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Role of Volatiles in Arthropod Vectors
and Plant Disease Interaction
KARTHIKEYAN, S (2015 800503)
Ph.D., Scholar,
Agricultural Entomology,
TNAU, Coimbatore.
Contents
• Introduction
• Pathogen Induced Plant Volatiles (PIPV)
• Fungus induced plant volatiles
• Bacteria induced plant volatiles
• Phytoplasma induced plant volatiles
• Virus induced plant volatiles
• PIPV in multitrophic interaction
• Applications
Volatile Organic Compounds (VOC)
• Plants use VOCs to communicate
• Plants emit a large variety of different
– terpenes
– fatty acid derivatives
– benzenoids
– phenylpropanoids
– amino-acid-derived metabolites
Pichersky et al. (2006)
Holopainen and Blande (2012)
VOCs Vs Secondary metabolites
• Over 1700 volatile compounds till date
• >90 plant families
• 1% of all plant secondary metabolites
Pichersky and Gershenzon (2002); Pichersky et al. (2006)
Plant VOC functions
• Internal plant hormones
• Ethylene, MeJA, and MeSA
• Communication with conspecific and
heterospecific plants
• Plant–plant communication
• Different trophic levels
Mann et al. (2012)
Semiochemically mediated interactions
• Plants, insects & microbes - prevalent & complex
• Biotic stressors change Volatile emission
– Quantitatively
– Qualitatively
Mann et al. (2012); Mas et al. (2014)
Toxoplasmosis
Vector
Phytopathogen PIPV
PIPV
Plant pathogens manipulate odor of host
Odor of infected plant - attractive to vector
Odor-mediated manipulation attracts vectors to spread
disease
Mann et al. (2012)
Dutch elm disease
• Dutch elm disease Ophiostoma novo-ulmi
• Elm bark beetle, Hylurgopinus rufipes.
• Semiochemicals
– monoterpene(K)-beta-pinene
– sesquiterpenes (K)-alpha-cubebene, (C)-
spiroaxa-5,7-diene and (C)-delta-cadinene)
McLeodet al. (2005)
McLeodet al., (2005)
Crucifers (Brassicaceae) - rust
• Puccinia monoica
• Infection causes a pseudoflower
• Attracts insects to sexually outcross
• Pseudoflowers - distinctive floral fragrances
– aromatic alcohols, aldehydes and esters.
Raguso et al. (1998)
Raguso et al. (1998)
Huanglongbing (HLB) disease of citrus
• Candidatus Liberibacter asiaticus (Las)
• Vector - Diaphorina citri Kuwayama
• VOC - methyl salicylate, methyl anthranilate
and D-limonene
Mann et al. (2012)
Mann et al., (2012)
Volatile differences
Response of D. citri to odors
olfactometer
Mann et al., (2012)
Settling preference
Mann et al., (2012)
Apple proliferation disease
• Candidatus Phytoplasma mali
• Vector-univoltine psyllid Cacopsylla picta
• β-caryophyllene
Mayor et al., (2008)
Mayor et al., (2008)
Potato Leaf Roll Virus (PLRV)
• Myzus persicae
• 11 headspace volatile components
– cis- 2-hexen-1-ol, n-nonane, nonanal,
undecane, β-myrcene, (R)-(+)-limonene,
(−)-transcaryophyllene, (+)-longifolene, α-
pinene, β-pinene, and α-humulene
Eigenbrode et al., (2002)
Eigenbrode et al., (2002)
Eigenbrode et al., (2002)
Aphid immigration and emigration
• Aphids in red light for 1 h
• Higher immigration onto the PLRV-infected
• Lower rates of emigration (per cent per 10
min) from infected leaflets,
• Net greater number of aphids on infected
than uninfected
Eigenbrode et al., (2002)
Settling preference
• Apterous M. persicae preferentially settled
onto PLRV-infected versus uninfected
• From 25 to 86 (mean = 59.7) of the 100 aphids
in each trial were located on the leaflets
Eigenbrode et al., (2002)
Aphid response to headspace above virus
infected and virus-free leaflets
• More aphids - above infected leaflets than
uninfected
Eigenbrode et al., (2002)
Headspace volatile analysis
• PLRV-infected contain 1.9-fold - total GC±
MS-detectable components than uninfected
• PLRV-infected plants produced higher
concentrations of 14 of the 21 components
• 1.6-fold (b -sesquiphellandrene) to 5-fold (2-
hexen-1-ol) over uninfected plants
Eigenbrode et al., (2002)
Barley Yellow Dwarf Virus
• Rhopalosiphum padi
• The total concentration of volatiles from
BYDV infected Lambert was significantly
greater than all other treatments including
noninfected and BYDV-infected
Jiménez-Martínez et al., (2004)
Jiménez-Martínez et al., (2004)
Citrus greening disease (HLB)
• Candidatus Liberibacter asiaticus
• Psyllid Diaphorina citri
• Evesdropping parasitoid Tamarixia radiata
Martini et al., (2014)
Martini et al., (2014)
Response of T. radiata
Martini et al., (2014)
Parasitization efficiency
Martini et al., (2014)
Apllications
• Disrupting host searching behavior
– D. citri attracted towards CLas-infected trees
– MeSA as a semiochemical disruptant
• Disrupting herbivore host preference with
plant volatiles for sustainable management
of insect vectors
Martini et al., (2016)
Possible Applications
• Microbe- and host-based attractants
• Microbe- and host-based repellents
• Semiochemicals as biopesticides
• Non-pheromonal insect pest attractants
• Enhancements or adjuvants for pheromones
• Biomarkers for detection of plant disease
• Semiochemicals for inviting NE
• Manipulate host searching behavior of vectors
• Manipulate foraging behavior of NE
Selected references
• Beck, J. J and R. L. Vanette. 2016. Harnessing Insect−Microbe
Chemical Communications to Control Insect Pests of
Agricultural Systems. J. Agric. Food Chem., 65, 23−28
• Eigenbrode, S. D., H. Ding, P. Shiel and P. H. Berger. 2002. Volatiles
from potato plants infected with potato leafroll virus attract and
arrest the virus vector, Myzus persicae (Homoptera; Aphididae).
Proc. R. Soc. Lond. B. Biol. Sci., 269: 455–460.
• Jiménez-Martínez, E. S. 2004. Volatile cues influence the response
of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow
dwarf virus-infected transgenic and untransformed wheat.
Environ. Entomol., 33: 1207–1216
• Martini, X., K. S. Pelz-Stelinski and L. L. Stelinski. 2014. Plant
pathogen-induced volatiles attract parasitoids to increase
parasitism of an insect vector. Front. Ecol. Evol., 2: 8. doi:
10.3389/fevo.2014.00008

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Role of volatiles in arthropod vectors and plant disease interaction

  • 1. Role of Volatiles in Arthropod Vectors and Plant Disease Interaction KARTHIKEYAN, S (2015 800503) Ph.D., Scholar, Agricultural Entomology, TNAU, Coimbatore.
  • 2. Contents • Introduction • Pathogen Induced Plant Volatiles (PIPV) • Fungus induced plant volatiles • Bacteria induced plant volatiles • Phytoplasma induced plant volatiles • Virus induced plant volatiles • PIPV in multitrophic interaction • Applications
  • 3. Volatile Organic Compounds (VOC) • Plants use VOCs to communicate • Plants emit a large variety of different – terpenes – fatty acid derivatives – benzenoids – phenylpropanoids – amino-acid-derived metabolites Pichersky et al. (2006) Holopainen and Blande (2012)
  • 4. VOCs Vs Secondary metabolites • Over 1700 volatile compounds till date • >90 plant families • 1% of all plant secondary metabolites Pichersky and Gershenzon (2002); Pichersky et al. (2006)
  • 5. Plant VOC functions • Internal plant hormones • Ethylene, MeJA, and MeSA • Communication with conspecific and heterospecific plants • Plant–plant communication • Different trophic levels Mann et al. (2012)
  • 6. Semiochemically mediated interactions • Plants, insects & microbes - prevalent & complex • Biotic stressors change Volatile emission – Quantitatively – Qualitatively Mann et al. (2012); Mas et al. (2014)
  • 7.
  • 8. Toxoplasmosis Vector Phytopathogen PIPV PIPV Plant pathogens manipulate odor of host Odor of infected plant - attractive to vector Odor-mediated manipulation attracts vectors to spread disease Mann et al. (2012)
  • 9.
  • 10. Dutch elm disease • Dutch elm disease Ophiostoma novo-ulmi • Elm bark beetle, Hylurgopinus rufipes. • Semiochemicals – monoterpene(K)-beta-pinene – sesquiterpenes (K)-alpha-cubebene, (C)- spiroaxa-5,7-diene and (C)-delta-cadinene) McLeodet al. (2005)
  • 12. Crucifers (Brassicaceae) - rust • Puccinia monoica • Infection causes a pseudoflower • Attracts insects to sexually outcross • Pseudoflowers - distinctive floral fragrances – aromatic alcohols, aldehydes and esters. Raguso et al. (1998)
  • 13. Raguso et al. (1998)
  • 14.
  • 15. Huanglongbing (HLB) disease of citrus • Candidatus Liberibacter asiaticus (Las) • Vector - Diaphorina citri Kuwayama • VOC - methyl salicylate, methyl anthranilate and D-limonene Mann et al. (2012)
  • 16. Mann et al., (2012) Volatile differences
  • 17. Response of D. citri to odors olfactometer Mann et al., (2012)
  • 19.
  • 20. Apple proliferation disease • Candidatus Phytoplasma mali • Vector-univoltine psyllid Cacopsylla picta • β-caryophyllene Mayor et al., (2008)
  • 21. Mayor et al., (2008)
  • 22.
  • 23. Potato Leaf Roll Virus (PLRV) • Myzus persicae • 11 headspace volatile components – cis- 2-hexen-1-ol, n-nonane, nonanal, undecane, β-myrcene, (R)-(+)-limonene, (−)-transcaryophyllene, (+)-longifolene, α- pinene, β-pinene, and α-humulene Eigenbrode et al., (2002)
  • 26. Aphid immigration and emigration • Aphids in red light for 1 h • Higher immigration onto the PLRV-infected • Lower rates of emigration (per cent per 10 min) from infected leaflets, • Net greater number of aphids on infected than uninfected Eigenbrode et al., (2002)
  • 27. Settling preference • Apterous M. persicae preferentially settled onto PLRV-infected versus uninfected • From 25 to 86 (mean = 59.7) of the 100 aphids in each trial were located on the leaflets Eigenbrode et al., (2002)
  • 28. Aphid response to headspace above virus infected and virus-free leaflets • More aphids - above infected leaflets than uninfected Eigenbrode et al., (2002)
  • 29. Headspace volatile analysis • PLRV-infected contain 1.9-fold - total GC± MS-detectable components than uninfected • PLRV-infected plants produced higher concentrations of 14 of the 21 components • 1.6-fold (b -sesquiphellandrene) to 5-fold (2- hexen-1-ol) over uninfected plants Eigenbrode et al., (2002)
  • 30. Barley Yellow Dwarf Virus • Rhopalosiphum padi • The total concentration of volatiles from BYDV infected Lambert was significantly greater than all other treatments including noninfected and BYDV-infected Jiménez-Martínez et al., (2004)
  • 32.
  • 33. Citrus greening disease (HLB) • Candidatus Liberibacter asiaticus • Psyllid Diaphorina citri • Evesdropping parasitoid Tamarixia radiata Martini et al., (2014)
  • 34. Martini et al., (2014)
  • 35. Response of T. radiata Martini et al., (2014)
  • 37.
  • 38. Apllications • Disrupting host searching behavior – D. citri attracted towards CLas-infected trees – MeSA as a semiochemical disruptant • Disrupting herbivore host preference with plant volatiles for sustainable management of insect vectors Martini et al., (2016)
  • 39. Possible Applications • Microbe- and host-based attractants • Microbe- and host-based repellents • Semiochemicals as biopesticides • Non-pheromonal insect pest attractants • Enhancements or adjuvants for pheromones • Biomarkers for detection of plant disease • Semiochemicals for inviting NE • Manipulate host searching behavior of vectors • Manipulate foraging behavior of NE
  • 40. Selected references • Beck, J. J and R. L. Vanette. 2016. Harnessing Insect−Microbe Chemical Communications to Control Insect Pests of Agricultural Systems. J. Agric. Food Chem., 65, 23−28 • Eigenbrode, S. D., H. Ding, P. Shiel and P. H. Berger. 2002. Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera; Aphididae). Proc. R. Soc. Lond. B. Biol. Sci., 269: 455–460. • Jiménez-Martínez, E. S. 2004. Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environ. Entomol., 33: 1207–1216 • Martini, X., K. S. Pelz-Stelinski and L. L. Stelinski. 2014. Plant pathogen-induced volatiles attract parasitoids to increase parasitism of an insect vector. Front. Ecol. Evol., 2: 8. doi: 10.3389/fevo.2014.00008

Editor's Notes

  1. In addition to simple compounds, such as oxygen, carbon dioxide, and water vapor,
  2. herbivores, pollinators, and enemies of herbivores.
  3. that include damage caused by herbivores and pathogens
  4. Figure 1. Gas chromatograms of volatiles (desorbed from Porapak Q) emanating from ground elm wood infected with the fungal pathogen Ophiostoma novo-ulmi. Hewlett Packard 5890A gas chromatograph with DB-5 column (30 m!0.32 mm i.d.; J&W Scientific, Folsom, CA 95630) with flame ionization (FID) or electroantennographic detector (EAD: male or female Hylurgopinus rufipes antenna); splitless injection; temperature program: 50 8C (2 min), then 10 8C minK1 to 280 8C.
  5. Summary of qualitative differences in volatile composition, as measured using headspace trapping and GC-MS analysis, between uninfected Arabis holboellii tissues (mostly fatty-acid-derived products), tissues infected with Puccinia monoica (dominated by aromatic compounds), and coblooming plants (rich in terpendoid volatiles). Chemical structures of representative compounds from each biochemical class are provided. (Complete data are given in Tables 1Ð4.)
  6. however after feeding, psyllids subsequently dispersed to non-infected rather than infected plants as their preferred settling point. Gram-negative, fastidious, phloem-limited bacterium
  7. Figure 5. Chromatograms displaying volatile differences between Las-infected and non-infected plants. Release of methyl salicylate was significantly greater from plants infected with Las, while release of D-limonene and methyl anthranilate was significantly greater from noninfected plants Feeding on citrus by D. citri adults also induced release of methyl salicylate, suggesting that it may be a cue revealing location of conspecifics on host plants
  8. Figure 1. Response of D. citri to odors emitted from Las infected versus non-infected citrus in a laboratory olfactometer.
  9. Settling preference of combined non-infected and Las-infected D. citri on Las-infected versus non-infected citrus plants Panel (A) shows response under light conditions and panel (B) shows response under dark conditions. Experiments with Las infected and non-infected plants under complete darkness yielded similar results to those recorded under light.
  10. C. picta, reared on uninfected plants without any contact with the phytoplasma during their ontogenesis (inexperienced), was attracted by the odor of infected plants (AP+; Fig. 1a; dependent paired t test, P<0.05). By contrast, C. picta that were reared on infected plants (experienced) showed the opposite behavior depending on their infection status when exposed to the different odor sources. The odor of infected apple was highly attractive for psyllids that had been infected by phytoplasma (P<0.001), while adults of C. picta that had not been infected were attracted by the odor of uninfected plants or repelled by the odor of infected plants, respectively (P<0.05).
  11. were elevated by PLRV infection but not by PVX or PVY infection or sham inoculation compared with non-infected plants.
  12. Mean±SEM proportional mV EAG responses by M. persicae to selected VOC elevated by PLRV infection (responses standardized to linalool=1 and control = paraffin oil)
  13. Figure 1. (a) Location of M. persicae apterae after 1 h in dual choice tests comparing potato lea¯ ets from PLRV-infected plants with either uninfected plants (UNINF), PVY- or PVX-infected plants. Of the 100 aphids in each test, a mean of 59.7 responded (were located on one of the two treatments). Each pair of columns represents data from a single experiment.
  14. 1. Arena used to conduct the headspace volatiles test. Aphids on screen above leaves were unable to contact leaf surfaces, and leaves remained attached to plants during bioassay.
  15. Preferential response of R. padi apterae after 2 h in a dual choice test comparing BYDV-infected versus noninfected plants of the wheat varietyLambert, when aphids had contact with the leaves. Error bars are SEM of the total number of aphids on and near leaves responding to either treatment. Comparison was signiÞcant based on a generalized linear model, assuming a binomial distribution with a logit link function (P 0.0054).
  16. FIGURE 2|Percentage of Tamarixia radiata responding to natural or synthetic odorants vs. blank or solvent negative controls, respectively, withina Y-tubeolfactometer. NR: Percentofnon-responders, n = 40. Asterisksindicatesignificantdifferencesbetweenthetwotreatments(∗∗P < 0.01, ∗∗∗P < 0.001).
  17. FIGURE 3|Numberof Diaphorina citri nymphs parasitized by Tamarixia radiata on: Las-infected vs. uninfected plants (A)oron uninfected plants treated with a methylsalicylate(MeSA) lure vs. uninfected plants left untreated(B).
  18. Exploitation of these host-specific microbe semiochemicals may provide important basis for future plant−insect−microbe chemical ecology investigations.