The association of leaf sulfur content with the leaf economics spectrum and plant adaptive strategies
Michele Dalle Fratte
A C , Simon Pierce B , Magda Zanzottera A and Bruno E. L. Cerabolini A
+ Author Affiliations
- Author Affiliations
A Department of Biotechnology and Life Sciences (DBSV), Università degli Studi dell’Insubria, Via J.H. Dunant 3, I-21100, Varese, Italy.
B Department of Agricultural and Environmental Sciences (DiSAA), Università degli Studi di Milano, Via G. Celoria 2, I-20133 Milan, Italy.
C Corresponding author. Email: michele.dallefratte@gmail.com
Functional Plant Biology 48(9) 924-935 https://doi.org/10.1071/FP20396
Submitted: 17 December 2020 Accepted: 26 April 2021 Published: 25 May 2021
Abstract
Sulfur is an essential macronutrient for plant primary metabolism. Its availability can modulate plant growth in most terrestrial ecosystems. However, its relationship with other leaf and nutrient traits, and hence its contribution to plant functioning, remains unclear. We analysed leaf and nutrient traits for 740 vascular plant species growing in a wide range of environmental conditions in Northern Italy. We determined whether leaf sulfur content per unit leaf dry mass (LSC) is associated with leaf economics spectrum, and whether its distribution among functional types (growth forms, leaf life span categories, and Grime’s CSR (Competitive, Stress-tolerant, Ruderal strategies) could help to elucidate adaptive differences within plant taxa. High LSC values were mainly associated with fast-growing species representative of R- and C- strategy selection, thus the acquisitive extreme of plant economics, reflecting strong potential connections with ecosystem properties such as biomass production or litter decomposability. In general, LSC was significantly and positively correlated with leaf nitrogen content, and nitrogen to sulfur ratio was constant throughout growth forms, leaf life span and CSR strategies, and phylogenetic effects were evident. Our findings highlight that LSC variation is strongly associated with the leaf economics spectrum, suggesting that additional nutrients seldom included in functional analyses may also be embroiled within the context of plant economics. However, different ratios among nitrogen and sulfur may be expected across different plant families, suggesting that deeper insight from functional groups can provide a bridge between plant stoichiometry and ecology, useful for the evaluation of ecological responses to global change.
Keywords: plant functional traits, global spectrum, Grime’s strategies, CSR, leaf nutrients, ecological stoichiometry.
References
Aas W, Mortier A, Bowersox V, Cherian R, Faluvegi G, Fagerli H, et al (2019) Global and regional trends of atmospheric sulfur. Scientific Reports 9, 953| Global and regional trends of atmospheric sulfur.Crossref | GoogleScholarGoogle Scholar | 30700755PubMed |
Aerts R, Chapin FS (1999) 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 |
Badenes-Perez FR, Gershenzon J, Heckel DG (2014) Insect attraction versus plant defense: young leaves high in glucosinolates stimulate oviposition by a specialist herbivore despite poor larval survival due to high saponin content. PLoS One 9, e95766
| Insect attraction versus plant defense: young leaves high in glucosinolates stimulate oviposition by a specialist herbivore despite poor larval survival due to high saponin content.Crossref | GoogleScholarGoogle Scholar | 24752069PubMed |
Bruelheide H, Dengler J, Purschke O, Lenoir J, Jiménez-Alfaro B, Hennekens SM, et al (2018) Global trait–environment relationships of plant communities. Nature Ecology & Evolution 2, 1906–1917.
| Global trait–environment relationships of plant communities.Crossref | GoogleScholarGoogle Scholar |
Bussotti F, Prancrazi M, Matteucci G, Gerosa G (2005) Leaf morphology and chemistry in Fagus sylvatica (beech) trees as affected by site factors and ozone: results from CONECOFOR permanent monitoring plots in Italy. Tree Physiology 25, 211–219.
| Leaf morphology and chemistry in Fagus sylvatica (beech) trees as affected by site factors and ozone: results from CONECOFOR permanent monitoring plots in Italy.Crossref | GoogleScholarGoogle Scholar | 15574402PubMed |
Cayuela L, Stein A, Oksanen J (2017) Taxonstand: taxonomic standardization of plant species names. R package version 2.0. R Foundation for Statistical Computing.
Chelli S, Marignani M, Barni E, Petraglia A, Puglielli G, Wellstein C, et al (2019) Plant–environment interactions through a functional traits perspective: a review of Italian studies. Plant Biosystems – An International Journal Dealing with all Aspects of Plant Biology 153, 853–869.
| Plant–environment interactions through a functional traits perspective: a review of Italian studies.Crossref | GoogleScholarGoogle Scholar |
Dalle Fratte M, Brusa G, Pierce S, Zanzottera M, Cerabolini BEL (2019) Plant trait variation along environmental indicators to infer global change impacts. Flora 254, 113–121.
| Plant trait variation along environmental indicators to infer global change impacts.Crossref | GoogleScholarGoogle Scholar |
De Kok LJ, Hawkesford MJ, Haneklaus SH, Schnug E (2017) Sulfur Metabolism in Higher Plants-Fundamental, Environmental and Agricultural Aspects. Springer International Publishing.
de la Riva EG, Villar R, Pérez-Ramos IM, Quero JL, Matías L, Poorter L, Marañón T (2018) Relationships between leaf mass per area and nutrient concentrations in 98 Mediterranean woody species are determined by phylogeny, habitat and leaf habit. Trees 32, 497–510.
| Relationships between leaf mass per area and nutrient concentrations in 98 Mediterranean woody species are determined by phylogeny, habitat and leaf habit.Crossref | GoogleScholarGoogle Scholar |
Díaz S, Kattge J, Cornelissen JHC, Wright IJ, Lavorel S, Dray S, et al (2016) The global spectrum of plant form and function. Nature 529, 167–171.
| The global spectrum of plant form and function.Crossref | GoogleScholarGoogle Scholar | 26700811PubMed |
Dijkshoorn W, Van Wijk AL (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.
| The sulphur requirements of plants as evidenced by the sulphur-nitrogen ratio in the organic matter a review of published data.Crossref | GoogleScholarGoogle Scholar |
Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynthesis Research 79, 331–348.
| Sulfur assimilation and the role of sulfur in plant metabolism: a survey.Crossref | GoogleScholarGoogle Scholar | 16328799PubMed |
EEA (2020) Air quality in Europe - 2020 report. European Environmental Agency, Report No 09/2020.
Elser JJ, Fagan WF, Kerkhoff AJ, Swenson NG, Enquist BJ (2010) Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytologist 186, 593–608.
| Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change.Crossref | GoogleScholarGoogle Scholar |
Freschet GT, Cornelissen JH, Van Logtestijn RS, Aerts R (2010) Evidence of the ‘plant economics spectrum’ in a subarctic flora. Journal of Ecology 98, 362–373.
| Evidence of the ‘plant economics spectrum’ in a subarctic flora.Crossref | GoogleScholarGoogle Scholar |
Gierlinger N, Sapei L, Paris O (2008) Insights into the chemical composition of Equisetum hyemale by high resolution Raman imaging. Planta 227, 969–980.
| Insights into the chemical composition of Equisetum hyemale by high resolution Raman imaging.Crossref | GoogleScholarGoogle Scholar | 18057960PubMed |
Grime JP (2006) Plant strategies, vegetation processes, and ecosystem properties. John Wiley & Sons.
Grime JP, Pierce S (2012) The Evolutionary Strategies that Shape Ecosystems. John Wiley & Sons.
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 |
Hamilton NE, Ferry M (2018) ggtern: Ternary diagrams using ggplot2. Journal of Statistical Software 87, 1–17.
Han WX, Fang JY, Reich PB, Ian Woodward F, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecology Letters 14, 788–796.
| Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China.Crossref | GoogleScholarGoogle Scholar | 21692962PubMed |
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM (2007) Plant structural traits and their role in anti-herbivore defence. Perspectives in Plant Ecology, Evolution and Systematics 8, 157–178.
| Plant structural traits and their role in anti-herbivore defence.Crossref | GoogleScholarGoogle Scholar |
Hasanuzzaman M, Fujita M, Oku H, Nahar K, Hawrylak-Nowak B (Eds.) (2018). Plant Nutrients and Abiotic Stress Tolerance. Springer.
Hawkesford MJ, De Kok LJ (2007) Sulfur in plants – An ecological perspective. London: Springer.
Hu X, Page MT, Sumida A, Tanaka A, Terry MJ, Tanaka R (2017) The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling. The Plant Journal 89, 1184–1194.
| The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling.Crossref | GoogleScholarGoogle Scholar | 28004871PubMed |
Husby C (2013) Biology and functional ecology of Equisetum with emphasis on the giant horsetails. Botanical Review 79, 147–177.
| Biology and functional ecology of Equisetum with emphasis on the giant horsetails.Crossref | GoogleScholarGoogle Scholar |
Johnson J, Graf Pannatier E, Carnicelli S, Cecchini G, Clarke N, Cools N, et al (2018) The response of soil solution chemistry in European forests to decreasing acid deposition. Global Change Biology 24, 3603–3619.
| The response of soil solution chemistry in European forests to decreasing acid deposition.Crossref | GoogleScholarGoogle Scholar | 29604157PubMed |
Kattge J, Bönisch G, Díaz S, Lavorel S, Prentice IC, Leadley P, et al (2020) TRY plant trait database–enhanced coverage and open access. Global Change Biology 26, 119–188.
| TRY plant trait database–enhanced coverage and open access.Crossref | GoogleScholarGoogle Scholar | 31891233PubMed |
Kay M, Wobbrock J (2016) ARTool: aligned rank transform for nonparametric factorial ANOVAs. R package version 0.10, 2.
Laliberté E, Shipley B, Norton DA, Scott D (2012) Which plant traits determine abundance under long‐term shifts in soil resource availability and grazing intensity? Journal of Ecology 100, 662–677.
| Which plant traits determine abundance under long‐term shifts in soil resource availability and grazing intensity?Crossref | GoogleScholarGoogle Scholar |
Lê S, Josse J, Mazet F (2008) Package ‘FactoMineR. Journal of Statistical Software 25, 1–18.
Legay N, Personeni E, Slezack-Deschaumes S, Piutti S, Cliquet JB (2014) Grassland species show similar strategies for sulphur and nitrogen acquisition. Plant and Soil 375, 113–126.
| Grassland species show similar strategies for sulphur and nitrogen acquisition.Crossref | GoogleScholarGoogle Scholar |
Lenth R, Singmann H, Love J, Buerkner P, Herve M (2018) Emmeans: Estimated marginal means, aka least-squares means. R package version, 1(1), 3.
Marschner H (2012) Marschner’s mineral nutrition of higher plants. Third Edition. Academic press.
Miatto RC, Batalha MA (2016) Leaf chemistry of woody species in the Brazilian cerrado and seasonal forest: response to soil and taxonomy and effects on decomposition rates. Plant Ecology 217, 1467–1479.
| Leaf chemistry of woody species in the Brazilian cerrado and seasonal forest: response to soil and taxonomy and effects on decomposition rates.Crossref | GoogleScholarGoogle Scholar |
Pérez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61, 167–234.
| New handbook for standardised measurement of plant functional traits worldwide.Crossref | GoogleScholarGoogle Scholar |
Pierce S, Ceriani RM, De Andreis R, Luzzaro A, Cerabolini BEL (2007) The leaf economics spectrum of Poaceae reflects variation in survival strategies. Plant Biosystems 141, 337–343.
| The leaf economics spectrum of Poaceae reflects variation in survival strategies.Crossref | GoogleScholarGoogle Scholar |
Pierce S, Brusa G, Vagge I, Cerabolini BEL (2013) Allocating CSR plant functional types: the use of leaf economics and size traits to classify woody and herbaceous vascular plants. Functional Ecology 27, 1002–1010.
| Allocating CSR plant functional types: the use of leaf economics and size traits to classify woody and herbaceous vascular plants.Crossref | GoogleScholarGoogle Scholar |
Pierce S, Negreiros D, Cerabolini BEL, Kattge J, Díaz S, Kleyer M, et al (2017) A global method for calculating plant CSR ecological strategies applied across biomes world‐wide. Functional Ecology 31, 444–457.
| A global method for calculating plant CSR ecological strategies applied across biomes world‐wide.Crossref | GoogleScholarGoogle Scholar |
Pignatti S (1982) Flora d’Italia. Edagricole, Bologna, vol. 1–3.
Poorter H, Niinemets Ü, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis. New Phytologist 182, 565–588.
| Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/
Reich PB (2014) The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102, 275–301.
| The world‐wide ‘fast–slow’ plant economics spectrum: a traits manifesto.Crossref | GoogleScholarGoogle Scholar |
Reich PB, Tjoelker MG, Pregitzer KS, Wright IJ, Oleksyn J, Machado JL (2008) Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants. Ecology Letters 11, 793–801.
| Scaling of respiration to nitrogen in leaves, stems and roots of higher land plants.Crossref | GoogleScholarGoogle Scholar | 18445031PubMed |
Resurreccion AP, Makino A, Bennett J, Mae T (2001) Effects of sulfur nutrition on the growth and photosynthesis of rice. Soil Science and Plant Nutrition 47, 611–620.
| Effects of sulfur nutrition on the growth and photosynthesis of rice.Crossref | GoogleScholarGoogle Scholar |
Rosenfield MV, Keller JK, Clausen C, Cyphers K, Funk JL (2020) Leaf traits can be used to predict rates of litter decomposition. Oikos 129, 1589–1596.
| Leaf traits can be used to predict rates of litter decomposition.Crossref | GoogleScholarGoogle Scholar |
Sardans J, Penuelas J, Ogaya R (2008) Drought’s impact on Ca, Fe, Mg, Mo and S concentration and accumulation patterns in the plants and soil of a Mediterranean evergreen Quercus ilex forest. Biogeochemistry 87, 49–69.
| Drought’s impact on Ca, Fe, Mg, Mo and S concentration and accumulation patterns in the plants and soil of a Mediterranean evergreen Quercus ilex forest.Crossref | GoogleScholarGoogle Scholar |
Sardans J, Alonso R, Carnicer J, Fernández-Martínez M, Vivanco MG, Peñuelas J (2016) Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain. Perspectives in Plant Ecology, Evolution and Systematics 18, 52–69.
| Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain.Crossref | GoogleScholarGoogle Scholar |
Shi S, Peng C, Wang M, Zhu Q, Yang G, Yang Y, et al (2016) A global meta-analysis of changes in soil carbon, nitrogen, phosphorus and sulfur, and stoichiometric shifts after forestation. Plant and Soil 407, 323–340.
| A global meta-analysis of changes in soil carbon, nitrogen, phosphorus and sulfur, and stoichiometric shifts after forestation.Crossref | GoogleScholarGoogle Scholar |
Villar R, Merino J (2001) Comparison of leaf construction costs in woody species with differing leaf life‐spans in contrasting ecosystems. New Phytologist 151, 213–226.
| Comparison of leaf construction costs in woody species with differing leaf life‐spans in contrasting ecosystems.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Cannon K (2001) Relationships between leaf lifespan and structural defences in a low‐nutrient, sclerophyll flora. Functional Ecology 15, 351–359.
| Relationships between leaf lifespan and structural defences in a low‐nutrient, sclerophyll flora.Crossref | GoogleScholarGoogle Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, et al (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| The worldwide leaf economics spectrum.Crossref | GoogleScholarGoogle Scholar | 15103368PubMed |
Wu Y, Liu H, Song Z, Yang X, Li Z, Hao Q, Liu L (2017) Ecological stoichiometry of nitrogen, phosphorus, and sulfur in China’s forests. Acta Geochimica 36, 525–530.
| Ecological stoichiometry of nitrogen, phosphorus, and sulfur in China’s forests.Crossref | GoogleScholarGoogle Scholar |
Zhang SB, Zhang JL, Slik JF, Cao KF (2012) Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment. Global Ecology and Biogeography 21, 809–818.
| Leaf element concentrations of terrestrial plants across China are influenced by taxonomy and the environment.Crossref | GoogleScholarGoogle Scholar |
