# Epidemiological, evolutionary and economic outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes: a case-study with the management of downy mildew in wine growing areas

Marta Zaffaroni, Loup Rimbaud, Julien Papaïx, Jean-François Rey, Laurent Deliere, Anne-Sophie Miclot, Adeline Ugaglia, Frédéric Fabre

## ► To cite this version:

Marta Zaffaroni, Loup Rimbaud, Julien Papaïx, Jean-François Rey, Laurent Deliere, et al.. Epidemiological, evolutionary and economic outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes: a case-study with the management of downy mildew in wine growing areas. 12. International congress of plant pathology (ICPP), Aug 2023, Lyon, France. . [hal-04195663v2](https://hal.inrae.fr/hal-04195663v2)

HAL Id: hal-04195663

https://hal.inrae.fr/hal-04195663v2

Submitted on 31 Jan 2024

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

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<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
# Epidemiological, evolutionary and economic outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes: a case-study with the management of downy mildew in wine growing areas

Marta Zaffaroni, Loup Rimbaud, Julien Papaïx, Jean-François Rey, Laurent Deliere, Anne-Sophie Miclot, Adeline Ugaglia, Frédéric Fabre

## ► To cite this version:

Marta Zaffaroni, Loup Rimbaud, Julien Papaïx, Jean-François Rey, Laurent Deliere, et al.. Epidemiological, evolutionary and economic outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes: a case-study with the management of downy mildew in wine growing areas. 12. International congress of plant pathology (ICPP), Aug 2023, Lyon, France. . [hal-04195663v2](https://hal.inrae.fr/hal-04195663v2)

HAL Id: hal-04195663

https://hal.inrae.fr/hal-04195663v2

Submitted on 31 Jan 2024

HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.

L'archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.

<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
12TH INTERNATIONAL CONGRESS
OF PLANT PATHOLOGY

20 - 25 August 2023

Lyon, France

Epidemiological, evolutionary and economic outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes: a case-study with the management of downy mildew in wine growing areas.

Marta Zaffaroni, Loup Rimbaud, Julien Papaïx, Jean-François Rey, Laurent Delière, Anne-Sophie Miclot, Adeline Ugaglia and Frédéric Fabre

Downy mildew represents a real threat for grapevines in all vine-growing areas of the world, leading to significant yield losses and massive recourse of fungicides. Over the past years, breeders have been engaged in breeding programs for resistance to grapevine downy mildew, resulting in the creation of several resistant varieties. At present, growers can plant monogenic (with mainly the resistance factors Rpv1, Rpv3 but also Rpv10 and Rpv12) or pyramided cultivars (mainly cumulating Rpv1 and Rpv3). Currently, the resistance factors Rpv1 and Rpv3 start to be deployed in France. These two resistance factors can be deployed in: (i) monogenic cultivars sown in the same field (mixture strategy), (ii) monogenic cultivars sown in different fields (mosaic strategy), (iii) pyramided cultivars (pyramid strategy) and (iv) in hybrid strategies that combine the three previous basic strategies. Here, we used the spatially explicit stochastic model *landsepi* to investigate the epidemiological, evolutionary and economic outcomes associated to these deployment strategies. Our results particularly highlight the risks for resistance durability associated to the coexistence of monogenic and pyramided cultivars in the same landscape. Finally, we discuss how the model *landsepi* has been used to design deployment scenarios and discuss their outcomes with the staff of a cooperative cellar growing nearly 2000 ha of grapevine in South-western France.
12TH INTERNATIONAL CONGRESS
OF PLANT PATHOLOGY

20 - 25 August 2023

Lyon, France

Epidemiological, evolutionary and economic outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes: a case-study with the management of downy mildew in wine growing areas.

Marta Zaffaroni, Loup Rimbaud, Julien Papaïx, Jean-François Rey, Laurent Delière, Anne-Sophie Miclot, Adeline Ugaglia and Frédéric Fabre

Downy mildew represents a real threat for grapevines in all vine-growing areas of the world, leading to significant yield losses and massive recourse of fungicides. Over the past years, breeders have been engaged in breeding programs for resistance to grapevine downy mildew, resulting in the creation of several resistant varieties. At present, growers can plant monogenic (with mainly the resistance factors Rpv1, Rpv3 but also Rpv10 and Rpv12) or pyramided cultivars (mainly cumulating Rpv1 and Rpv3). Currently, the resistance factors Rpv1 and Rpv3 start to be deployed in France. These two resistance factors can be deployed in: (i) monogenic cultivars sown in the same field (mixture strategy), (ii) monogenic cultivars sown in different fields (mosaic strategy), (iii) pyramided cultivars (pyramid strategy) and (iv) in hybrid strategies that combine the three previous basic strategies. Here, we used the spatially explicit stochastic model *landsepi* to investigate the epidemiological, evolutionary and economic outcomes associated to these deployment strategies. Our results particularly highlight the risks for resistance durability associated to the coexistence of monogenic and pyramided cultivars in the same landscape. Finally, we discuss how the model *landsepi* has been used to design deployment scenarios and discuss their outcomes with the staff of a cooperative cellar growing nearly 2000 ha of grapevine in South-western France.
<figure><img src="image_2.png" /></figure>

<figure><img src="image_3.png" /></figure>

# Epidemiological and evolutionary outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes

Marta Zaffaroni¹,³, Loup Rimbaud², Julien Papaix³, Jean-François Rey³, Laurent Delière¹, anne-Sophie Miclot¹, Adeline Ugaglia¹ & Frédéric Fabre¹

¹ INRAE - SAVE, 33882 Villenave d'Ornon, France, ² INRAE - Pathologie Végétale, 84140, Montfavet, France ³ INRAE - BioSP, 84914, Avignon, France

## 1 Introduction & objectives

* The deployment of resistant cultivars in agricultural landscapes is an effective way to protect crops from plant pathogens, but pathogens may quickly adapt to the deployed resistance [1]. The way resistant cultivars are deployed impact their efficiency in maintaining an effective disease protection over short and long terms.

* Downy mildew is a real threat for grapevines in all vine-growing areas of the world. Breeders have been engaged in breeding programs for resistance to grapevine downy mildew, resulting in the creation of several resistant varieties. At present, growers in France can start to plant monogenic (with mainly the resistance factors Rpv1, Rpv3) or pyramided cultivars (mainly cumulating Rpv1 and Rpv3).

* What is the best strategy to deploy these monogenic and pyramided cultivars in agricultural landscapes? Growers can deploy (i) only monogenic cultivars sown in the same field (mixture strategy), (ii) only monogenic cultivars sown in different fields (mosaic strategy), (iii) only pyramided cultivars (pyramid strategy) or (iv) choose hybrid strategy that combine the three previous basic strategies. Here, we used the spatially explicit stochastic model (landsepi [2,3]) to investigate the epidemiological and evolutionary outcomes associated to these strategies.

## 2 landsepi, a demo-genetic spatially-explicit temporal stochastic model

### Pathogen epidemic and evolutionary dynamics

Resistance efficiency

<figure><img src="image_4.png" /></figure>

Qualitative

<figure><img src="image_5.png" /></figure>

<figure><img src="image_6.png" /></figure>

The R package landsepi provides a modelling framework to compare plant resistance deployment strategies and understand the impact of epidemiological, evolutionary and genetic factors for a wide range of pathosystems.

### Gene-for-gene interaction

<figure><img src="image_7.png" /><figcaption>Cultivars</figcaption></figure>

* Possible fitness cost

### Epidemics in a diversified landscape of 400 fields

<figure><img src="image_8.png" /></figure>

<figure><img src="image_9.png" /></figure>

## 3 Hybrid strategies reduce the advantage of resistance genes pyramiding...

<figure><img src="image_10.png" /></figure>

## 4 ... even for low proportion of monogenic cultivars

<figure><img src="image_11.png" /></figure>

Factors studied: ① Cropping ratio: proportion of fields with R cultivars; ② FC: fitness cost

③ Mutation rate (2 levels); ④ Strategies (5 levels); ⑤ Proportion $\phi_2$: relative proportion of fields with R12 cultivars

Outcomes: ① Evolutionary outcomes: $pr(E_{Sp}=1)$, probability of superpathogen SP pathogen establishment

② Epidemiological outcomes: AUDPC, relative AUDPC during 30 years at landscape scale

## 5 Conclusions

* Knowledge of the mutation probability determines if the pyramiding strategy provides a substantial benefit over mixture and mosaic strategies.

* Going further a study of Lof and colleagues (2017) [4], we showed that, at low mutation probability, deploying hybrid strategies drastically decreases the advantage of resistance genes pyramiding, even for low proportion of monogenic cultivars.

* Socio-economic studies are needed to assess how regulatory policies could be mobilized to manage resistance cultivars deployment in agricultural landscapes in order to preserve the advantage of resistance genes pyramiding.
<figure><img src="image_2.png" /></figure>

RÉPUBLIQUE
FRANÇAISE

Liberté
Égalité
Fraternité

INRAE

<figure><img src="image_3.png" /></figure>

<figure><img src="image_4.png" /></figure>

# Epidemiological and evolutionary outcomes associated to the coexistence of monogenic and pyramided resistant cultivars in agricultural landscapes

Marta Zaffaroni¹,³, Loup Rimbaud², Julien Papaix³, Jean-François Rey³, Laurent Delière¹, anne-Sophie Miclot¹, Adeline Ugaglia¹ & Frédéric Fabre¹

¹ INRAE - SAVE, 33882 Villenave d'Ornon, France, ² INRAE - Pathologie Végétale, 84140, Montfavet, France ³ INRAE - BioSP, 84914, Avignon, France

## 1 Introduction & objectives

* The deployment of resistant cultivars in agricultural landscapes is an effective way to protect crops from plant pathogens, but pathogens may quickly adapt to the deployed resistance [1]. The way resistant cultivars are deployed impact their efficiency in maintaining an effective disease protection over short and long terms.

* Downy mildew is a real threat for grapevines in all vine-growing areas of the world. Breeders have been engaged in breeding programs for resistance to grapevine downy mildew, resulting in the creation of several resistant varieties. At present, growers in France can start to plant monogenic (with mainly the resistance factors Rpv1, Rpv3) or pyramided cultivars (mainly cumulating Rpv1 and Rpv3).

* What is the best strategy to deploy these monogenic and pyramided cultivars in agricultural landscapes? Growers can deploy (i) only monogenic cultivars sown in the same field (mixture strategy), (ii) only monogenic cultivars sown in different fields (mosaic strategy), (iii) only pyramided cultivars (pyramid strategy) or (iv) choose hybrid strategy that combine the three previous basic strategies. Here, we used the spatially explicit stochastic model (landsepi [2,3]) to investigate the epidemiological and evolutionary outcomes associated to these strategies.

## 2 landsepi, a demo-genetic spatially-explicit temporal stochastic model

### Pathogen epidemic and evolutionary dynamics

<figure><img src="image_5.png" /></figure>

<figure><img src="image_6.png" /></figure>

The R package landsepi provides a modelling framework to compare plant resistance deployment strategies and understand the impact of epidemiological, evolutionary and genetic factors for a wide range of pathosystems.

### Gene-for-gene interaction

#### Cultivars

<figure><img src="image_7.png" /></figure>

### Epidemics in a diversified landscape of 400 fields

<figure><img src="image_8.png" /></figure>

## 3 Hybrid strategies reduce the advantage of resistance genes pyramiding...

<figure><img src="image_9.png" /></figure>

## 4 ... even for low proportion of monogenic cultivars

<figure><img src="image_10.png" /></figure>

Factors studied: ① Cropping ratio: proportion of fields with R cultivars; ② FC: fitness cost

③ Mutation rate (2 levels); ④ Strategies (5 levels); ⑤ Proportion $\phi_2$: relative proportion of fields with R12 cultivars

Outcomes: ① Evolutionary outcomes: $pr(E_{SP}=1)$, probability of superpathogen SP pathogen establishment

② Epidemiological outcomes: AUDPC, relative AUDPC during 30 years at landscape scale

## 5 Conclusions

* Knowledge of the mutation probability determines if the pyramiding strategy provides a substantial benefit over mixture and mosaic strategies.

* Going further a study of Lof and colleagues (2017) [4], we showed that, at low mutation probability, deploying hybrid strategies drastically decreases the advantage of resistance genes pyramiding, even for low proportion of monogenic cultivars.

* Socio-economic studies are needed to assess how regulatory policies could be mobilized to manage resistance cultivars deployment in agricultural landscapes in order to preserve the advantage of resistance genes pyramiding.

FINANCIAL SUPPORT

This work benefited from OFB Ecophyto "Leviers territoriaux" (Project Médée, 2020-2023) and from ANR (project COMBINE, 2023-2026).

LINKS

Web app: https://khra.bcg.dna.fr/amb directing/
R package: https://cran.r-project.org/web/sites/landsapi/index.html

REFERENCES

[1] Rimbaud L, et al. (2021) Annu. Rev. Phytopathol. 59:125-152. [2] Rimbaud L, et al (2018)

PloS Comput. Biol. 14:e1006067.

[3] Zaffaroni M., et al. (2022), Bioarxiv, 10.1101/2022.02.28.006001.