# Loïc Pagès, founding scientist in root ecology and modelling

Jean-François Barczi, Amira Beroueg, Gerhard Buck-Sorlin, Valentin Couvreur, Frédéric Danjon, Benjamin M. Delory, Claude Doussan, Tom de Swaef, Xavier Draye, Jean-Louis Drouet, et al.

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## To cite this version:

Jean-François Barczi, Amira Beroueg, Gerhard Buck-Sorlin, Valentin Couvreur, Frédéric Danjon, et al. Loïc Pagès, founding scientist in root ecology and modelling. in silico Plants, 2021, 3 (2), 10.1093/insilicoplants/diab035. hal-03517541

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Submitted on 24 May 2022

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Distributed under a Creative Commons Attribution 4.0 International License
Loïc Pagès, founding scientist in root ecology and
modelling

Root system scientists strive to understand how a single root, emerging from a plant's seed, can form a complex, dynamic and plastic network of thousands of individual roots. They investigate how such a network is ideally suited to perform a number of functions required for the harmonious development of the whole plant. Everyone in the community also knows how complicated it can be to study root systems, with tasks ranging from digging plants out of the soil, creating experimental setups that allow the observation of the roots, to quantifying the root network itself or the processes underlying its formation. Within the community, there is one person, Dr Loïc Pagès, who has been working on all these tasks for many years, and who has moved the field forward numerous times. On the occasion of his soon-to-be retirement, we would like to express our appreciation to him via this editorial.

Loïc Pagès started studying the development of root systems almost 40 years ago and has not stopped ever since. Providing an exhaustive summary of Loïc's achievements would be a daunting task (according to Scopus, Loïc has published over 130 papers, with more than 249 collaborators; Fig. 1). Here we would like to highlight some of his key contributions to the field.

Loïc has been working on many facets of root research. Most importantly, Loïc spent a lot of time observing roots. He dug out and quantified thousands of root systems of more than 60 different plant species, sometimes from his own garden (Pagès and Kervella 2018). One root system at a time, this rich experimental work was Loïc's foundation for the discovery and conceptualization of a parsimonious set of developmental rules that he was able to apply to a wide range of plant species (Lecompte et al. 2001; Pagès 2016; Pagès and Kervella 2018). Briefly, these rules highlight the importance of the range—and not the average—of root diameters that can be found within a root system and the allometric relationship between roots of different orders. The unique approach of Loïc was to rely on these rules for designing and implementing computational root models.

Loïc Pagès is one of the founding fathers of root system modelling. When he published his first computational model, SARAH, in 1988 (Pagès and Ariès 1988), there were only a handful of scientists working in this emerging research area: him, D. Lungley (Lungley 1973), A. Fitter (Fitter 1987) and A. Diggle (Diggle 1988). SARAH was a simple root growth model that included all the available knowledge about root system development. This was so new at the time that it is easy to imagine the scepticism of some contemporary agronomists (Loïc's personal communication). But this did not stop him from continuing on this path. Since then, Loïc has published more than 15 different root models (Fig. 2). His modelling work spanned from purely structural models of single species (maize (Pagès et al. 1989), peach tree (Pagès et al. 1992), rubber tree (Thaler and Pagès 1998), Arabidopsis thaliana

(Brun et al. 2010)), to generic structural models capable of representing a broad range of root systems, from grasses to trees (RootTyp (Pagès et al. 2004) or RSCone (Pagès et al. 2020b)). Loïc has also developed functional-structural models that included various functions such as water flow (Doussan et al. 1998), carbon allocation (GRAAL (Drouet and Pagès 2003), MassFlowDyn (Bidel et al. 2000)), nutrient allocation (GRAAL-CN (Drouet and Pagès 2007)) or interaction with the surrounding soil (Gérard et al. 2017; Cast et al. 2019). However, the model that best sums up Loïc's work is probably ArchiSimple (Pagès et al. 2014). As its name suggests, ArchiSimple (SuperSimple in English) requires less than 10 parameters to simulate a complex root system, but is nonetheless able to represent a wide range of complex root architectures (Pagès and Picon-Cochard 2014; Lobet et al. 2017). As such, ArchiSimple is a powerful tool to synthesize complex and diverse architectures with a small set of data points.

Loïc never stopped questioning his modelling approaches: from the use of meta-modelling approaches (Pagès et al. 2020) to the suggestion of new ways of representing the relationship between apical root growth, root diameter and local carbon availability (Pagès et al. 2020). In addition to his modelling work, Loïc has been involved into the thinking and development of sampling techniques in the field (Pellerin et al. 1994; Pagès et al. 2012) and under controlled conditions by designing rhizotrons (Drouet et al. 2005), root image analysis tools (DART (Le Bot et al. 2010), SmartRoot (Lobet et al. 2011)) and root data analysis pipelines (archiDART (Delory et al. 2016), Root System Markup Language (Lobet et al. 2015)). Recently, Loïc has also contributed to the writing of an exhaustive root ecology handbook that provides detailed guidelines and standardized protocols for sampling and classifying roots as well as measuring root traits (Freschet et al. 2021).

Finally, in addition to being a leading research scholar and, for part of his career, the head of his department at INRA Avignon, France, Loïc has been a supervisor, a mentor and an enthusiastic colleague and friend to many of us in the field. His door was open to discuss everything related to root system development and beyond, and his advice was always helpful.

Dear Loïc, as root researchers, we would like to thank you for everything you have brought to the community, for every model you have developed, for every new concept you have formalized, as well as for all the advice and heated debates you have shared with many of us. We thank you and wish you a long and happy retirement, taking care of your gardens, grandchildren and bees. Thank you, Loïc!

SIGNATORIES

Jean-François Barczi, Amap, Cirad, Montpellier, France
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Figure 1. Author citation map based on root system modelling papers from the years 1980–2021 (109 authors in the citation network). The connecting lines indicate the 500 strongest citation links between authors. The size of the nodes stands for the total number of citations. Loïc's major contribution to this research field is highlighted by his central position and the highest number of papers (33), citations (1394) and links with other authors (99). Sources: Scopus, Software: VOSviewer.

<figure><img src="image_4.png" /><figcaption>SARAH, 1988</figcaption></figure>

<figure><img src="image_5.png" /><figcaption>Maize model, 1999</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>RootTyp, 2004</figcaption></figure>

<figure><img src="image_7.png" /><figcaption>ArchiSimple, 2014</figcaption></figure>

Figure 2. Visual output of four models developed by Loïc. We should add here that Loïc strongly prefers showing graphs illustrating and analysing the model outputs rather than the model visual outputs themselves. We hope he forgives us for this.

Amira Beroueg, unité PSH, INRAE-Avignon, France

Gerhard Buck-Sorlin, IRHS, INRAE, l'Institut Agro - Agrocampus Ouest, Université d'Angers, Beaucouzé, France

Valentin Couvreur, Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Belgium

Frédéric Danjon, INRAE, Univ. Bordeaux, BIOGECO, F-33610 Cestas, France

Benjamin M. Delory, Institute of Ecology, Leuphana University of Lüneburg, Lüneburg, Germany

Claude Doussan, INRAE-Avignon Université, UMR EMMAH, Avignon, France

Tom De Swaef, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Merelbeke, Belgium

Xavier Draye, Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Belgium

Jean-Louis Drouet, INRAE, AgroParisTech, Université Paris-Saclay, UMR ECOSYS, Thiverval-Grignon, France

Lionel Dupuy, (1) Department of Conservation of Natural Resources, NEIKER, Derio 48160, Spain (2) IKERBASQUE, Basque Foundation for Science, Bilbao 48009, Spain

Sarah Garre, Flanders Research Institute for Agriculture, Fisheries and Food (ILVO), Merelbeke, Belgium

Frédéric Gérard, Eco&Sols, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France

Adrien Heymans, Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Belgium

Philippe Hinsinger, Eco&Sols, Univ Montpellier, CIRAD, INRAE, Institut Agro, IRD, Montpellier, France

Mathieu Javaux, Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Belgium and Agrosphere Institute (IBG3), Forschungszentrum Jülich, Jülich, Germany

Axelle Koch, Earth and Life Institute, Université catholique de Louvain, Louvain-la-Neuve, Belgium

Magdalena Landl, Agrosphere Institute (IBG3), Forschungszentrum Jülich, Jülich, Germany

François Lecompte, unité PSH, INRAE-Avignon, France

Daniel Leitner, Simulationswerkstatt, Ortmayrstrasse 20, A-4060 Leonding, Austria

Guillaume Lobet, Forschungszentrum Jülich, Agrosphere Institute

Jonathan Lynch, Department of Plant Science, The Pennsylvania State University, University Park, PA, USA

Pierre Martre, LEPSE, Univ Montpellier, INRAE, Institut Agro Montpellier SupAgro, Montpellier, France

Céline Meredieu, INRAE, BIOGECO, Cestas, France
Felicien Meunier, Computational and Applied Vegetation Ecology,
Department of Environment, Ghent University

Alain Mollier, UMR ISPA, INRAE Villenave d'Ornon, France

Bertrand Muller, LEPSE, Univ Montpellier, INRAE, Institut Agro,
Montpellier SupAgro, Montpellier, France

Christophe Nguyen, UMR Ispa, INRAE, Centre de Bordeaux
Nouvelle Aquitaine, Villenave d'Ornon, France

Catherine Picon-Cochard, Université Clermont Auvergne, INRAE,
VetAgro Sup, UREP, Clermont-Ferrand, France

Johannes A. Postma, Plant Sciences, IBG2, Forschungszentrum
Jülich GmbH, Juelich, Germany

Christophe Pradal, CIRAD, UMR AGAP Institut, Montpellier,
France

Frédéric Rees, INRAE, AgroParisTech, Université Paris-Saclay,
UMR ECOSYS, Thiverval-Grignon, France

Céline Richard-Molard, INRAE, AgroParisTech, Université Paris-Saclay, UMR ECOSYS, Thiverval-Grignon, France

Tiina Roosevelt, University of Southampton

Clément Saint Cast, Earth and Life Institute, Université catholique
de Louvain, Louvain-la-Neuve, Belgium

Andrea Schnepf, Forschungszentrum Jülich, Agrosphere Institute

Philippe Thaler, Eco&Sols, Univ Montpellier, CIRAD, INRAE,
Institut Agro, IRD, Montpellier, France

Jan Vanderborght, Forschungszentrum Jülich, Agrosphere Institute

Lianhai Wu, Sustainable Agriculture Sciences, Rothamsted
Research, North Wyke, UK

Xiaoran Zhou, Forschungszentrum Jülich, Bioinformatics Institute

LITERATURE CITED

Bidel L, Pagès L, Riviere L, Pelloux G, Lorendeau J. 2000. MassFlowDyn
I: a carbon transport and partitioning model for root system archi-
tecture. *Annals of Botany* **85**:869–886.

Brun F, Richard-Molard C, Pagès L, Chelle M, Ney B. 2010. To what extent may changes in the root system architecture of *Arabidopsis thaliana* grown under contrasted homogenous nitrogen regimes be explained by changes in carbon supply? A modelling approach. *Journal of Experimental Botany* **61**:2157–2169.

Cast CS, Meredieu C, Défossez P, Pagès L, Danjon F. 2019. Modelling root system development for anchorage of forest trees up to the mature stage, including acclimation to soil constraints: the case of *Pinus pinaster*. *Plant and Soil* **439**:405–430.

Delory BM, Baudson C, Brostaux Y, Lobet G, du Jardin P, Pagès L,
Delaplace P. 2016. archiDART: an R package for the automated
computation of plant root architectural traits. *Plant and Soil*
**398**:351–365.

Diggle AJ. 1988. ROOTMAP—a model in three-dimensional coordinates of the growth and structure of fibrous root systems. *Plant and Soil* **105**:169178.

Doussan C, Pagès L, Vercambre G. 1998. Modelling of the hydrau-
lic architecture of root systems: an integrated approach to water
absorption–model description. *Annals of Botany* **81**:213–223.

Drouet J-L, Pagès L. 2003. GRAAL: a model of GRowth, Architecture and carbon ALocation during the vegetative phase of the whole maize plant. *Ecological Modelling* **165**:147–173.

Drouet J-L, Pagès L. 2007. GRAAL-CN: a model of GRowth, Architecture and ALocation for Carbon and Nitrogen dynamics within whole plants formalised at the organ level. *Ecological Modelling* **206**:231–249.

Drouet J-L, Pagès L, Serra V. 2005. Dynamics of leaf mass per unit leaf area and root mass per unit root volume of young maize plants: implications for growth models. *European Journal of Agronomy* **22**:185–193.

Fitter AH. 1987. An architectural approach to the comparative ecology of plant root systems. *The New Phytologist* **106**:61–77.

Freschet GT, Pagès L, Iversen CM, Comas LH, Rewald B, Roumet C, Klimešová J, Zadworny M, Poorter H, Postma JA, Adams TS, Bagniewska-Zadworna A, Bengough AG, Blancaflor EB, Brunner I, Cornelissen JHC, Garnier E, Gessler A, Hobbie SE, Meier IC, Mommer L, Picon-Cochard C, Rose L, Ryser P, Scherer-Lorenzen M, Soudzilovskaia NA, Stokes A, Sun T, Valverde-Barrantes OJ, Weemstra M, Weigelt A, Wurzburger N, York LM, Batterman SA, Gomes de Moraes M, Janeček Š, Lambers H, Salmon V, Tharayil N, McCormack ML. 2021. A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements. *The New Phytologist* **232**:973–1122.

Gérard F, Blitz-Frayret C, Hinsinger P, Pagès L. 2017. Modelling the interactions between root system architecture, root functions and reactive transport processes in soil. *Plant and Soil* **413**:161–180.

Le Bot J, Serra V, Fabre J, Draye X, Adamowicz S, Pagès L. 2010. DART: a software to analyse root system architecture and development from captured images. *Plant and Soil* **326**:261–273.

Lecompte F, Ozier-Lafontaine H, Pagès L. 2001. The relationships between static and dynamic variables in the description of root growth. Consequences for field interpretation of rooting variability. *Plant and Soil* **236**:19–31.

Lobet G, Koevoets IT, Noll M, Meyer PE, Tocquin P, Pagès L, Pèrilleux C. 2017. Using a structural root system model to evaluate and improve the accuracy of root image analysis pipelines. *Frontiers in Plant Science* **8**:447.

Lobet G, Pagès L, Draye X. 2011. A novel image-analysis toolbox enabling quantitative analysis of root system architecture. *Plant Physiology* **157**:29–39.

Lobet G, Pound MP, Diener J, Pradal C, Draye X, Godin C, Javaux M, Leitner D, Meunier F, Nacry P, Pridmore TP, Schnepf A. 2015. Root system markup language: toward a unified root architecture description language. *Plant Physiology* **167**:617–627.

Lungley DR. 1973. The growth of root systems? A numerical computer simulation model. *Plant and Soil* **38**:145–159.

Pagès L. 2016. Branching patterns of root systems: comparison of monocotyledonous and dicotyledonous species. *Annals of Botany* **118**:1337–1346.

Pagès L, Ariès F. 1988. SARAH: modele de simulation de la croissance,
du developpement et de l'architecture des sytemes racinaires.
*Agronomie* **8**:889–896.

Pagès L, Bécel C, Boukcim H, Moreau D, Nguyen C, Voisin A-S. 2014. Calibration and evaluation of ArchiSimple, a simple model of root system architecture. *Ecological Modelling* **290**:76–84.

Pagès L, Bernert M, Pagès G. 2020a. Modelling time variations of root diameter and elongation rate as related to assimilate supply and demand. *Journal of Experimental Botany* **71**:3524–3534.
Pagès L, Bruchou C, Garré S. 2012. Links between root length density profiles and models of the root system architecture. *Vadose Zone Journal* **11**:vzj2011.0152.

Pagès L, Chadoeuf J, Kervella J. 1992. Stochastic modeling of growth and development of the root-system of young peach-tree seedlings. 1. Estimation and validation of the model. *Agronomie* **12**:447-458.

Pages L, Jordan MO, Picard D. 1989. A simulation model of the three-dimensional architecture of the maize root system. *Plant and Soil* **119**:147-154.

Pagès L, Kervella J. 2018. Seeking stable traits to characterize the root system architecture. Study on 60 species located at two sites in natura. *Annals of Botany* **122**:107-115.

Pagès L, Loïc P, Gilles V, Jean-Louis D, François L, Catherine C, Le Bot J. 2004. Root Typ: a generic model to depict and analyse the root system architecture. *Plant and Soil* **258**:103-119.

Pagès L, Picon-Cochard C. 2014. Modelling the root system architecture of Poaceae. Can we simulate integrated traits from morphological parameters of growth and branching? *The New Phytologist* **204**:149-158.

Pagès L, Pointurier O, Moreau D, Voisin A-S, Colbach N. 2020b. Metamodelling a 3D architectural root-system model to provide a simple model based on key processes and species functional groups. *Plant and Soil* **448**:231-251.

Pellerin S, Sylvain P, Loïc P. 1994. Evaluation of parameters describing the root system architecture of field grown maize plants (*Zea mays* L.). *Plant and Soil* **164**:155-167.

Thaler P, Pagès L. 1998. Modelling the influence of assimilate availability on root growth and architecture. *Plant and Soil* **201**:307-320.