1 million known insect species

Transcription

1 Multitrophic plant-insect-microbe interactions Marcel Dicke Laboratory of Entomology, Wageningen University, The Picture Nina Fatouros Picture Marcel Dicke Picture Tibor Bukovinszky Picture Nina Fatouros 1 million known insect species 50% herbivore many carnivores also dependent on plants Videos by Hans Smid 1

2 Trophic level 16/07/ hyperparasitoids parasitoids herbivores Plantassociated community Stam, Kroes, Li et al Annual Review of Plant Biology 65: Plant mediates interactions between insect community members Stam, Kroes, Li et al Annual Review of Plant Biology 65:

3 Insect-plant interactions Picture Tibor Bukovinszky Picture Hans Smid Insect-plant interactions and microbes at 3 trophic levels Picture Tibor Bukovinszky Picture Hans Smid 3

4 Insect-plant interactions central position plant Picture Erik Poelman Stam, Kroes, Li et al Annual Review of Plant Biology 65:

5 Trophic levels 16/07/ secondary parasitoid 10 species 3 2 primary parasitoid 5 species herbivore 2 species 1 Picture Rieta Gols one food chain of the food web Tibor Bukovinszky Bukovinszky et al. Science 319: (2008) Quantitative food web Relative abundance Bukovinszky et al. Science 319: (2008) 5

6 Feral Brassica oleracea Brussels sprout = Cultivated Brassica oleracea Bukovinszky et al. Science 319: (2008) Density-mediated effects Size-mediated effects 2 Brassica oleracea genotypes very different food webs quantitative and qualitative differences different community compositions feral domesticated effects of plant on 2 nd trophic level percolate up to 4 th trophic level Bukovinszky et al. Science 319: (2008) 6

7 Plant genotype structures community at multiple trophic levels Organisms as independent singular entities? 7

8 Microbes as hidden players Trends in Ecology and Evolution 2012 Microbes as hidden players 1 st trophic level 8

9 Rhizobacteria Mycorrhizal fungi Plant growth promotion Induced systemic resistance Pineda et al., Trends in Plant Science; Van der Putten et al., 2001; Bezemer & van Dam, 2005; Pieterse & Dicke 2007; Gehring & Bennett 2009; Hartley & Gange Pseudomonas simiae Arabidopsis thaliana Myzus persicae The treatments C: Control plants R: Rhizobacteria; in soil during transplant CA: Control plants with Aphids RA: Rhizobacteria-treated plants with Aphids Diaeretiella rapae Pineda et al Plant Cell and Environment 36:

10 PLS2 [12%] 16/07/2018 Preference of parasitoid Diaeretiella rapae Nr tested (nr response) Col-0 Ana Pineda 71 (54) C *** 80 (48) R ns C 75 (54) RA *** 78 (57) R ** RA CA CA!!! % of parasitoids to odor source Pineda et al Plant Cell and Environment 36: Volatiles: CA vs. RA 5samplesNF=0.M3 (PLS-DA) t[comp. 1]/t[Comp. 2] Colored according to classes in M CA1 CA3 Rhizobacteria alter 1- aphid-induced volatiles and 2- parasitoid behaviour t[2] 2 RA3 0 RA2-2 RA5 RA t[1] PLS1 [39%] R2X[1] = R2X[2] = Ellipse: Hotelling T2 (0.95) RA1 RA *** CA2 CA5 CA4 SIMCA-P :14:25 (UTC+1) 16 compounds RA>CA CA Pineda et al Plant Cell and Environment 36:

11 Differential effects Pseudomonas simiae Phloem feeders Chewing insects 1 B. brassicae specialists P. rapae M. persicae generalists S. exigua generalist M. brassicae 2 Diaeretiella rapae Microplitis mediator van Oosten et al., 2008 MPMI Pineda et al Plant Biol; Pineda et al Plant Cell Envir Pangesti et al 2015, Oecologia Pangesti et al Plant Biol Differential effects Pseudomonas simiae Phloem feeders Pseudomonas simiae differentially affects different P. rapae members of B. brassicae 1 specialists Chewing insects the insect herbivore community so... M. persicae generalists S. exigua generalist M. brassicae Rhizobacteria may influence community structure 2 Diaeretiella rapae Microplitis mediator van Oosten et al., 2008 MPMI Pineda et al Plant Biol; Pineda et al Plant Cell Envir Pangesti et al 2015, Oecologia Pangesti et al Plant Biol 11

12 1 Plant genotype structures community at different trophic levels Rhizobacteria modify HIPV and insect community HIPV = Herbivore-Induced Plant Volatiles Vicia faba Acyrthosiphon pisum Aphidius ervi 2 nd trophic level Enric Frago Symbiont effects on plant-mediated interactions? Frago et al Nature Communications 8:

13 Manipulating aphid symbionts 1. Oral antibiotic curing method 2. Microinjection 101(Hamiltonella) 101(with Hamiltonella) 101 (without Hamiltonella) 101(with Hamiltonella) 101 (without Hamiltonella) Clone101(H + ) Clone101(H - ) Clone101(H + ) Clone101(H - ) olfactometer Frago et al Nature Communications 8:

14 Proportion of time spent by wasps above plant with symbiont carrying aphids 16/07/2018 Parasitoid preference in 2-choice setup Aphidius ervi Bacterium Hamiltonella defensa 101(H+) 101(H-) ** Parasitoids prefer HIPV related to symbiontfree aphids Parasitoid time allocation (seconds) Frago et al Nature Communications 8: choice setup Marcel 0.40 Dicke, Wageningen University Antibiotic treatment Injec tion Systemic Frago et al Nature Communications 8:

15 Plant-emitted volatiles (HIPVs) differ between plants infested with symbiont carrying aphids and cured aphids Frago et al Nature Communications 8: 1860 Effects of aphid endosymbionts provide nutrients to aphids Douglas 1998 Annu Rev Entomol 43: enhance aphid resistance to parasitoids Oliver et al PNAS 102: The suppress Netherlands, induction of herbivore-induced ECE2018 plant volatiles Naples Frago et al Nature Communications 8: 1860 Sanders et al Ecol Lett 19: influence community dynamics of multiple plant-aphid-parasitoid systems Sanders et al Ecology Letters 19:

16 1 Microbial 2 Plant genotype structures community at different trophic levels Rhizobacteria symbionts of modify HIPV and herbivore modify HIPV insect insect community via community plant-mediated effects HIPV = Herbivore-Induced Plant Volatiles Microbes as hidden players 3 rd Marcel trophic Dicke, Wageningen level University Picture Hans Smid 16

17 Caterpillar spit: contains elicitors of plant volatiles Mattiacci et al PNAS 92: Effects parasitisation on caterpillar regurgitant plant gene expression performance of other herbivores performance of parasitoid in other herbivore on same plant colonization of herbivores Parasitoids: Cotesia glomerata & Hyposoter ebeninus Herbivores: Pieris brassicae & Pieris rapae So major effect on platn phenotype with consequences for interactions with various Poelman, Zheng et al. (2011) PNAS 108:

18 PLS2 (19.83%) 16/07/2018 Cotesia glomerata Cotesia glomerata Pieris brassicae PB Pieris brassicae Pieris rapae PB-CG PR Pieris rapae PR-CG Zhu et al Molecular Ecology 24: Brassica microarray analysis PR PB PR-CG PB-CG (FC > 2; FDR < 0.05) PLS1 (24.17%) Parasitoid influences expression of plant genes in response to caterpillar feeding Feng Zhu Zhu et al Molecular Ecology 24:

19 HIPV Erik Poelman Berhane Weldegergis Feng Zhu Poelman et al PLoS Biology 10(11): e Lysibia nana hyperparasitoids in Y-tube olfactometer ECE2018 YNaples Poelman et al Plos Biology Poelman et al Plos Biology 10(11): e

20 Field responses hyperparasitoids Picture Erik Poelman Picture Erik Poelman Erik Poelman Feng Zhu Poelman et al PLoS Biology 10(11): e Field responses hyperparasitoids Matches lab responses Erik Poelman Feng Zhu Poelman et al PLoS Biology 10(11): e

21 Is the effect really caused by parasitoid larvae??? Antonino Cusumano Polydnavirus (PDV) Picture Tibor Bukovinszky Venom Eggs 21

22 Polydnavirus (PDV) Venom ECE2018 Eggs Naples Antonino Cusumano Polydnavirus: replicates in parasitoid suppresses immune system of caterpilar Zhu, Cusumano et al PNAS 115: parasitoid hyperparasitoid Time Zhu, Cusumano et al PNAS 115:

23 Polydnavirus (PDV) Eggs Marcel Venom Dicke, Wageningen University Not the parasitoid eggs but polydnavirus plus venom influence caterpillar-plant interaction Feng Zhu Antonino Cusumano Zhu, Cusumano et al PNAS 115: d = salivary gland of caterpillar Zhu, Cusumano et al PNAS 115:

24 d = salivary gland of caterpillar Caterpillar salivary glands essential for effect parasitoid on caterpillar-plant interactions Zhu, Cusumano et al PNAS 115: d = salivary gland of caterpillar Caterpillar salivary glands essential for effect parasitoid on caterpillar-plant interactions Zhu, Cusumano et al PNAS 115:

25 Salivary gland critical in Herbivore-induced plant volatiles induced by parasitized caterpillars Zhu, Cusumano et al PNAS 115: Multiple and multitrophic effects of polydnaviruses PolyDNA virus (PDV) Eggs 1- suppress the caterpillar s immune response Edson et al Science 211: enhance food quality for caterpillar and Marcel parasitoids in the caterpillar Venom Dicke, Wageningen University Tan et al PNAS 15: ECE Plutella Naples xylostella moths avoid plant for oviposition Cusumano et al Ecology Letters 21: Lysibia nana hyperparasitoids are attracted and parasitize primary parasitoid Zhu, Cusumano et al PNAS 115:

26 1 Microbial 2 3 Plant genotype structures community at different trophic levels Rhizobacteria modify HIPV and insect community symbionts of herbivore modify HIPV and insect community via plant-mediated effects Parasitioid-associated virus influences multitrophic plantmediated interactions Plant mediates interactions among community members Microorganisms modulate plant-mediated interactions HIPV = Herbivore-Induced Plant Volatiles The team Entomology, Wageningen University Janneke Bloem Tibor Bukovinszky Antonio Cusumano Nina Fatouros Enric Frago Rieta Gols Yde Jongema Joop van Loon Mukta Mala Ana Pineda Erik Poelman Alexandre Villela Berhane Weldegergis Si-Jun Zhen Feng Zhu Netherlands Institute of Ecology Jeff Harvey Max Planck Institute for Chemical Ecology Heiko Vogel University of Oxford Charles Godfray Ailsa Maclean University of Exeter Dirk Sanders Frank van Veen University of Rennes Anne Marie Cortesero Open competition Veni Vici Spinoza 26

27 1 Microbial 2 3 Plant genotype structures community at different trophic levels Rhizobacteria modify HIPV and insect community symbionts of herbivore modify HIPV and insect community via plant-mediated effects Parasitioid-associated virus influences multitrophic plantmediated interactions Plant mediates interactions among community members Microorganisms modulate plant-mediated interactions HIPV = Herbivore-Induced Plant Volatiles 27