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The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions

Benoît Moury, Jean-Marc Audergon, Sylvie Baudracco-Arnas, Safa Ben Krima, François Bertrand, Nathalie Boissot, Mireille Buisson, Valérie Caffier, Mélissa Cantet, Sylvia Chanéac, Carole Constant, François Delmotte, Catherine Dogimont, Juliette Doumayrou, Frédéric Fabre, Sylvain Fournet, Valérie Grimault, Thierry Jaunet, Isabelle Justafré, Véronique Lefebvre, Denis Losdat, Thierry Marcel, Josselin Montarry, Cindy E. Morris, Mariem Omrani, Manon Paineau, Sophie Perrot, Marie-Laure Pilet-Nayel, Youna Ruellan
doi: https://doi.org/10.1101/2021.03.03.433745
Benoît Moury
1Pathologie Végétale, INRAE, 84140 Montfavet, France
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  • For correspondence: benoit.moury@inrae.fr
Jean-Marc Audergon
2GAFL, INRAE, 84140, Montfavet, France
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Sylvie Baudracco-Arnas
3Laboratoires ASL, 755 chemin de Meinajaries, 84140 Montfavet, France
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Safa Ben Krima
4University of Paris-Saclay, INRAE, AgroParisTech, UMR BIOGER, 78850 Thiverval-Grignon, France
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François Bertrand
5Bayer Seeds SAS, Chemin de Roquemartine Mas Lamy, 13670, Saint-Andiol, France
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Nathalie Boissot
2GAFL, INRAE, 84140, Montfavet, France
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Mireille Buisson
6GAUTIER SEMENCES, Route d’Avignon, 13630 Eyragues, France
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Valérie Caffier
7Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, 49000 Angers, France
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Mélissa Cantet
2GAFL, INRAE, 84140, Montfavet, France
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Sylvia Chanéac
8TAKII FRANCE SAS, 660 Chemin de la Crau, 13630 EYRAGUES, France
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Carole Constant
9Sakata Vegetables Europe, Domaine de Sablas, rue du moulin, 30620 Uchaud, France
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François Delmotte
10SAVE, INRAE, Bordeaux Sciences Agro, ISVV, 33140 Villenave d’Ornon, France
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Catherine Dogimont
2GAFL, INRAE, 84140, Montfavet, France
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Juliette Doumayrou
1Pathologie Végétale, INRAE, 84140 Montfavet, France
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Frédéric Fabre
10SAVE, INRAE, Bordeaux Sciences Agro, ISVV, 33140 Villenave d’Ornon, France
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Sylvain Fournet
11IGEPP, INRAE, Institut Agro, Univ. Rennes, 35653 Le Rheu, France
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Valérie Grimault
12GEVES, 25 rue Georges Morel, CS 900024, 49071 Beaucouzé, France
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Thierry Jaunet
13HM.Clause, 1 chemin du Moulin des Ronzières, 49800 La Bohalle, France
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Isabelle Justafré
14Vilmorin, Mas Pazac, 30210 Ledenon, France
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Véronique Lefebvre
2GAFL, INRAE, 84140, Montfavet, France
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Denis Losdat
15RIJK ZWAAN France, La Vernède, 30390 Aramon, France
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Thierry Marcel
4University of Paris-Saclay, INRAE, AgroParisTech, UMR BIOGER, 78850 Thiverval-Grignon, France
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Josselin Montarry
11IGEPP, INRAE, Institut Agro, Univ. Rennes, 35653 Le Rheu, France
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Cindy E. Morris
1Pathologie Végétale, INRAE, 84140 Montfavet, France
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Mariem Omrani
1Pathologie Végétale, INRAE, 84140 Montfavet, France
2GAFL, INRAE, 84140, Montfavet, France
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Manon Paineau
10SAVE, INRAE, Bordeaux Sciences Agro, ISVV, 33140 Villenave d’Ornon, France
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Sophie Perrot
12GEVES, 25 rue Georges Morel, CS 900024, 49071 Beaucouzé, France
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Marie-Laure Pilet-Nayel
11IGEPP, INRAE, Institut Agro, Univ. Rennes, 35653 Le Rheu, France
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Youna Ruellan
2GAFL, INRAE, 84140, Montfavet, France
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Abstract

Understanding the relationships between host range and pathogenicity for parasites, and between the efficiency and scope of immunity for hosts are essential to implement efficient disease control strategies. In the case of plant parasites, most studies have focused on describing qualitative interactions and a variety of genetic and evolutionary models has been proposed in this context. Although plant quantitative resistance benefits from advantages in terms of durability, we presently lack models that account for quantitative interactions between plants and their parasites and the evolution of these interactions. Nestedness and modularity are important features to unravel the overall structure of host-parasite interaction matrices. Here, we analysed these two features on 32 matrices of quantitative pathogenicity trait data gathered from 15 plant-parasite pathosystems consisting of either annual or perennial plants along with fungi or oomycetes, bacteria, nematodes, insects and viruses. The performance of several nestedness and modularity algorithms was evaluated through a simulation approach, which helped interpretation of the results. We observed significant modularity in only six of the 32 matrices, with two or three modules detected. For three of these matrices, modules could be related to resistance quantitative trait loci present in the host. In contrast, we found high and significant nestedness in 30 of the 32 matrices. Nestedness was linked to other properties of plant-parasite interactions. First, pathogenicity trait values were explained in majority by a parasite strain effect and a plant accession effect, with no parasite-plant interaction term. Second, correlations between the efficiency and scope of the resistance of plant genotypes, and between the host range breadth and pathogenicity level of parasite strains were overall positive. This latter result questions the efficiency of strategies based on the deployment of several genetically-differentiated cultivars of a given crop species in the case of quantitative plant immunity.

Competing Interest Statement

The authors of this manuscript declare that they have no financial conflict of interest with the content of this article. Benoit Moury in one of the Peer Community In Evolutionary Biology recommenders.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions
Benoît Moury, Jean-Marc Audergon, Sylvie Baudracco-Arnas, Safa Ben Krima, François Bertrand, Nathalie Boissot, Mireille Buisson, Valérie Caffier, Mélissa Cantet, Sylvia Chanéac, Carole Constant, François Delmotte, Catherine Dogimont, Juliette Doumayrou, Frédéric Fabre, Sylvain Fournet, Valérie Grimault, Thierry Jaunet, Isabelle Justafré, Véronique Lefebvre, Denis Losdat, Thierry Marcel, Josselin Montarry, Cindy E. Morris, Mariem Omrani, Manon Paineau, Sophie Perrot, Marie-Laure Pilet-Nayel, Youna Ruellan
bioRxiv 2021.03.03.433745; doi: https://doi.org/10.1101/2021.03.03.433745
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The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions
Benoît Moury, Jean-Marc Audergon, Sylvie Baudracco-Arnas, Safa Ben Krima, François Bertrand, Nathalie Boissot, Mireille Buisson, Valérie Caffier, Mélissa Cantet, Sylvia Chanéac, Carole Constant, François Delmotte, Catherine Dogimont, Juliette Doumayrou, Frédéric Fabre, Sylvain Fournet, Valérie Grimault, Thierry Jaunet, Isabelle Justafré, Véronique Lefebvre, Denis Losdat, Thierry Marcel, Josselin Montarry, Cindy E. Morris, Mariem Omrani, Manon Paineau, Sophie Perrot, Marie-Laure Pilet-Nayel, Youna Ruellan
bioRxiv 2021.03.03.433745; doi: https://doi.org/10.1101/2021.03.03.433745

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