Comparison of four light-response models using relative curvature measures of nonlinearity.

Close-to-linear behavior Goodness of fit Nonlinear regression Parameter-effects curvature Photosynthetic light response curves

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
14 10 2024
Historique:
received: 25 05 2024
accepted: 04 10 2024
medline: 15 10 2024
pubmed: 15 10 2024
entrez: 14 10 2024
Statut: epublish

Résumé

Photosynthetic light response curves serve as powerful mathematical tools for quantitatively describing the rate of photosynthesis of plants in response to changes in irradiance. However, in practical applications, the daunting task of selecting an appropriate nonlinear model to accurately fit these curves persists as a significant challenge. Thus, there arises a need for a method to systematically evaluate the efficacy of such models. In the present study, four distinct nonlinear models, namely Exponential Model (EM), Rectangular Hyperbola Model (RHM), Nonrectangular Hyperbola Model (NHM), and Modified Rectangular Hyperbola Model (MRHM), were used to fit the relationship between light intensity and the rate of photosynthesis across 42 empirical datasets. The goodness of fit for each model was assessed using the root-mean-square error, and relative curvature measures of nonlinearity were employed to assess the nonlinear behavior of the models. In terms of goodness of fit, pairwise difference tests of the root-mean-square error revealed that there was little to choose among the four models, although RHM gave a marginally poorer fit. However, in terms of nonlinear behavior, EM not only provided the most favorable linear approximation performance at the global level, but also exhibited the best close-to-linear behavior at the individual parameter level among the four models across the 42 datasets. Consequently, the results strongly advocate for EM as the most suitable mathematical framework for fitting photosynthetic light response curves. These findings provide insights into the model assessment for nonlinear regression in describing the relationship between the photosynthetic rate and light intensity.

Identifiants

pubmed: 39402162
doi: 10.1038/s41598-024-75325-0
pii: 10.1038/s41598-024-75325-0
doi:

Types de publication

Journal Article Comparative Study

Langues

eng

Sous-ensembles de citation

IM

Pagination

24058

Informations de copyright

© 2024. The Author(s).

Références

Li, X. et al. COR27 and COR28 are novel regulators of the COP1-HY5 regulatory hub and photomorphogenesis in Arabidopsis. Plant. Cell. 32, 3139–3154. https://doi.org/10.1105/tpc.20.00195 (2020).
doi: 10.1105/tpc.20.00195 pubmed: 32769132 pmcid: 7534460
Terashima, I. & Saeki, T. Light environment within a leaf I. Optical properties of paradermal sections of Camellia leaves with special reference to differences in the optical properties of palisade and spongy tissues. Plant. Cell. Physiol. 24, 1493–1501. https://doi.org/10.1093/oxfordjournals.pcp.a076672 (1983).
doi: 10.1093/oxfordjournals.pcp.a076672
Ögren, E. Convexity of the photosynthetic light-response curve in relation to intensity and direction of light during growth. Plant. Physiol. 101, 1013–1019. https://doi.org/10.1104/pp.101.3.1013 (1993).
doi: 10.1104/pp.101.3.1013 pubmed: 12231754 pmcid: 158720
Chen, Y. & Xu, D. Two patterns of leaf photosynthetic response to irradiance transition from saturating to limiting one in some plant species. New. Phytol. 169, 789–798. https://doi.org/10.1111/j.1469-8137.2005.01624.x (2006).
doi: 10.1111/j.1469-8137.2005.01624.x pubmed: 16441759
Ye, Z. & Yu, Q. A coupled model of stomatal conductance and photosynthesis for winter wheat. Photosynthetica 46, 637–640. https://doi.org/10.1007/s11099-008-0110-0 (2008).
doi: 10.1007/s11099-008-0110-0
dos Santos Junior, U. M., de Carvalho Gonçalves, J. F. & Fearnside, P. M. Measuring the impact of flooding on amazonian trees: photosynthetic response models for ten species flooded by hydroelectric dams. Trees 27, 193–210. https://doi.org/10.1007/s00468-012-0788-2 (2013).
doi: 10.1007/s00468-012-0788-2
Darvehei, P., Bahri, P. A. & Moheimani, N. R. Model development for the growth of microalgae: a review. Renew. Sust Energ. Rev. 97, 233–258. https://doi.org/10.1016/j.rser.2018.08.027 (2018).
doi: 10.1016/j.rser.2018.08.027
Webb, W. L., Newton, M. & Starr, D. Carbon dioxide exchange of Alnus rubra. A mathematical model. Oecologia 17, 281–291. https://doi.org/10.1007/BF00345747 (1974).
doi: 10.1007/BF00345747 pubmed: 28308943
Jassby, A. D. & Platt, T. Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol. Oceanogr. 21, 540–547. https://doi.org/10.4319/lo.1976.21.4.0540 (1976).
doi: 10.4319/lo.1976.21.4.0540
Platt, T. & Jassby, A. D. The relationship between photosynthesis and light for natural assemblages of coastal marine phytoplankton. J. Phycol. 12, 421–430. https://doi.org/10.1111/j.1529-8817.1976.tb02866.x (1976).
doi: 10.1111/j.1529-8817.1976.tb02866.x
Platt, T., Gallegos, C. & Harrison, W. G. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J. Mar. Res. 38, 687–701 (1980).
Platt, T., Harrison, W. G., Irwin, B., Horne, E. P. & Gallegos, C. L. Photosynthesis and photoadaptation of marine phytoplankton in the arctic. Deep Sea Res. Part A Oceanogr. Res. Pap. 29, 1159–1170. https://doi.org/10.1016/0198-149(82)90087-5 (1982).
doi: 10.1016/0198-149(82)90087-5
Lieth, J. & Reynolds, J. The nonrectangular hyperbola as a photosynthetic light response model: geometrical interpretation and estimation of the parameter. Photosynthetica 21, 363–365 (1987).
Eilers, P. H. C. & Peeters, J. C. H. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecol. Model. 42, 199–215. https://doi.org/10.1016/0304-3800(88)90057-9 (1988).
doi: 10.1016/0304-3800(88)90057-9
Archontoulis, S. V. & Miguez, F. E. Nonlinear regression models and applications in agricultural research. Agron. J. 107, 786–798. https://doi.org/10.2134/agronj2012.0506 (2015).
doi: 10.2134/agronj2012.0506
Kyei-Boahen, S., Lada, R., Astatkie, T., Gordon, R. & Caldwell, C. Photosynthetic response of carrots to varying irradiances. Photosynthetica 41, 301–305. https://doi.org/10.1023/B:PHOT.0000011967.74465.cc (2003).
doi: 10.1023/B:PHOT.0000011967.74465.cc
Marshall, B. & Biscoe, P. A model for C3 leaves describing the dependence of net photosynthesis on irradiance. J. Exp. Bot. 31, 41–48. https://doi.org/10.1093/jxb/31.1.41 (1980).
doi: 10.1093/jxb/31.1.41
Thornley, J. Dynamic model of leaf photosynthesis with acclimation to light and nitrogen. Ann. Bot. 81, 421–430. https://doi.org/10.1006/anbo.1997.0575 (1998).
doi: 10.1006/anbo.1997.0575
Ye, Z. A new model for relationship between irradiance and the rate of photosynthesis in Oryza sativa. Photosynthetica 45, 637–640. https://doi.org/10.1007/s11099-007-0110-5 (2007).
doi: 10.1007/s11099-007-0110-5
Ye, Z., Suggett, D. J., Robakowski, P. & Kang, H. A mechanistic model for the photosynthesis-light response based on the photosynthetic electron transport of photosystem II in C3 and C4 species. New Phytol. 199, 110–120. https://doi.org/10.1111/nph.12242 (2013).
doi: 10.1111/nph.12242 pubmed: 23521402
Chen, L. et al. A general method for parameter estimation in light-response models. Sci. Rep. 6, 27905. https://doi.org/10.1038/srep27905 (2016).
doi: 10.1038/srep27905 pubmed: 27291688 pmcid: 4904205
Yang, X. L. et al. Quantifying photosynthetic performance of phytoplankton based on photosynthesis–irradiance response models. Environ. Sci. Eur. 32, 1–13. https://doi.org/10.1186/s12302-020-00306-9 (2020).
doi: 10.1186/s12302-020-00306-9
Bates, D. M. & Watts, D. G. Relative curvature measures of nonlinearity (with discussion). J. R. Statist. Soc., Ser. B. 42, 1–25. https://doi.org/10.1111/j.2517-6161.1980.tb01094.x (1980).
doi: 10.1111/j.2517-6161.1980.tb01094.x
Bassman, J. H. & Zwier, J. C. Gas exchange characteristics of Populus trichocarpa, Populus deltoides and Populus trichocarpa × P. deltoides clones. Tree Physiol. 8, 145–159. https://doi.org/10.1093/treephys/8.2.145 (1991).
doi: 10.1093/treephys/8.2.145 pubmed: 14972886
Box, G. E. P. & Lucas, H. L. Design of experiments in nonlinear situations. Biometrika 46, 77–90. https://doi.org/10.2307/2332810 (1959).
doi: 10.2307/2332810
Ratkowsky, D. A. & Reddy, G. V. P. Empirical model with excellent statistical properties for describing temperature-dependent developmental rates of insects and mites. Ann. Entomol. Soc. Am. 110, 302–309. https://doi.org/10.1093/aesa/saw098 (2017).
doi: 10.1093/aesa/saw098
Ratkowsky, D. A. Nonlinear Regression Modeling: A Unified Practical Approach (Marcel Dekker, 1983).
Ratkowsky, D. A. Handbook of Nonlinear Regression Models (Marcel Dekker, 1990).
Bates, D. M. & Watts, D. G. Nonlinear Regression Analysis and its Applications (Wiley, 1988).
Beale, E. M. L. Confidence regions in non-linear estimation (with discussion). J. R. Statist. Soc., Ser. B. 22, 41–76. https://doi.org/10.1111/j.2517-6161.1960.tb00353.x (1960).
doi: 10.1111/j.2517-6161.1960.tb00353.x
Box, M. J. Bias in nonlinear estimation (with discussion). J. R. Statist. Soc., Ser. B. 33, 171–201. https://doi.org/10.1111/j.2517-6161.1971.tb00871.x (1971).
doi: 10.1111/j.2517-6161.1971.tb00871.x
Hougaard, P. The appropriateness of the asymptotic distribution in a nonlinear regression model in relation to curvature. J. R. Statist. Soc., Ser. B. 47, 103–114. https://doi.org/10.1111/j.2517-6161.1985.tb01336.x (1985).
doi: 10.1111/j.2517-6161.1985.tb01336.x
Lipschutz, M. M. Schaum’s outline of theory and problems of differential geometry (McGraw-Hill, 1969).
Haines, L. M., O’Brien, T. E. & Clarke, G. P. Y. Kurtosis and curvature measures for nonlinear regression models. Stat. Sin. 14, 547–570 (2004).
Nelder, J. A. & Mead, R. A simplex method for function minimization. Comput. J. 7, 308–313. https://doi.org/10.1093/comjnl/7.4.308 (1965).
doi: 10.1093/comjnl/7.4.308
Shi, P., Ridland, P., Ratkowsky, D. A. & Li, Y. IPEC: root mean square curvature calculation. R package version 1.1.0.  https://CRAN.R-project.org/package=IPEC (2024).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (2022). https://www.rproject.org/  (Data of access: 7/1/2022).
Burnham, K. P. & Anderson, D. R. Multimodel inference: understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304. https://doi.org/10.1177/0049124104268644 (2004).
doi: 10.1177/0049124104268644
Wang, L. et al. Comparison of four performance models in quantifying the inequality of leaf and fruit size distribution. Ecol. Evol. 14, e11072. https://doi.org/10.1002/ece3.11072 (2024).
doi: 10.1002/ece3.11072 pubmed: 38435001 pmcid: 10905244

Auteurs

Ke He (K)

School of Architecture, Huaqiao University, Xiamen, 361021, China.

Lin Wang (L)

Co-Innovation Centre for Sustainable Forestry in Southern China, Bamboo Research Institute, Nanjing Forestry University, Nanjing, 210037, China.
College of Life Sciences, Sichuan University, Chengdu, 610065, China.

David A Ratkowsky (DA)

Tasmanian Institute of Agriculture, University of Tasmania, Hobart, TAS, 7001, Australia.

Peijian Shi (P)

Co-Innovation Centre for Sustainable Forestry in Southern China, Bamboo Research Institute, Nanjing Forestry University, Nanjing, 210037, China. pjshi@njfu.edu.cn.

Articles similaires

Photosynthesis Ribulose-Bisphosphate Carboxylase Carbon Dioxide Molecular Dynamics Simulation Cyanobacteria
Vancomycin Polyesters Anti-Bacterial Agents Models, Theoretical Drug Liberation
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria

High-throughput Bronchus-on-a-Chip system for modeling the human bronchus.

Akina Mori, Marjolein Vermeer, Lenie J van den Broek et al.
1.00
Humans Bronchi Lab-On-A-Chip Devices Epithelial Cells Goblet Cells

Classifications MeSH