Calcagno, Vincent

Castagnone-Sereno, Philippe

Djian-Caporalino, Caroline

Mailleret, Ludovic

Nilusmas, Samuel

Touzeau, Suzanne

International audienceRoot-knot nematodes (RKN) are soil-borne, little mobile, polyphagous pests which threaten important sheltered crops such as vegetables or small fruits. They attack plant roots to feed and reproduce and have a major impact on crop yield. Most modern eco-friendly plant protection strategies against RKN are based on the use of resistant crops. The emergence of virulent RKN variants, which are adapted to crop resistance, challenges the durability of such methods. Because virulent RKN exhibit reduced fitness on non-resistant crops, combining both resistant and non-resistant plants can help increase the efficacy and sustainability of resistance-based nematode control. Indeed, if resistant crops select virulent nematodes, non-resistant crops counter-select these less fit nematodes. Furthermore, since nematodes have poor intrinsic dispersal ability, the association between resistant and non-resistant  plants should rely on crop rotation over cropping seasons, rather than on spatial arrangements. We proposed a semi-discrete model describing the population dynamics of plant roots infection by  nematodes within and over cropping seasons. This model, rooted in epidemiological concepts, was fitted to literature data on within-season dynamics of non-resistant plants and avirulent nematodes, and further extended to account for resistant plants and virulent parasites. The model was used to compute optimal crop rotation strategies with respect to a proxy of crop yield over several cropping seasons,  for different epidemiological scenarios. In many instances, crop rotation remarkably enhanced crop yield. Robustness of the results to parameter  uncertainty was also assessed

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A demo-genetic model of root-knot nematod dynamics with applications to the deployment of plant resistance

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HAL Id: hal-02393318https://hal.inria.fr/hal-02393318Submitted on 6 Dec 2019HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoirespublics ou privés.A demo-genetic model of root-knot nematod dynamicswith applications to the deployment of plant resistanceLudovic Mailleret, Samuel Nilusmas, Suzanne Touzeau, Vincent Calcagno,Caroline Djian-Caporalino, Philippe Castagnone-SerenoTo cite this version:Ludovic Mailleret, Samuel Nilusmas, Suzanne Touzeau, Vincent Calcagno, Caroline Djian-Caporalino,et al.. A demo-genetic model of root-knot nematod dynamics with applications to the deploymentof plant resistance. Journée MODECO - Modélisation des Dynamiques Ecologiques, Jul 2019, Nice,France. ￿hal-02393318￿A demo-genetic model of root-knot nematode dynamicswith applications to the deployment of plant resistanceLudovic Mailleretwith S. Nilusmas, S. Touzeau, V. Calcagno,C. Caporalino, P. CastagnoneM2P2 & IPN, UMR ISA, INRA, CNRS, Université Côte d’AzurBiocore, Inria Sophia Antipolis MéditerranéeIntroductionNematodes• very small slender worms (0.1-2.5 mm)• over 40,000 species, present in virtually anyecosystem• free living and parasites of animals and plantsPlant parasitic nematodes• ∼ 4, 000 species, causing billions of dollars of croplosses each year (temperate & tropical agrosystems)• root knot nematodes (RKN) rank first in terms ofdamage at the world scaleRoot knot nematodes• polyphagous (> 5, 000 host plants), distributedworlwide, but sedentary• cause galls on roots, which alter plants developmenttest- L. Mailleret - RKN dynamics - 1/16IntroductionNematodes• very small slender worms (0.1-2.5 mm)• over 40,000 species, present in virtually anyecosystem• free living and parasites of animals and plantsPlant parasitic nematodes• ∼ 4, 000 species, causing billions of dollars of croplosses each year (temperate & tropical agrosystems)• root knot nematodes (RKN) rank first in terms ofdamage at the world scaleRoot knot nematodes• polyphagous (> 5, 000 host plants), distributedworlwide, but sedentary• cause galls on roots, which alter plants developmenttest- L. Mailleret - RKN dynamics - 1/16IntroductionNematodes• very small slender worms (0.1-2.5 mm)• over 40,000 species, present in virtually anyecosystem• free living and parasites of animals and plantsPlant parasitic nematodes• ∼ 4, 000 species, causing billions of dollars of croplosses each year (temperate & tropical agrosystems)• root knot nematodes (RKN) rank first in terms ofdamage at the world scaleRoot knot nematodes• polyphagous (> 5, 000 host plants), distributedworlwide, but sedentary• cause galls on roots, which alter plants developmenttest- L. Mailleret - RKN dynamics - 1/16RKN control methodsLong relied on hardcore chemical use• soil fumigation• restricted or bannedBiological control offers limited optionsResistant plant based control• powerful eco-friendly method• few R-genes• R can be broken down by virulent strains, whichlimits the durability of the methodAim of this work• understand if and how it is possible to optimizethe use of resistant cultivars to control RKN inseasonal agrosystems (market gardening)test- L. Mailleret - RKN dynamics - 2/16RKN control methodsLong relied on hardcore chemical use• soil fumigation• restricted or bannedBiological control offers limited optionsResistant plant based control• powerful eco-friendly method• few R-genes• R can be broken down by virulent strains, whichlimits the durability of the methodAim of this work• understand if and how it is possible to optimizethe use of resistant cultivars to control RKN inseasonal agrosystems (market gardening)test- L. Mailleret - RKN dynamics - 2/16RKN control methodsLong relied on hardcore chemical use• soil fumigation• restricted or bannedBiological control offers limited optionsResistant plant based control• powerful eco-friendly method• few R-genes• R can be broken down by virulent strains, whichlimits the durability of the methodAim of this work• understand if and how it is possible to optimizethe use of resistant cultivars to control RKN inseasonal agrosystems (market gardening)test- L. Mailleret - RKN dynamics - 2/16RKN Life CycleIn the soil, near a plant root• free living infective juveniles• contact with the root and penetrate it• giant cells formation• maturate and produce eggs (clonal)• released into the soil and hatchAt the plant root system scale• parasites with a free-living stage• causing an epidemic within apopulation of rootsinfec�ve juvenileRootVascular cylindertest- L. Mailleret - RKN dynamics - 3/16RKN Life CycleIn the soil, near a plant root• free living infective juveniles• contact with the root and penetrate it• giant cells formation• maturate and produce eggs (clonal)• released into the soil and hatchAt the plant root system scale• parasites with a free-living stage• causing an epidemic within apopulation of rootsinfec�ve juvenileRootmigra�onVascular cylindertest- L. Mailleret - RKN dynamics - 3/16RKN Life CycleIn the soil, near a plant root• free living infective juveniles• contact with the root and penetrate it• giant cells formation• maturate and produce eggs (clonal)• released into the soil and hatchAt the plant root system scale• parasites with a free-living stage• causing an epidemic within apopulation of rootsinfec�ve juvenile•• Giant cellsRootmigra�onVascular cylindertest- L. Mailleret - RKN dynamics - 3/16RKN Life CycleIn the soil, near a plant root• free living infective juveniles• contact with the root and penetrate it• giant cells formation• maturate and produce eggs (clonal)• released into the soil and hatchAt the plant root system scale• parasites with a free-living stage• causing an epidemic within apopulation of roots•infec�ve juvenile••egg massGiant cellsRootmigra�onVascular cylinderadulttest- L. Mailleret - RKN dynamics - 3/16RKN Life CycleIn the soil, near a plant root• free living infective juveniles• contact with the root and penetrate it• giant cells formation• maturate and produce eggs (clonal)• released into the soil and hatchAt the plant root system scale• parasites with a free-living stage• causing an epidemic within apopulation of roots•infec�ve juvenile••egg massGiant cellsRootmigra�onVascular cylindereggshatchadulttest- L. Mailleret - RKN dynamics - 3/16RKN Life CycleIn the soil, near a plant root• free living infective juveniles• contact with the root and penetrate it• giant cells formation• maturate and produce eggs (clonal)• released into the soil and hatchAt the plant root system scale• parasites with a free-living stage• causing an epidemic within apopulation of roots•infec�ve juvenile••egg massGiant cellsRootmigra�onVascular cylindereggshatchadulttest- L. Mailleret - RKN dynamics - 3/16An epidemic among a growing populationsimulationperformedwithopensimrootAlong the course of a season• plant root system grows• recruits new infective nematodesNematode infection represses plant rootsdevelopmentAn unusual epidemic• parasites with a free-living stage• developing on a growing population• whose growth is negatively affected by infection• in a seasonal contexttest- L. Mailleret - RKN dynamics - 4/16An epidemic among a growing populationsimulationperformedwithopensimrootAlong the course of a season• plant root system grows• recruits new infective nematodesNematode infection represses plant rootsdevelopmentAn unusual epidemic• parasites with a free-living stage• developing on a growing population• whose growth is negatively affected by infection• in a seasonal contexttest- L. Mailleret - RKN dynamics - 4/16An epidemic among a growing populationsimulationperformedwithopensimrootAlong the course of a season• plant root system grows• recruits new infective nematodesNematode infection represses plant rootsdevelopmentAn unusual epidemic• parasites with a free-living stage• developing on a growing population• whose growth is negatively affected by infection• in a seasonal contexttest- L. Mailleret - RKN dynamics - 4/16Compartmental modelṖ = −βPH − ηP + rIḢ = µf (H,E , I ) − εβPHĖ = εβPH − λEİ = λE − αI• P free living nematodes• H healthy root sites• E maturating nematodes• I egg laying nematodestest- L. Mailleret - RKN dynamics - 5/16Model fitting05101520250.03 0.16 0.8 4 20Initial nematode density  Final nematode density in roots(a)00.51.01.50.03 0.16 0.8 4 2042 days (prediction)135 days (training set) 135 days (training set)42 days (prediction)(b)Relative root biomassInitial nematode density  data:Ehwaetietal.1998,2000Parameterization• most parameter values were foundin literature• some had to be estimated fromexperimental data: β, f (.)Scenarios derivation• ± 30% parameters• low, medium (default), high,extreme scenariostest- L. Mailleret - RKN dynamics - 6/16Model fitting05101520250.03 0.16 0.8 4 20Initial nematode density  Final nematode density in roots(a)00.51.01.50.03 0.16 0.8 4 2042 days (prediction)135 days (training set) 135 days (training set)42 days (prediction)(b)Relative root biomassInitial nematode density  data:Ehwaetietal.1998,2000Parameterization• most parameter values were foundin literature• some had to be estimated fromexperimental data: β, f (.)Scenarios derivation• ± 30% parameters• low, medium (default), high,extreme scenariostest- L. Mailleret - RKN dynamics - 6/16Plant resistance, nematode virulence• plants are either R or S• nematode pop. structured in avirulent and virulent phenotypes• avirulents do not develop on R plants• both avirulents and virulents develop on S plants• a fraction δ of avirulent offspring turns into virulenttest- L. Mailleret - RKN dynamics - 7/16R Svir avirPlant resistance, nematode virulence• plants are either R or S• nematode pop. structured in avirulent and virulent phenotypes• avirulents do not develop on R plants• both avirulents and virulents develop on S plants• a fraction δ of avirulent offspring turns into virulenttest- L. Mailleret - RKN dynamics - 7/16R Svir avirPlant resistance, nematode virulence• plants are either R or S• nematode pop. structured in avirulent and virulent phenotypes• avirulents do not develop on R plants• both avirulents and virulents develop on S plants• a fraction δ of avirulent offspring turns into virulenttest- L. Mailleret - RKN dynamics - 7/16R Svir avirPlant resistance, nematode virulenceFitness costs of virulence• infectiveness: βv = (1− wβ)βa• reproduction: rv = (1− wr )ratest- L. Mailleret - RKN dynamics - 7/16R Svir avirInfec�veness Reproduc�onCastagnoneetal.2007,Djianetal.2011Seasonal context, crop rotations, optimizationR S�me...season 1 season 2 season 3Seasonal agrosystems• crops planted and harvestedsequentially over time• cultivar rotations to enhance cropyield (vs. pure S and pure R)Yield proxy• Cumulated Healthy Root DensityCHRD =1n∑seasons∫ T0H(τ)dτtest- L. Mailleret - RKN dynamics - 8/16Seasonal context, crop rotations, optimizationR S�me...season 1 season 2 season 3Seasonal agrosystems• crops planted and harvestedsequentially over time• cultivar rotations to enhance cropyield (vs. pure S and pure R)Yield proxy• Cumulated Healthy Root DensityCHRD =1n∑seasons∫ T0H(τ)dτtest- L. Mailleret - RKN dynamics - 8/16Seasonal context, crop rotations, optimizationR S�me...season 1 season 2 season 3Seasonal agrosystems• crops planted and harvestedsequentially over time• cultivar rotations to enhance cropyield (vs. pure S and pure R)Yield proxy• Cumulated Healthy Root DensityCHRD =1n∑seasons∫ T0H(τ)dτtest- L. Mailleret - RKN dynamics - 8/16Optimal cultivar rotationdefault scenario, 10 seasons           Number of seasons with resistant plantsNumber of seasons with suscep�ble plants1 2 3 4 5 6 7 8 9 123456789  2500225017502000100% R100% S• computation of all periodic croprotations over given time horizon• best rotation > pure R > pure Stest- L. Mailleret - RKN dynamics - 9/16Optimal cultivar rotationdefault scenariotΔ1Δ2Temporal horizon0 10 15 20 253750250012500op�mal unconstrainedop�mal periodic rota�on100 % S100 % Rrela�ve gain = 5 30• R efficacy quickly drops withtemporal horizon• optimal periodic rotation nearlyas efficient as the best strategy• optimal R plants ratio much lowerthan agricultural practice (pure R)test- L. Mailleret - RKN dynamics - 10/16Optimal cultivar rotationdefault scenariotΔ1Δ2Temporal horizon0 10 15 20 253750250012500op�mal unconstrainedop�mal periodic rota�on100 % S100 % Rrela�ve gain = 5 30020406080100Ra�o of resistant plantsTemporal horizon0 10 15 20 255 30• R efficacy quickly drops withtemporal horizon• optimal periodic rotation nearlyas efficient as the best strategy• optimal R plants ratio much lowerthan agricultural practice (pure R)test- L. Mailleret - RKN dynamics - 10/16R characteristics: fitness costs of virulencedefault scenario, 15 seasonsCastagnoneetal.2007,DjianCap.etal.2011• no advantage of rotations whenhigh or low fitness costs• experimental data (Mi-tomato):>30% gain with optimal rotations• wr and wβ have symmetricalinfluence but interact negativelyR0,v = f (1− (1−wβ)(1−wr )) = f (w)test- L. Mailleret - RKN dynamics - 11/16R characteristics: fitness costs of virulencedefault scenario, 15 seasonsCastagnoneetal.2007,DjianCap.etal.2011• no advantage of rotations whenhigh or low fitness costs• experimental data (Mi-tomato):>30% gain with optimal rotations• wr and wβ have symmetricalinfluence but interact negativelyR0,v = f (1− (1−wβ)(1−wr )) = f (w)test- L. Mailleret - RKN dynamics - 11/16R characteristics: fitness costs of virulencedefault scenario, 15 seasonsCastagnoneetal.2007,DjianCap.etal.2011• no advantage of rotations whenhigh or low fitness costs• experimental data (Mi-tomato):>30% gain with optimal rotations• wr and wβ have symmetricalinfluence but interact negativelyR0,v = f (1− (1−wβ)(1−wr )) = f (w)test- L. Mailleret - RKN dynamics - 11/16Fitness cost × epidemiological scenarios15 seasons, different virulence emergence rates0 0.5 1 0 0.5 1 0 0.5 1 0 0.5 10204060rela�ve gainw w w wlow moderate high extreme1e-061e-041e-03pure Rop�mal• strong influence of diseaseseverity on advantage ofrotations: increases with severity• gain maximized for mediumfitness costs• mild influence of virulenceemergence rate on advantage ofrotations: decreases with ratetest- L. Mailleret - RKN dynamics - 12/16Fitness cost × epidemiological scenarios15 seasons, different virulence emergence rates0 0.5 1 0 0.5 1 0 0.5 1 0 0.5 10204060rela�ve gainw w w wlow moderate high extreme1e-061e-041e-03pure Rop�mal• strong influence of diseaseseverity on advantage ofrotations: increases with severity• gain maximized for mediumfitness costs• mild influence of virulenceemergence rate on advantage ofrotations: decreases with ratetest- L. Mailleret - RKN dynamics - 12/16Fitness cost × epidemiological scenarios15 seasons, different virulence emergence rates0 0.5 1 0 0.5 1 0 0.5 1 0 0.5 10204060rela�ve gainw w w wlow moderate high extreme1e-061e-041e-03pure Rop�mal• strong influence of diseaseseverity on advantage ofrotations: increases with severity• gain maximized for mediumfitness costs• mild influence of virulenceemergence rate on advantage ofrotations: decreases with ratetest- L. Mailleret - RKN dynamics - 12/16Robustness15 seasons, ±10% on all parameter values0102010304050moderate high extremerealized rela�ve gain• sub-optimal rotations always outperformpure R strategies• benefit of optimal rotations little affectedby uncertainty on parameterstest- L. Mailleret - RKN dynamics - 13/16Using plant Resistance against RKNAlternating R and S cultivars• more efficient than classical agricultural practice• optimal periodic rotations approach best deployment performanceFitness costs of virulence• interact negatively• 1 large cost + 1 small cost > 2 medium costsOptimal rotations significantly outperform pure R• when nematode infestation is moderate to severe• when fitness costs are medium• over longer time scales (not shown)Robustness• optimal rotation efficacy preserved despite uncertainty in modelparameter estimatestest- L. Mailleret - RKN dynamics - 14/16Using plant Resistance against RKNAlternating R and S cultivars• more efficient than classical agricultural practice• optimal periodic rotations approach best deployment performanceFitness costs of virulence• interact negatively• 1 large cost + 1 small cost > 2 medium costsOptimal rotations significantly outperform pure R• when nematode infestation is moderate to severe• when fitness costs are medium• over longer time scales (not shown)Robustness• optimal rotation efficacy preserved despite uncertainty in modelparameter estimatestest- L. Mailleret - RKN dynamics - 14/16Using plant Resistance against RKNAlternating R and S cultivars• more efficient than classical agricultural practice• optimal periodic rotations approach best deployment performanceFitness costs of virulence• interact negatively• 1 large cost + 1 small cost > 2 medium costsOptimal rotations significantly outperform pure R• when nematode infestation is moderate to severe• when fitness costs are medium• over longer time scales (not shown)Robustness• optimal rotation efficacy preserved despite uncertainty in modelparameter estimatestest- L. Mailleret - RKN dynamics - 14/16Using plant Resistance against RKNAlternating R and S cultivars• more efficient than classical agricultural practice• optimal periodic rotations approach best deployment performanceFitness costs of virulence• interact negatively• 1 large cost + 1 small cost > 2 medium costsOptimal rotations significantly outperform pure R• when nematode infestation is moderate to severe• when fitness costs are medium• over longer time scales (not shown)Robustness• optimal rotation efficacy preserved despite uncertainty in modelparameter estimatestest- L. Mailleret - RKN dynamics - 14/16Thank You !any questions?test- L. Mailleret - RKN dynamics - 15/16Appendix: R0,vSeason-to-season basic reproduction number of virulent nematodesR0,v = φ exp([((1− wβ)(1− wr )εrα− 1)(H0 +µT2)β − η]T)• obtained from the Ṗv/Pv dynamics• in the limit Pa,Pv → 0• assuming E and I at quasi-equilibriumtest- L. Mailleret - RKN dynamics - 16/16

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A demo-genetic model of root-knot nematod dynamics with applications to the deployment of plant resistance

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