Assessment of phylogenetic signal in the germination ability of broomrape (Phelipanche ramosa) on Brassicaceae hosts

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Le Corre 1 AgroSupDijon, UMR1347 Agroécologie, F-21000 Dijon, France 2 INRA, UMR1347

1 Assessment of phylogenetic signal in the germination ability of broomrape (Phelipanche ramosa) on Brassicaceae hosts S. Gibot-Leclerc, R. Perronne, F. Dessaint, C. Reibel, V. Le Corre 1 AgroSupDijon, UMR1347 Agroécologie, F Dijon, France 2 INRA, UMR1347 Agroécologie, F Dijon, France corresponding author: stephanie.gibot-leclerc@dijon.inra.fr

2 Ecological and biological background Branched broomrape (Phelipanche ramosa (L.) Pomel): a root-holoparasitic angiosperm (no photosynthetic activity) a generalist parasitic weed with a broad host range: several major crops: tobacco (Gibot-Leclerc et al. 2013) hemp (Brault et al. 2013) winter oilseed rape (Gibot-Leclerc et al. 2004, 2012) many arable weeds (Gibot-Leclerc et al. 2003; 2015) responsible for high crop production loss (Parker, 2009) Phelipanche ramosa

3 Oilseed rape: a new host for branched broomrape first infestations reported in the beginning of the 1990s (Gibot-Leclerc et al. 2003) Phelipanche ramosa in oilseed rape

4 Oilseed rape: a new host for branched broomrape first infestations reported in the beginning of the 1990s (Gibot-Leclerc et al. 2003) currently spread over western France (some reports in north-eastern) Phelipanche ramosa in oilseed rape map of infestations in oilseed rape in 2015 data from CETIOM (

5 Questions addressed Host-associated genetic divergence: Are broomrape populations infesting oilseed rape genetically different from broomrape populations infesting other crops? Host range : Are Brassicaceae weeds hosts for broomrape? Phylogenetic signal : Does phylogenetic distance among Brassicaceae can predict their susceptibility to broomrape?

Investigation of genetic variation within branched

severe infestations in fields of different crops (16

population) oilseed rape (4 populations) classic host

6 Investigation of genetic variation within branched broomrape Material: 6 broomrape populations with severe infestations in fields of different crops (16 plants per population) hemp (1 population) tobacco (1 population) oilseed rape (4 populations) classic host crops new host crop 11 newly developed microsatellite markers

7 Host-associated genetic divergence low level of polymorphism within population (1.3 alleles per locus on average), consistent with a high rate of selfing strong genetic structure related to host crop Axis 1 (56%) and axis 2 (12%) of a Principal Component Analysis see Le Corre et al for details

8 Host-associated genetic divergence low level of polymorphism within population (1.3 alleles per locus on average), consistent with a high rate of selfing strong genetic structure related to host crop branched broomrape infecting oilseed rape in France belongs to a recently evolved but highly genetically divergent pathovar Axis 1 (56%) and axis 2 (12%) of a Principal Component Analysis see Le Corre et al for details

9 Investigation of the susceptibility of Brassicaceae species 14 Brassicaceae weeds, one oilseed rape variety some weed species: Capsella bursa-pastoris Cardaria draba Thlaspi arvense Sisymbrium officinale 3 broomrape pathovars : hemp, tobacco, oilseed rape

10 Investigation of the susceptibility of Brassicaceae species 14 Brassicaceae weeds, one oilseed rape variety some weed species: Capsella bursa-pastoris Cardaria draba Thlaspi arvense Sisymbrium officinale 3 broomrape pathovars : hemp, tobacco, oilseed rape in vitro assays : germination rate of seeds on host seedlings Brassicaceae seeds germination (2 weeks) P. ramosa / Brassicaceae weeds co-cultivation (3 weeks) preconditioning of P. ramosa seeds (2 weeks) investigation germination rate

11 Germination rates of broomrape pathovars on Brassicaceae weeds and oilseed rape germination rate (%) 'oilseed rape' pathovar oilseed rape 14 Brassicaceae weeds 'hemp' pathovar 'tobacco' pathovar pathovar tobacco has a low germination rate on oilseed rape and high germination rate on weeds pathovars oilseed rape and hemp present similar rates of germination on both oilseed rape and Brassicaceae weeds highest germination rate on oilseed rape observed for pathovar oilseed rape

12 Germination rates of broomrape pathovar oilseed rape on Brassicaceae weeds odd-ratios: probability of germination on each weed species as compared to the probability of germination on oilseed rape oilseed rape (reference) six weed species are more susceptible than oilseed rape results only for pathovar oilseed rape based on glm estimate

13 Investigations of phylogenetic signal in the germination rate on Brassicaceae construction of a maximum likelihood phylogenetic tree: 15 Brassicaceae (14 weeds + oilseed rape) 4 chloroplast DNA sequences (rbcl, matk, trnl-trnf, trnl-intron)

14 Investigations of phylogenetic signal in the germination rate on Brassicaceae construction of a maximum likelihood phylogenetic tree: 15 Brassicaceae (14 weeds + oilseed rape) 4 chloroplast DNA sequences (rbcl, matk, trnl-trnf, trnl-intron) phylogenetic signal: Blomberg s K statistic as a measure of correlation between phylogenetic distances and phenotypic distances permutation test of the null hypothesis that trait values are randomly distributed across the phylogenetic tree relative contribution of lineages, tribes and genera on signal: S3 root skewness test Pavoine & Ricotta (2013) Evolution Pavoine et al. (2010) Journal of Ecology

15 Phylogenetic tree of Brassicaceae Lineage II Brassica rapa Brassica napus oilseed rape Raphanus raphanistrum Eruca vesicaria subsp. sativa Sinapis arvensis Rapistrum rugosum phylogenetic tree: OILSEED RAPE HEMP TOBACCO 2 Lineages observed Lineage I: Capsella, Cardamine, Lepidium Lineage II: Sinapis, Rapistrum, Raphanus, oilseed rape Sisymbrium officinale Thlaspi arvense Lepidium draba Lepidium campestre Cardamine hirsuta Barbarea vulgaris Arabidopsis thaliana Lineage I Lineage II Expanded lineage II Lineage I Capsella rubella Capsella bursa-pastoris

16 Detection of a phylogenetic signal in the germination rate for the pathovar oilseed rape phylogenetic tree Lineage II Brassica rapa Brassica napus oilseed rape Raphanus raphanistrum Eruca vesicaria subsp. sativa Sinapis arvensis Rapistrum rugosum germination rate per pathovar OILSEED RAPE HEMP TOBACCO 1. a phylogenetic signal is highlighted only for pathovar oilseed rape K = (p-value < 0.05) Sisymbrium officinale Lineage I Lineage II Expanded lineage II Lineage I Thlaspi arvense Lepidium draba Lepidium campestre Cardamine hirsuta Barbarea vulgaris Arabidopsis thaliana Capsella rubella Capsella bursa-pastoris most of Brassicaceae species of Lineage I present a higher germination rate than in Lineage II (oilseed rape) S3 = (p-value = 0.08)

17 Main conclusions about phylogenetic signal Phylogenetic signal in the germination rate of a parasitic weed: In accordance with a previous study (Gilbert et al Evolutionary Applications), but within a single taxonomic family only for a pathovar infecting a crop of the same family mainly explained by differences in germination rates between ancient lineages Perspective: phylogenetic signal could be a new tool for pest risk assessment

18 Take-home messages at least 3 genetically divergent pathovars exist in branched broomrape some Brassicaceae weed species are more susceptible to broomrape than oilseed rape, and may serve as reservoir for this parasite some phylogenetic signal in host susceptibility has been detected, but this result need: to be confirmed on a larger phylogenetic tree for Brassicaceae to be studied also for other taxonomic groups

19 Thank you for your attention This work was funded by AgroSup Dijon (AOS 2013). I thank the EWRS for subsidy for registration fees. stephanie.gibot-leclerc@dijon.inra.fr remi.perronne@moulon.inra.fr

20 Literature References Brault M, Betsou F, Jeune B, Tuquet C, Sallé G Variability of Orobanche ramosa populations in France as revealed by cross infestations and molecular markers. Environmental and Experimental Botany 67: Gibot-Leclerc S, Reibel C, Le Corre V, Dessaint F Unexpected fast development of branched broomrape on slowgrowing Brassicaceae. Agronomy for Sustainable Development. 35: Le Corre V, Reibel C, Gibot-Leclerc S Development of microsatellite markers in branched broomrape Phelipanche ramosa L. (Pomel) and evidence for host-associated genetic divergence. International Journal of Molecular Sciences 15: Gibot-Leclerc S, Dessaint F, Reibel C, Le Corre V Phelipanche ramosa (L.) Pomel populations differ in life-history and infection response to hosts. Flora 208: Gibot-Leclerc S, Abdennebi-Abdemessed N, Reibel C, Colbach N, Non-host facilitators, a new category that unexpectedly favors parasitic weeds. Agronomy for Sustainable Development 33: Gibot-Leclerc S, Sallé G, Reboud X, Moreau D What are the traits of Phelipanche ramosa (L.) Pomel that contribute to the success of its biological cycle on its host Brassica napus L.? Flora 207: Gibot-Leclerc S, Corbineau F, Sallé G, Côme D Responsiveness of Orobanche ramosa L. seeds to GR 24 as related to temperature, oxygen availability and water potential during preconditioning and subsequent germination. Plant Growth Regulation 43: Gibot-Leclerc S, Brault M, Pinochet X, Sallé G Potential role of winter rape weeds in the extension of broomrape in Poitou-Charentes. Comptes Rendus de Biologie 326: Parker C, Observations on the current status of Orobanche and Striga problems worldwide. Pest Management Science 65: Pavoine S, Baguette M, Bonsall M, Decomposition of trait diversity among the nodes of a phylogenetic tree. Ecological Monographs 80: Pavoine S, Ricotta C, Testing for phylogenetic signal in biological traits: the ubiquity of cross-product statistics. Evolution 67-3:

Non-host facilitators, a new category that unexpectedly favours parasitic weeds

Non-host facilitators, a new category that unexpectedly favours parasitic weeds Stéphanie Gibot-Leclerc, Nadia Abdennebi-Abdemessed, Carole Reibel, Nathalie Colbach To cite this version: Stéphanie Gibot-Leclerc,