Skip to main content
SpringerLink
Log in

Minor cultures as hosts for vectors of extensive crop diseases: Does Salvia sclarea act as a pathogen and vector reservoir for lavender decline?

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Stolbur is a phytoplasma disease affecting crops worldwide. The planthopper Hyalesthes obsoletus is the main natural vector of ‘Candidatus Phytoplasma solani’ responsible of stolbur. In France, lavender (Lavandula angustifolia) and lavandin (Lavandula × intermedia) are strongly affected by this phytoplasma. These plant species are both hosts for the phytoplasma and its insect vector. In 2011, catches of adults were exceptionally sizable on one of the clones of lavandin most tolerant to lavender decline. A high population level of ‘Ca. P. solani’ vector was also observed on the adjacent plot of clary sage, Salvia sclarea. In order to clarify the potential role of S. sclarea as a host plant for H. obsoletus and ‘Ca. P. solani,’ we conducted field surveys and laboratory experiments. The uprooting of clary sage and root examination showed the presence of nymphs during winter. Harvested nymphs have been reared on S. sclarea from seedlings in a greenhouse for many generations. By performing its whole lifecycle on clary sage, we demonstrated for the first time that S. sclarea is a host plant of H. obsoletus and could be a source of stolbur vector. Nevertheless, status of clary sage as host plant of phytoplasma in the field up to now is not so clear. On 42 Q-PCR runs done on S. sclarea, 41 were negative to the phytoplasma, and one positive. Experimental transmission with infected H. obsoletus sampled on infected lavender showed that clary sage plant could be infected, expressed symptoms and multiplied ‘Ca. P. solani.’

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almeida RPP (2008) Ecology of emerging vector-borne plant diseases. In: Lemon SM, Sparling PF, Hamburg MA, Relman DA, Choffnes ER, Mack A (eds) Vector-borne diseases: understanding the environmental, human health, and ecological connections, workshop summary (forum on microbial threats). The National Academies Press, Washington, D.C., pp 70–77

    Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Ann Rev Entomol 47:817–844. doi:10.1146/annurev.ento.47.091201.145300

    Article  CAS  Google Scholar 

  • Bekele B, Hodgetts J, Tomlinson J, Boonham N, Nikolic P, Swarbrick P, Dickinson M (2011) Use of a real-time LAMP isothermal assay for detecting 16SrII and XII phytoplasmas in fruit and weeds of the Ethiopian Rift Valley. Plant Pathol 60:345–355. doi:10.1111/j.1365-3059.2010.02384.x

    Article  CAS  Google Scholar 

  • Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Ann Rev Entomol 46:703–727. doi:10.1146/annurev.ento.46.1.703

    Article  CAS  Google Scholar 

  • Bertin S, Picciau L, Acs Z, Alma A, Bosco D (2010) Molecular identification of the Hyalesthes species (Hemiptera: Cixiidae) occurring in vineyard agroecosystems. Ann Appl Biol 157:435–445. doi:10.1111/j.1744-7348.2010.00434.x

    Article  CAS  Google Scholar 

  • Bonfield JK, Smith KF, Staden R (1995) A new DNA sequence assembly program. Nucleic Acids Res 23:4992–4999. doi:10.1093/nar/23.24.4992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boudon-Padieu E, Cousin MT (1999) Yellow decline of Lavandula hybrida Rev and L. vera DC. Int J Trop Plant Dis 17:1–34

    Google Scholar 

  • Bressan A, Sémétey O, Nusillard B, Clair D, Boudon-Padieu E (2008) Insect vectors (Hemiptera: Cixiidae) and pathogens associated with the disease syndrome “Basses Richesses” of sugar beet in France. Plant Dis 92:113–119. doi:10.1094/pdis-92-1-0113

    Article  CAS  Google Scholar 

  • Bressan A, Holzinger WE, Nusillard B, Semetey O, Gatineau F, Simonato M, Boudon-Padieu E (2009) Identification and biological traits of a planthopper from the genus Pentastiridius (Hemiptera: Cixiidae) adapted to an annual cropping rotation. Eur J Entomol 106:405–413. doi:10.14411/eje.2009.052

    Article  CAS  Google Scholar 

  • Brown JM, Abrahamson WG, Way PA (1996) Mitochondrial DNA phylogeography of host races of the goldenrod ball gallmaker, Eurosta solidaginis (Diptera: Tephritidae). Evolution 50:777–786. doi:10.2307/2410850

    Article  CAS  PubMed  Google Scholar 

  • Carraro L, Ferrini E, Martini M, Ermacora P, Loi N (2008) A serious epidemic of stolbur on celery. J Plant Pathol 90:131–135. doi:10.4454/jpp.v90i1.604

    Google Scholar 

  • Chuche J, Thiéry D (2014) Biology and ecology of the Flavescence dorée vector Scaphoideus titanus: a review. Agron Sustain Dev 34:381–403. doi:10.1007/s13593-014-0208-7

    Article  Google Scholar 

  • Chuche J, Danet JL, Salar P, Foissac X, Thiéry D (2016) Transmission of ‘Candidatus Phytoplasma solani’ by Reptalus quinquecostatus (Hemiptera: Cixiidae). Ann Appl Biol 169:214–223. doi:10.1111/aab.12291

    Article  Google Scholar 

  • Chuche J, Auricau-Bouvery N, Danet J-L, Thiéry D (2017) Use the insiders: could insect facultative symbionts control vector-borne plant diseases? J Pest Sci 90:51–68. doi:10.1007/s10340-016-0782-3

    Article  Google Scholar 

  • Chung BN, Jeong MI, Choi SK, Joa JH, Choi KS, Choi IM (2016) Occurrence of stolbur phytoplasma disease in spreading type Petunia hybrida cultivars in Korea. Plant Pathol J 29:465–470. doi:10.5423/ppj.oa.05.2013.0048

    Article  Google Scholar 

  • Cimerman A, Pacifico D, Salar P, Marzachì C, Foissac X (2009) Striking diversity of vmp1, a variable gene encoding a putative membrane protein of the stolbur phytoplasma. Appl Environ Microbiol 75:2951–2957. doi:10.1128/aem.02613-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabre A, Danet JL, Foissac X (2011) The stolbur phytoplasma antigenic membrane protein gene stamp is submitted to diversifying positive selection. Gene 472:37–41. doi:10.1016/j.gene.2010.10.012

    Article  CAS  PubMed  Google Scholar 

  • Fialova R, Valova P, Balakishiyeva G, Danet JL, Safarova D, Foissac X, Navratil M (2009) Genetic variability of stolbur phytoplasma in annual crop and wild plant species in South Moravia. J Plant Pathol 91:411–416. doi:10.4454/jpp.v91i2.971

    CAS  Google Scholar 

  • Foissac X, Carle P, Fabre A, Salar P, Danet JL, STOLBUREUROMED consortium (2013) ‘Candidatus Phytoplasma solani’ genome project and genetic diversity in the Euro-Mediterranean basin. In: Torres E, Lavina A, Batlle A (eds) Third European bois noir workshop, Invited conference, Barcelona, Spain, pp 11–13

  • Gaudin J, Semetey O, Foissac X, Eveillard S (2011) Phytoplasma titer in diseased lavender is not correlated to lavender tolerance to stolbur phytoplasma. Bull Insectol 64:S179–S180

    Google Scholar 

  • Hedin MC (1997) Molecular phylogenetics at the population/species interface in cave spiders of the southern Appalachians (Araneae: Nesticidae: Nesticus). Mol Biol Evol 14:309–324. doi:10.1093/oxfordjournals.molbev.a025766

    Article  CAS  PubMed  Google Scholar 

  • Holzinger WE, Kammerlander I, Nickel H (2003) The Auchenorrhyncha of Central Europe. In: Fulgoromorpha, Cicadomorpha excl. Cicadellidae, vol 1. Brill, Leiden

  • Johannesen J, Lux B, Michel K, Seitz A, Maixner M (2008) Invasion biology and host specificity of the grapevine yellows disease vector Hyalesthes obsoletus in Europe. Entomol Exp Appl 126:217–227. doi:10.1111/j.1570-7458.2007.00655.x

    Article  Google Scholar 

  • Johannesen J, Foissac X, Kehrli P, Maixner M (2012) Impact of vector dispersal and host-plant fidelity on the dissemination of an emerging plant pathogen. PLoS ONE 7:e51809. doi:10.1371/journal.pone.0051809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kehrli P, Delabays N (2012) Controlling ‘bois noir’ disease on grapevine: does the timing of herbicide application affect vector emergence? J Appl Entomol 136:234–237. doi:10.1111/j.1439-0418.2011.01635.x

    Article  Google Scholar 

  • Kosovac A, Radonjic S, Hrncic S, Krstic O, Tosevski I, Jovic J (2016) Molecular tracing of the transmission routes of bois noir in Mediterranean vineyards of Montenegro and experimental evidence for the epidemiological role of Vitex agnus-castus (Lamiaceae) and associated Hyalesthes obsoletus (Cixiidae). Plant Pathol 65:285–298. doi:10.1111/ppa.12409

    Article  CAS  Google Scholar 

  • Maixner M, Ahrens U, Seemüller E (1995) Detection of the German grapevine yellows (Vergilbungskrankheit) MLO in grapevine, alternative hosts and a vector by a specific PCR procedure. Eur J Plant Pathol 101:241–250. doi:10.1007/BF01874780

    Article  CAS  Google Scholar 

  • Marchi G, Cinelli T, Rizzo D, Stefani L, Goti E, Della Bartola M, Luvisi A, Panattoni A, Materazzi A (2015) Occurrence of different phytoplasma infections in wild herbaceous dicots growing in vineyards affected by bois noir in Tuscany (Italy). Phytopathol Mediterr 54:504–515. doi:10.14601/Phytopathol_Mediterr-16239

    Google Scholar 

  • Mitrović M, Jakovljevic M, Jović J, Krstić O, Kosovac A, Trivellone V, Jermini M, Toševski I, Cvrković T (2016) ‘Candidatus phytoplasma solani’ genotypes associated with potato stolbur in Serbia and the role of Hyalesthes obsoletus and Reptalus panzeri (hemiptera, cixiidae) as natural vectors. Eur J Plant Pathol 144:619–630. doi:10.1007/s10658-015-0800-y

    Article  Google Scholar 

  • Moreau JP, Cousin MT, Staron T, Faivre-Amiot A (1970) Essais de traitement curatif du “Dépérissement jaune” du Lavandin. Ann Pytopathol 2:239–243

    Google Scholar 

  • Murolo S, Romanazzi G (2015) In-vineyard population structure of ‘Candidatus Phytoplasma solani’ using multilocus sequence typing analysis. Infect Genet Evol 31:221–230. doi:10.1016/j.meegid.2015.01.028

    Article  PubMed  Google Scholar 

  • Olivier CY, Lowery DT, Stobbs LW (2009) Phytoplasma diseases and their relationships with insect and plant hosts in Canadian horticultural and field crops. Can Entomol 141:425–462. doi:10.4039/n08-CPA02

    Article  Google Scholar 

  • Purcell AH, Almeida RPP (2005) Insects as vectors of disease agents. In: Goodman R (ed) Encyclopedia of plant and crop science. Taylor & Francis, Bosa Roca, pp 1–14

    Google Scholar 

  • Quaglino F, Zhao Y, Casati P, Bulgari D, Bianco PA, Wei W, Davis RE (2013) ‘Candidatus phytoplasma solani’, a novel taxon associated with stolbur and bois noir related diseases of plants. Int J Syst Evol Microbiol 63:2879–2894. doi:10.1099/ijs.0.044750-0

    Article  CAS  PubMed  Google Scholar 

  • Quaglino F, Maghradze D, Casati P, Chkhaidze N, Lobjanidze M, Ravasio A, Passera A, Venturini G, Failla O, Bianco PA (2016) Identification and characterization of new ‘Candidatus phytoplasma solani’ strains associated with bois noir disease in Vitis vinifera L. cultivars showing a range of symptom severity in Georgia, the Caucasus region. Plant Dis 100:904–915. doi:10.1094/pdis-09-15-0978-re

    Article  CAS  Google Scholar 

  • Rashidi M, Habili N, Ghasemi A (2010) First report of a stolbur phytoplasma associated with witches’ broom of Japanese spindle (Euonymus japonicus). Plant Pathol 59:796. doi:10.1111/j.1365-3059.2009.02245.x

    Article  Google Scholar 

  • Riolo P, Minuz R, Anfora G, Stacconi M, Carlin S, Isidoro N, Romani R (2012) Perception of host plant volatiles in Hyalesthes obsoletus: behavior, morphology, and electrophysiology. J Chem Ecol 38:1017–1030. doi:10.1007/s10886-012-0154-2

    Article  PubMed  Google Scholar 

  • Sharon R, Harari AR, Zahavi T, Raz R, Dafny-Yelin M, Tomer M, Sofer-Arad C, Weintraub PG, Naor V (2015) A yellows disease system with differing principal host plants for the obligatory pathogen and its vector. Plant Pathol 67:785–791. doi:10.1111/ppa.12316

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann Entomol Soc Am 87:651–701. doi:10.1093/aesa/87.6.651

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trkulja V, Adamovic D, Dalovic I, Mitrovic P, Kovacic-Josic D, Lukac Z, Komic J (2016) First report of stolbur phytoplasma associated with Anethum graveolens in Serbia. Plant Dis 100:516–517. doi:10.1094/pdis-07-15-0822-pdn

    Article  Google Scholar 

  • Vali Sichani F, Bahar M, Zirak L (2011) Characterization of stolbur (16SrXII) group phytoplasmas associated with Cannabis sativa witches’-broom disease in Iran. Plant Pathol J 10:161–167. doi:10.3923/ppj.2011.161.167

    Article  Google Scholar 

  • Yvin C (2013) Compte rendu 2013 du programme Casdar IP 1104. Dépérissement de la lavande et du lavandin: mise en oeuvre d’un programme de recherches appliquées afin d’apporter des solutions de lutte aux producteurs. p 149

Download references

Acknowledgements

This study has been funded by the Casdar projects EchoStol and IP 1104. We thank Dr. Christine Griffin (Maynooth University) for her manuscript editing, and Kaëlig Guionneaud and Denis Lacaze for maintaining plants and insect colonies in the greenhouse facility.

Author information

Authors and Affiliations

  1. UMR 1065 Santé et Agroécologie du Vignoble, INRA, ISVV, Bordeaux Sciences Agro, 33882, Villenave d’Ornon Cedex, France

    Julien Chuche & Denis Thiéry

  2. Department of Biology, Maynooth University, Maynooth, County Kildare, Ireland

    Julien Chuche

  3. UMR 1332 Biologie du Fruit et Pathologie, INRA, Université de Bordeaux, 33882, Villenave d’Ornon Cedex, France

    Jean-Luc Danet & Nathalie Arricau-Bouvery

  4. CRIEPPAM, Les Quintrands, Route de Volx, 04100, Manosque, France

    Jean-Baptiste Rivoal

Authors
  1. Julien Chuche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jean-Luc Danet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-Baptiste Rivoal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nathalie Arricau-Bouvery
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Denis Thiéry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Denis Thiéry.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by N. Agusti.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chuche, J., Danet, JL., Rivoal, JB. et al. Minor cultures as hosts for vectors of extensive crop diseases: Does Salvia sclarea act as a pathogen and vector reservoir for lavender decline?. J Pest Sci 91, 145–155 (2018). https://doi.org/10.1007/s10340-017-0885-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-017-0885-5

Keywords

Search

Navigation