Section: Evolutionary Biology
Topic: Evolution, Biology of interactions, Plant biology

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

10.24072/pcjournal.51 - Peer Community Journal, Volume 1 (2021), article no. e44.

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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 or minor 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.
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DOI: 10.24072/pcjournal.51
Type: Research article

Moury, Benoît 1; Audergon, Jean-Marc 2; Baudracco-Arnas, Sylvie 3; Ben Krima, Safa 4; Bertrand, François 5; Boissot, Nathalie 2; Buisson, Mireille 6; Caffier, Valérie 7; Cantet, Mélissa 2; Chanéac, Sylvia 8; Constant, Carole 9; Delmotte, François 10; Dogimont, Catherine 2; Doumayrou, Juliette 1; Fabre, Frédéric 10; Fournet, Sylvain 11; Grimault, Valérie 12; Jaunet, Thierry 13; Justafré, Isabelle 14; Lefebvre, Véronique 2; Losdat, Denis 15; Marcel, Thierry C. 4; Montarry, Josselin 11; Morris, Cindy E. 1; Omrani, Mariem 2, 1; Paineau, Manon 10; Perrot, Sophie 12; Pilet-Nayel, Marie-Laure 11; Ruellan, Youna 2

1 Pathologie Végétale, INRAE, 84140 Montfavet, France
2 GAFL, INRAE, 84140, Montfavet, France
3 Laboratoires ASL, 755 chemin de Meinajaries, 84140 Montfavet, France
4 University of Paris-Saclay, INRAE, AgroParisTech, UMR BIOGER, 78850 Thiverval-Grignon, France
5 Bayer Seeds SAS, Chemin de Roquemartine Mas Lamy, 13670, Saint-Andiol, France
6 GAUTIER SEMENCES, Route d’Avignon, 13630 Eyragues, France
7 Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, 49000 Angers, France
8 TAKII FRANCE SAS, 660 Chemin de la Crau, 13630 EYRAGUES, France
9 Sakata Vegetables Europe, Domaine de Sablas, rue du moulin, 30620 Uchaud, France
10 SAVE, INRAE, Bordeaux Sciences Agro, ISVV, 33140 Villenave d’Ornon, France
11 IGEPP, INRAE, Institut Agro, Univ. Rennes, 35653 Le Rheu, France
12 GEVES, 25 rue Georges Morel, CS 900024, 49071 Beaucouzé, France
13 HM.Clause, 1 chemin du Moulin des Ronzières, 49800 La Bohalle, France
14 Vilmorin & Cie, Mas Pazac, 30210 Ledenon, France
15 RIJK ZWAAN France, La Vernède, 30390 Aramon, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Moury, Beno{\^\i}t and Audergon, Jean-Marc and Baudracco-Arnas, Sylvie and Ben Krima, Safa and Bertrand, Fran\c{c}ois and Boissot, Nathalie and Buisson, Mireille and Caffier, Val\'erie and Cantet, M\'elissa and Chan\'eac, Sylvia and Constant, Carole and Delmotte, Fran\c{c}ois and Dogimont, Catherine and Doumayrou, Juliette and Fabre, Fr\'ed\'eric and Fournet, Sylvain and Grimault, Val\'erie and Jaunet, Thierry and Justafr\'e, Isabelle and Lefebvre, V\'eronique and Losdat, Denis and Marcel, Thierry C. and Montarry, Josselin and Morris, Cindy E. and Omrani, Mariem and Paineau, Manon and Perrot, Sophie and Pilet-Nayel, Marie-Laure and Ruellan, Youna},
     title = {The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions},
     journal = {Peer Community Journal},
     eid = {e44},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.51},
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AU  - Boissot, Nathalie
AU  - Buisson, Mireille
AU  - Caffier, Valérie
AU  - Cantet, Mélissa
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AU  - Losdat, Denis
AU  - Marcel, Thierry C.
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AU  - Morris, Cindy E.
AU  - Omrani, Mariem
AU  - Paineau, Manon
AU  - Perrot, Sophie
AU  - Pilet-Nayel, Marie-Laure
AU  - Ruellan, Youna
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%A Audergon, Jean-Marc
%A Baudracco-Arnas, Sylvie
%A Ben Krima, Safa
%A Bertrand, François
%A Boissot, Nathalie
%A Buisson, Mireille
%A Caffier, Valérie
%A Cantet, Mélissa
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%A Constant, Carole
%A Delmotte, François
%A Dogimont, Catherine
%A Doumayrou, Juliette
%A Fabre, Frédéric
%A Fournet, Sylvain
%A Grimault, Valérie
%A Jaunet, Thierry
%A Justafré, Isabelle
%A Lefebvre, Véronique
%A Losdat, Denis
%A Marcel, Thierry C.
%A Montarry, Josselin
%A Morris, Cindy E.
%A Omrani, Mariem
%A Paineau, Manon
%A Perrot, Sophie
%A Pilet-Nayel, Marie-Laure
%A Ruellan, Youna
%T The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions
%J Peer Community Journal
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Moury, Benoît; Audergon, Jean-Marc; Baudracco-Arnas, Sylvie; Ben Krima, Safa; Bertrand, François; Boissot, Nathalie; Buisson, Mireille; Caffier, Valérie; Cantet, Mélissa; Chanéac, Sylvia; Constant, Carole; Delmotte, François; Dogimont, Catherine; Doumayrou, Juliette; Fabre, Frédéric; Fournet, Sylvain; Grimault, Valérie; Jaunet, Thierry; Justafré, Isabelle; Lefebvre, Véronique; Losdat, Denis; Marcel, Thierry C.; Montarry, Josselin; Morris, Cindy E.; Omrani, Mariem; Paineau, Manon; Perrot, Sophie; Pilet-Nayel, Marie-Laure; Ruellan, Youna. The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions. Peer Community Journal, Volume 1 (2021), article  no. e44. doi : 10.24072/pcjournal.51.

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100132

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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