Hostname: page-component-669899f699-swprf Total loading time: 0 Render date: 2025-04-26T09:05:02.407Z Has data issue: false hasContentIssue false

Dissecting the relationships between the insect vector Empoasca paraparvipenis with Camptotheca acuminata witches’ broom phytoplasma

Published online by Cambridge University Press:  21 November 2024

Hong Cai
Affiliation:
Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming 650201, China
Menglan He
Affiliation:
Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming 650201, China
Yinfeng Cai
Affiliation:
Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming 650201, China
Kai Qiao
Affiliation:
Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming 650201, China
Weiyi Huang
Affiliation:
Key Laboratory of Agro-Biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming 650201, China
Shahzad Munir*
Affiliation:
State Key Laboratory for Conservation and Utilization of Bio-resources in Yunnan, Yunnan Agricultural University, Kunming 650201, China
*
Corresponding author: Shahzad Munir; Email: [email protected]

Abstract

Phytoplasmas are phloem-limited bacteria that are primarily transmitted by hemipteran insects and are emerging threats to Camptotheca acuminata Decne plants due to their associations with a witches’ broom disease. Despite numerous studies, there has been no report on insect transmission of phytoplasma among C. acuminata. Here, transmission characteristics of the leafhopper, Empoasca paraparvipenis Zhang and Liu, 2008 and the phytoplasma in plant leaves through PCR quantification are described. The interaction between C. acuminata-phytoplasma and insect vectors was examined by analysing the impact on the life characteristics and progeny population in a temperature-dependent manner. Phytoplasma-infected C. acuminata plant exhibited symptoms including shorter internodes, weak and clustered branches, shrunken and yellowed leaves, and red leaf margins. The acquisition and transmission time of bacterial-infected third-instar nymphs of insect vectors were 10 (11.11%) and 30 min (33.33%), respectively. A single insect vector can infect a plant after 72 h of feeding, and the incidence rate of disease increases with the number of insects following 11–100% from single to 20 insects. The development time of the infected insect vectors (1–3 instars) was significantly shorter than that of the healthy insects, and the development duration of instar individuals was longer. In progeny populations, the higher the phytoplasma concentration (88–0% for 1–5 instars nymph, female and male adults), the shorter the development time and the longer the adult lifetime (both male and female). These findings provided research evidence of phytoplasma transmission by insect vectors; however, further investigation of the mechanisms for prevention and management of phytoplasma diseases is needed.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Abou-Jawdah, Y, Abdel Sater, A, Jawhari, M, Sobh, H, Abdul-Nour, H, Bianco, P, Molino Lova, M and Alma, A (2014) Asymmetrasca decedens (Cicadellidae, Typhlocybinae), a natural vector of ‘Candidatus Phytoplasma phoenicium’. Annals of Applied Biology 165, 395403.CrossRefGoogle Scholar
Agasyeva, IS, Ismailov, VY, Petrishcheva, M and Nastasiy, AS (2024) Use of biological agents to control the number of Halyomorpha halys Stål. Advancements in Life Sciences 11, 696702.CrossRefGoogle Scholar
Bertaccini, A, Fiore, N, Zamorano, A, Tiwari, AK and Rao, GP (2019) Molecular and serological approaches in detection of phytoplasmas in plants and insects. Phytoplasmas: Plant Pathogenic Bacteria-III: Genomics, Host Pathogen Interactions Diagnosis, 105136.CrossRefGoogle Scholar
Bosco, D and Tedeschi, R (2013) Insect vector transmission assays. In Dickinson, M and Hodgetts, J. (eds), Phytoplasma. Methods in Molecular Biology, vol 938. Totowa, NJ: Humana Press, pp. 7385.Google Scholar
Carr, JP, Donnelly, R, Tungadi, T, Murphy, AM, Jiang, S, Bravo-Cazar, A, Yoon, J-Y, Cunniffe, NJ, Glover, BJ and Gilligan, CA (2018) Viral manipulation of plant stress responses and host interactions with insects. Advances in virus Research 102, 177197.CrossRefGoogle ScholarPubMed
Dermastia, M (2019) Plant hormones in phytoplasma infected plants. Frontiers in Plant Science 10, 477.CrossRefGoogle ScholarPubMed
Hemmati, C, Nikooei, M, Al-Subhi, AM and Al-Sadi, AM (2021) History and current status of phytoplasma diseases in the Middle East. Biology 10, 226.CrossRefGoogle ScholarPubMed
Killiny, N and Almeida, RP (2014) Factors affecting the initial adhesion and retention of the plant pathogen Xylella fastidiosa in the foregut of an insect vector. Applied and Environmental Microbiology 80, 420426.CrossRefGoogle ScholarPubMed
Kumari, S, Nagendran, K, Rai, AB, Singh, B, Rao, GP and Bertaccini, A (2019) Global status of phytoplasma diseases in vegetable crops. Frontiers in Microbiology 10, 1349.CrossRefGoogle ScholarPubMed
Lee, IM (1993) Universal amplification and analysis of pathogen 16S rDNA for classification and identification of mycoplasma like organisms. Phytopathology 83, 834842.CrossRefGoogle Scholar
Li, P, Jie, Z and Yue, Y (2020) Effects of rice stripe mosaic virus on the growth, reproduction and feeding behavior of the mediator electric leafhopper. Acta Entomologica Sinica 2, 174180.Google Scholar
Marcone, C (2009) Movement of phytoplasmas and the development of disease in the plant. In Phytoplasmas: Genomes, Plant Hosts and Vectors. Wallingford: CABI International, pp. 114131.CrossRefGoogle Scholar
Marcone, C (2014) Molecular biology and pathogenicity of phytoplasmas. Annals of Applied Biology 165, 199221.CrossRefGoogle Scholar
Marzachì, C, Milne, RG and Bosco, D (2004) Phytoplasma-plant-vector relationships. Recent Research Developments in Plant Pathology 3, 211241.Google Scholar
Mou, D-F, Di Lella, B, Halbert, SE, Bextine, B, Helmick, EE and Bahder, BW (2022) Acquisition and transmission of the lethal bronzing phytoplasma by Haplaxius crudus using infected palm spear leaves and artificial feeding media. Phytopathology® 112, 20522061.CrossRefGoogle ScholarPubMed
Palermo, S, Arzone, A and Bosco, D (2001) Vector-pathogen-host plant relationships of chrysanthemum yellows (CY) phytoplasma and the vector leafhoppers Macrosteles quadripunctulatus and Euscelidius variegatus. Entomologia experimentalis et applicata 99, 347354.CrossRefGoogle Scholar
Quaglino, F, Sanna, F, Moussa, A, Faccincani, M, Passera, A, Casati, P, Bianco, PA and Mori, N (2019) Identification and ecology of alternative insect vectors of ‘Candidatus Phytoplasma solani’ to grapevine. Scientific Reports 9, 19522.CrossRefGoogle ScholarPubMed
Ranebennur, H, Rawat, K, Rao, A, Kumari, P, Chalam, VC, Meshram, N and Rao, GP (2022) Transmission efficiency of a ‘Candidatus Phytoplasma australasia’ (16SrII-D) related strain associated with sesame phyllody by dodder, grafting and leafhoppers. European Journal of Plant Pathology 164, 193208.CrossRefGoogle Scholar
Schmittgen, TD and Livak, KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 11011108.CrossRefGoogle Scholar
Schneider, B, Ahrens, U, Kirkpatrick, B and SeemuLler, E (1993) Classification of plant-apthogenic mycoplasma-like organism using restriction-site analysis of PCR-amplified 16S rDNA. Microbiology-sgm 139, 519527. https://doi.org/10.1099/00221287-139-3-519Google Scholar
Sun, X, Dongsheng, J and Ping, Z (2017) Infection of rice stripe mosaic virus in the mediator electronic-leaf cicada. Chinese Society of Plant Pathology (Abstract), 285287.Google Scholar
Trivellone, V, Cao, Y and Dietrich, CH (2022) Comparison of traditional and next-generation approaches for uncovering phytoplasma diversity, with discovery of new groups, subgroups and potential vectors. Biology 11, 977.CrossRefGoogle ScholarPubMed
Wan, Y, Hussain, S, Merchant, A, Xu, B, Xie, W, Wang, S, Zhang, Y, Zhou, X and Wu, Q (2020) Tomato spotted wilt orthotospovirus influences the reproduction of its insect vector, western flower thrips, Frankliniella occidentalis, to facilitate transmission. Pest Management Science 76, 24062414.CrossRefGoogle ScholarPubMed
Wang, Z (2018) Detection of Camptotheca acuminata mycoplasma and identification and verification of vector insect leafhopper. Master thesis. Yunnan Agricultural University.Google Scholar
Wang, C, Chien, Y, Liao, P, Chiu, Y, Chen, Y and Yang, J (2021a) First report of 16SrII-V phytoplasma associated with green manure soybean (Glycine max) in Taiwan. Plant Disease 105, 2012.CrossRefGoogle Scholar
Wang, Z, Yuan, E, Su, F, Wan, Q and Cai, H (2021b) Identification of Camptotheca acuminate witches-broom phytoplasma and TagMan-based fluorescence qPCR method for detection. Acta Phytopathologica Sinica 51, 429440.Google Scholar
Wang, Z-H, Wang, W-P, Yuan, E-P, Su, F, Mao, Q-Y, Wan, Q-L and Cai, H (2021c) Identification of Camptotheca acuminate witches’-broom Phytoplasma and Taq man-based fluorescence qPCR method for detection. Acta Phytopathologica 51, 429440.Google Scholar
Wei, W, Jiang, L and Depo, Y (2006) Camptotheca acuminata planting in limestone mountains and its comprehensive control of brown spot. Practical Forestry Technology 11, 911.Google Scholar
Xing, L (2004) Distribution status, medicinal value and development prospect of Camptotheca acuminata. Journal of Shaanxi Normal University 32, 6973.Google Scholar
Xu, X, Gang, X and Wanbin, M (2009) Control test of Camptotheca acuminata canker. Jiangsu Forestry Science and Technology 36, 4454.Google Scholar
Yan, F (2020) Plant pathogen-vector interaction: research progress and prospect. Journal of Insects 63, 123130.Google Scholar
Zhang, S, Shunli, C and Feiping, Z (2002) Study on the life table of natural populations of Camptotheca acuminata. Journal of Fujian Forestry University 2, 45.Google Scholar
Zhu, XJ, Zhang, ZJ and Lu, YB (2011) Effects of inoculation of host plants with tomato spotted wilt virus on populations of the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Acta Entomologica Sinica 54, 425431.Google Scholar
Supplementary material: File

Cai et al. supplementary material

Cai et al. supplementary material
Download Cai et al. supplementary material(File)
File 1.4 MB