Identification of yeast and yeast-like symbionts associated with Hishimonus phycitis (Hemiptera: Cicadellidae), the insect vector of lime witches' broom phytoplasma

Hemmati, Chamran; Moharramipour, Saeid; Askari Siahooei, Majeed; Bagheri, Abdoolnabi; Mehrabadi, Mohammad

doi:10.48311/jcp.2017.1358

Identification of yeast and yeast-like symbionts associated with Hishimonus phycitis (Hemiptera: Cicadellidae), the insect vector of lime witches' broom phytoplasma

https://doi.org/10.48311/jcp.2017.1358

Volume 6, Issue 4
December 2017

Pages 439-446

Authors

C. Hemmati ¹

S. Moharramipour ¹

M. Askari Siahooei ²

A. Bagheri ²

M. Mehrabadi ¹

¹ Department of Entomology, Faculty of Agriculture, Tarbiat Modares University, Tehran, Iran.

² Plant Protection Research Department, Hormozgan Agricultural and Natural Resources Research and Education Center, Agricultural Research Education and Extension Organization (AREEO), Bandar Abbas, Iran.

Abstract

Witches' broom disease of lime (WBDL) is a lime disease that has destroyed several citrus orchards in Oman, United Arab Emirates and Iran. WBDL is caused by a bacterium ''Candidatus Phytoplasma aurantifolia'' which is spread through the citrus orchards by a leafhopper, Hishimonus phycitis (Distant) (Hemiptera: Cicadellidae). Leafhoppers are associated with symbiotic microorganisms which provide them with essential amino acids lacking in their diets. Yeast-like relationships with insects are known as common and obligate symbiotic relationship. A prerequisite for the development of future strategies for the symbiotic control of insect pests and insect-vector competence is the identiﬁcation of insect-associated yeast-like symbionts. In the present study, yeast-like symbionts housed in H. phycitis were investigated in insects collected from 13 districts of citrus orchards distributed in southern Iran (Hormozgan, Kerman, Sistan-Balushestan and Fars provinces). Insects were collected from infected lime trees by a D-Vac and stored at -20 ºC up to the DNA extraction. Total DNA was extracted and PCR was conducted with specific primer sets targeting 18S rRNA and 26S rRNA genes of the symbionts. Results revealed that the vector harboured two yeast symbionts, namely Yeast like symbiont of H. phycitis (Hp-YLS)and Candida pimensis,with a similarity of (98-99%) to those reported from the other Cicadellids. These results substantiate the association of these two endosymbiotic microbiota with H. phycitis which may suggest their ecological interactions. To establish any endosymbiotic relationship and probable interfering in pathogen transmission, further studies are needed.

Keywords

Hishimonus phycitis

yeast-like symbionts

Candida pimensis

20.1001.1.22519041.2017.6.4.2.4

Bagheri, A., Salehi, M., Faghihi, M. M., Samavi, S. and Sadeghi, A. 2009. Transmission of Candidatus Phytoplasma aurantifolia to Mexican lime by the leafhopper Hishimonus phycitis in Iran. Journal of Plant Pathology, 91 (4): 105.

Beard, C. B., Cordon-Rosales, C. and Durvasula, R. V. 2002. Bacterial symbionts of the triatominae and their potential use in control of Chagas disease transmission. Annual Review of Entomology, 47 (1): 123-141.

Beard, C. B., Durvasula, R. V. and Richards, F. F. 1998. Bacterial symbiosis in arthropods and the control of disease transmission. Emerging Infectious Diseases, 4 (4): 581.

Bennett, G. M. and Moran, N. A. 2015. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proceedings of the National Academy of Sciences, 112 (33): 10169-10176.

Bove, J. M., Danet, J. L., Bananej, K., Hsaanzadeh, N, Taghizadeh, M., Salehi, M. and Garnier, M. 2000. Witches’ Broom Disease of Lime (WBDL) in Iran. In: Proceeding14th conference on IOCV, IOCV, Riverside, CA, pp 207-212.

Douglas, A. E. 2011. Lessons from studying insect symbioses. Cell Host and Microbe, 10 (4): 359-367.

Fukatsu, T. 1999. Acetone preservation: a practical technique for molecular analysis. Molecular Ecology, 8 (11): 1935-45.

Hongoh, Y. and Ishikawa, H. 2000. Evolutionary studies on uricases of fungal endosymbionts of aphids and planthoppers. Journal of Molecular Evolution, 51 (3): 265-277.

Hughes, G. L., Allsopp, P. G., Webb, R. I., Yamada, R., Iturbe-Ormaetxe, I., Brumbley, S. M. and O’Neill, S. L. 2011. Identification of yeast associated with the planthopper, Perkinsiella saccharicida: potential applications for Fiji leaf gall control. Current Microbiology, 63 (4): 392.

Ibrahim, M. A., Kainulainen, P. and Aflatuni, A. 2008. Insecticidal, repellent, antimicrobial activity and phytotoxicity of essential oils: with special reference to limonene and its suitability for control of insect pests. Agricultural and Food Science, 10 (3): 243-259.

McCutcheon, J. P. 2010. The bacterial essence of tiny symbiont genomes. Current Opinion in Microbiology, 13 (1): 73-78.

Moran, N. A. and Bennett, G. M. 2014. The tiniest tiny genomes. Annual Review of Microbiology, 68: 195-215.

Nishino, T., Tanahashi, M., Lin, C. P., Koga, R. and Fukatsu, T. 2016. Fungal and bacterial endosymbionts of eared leafhoppers of the subfamily Ledrinae (Hemiptera: Cicadellidae). Applied Entomology and Zoology, 51 (3): 465-477.

Noda, H. and Saito, T. 1979. The role of intracellular yeastlike symbiotes in the development of Laodelphax striatellus (Homoptera: Delphacidae). Applied Entomology and Zoology, 14(4): 453-458.

Reineke, A. P., P. Karlovsky, P. and Zebitz, C. P. W. 1998. Preparation and purification of DNA from insects for AFLP analysis. Insect Molecular Biology, 7 (1): 95-99.

Ricci, I., Damiani, C., Scuppa, P., Mosca, M., Crotti, E., Rossi, P. and Chouaia, B. 2011. The yeast Wickerhamomyces anomalus (Pichia anomala) inhabits the midgut and reproductive system of the Asian malaria vector Anopheles stephensi. Environmental Microbiology, 13 (4): 911-921.

Sacchi, L., Genchi, M., Clementi, E., Bigliardi, E, Avanzati, A. M., Pajoro, M., Marzorati, M., Gonella, E. Alma, A., Daffonchio, D. Bandi, R. and Negri. I. 2012. Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): Details of transovarial transmissionof Cardinium sp. and yeast-like endosymbionts. Tissue and Cell, 40: 231-242.

Sasaki, T., Kawamura, M. and Ishikawa, H. 1996. Nitrogen recycling in the brown planthopper, Nilaparvata lugens: involvement of yeast-like endosymbionts in uric acid metabolism. Journal of Insect Physiology, 42 (2): 125-129.

Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30 (12): 2725-2729.

Vega, F. E. and Dowd, P. F. 2005. The role of yeasts as insect endosymbionts. In: Vega, F. E. and Blackwell, M. (Eds.), Insect-Fungal Associations: Ecology and Evolution. Oxford University Press, New York, pp: 211-243.

Vogel, K. J. and Moran, N. A. 2013. Functional and evolutionary analysis of the genome of an obligate fungal symbiont. Genome Biology and Evolution, 5 (5): 891-904.

Xue, J., Zhou, X., Zhang, C. X., Yu, L. L., Fan, H. W., Wang, Z. and Pan, P. L. 2014. Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation.Genome Biology, 15 (12): 521.

XML

PDF 1.05 M