholar |

Avolio ML, Koerner SE, La Pierre KJ, Wilcox KR, Wilson GWT, Smith MD, Collins SL (2014) Changes in plant community composition, not diversity, during a decade of nitrogen and phosphorus additions drive above-ground productivity in a tallgrass prairie. Journal of Ecology 102, 1649–1660.
Changes in plant community composition, not diversity, during a decade of nitrogen and phosphorus additions drive above-ground productivity in a tallgrass prairie.Crossref | GoogleScholarGoogle Scholar |

Beadle NCW (1962) Soil phosphate and the delimitation on plant communities in eastern Australia II. Ecology 43, 281–288.
Soil phosphate and the delimitation on plant communities in eastern Australia II.Crossref | GoogleScholarGoogle Scholar |

Bobbink R, Ashmore MR, Braun S, Flückiger W, Van den Wyngaert IJ, Van Den IJJ (2003) Empirical nitrogen critical loads for natural and semi-natural ecosystems: 2002 update. In ‘Empirical critical loads for nitrogen’. (Eds B. Achermann, R. Bobbink.) pp. 43–170. (Swiss Agency for Environment, Forest and Landscape SAEFL: Berne, Switzerland.)

Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications 20, 30–59.
Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis.Crossref | GoogleScholarGoogle Scholar | 20349829PubMed |

Ceulemans T, Merckx R, Hens M, Honnay O (2011) A trait-based analysis of the role of phosphorus vs. nitrogen enrichment in plant species loss across North-west European grasslands. Journal of Applied Ecology 48, 1155–1163.
A trait-based analysis of the role of phosphorus vs. nitrogen enrichment in plant species loss across North-west European grasslands.Crossref | GoogleScholarGoogle Scholar |

Ceulemans T, Merckx R, Hens M, Honnay O (2013) Plant species loss from European semi-natural grasslands following nutrient enrichment – is it nitrogen or is it phosphorus? Global Ecology and Biogeography 22, 73–82.
Plant species loss from European semi-natural grasslands following nutrient enrichment – is it nitrogen or is it phosphorus?Crossref | GoogleScholarGoogle Scholar |

Chrysargyris A, Panayiotou C, Tzortzakis N (2016) Nitrogen and phosphorus levels affected plant growth, essential oil composition and antioxidant status of lavender plant (Lavandula angustifolia Mill.). Industrial Crops and Products 83, 577–586.
Nitrogen and phosphorus levels affected plant growth, essential oil composition and antioxidant status of lavender plant (Lavandula angustifolia Mill.).Crossref | GoogleScholarGoogle Scholar |

Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51, 335–380.
A handbook of protocols for standardised and easy measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |

De Groot CC, Marcelis LFM, van Den Boogaard R, Kaiser WM, Lambers H (2003) Interaction of nitrogen and phosphorus nutrition in determining growth. Plant and Soil 248, 257–268.
Interaction of nitrogen and phosphorus nutrition in determining growth.Crossref | GoogleScholarGoogle Scholar |

Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000) Biological stoichiometry from genes to ecosystems. Ecology Letters 3, 540–550.
Biological stoichiometry from genes to ecosystems.Crossref | GoogleScholarGoogle Scholar |

Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment 24, 755–767.
Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain.Crossref | GoogleScholarGoogle Scholar |

Fay P, Mitchell DT, Osborne BA (1996) Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus. New Phytologist 132, 425–433.
Photosynthesis and nutrient-use efficiency of barley in response to low arbuscular mycorrhizal colonization and addition of phosphorus.Crossref | GoogleScholarGoogle Scholar |

Flückiger W, Braun S (1998) Nitrogen deposition in Swiss forests and its possible relevance for leaf nutrient status, parasite attacks and soil acidification. Environmental Pollution 102, 69–76.
Nitrogen deposition in Swiss forests and its possible relevance for leaf nutrient status, parasite attacks and soil acidification.Crossref | GoogleScholarGoogle Scholar |

Fujita Y, Robroek BJM, de Ruiter PC, Heil GW, Wassen MJ (2010) Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity. Oikos 119, 1665–1673.
Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity.Crossref | GoogleScholarGoogle Scholar |

Fujita Y, Venterink HO, van Bodegom PM, Douma JC, Heil GW, Hölzel N, Jabłońska E, Kotowski W, Okruszko T, Pawlikowski P, de Ruiter PC, Wassen MJ (2014) Low investment in sexual reproduction threatens plants adapted to phosphorus limitation. Nature 505, 82–86.
Low investment in sexual reproduction threatens plants adapted to phosphorus limitation.Crossref | GoogleScholarGoogle Scholar | 24240278PubMed |

Ghannoum O, Conroy JP (2007) Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses. Functional Plant Biology 34, 72–81.
Phosphorus deficiency inhibits growth in parallel with photosynthesis in a C3 (Panicum laxum) but not two C4 (P. coloratum and Cenchrus ciliaris) grasses.Crossref | GoogleScholarGoogle Scholar | 32689333PubMed |

Ghannoum O, Paul MJ, Ward JL, Beale MH, Corol DI, Conroy JP (2008) The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses. Functional Plant Biology 35, 213–221.
The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses.Crossref | GoogleScholarGoogle Scholar | 32688775PubMed |

Gifford RM (1974) A comparison of potential photosynthesis, productivity and yield of plant species with differing photosynthetic metabolism. Australian Journal of Plant Physiology 1, 107–117.
A comparison of potential photosynthesis, productivity and yield of plant species with differing photosynthetic metabolism.Crossref | GoogleScholarGoogle Scholar |

Güsewell S (2004) N :P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266.
N :P ratios in terrestrial plants: variation and functional significance.Crossref | GoogleScholarGoogle Scholar |

Güsewell S (2005) High nitrogen : phosphorus ratios reduce nutrient retention and second-year growth of wetland sedges. New Phytologist 166, 537–550.
High nitrogen : phosphorus ratios reduce nutrient retention and second-year growth of wetland sedges.Crossref | GoogleScholarGoogle Scholar |

Hautier Y, Niklaus PA, Hector A (2009) Competition for light causes plant biodiversity loss after eutrophication. Science 324, 636–638.
Competition for light causes plant biodiversity loss after eutrophication.Crossref | GoogleScholarGoogle Scholar | 19407202PubMed |

Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11, 610–617.
How do plants respond to nutrient shortage by biomass allocation?Crossref | GoogleScholarGoogle Scholar | 17092760PubMed |

Herold A (1980) Regulation of photosynthesis by sink activity – the missing link. New Phytologist 86, 131–144.
Regulation of photosynthesis by sink activity – the missing link.Crossref | GoogleScholarGoogle Scholar |

Huston M (1980) Soil nutrients and tree species richness in Costa Rican forests. Journal of Biogeography 7, 147–157.
Soil nutrients and tree species richness in Costa Rican forests.Crossref | GoogleScholarGoogle Scholar |

Johnson CR (1984) Phosphorus nutrition on mycorrhizal colonization, photosynthesis, growth and nutrient composition of Citrus aurantium. Plant and Soil 80, 35–42.
Phosphorus nutrition on mycorrhizal colonization, photosynthesis, growth and nutrient composition of Citrus aurantium.Crossref | GoogleScholarGoogle Scholar |

Kachi N, Hirose T (1983) Limiting nutrients for plant growth in coastal sand dune soils. Journal of Ecology 71, 937–944.
Limiting nutrients for plant growth in coastal sand dune soils.Crossref | GoogleScholarGoogle Scholar |

Keddy P, Fraser LH, Keogh TA (2001) Responses of 21 wetland species to shortages of light, nitrogen and phosphorus. Bulletin of the Geobotanical Institute ETH 67, 13–25.

Köhler B, Ryser P, Güsewell S, Gigon A (2001) Nutrient availability and limitation in traditionally mown and in abandoned limestone grasslands: a bioassay experiment. Plant and Soil 230, 323–332.
Nutrient availability and limitation in traditionally mown and in abandoned limestone grasslands: a bioassay experiment.Crossref | GoogleScholarGoogle Scholar |

Körner C (2003) Carbon limitation in trees. Journal of Ecology 91, 4–17.
Carbon limitation in trees.Crossref | GoogleScholarGoogle Scholar |

Körner C (2015) Paradigm shift in plant growth control. Current Opinion in Plant Biology 25, 107–114.
Paradigm shift in plant growth control.Crossref | GoogleScholarGoogle Scholar | 26037389PubMed |

Kuppers M, Koch G, Mooney H (1988) Compensating effects to growth of changes in dry matter allocation in response to variation in photosynthetic characteristics induced by photoperiod, light and nitrogen. Australian Journal of Plant Physiology 15, 287–298.
Compensating effects to growth of changes in dry matter allocation in response to variation in photosynthetic characteristics induced by photoperiod, light and nitrogen.Crossref | GoogleScholarGoogle Scholar |

Liebig J (1842) ‘Die organische Chemie in ihrer Anwendung auf Agricultur und Physiologie.’ (Friedrich Vieweg und Sohn: Braunschweig, Germany.)

Marion GM, Hastings SJ, Oberbauer SF, Oechel WC (1989) Soil–plant element relationships in a tundra ecosystem. Holarctic Ecology 12, 296–303.
Soil–plant element relationships in a tundra ecosystem.Crossref | GoogleScholarGoogle Scholar |

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press: London, UK.)

Muller B, Pantin F, Génard M, Turc O, Freixes S, Piques M, Gibon Y (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany 62, 1715–1729.
Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs.Crossref | GoogleScholarGoogle Scholar | 21239376PubMed |

Olde Venterink H (2011) Does phosphorus limitation promote species-rich plant communities? Plant and Soil 345, 1–9.
Does phosphorus limitation promote species-rich plant communities?Crossref | GoogleScholarGoogle Scholar |

Poorter H, van der Werf A (1998) Is inherent variation in RGR determined by LAR at low light and by NAR at high light? A review of herbaceous species. In ‘Inherent variation in plant growth’. (Eds H. Lambers, H. Poorter and M. M. I. van Vuuren.) pp. 309–336. (Backhuys Publishers: Leiden, The Netherlands.)

Reich PB, Hobbie SE (2013) Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass. Nature Climate Change 3, 278–282.
Decade-long soil nitrogen constraint on the CO2 fertilization of plant biomass.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Walters MB (1994) Photosynthesis–nitrogen relations in Amazonian tree species. Oecologia 97, 73–81.
Photosynthesis–nitrogen relations in Amazonian tree species.Crossref | GoogleScholarGoogle Scholar | 28313591PubMed |

Reich PB, Walters MB, Ellsworth DS (1992) Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecological Monographs 62, 365–392.
Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems.Crossref | GoogleScholarGoogle Scholar |

Reich PB, Oleksyn J, Wright IJ (2009) Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160, 207–212.
Leaf phosphorus influences the photosynthesis–nitrogen relation: a cross-biome analysis of 314 species.Crossref | GoogleScholarGoogle Scholar | 19212782PubMed |

Reich PB, Hobbie SE, Lee TD, Pastore MA (2018) Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment. Science 360, 317–320.
Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment.Crossref | GoogleScholarGoogle Scholar | 29674593PubMed |

Roeling IS, Ozinga WA, van Dijk J, Eppinga MB, Wassen MJ (2018) Plant species occurrence patterns in Eurasian grasslands reflect adaptation to nutrient ratios. Oecologia 186, 1055–1067.
Plant species occurrence patterns in Eurasian grasslands reflect adaptation to nutrient ratios.Crossref | GoogleScholarGoogle Scholar | 29450649PubMed |

Shaver GR, Kummerow J (1992) Phenology, resource allocation and growth of arctic vascular plants. In ‘Arctic ecosystems in a changing climate’. (Eds F. S. Chaplin III, R. L. Jefferies, J. F. Reynolds, G. R. Shavers and J. Svoboda.) pp. 193–211. (Academic Press: California, USA.)

Shen J, Rengel Z, Tang C, Zhang F (2003) Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus. Plant and Soil 248, 199–206.
Role of phosphorus nutrition in development of cluster roots and release of carboxylates in soil-grown Lupinus albus.Crossref | GoogleScholarGoogle Scholar |

Sims JT, Simard RR, Joern BC (1998) Phosphorus loss in agricultural drainage: historical perspective and current research. Journal of Environmental Quality 27, 277–293.
Phosphorus loss in agricultural drainage: historical perspective and current research.Crossref | GoogleScholarGoogle Scholar |

Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100, 179–196.
Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar | 15093117PubMed |

Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the richness of grasslands. Science 303, 1876–1879.
Impact of nitrogen deposition on the richness of grasslands.Crossref | GoogleScholarGoogle Scholar | 15031507PubMed |

Terry N, Ulrich A (1973) Effects of phosphorus deficiency on the photosynthesis and respiration of leaves of sugar beet. Plant Physiology 51, 43–47.
Effects of phosphorus deficiency on the photosynthesis and respiration of leaves of sugar beet.Crossref | GoogleScholarGoogle Scholar | 16658294PubMed |

Tuohy JM, Prior JAB, Stewart GR (1991) Photosynthesis in relation to leaf nitrogen and phosphorus content in Zimbabwean trees. Oecologia 88, 378–382.
Photosynthesis in relation to leaf nitrogen and phosphorus content in Zimbabwean trees.Crossref | GoogleScholarGoogle Scholar | 28313800PubMed |

Usuda H (1995) Phosphate deficiency in maize. V. Mobilization of nitrogen and phosphorus within shoots of young plants and its relationship to senescence. Plant & Cell Physiology 36, 1041–1049.
Phosphate deficiency in maize. V. Mobilization of nitrogen and phosphorus within shoots of young plants and its relationship to senescence.Crossref | GoogleScholarGoogle Scholar |

Veresoglou ADS, Fitter AH (1984) Spatial and temporal patterns of growth and nutrient uptake of five co-existing grasses. Journal of Ecology 72, 259–272.
Spatial and temporal patterns of growth and nutrient uptake of five co-existing grasses.Crossref | GoogleScholarGoogle Scholar |

Vermeer JG, Berendse F (1983) The relationship between nutrient availability, shoot biomass and species richness in grassland and wetland communities. Vegetatio 53, 121–126.
The relationship between nutrient availability, shoot biomass and species richness in grassland and wetland communities.Crossref | GoogleScholarGoogle Scholar |

Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115.
Nitrogen limitation on land and in the sea: how can it occur?Crossref | GoogleScholarGoogle Scholar |

Vitousek PM, Aber JD, Howarth RH, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: source and consequences. Ecological Applications 7, 737–750.
Human alteration of the global nitrogen cycle: source and consequences.Crossref | GoogleScholarGoogle Scholar |

Walker AP, Beckerman AP, Gu L, Kattge J, Cernusak LA, Domingues TF, Scales JC, Wohlfahrt G, Wullschleger SD, Woodward FI (2014) The relationship of leaf photosynthetic traits – Vcmax and Jmax – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study. Ecology and Evolution 4, 3218–3235.
The relationship of leaf photosynthetic traits – Vcmax and Jmax – to leaf nitrogen, leaf phosphorus, and specific leaf area: a meta-analysis and modeling study.Crossref | GoogleScholarGoogle Scholar | 25473475PubMed |

Wang S, van Dijk J, Wassen MJ (2019) Sexual reproduction traits of Holcus lanatus L. and Parnassia palustris L. in response to absolute and relative supply of nitrogen and phosphorus. Environmental and Experimental Botany 168, 103813
Sexual reproduction traits of Holcus lanatus L. and Parnassia palustris L. in response to absolute and relative supply of nitrogen and phosphorus.Crossref | GoogleScholarGoogle Scholar |

Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytologist 116, 341–381.
The control of carbon partitioning in plants.Crossref | GoogleScholarGoogle Scholar |

Wassen MJ, Venterink HO, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437, 547–550.
Endangered plants persist under phosphorus limitation.Crossref | GoogleScholarGoogle Scholar | 16177790PubMed |

Wheeler BD, Shaw SC (1991) Above-ground crop mass and species richness of the principal types of herbaceous rich-fen vegetation of lowland England and Wales. Journal of Ecology 79, 285–301.
Above-ground crop mass and species richness of the principal types of herbaceous rich-fen vegetation of lowland England and Wales.Crossref | GoogleScholarGoogle Scholar |

Wielgolaski FE, Bliss LC, Svoboda J, Doyle G (1981) Primary production of tundra. In ‘Tundra ecosystems: A comparative analysis’. (Eds L. C. Bliss, O. W. Heal and J. J. Moore.) pp. 187–225. (Cambridge University Press: Cambridge, UK.)