Phytoplasma infection renders cranberries more susceptible to above- and belowground insect herbivores

Cesar Rodriguez-Saona , Paolo Salazar-Mendoza , Robert Holdcraft , James Polashock

Insect Science ›› 2025, Vol. 32 ›› Issue (3) : 957 -972.

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Insect Science ›› 2025, Vol. 32 ›› Issue (3) : 957 -972. DOI: 10.1111/1744-7917.13444
ORIGINAL ARTICLE

Phytoplasma infection renders cranberries more susceptible to above- and belowground insect herbivores

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Abstract

While phytoplasma infections in plants are known to affect their interactions with aboveground herbivores, the impact of different genotypes on these infections and their effects on belowground herbivores remains largely unexplored. In cranberry (Vaccinium macrocarpon), infection by the phytoplasma Candidatus Phytoplasma sp. subgroup 16SrIII-Y leads to false blossom disease. This study investigates whether cranberry infection by this phytoplasma affects the performance and feeding behavior of a foliar feeder (spongy moth, Lymantria dispar) and a root feeder (oriental beetle, Anomala orientalis). Using phytoplasma-infected and uninfected cranberries of two genotypes (“Ben Lear” and “Crimson Queen”), the survival, growth and consumption of L. dispar and A. orientalis larvae were measured. To assess the effects on plant morphological and chemical traits, we also examined the impact of phytoplasma infection on shoot and root growth, carbon and nitrogen content, and the levels of defensive compounds such as proanthocyanidins (PACs). Results indicate that larvae of L. dispar and A. orientalis generally showed larger size and more efficient tissue consumption on infected plants, with these effects varying by cranberry genotype, possibly due to differences in phytoplasma titer. Phytoplasma infection was associated with stunted growth, elevated nitrogen content, and lower PAC levels in both shoots and roots of infected cranberry plants compared to uninfected ones. These findings indicate that phytoplasma infection potentially manipulates plant chemical composition by increasing nutrient levels and decreasing defensive compounds, enhancing herbivore performance both above and belowground. This study sheds light on the intricate interplay among plants, phytoplasma infection, and insect herbivore communities.

Keywords

consumption / larval plant–insect interactions / oriental beetle / performance / spongy moth / Vaccinium macrocarpon

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Cesar Rodriguez-Saona, Paolo Salazar-Mendoza, Robert Holdcraft, James Polashock. Phytoplasma infection renders cranberries more susceptible to above- and belowground insect herbivores. Insect Science, 2025, 32(3): 957-972 DOI:10.1111/1744-7917.13444

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References

[1]

Al-Yahyai, R. Al-Subhi, A. Al-Sabahi, J. Al-Said, F. Al-Wahaibi, K. and Al-Sadi, A. (2014) Chemical composition of acid lime leaves infected with Candidatus Phytoplasma aurantifolia. Agricultural Sciences, 5, 66-70.

[2]

An, J.P. Xu, R.R. Liu, X. Zhang, J.C. Wang, X.F. You, C.X. et al. (2021) Jasmonate induces biosynthesis of anthocyanin and proanthocyanidin in apple by mediating the JAZ1-TRB1-MYB9 complex. The Plant Journal, 106, 1414-1430.

[3]

An, X.H. Tian, Y. Chen, K.Q. Liu, X.J. Liu, D.D. Xie, X.B. et al. (2015) MdMYB9 and MdMYB11 are involved in the regulation of the JA-induced biosynthesis of anthocyanin and proanthocyanidin in apples. Plant and Cell Physiology, 56, 650-662.

[4]

Bagadia, P.G. Polashock, J. Bottner-Parker, K.D. Zhao, Y. Davis, R.E. and Lee, I.M. (2013) Characterization and molecular differentiation of 16SrI-E and 16SrIX-E phytoplasmas associated with blueberry stunt disease in New Jersey. Molecular and Cellular Probes, 27, 90-97.

[5]

Beckwith, C.S. and Hutton, S.B. (1929) Cranberry false blossom and the blunt-nosed leafhopper. New Jersey Agricultural Experiment Station Bulletin, 491, 1-16.

[6]

Bertaccini, A. (2007) Phytoplasmas: diversity, taxonomy, and epidemiology. Frontiers in Bioscience, 12, 673-689.

[7]

Bertaccini, A. (2022) Plants and phytoplasmas: when bacteria modify plants. Plants, 11, 1425.

[8]

Chang, C.J. (1998) Pathogenicity of aster yellows phytoplasma and Spiroplasma citri on periwinkle. Phytopathology, 88, 1347-1350.

[9]

Chen, Y.H. Gols, R. and Benrey, B. (2015) Crop domestication and its impact on naturally selected trophic interactions. Annual Review of Entomology, 60, 35-58.

[10]

Clark, J.R. and Finn, C.E. (2010) Register of new fruit and nut cultivars list 45. Hortscience, 45, 716-756.

[11]

Cory, J.S. and Hoover, K. (2006) Plant-mediated effects in insect-pathogen interactions. Trends in Ecology & Evolution, 21, 278-286.

[12]

Daverdin, G. Johnson-Cicalese, J. Zalapa, J. Vorsa, N. and Polashock, J. (2017) Identification and mapping of fruit rot resistance QTL in American cranberry using GBS. Molecular Breeding, 37, 38.

[13]

de Lange, E.S. Kyryczenko-Roth, V. Johnson-Cicalese, J. Davenport, J. Vorsa, N. and Rodriguez-Saona, C. (2019) Increased nutrient availability decreases insect resistance in cranberry. Agricultural and Forest Entomology, 21, 326-335.

[14]

Dermastia, M. (2019) Plant hormones in phytoplasma infected plants. Frontiers in Plant Science, 10, 477.

[15]

Desurmont, G.A. Xu, H. and Turlings, T.C. (2016) Powdery mildew suppresses herbivore-induced plant volatiles and interferes with parasitoid attraction in Brassica rapa. Plant, Cell & Environment, 39, 1920-1927.

[16]

Dixon, R.A. and Sarnala, S. (2020) Proanthocyanidin biosynthesis—a matter of protection. Plant Physiology, 184, 579-591.

[17]

Dobroscky, I.D. (1929) Cranberry false-blossom disease spread by a leafhopper. Science, 70, 635-635.

[18]

Dobroscky, I.D. (1931) Studies on cranberry false blossom disease and its insect vector. Contributions from Boyce Thompson Institute, 3, 59-83.

[19]

Doherty, J.F. (2020) When fiction becomes fact: exaggerating host manipulation by parasites. Proceedings of the Royal Society B, 287, 20201081.

[20]

Eck, P. (1990) The American Cranberry. Rutgers University Press, NJ, USA.

[21]

Fernandez-Conradi, P. Jactel, H. Robin, C. Tack, A.J. and Castagneyrol, B. (2018) Fungi reduce preference and performance of insect herbivores on challenged plants. Ecology, 99, 300-311.

[22]

Franco, F.P. Túler, A.C. Gallan, D.Z. Gonçalves, F.G. Favaris, A.P. Peñaflor, M.F.G. et al. (2021) Fungal phytopathogen modulates plant and insect responses to promote its dissemination. The ISME Journal, 15, 3522-3533.

[23]

Gaillard, M.D. Glauser, G. Robert, C.A. and Turlings, T.C. (2018) Fine-tuning the “plant domestication-reduced defense” hypothesis: specialist vs generalist herbivores. New Phytologist, 217, 355-366.

[24]

Görg, L.M. Gallinger, J. and Gross, J. (2021) The phytopathogen “Candidatus Phytoplasma mali” alters apple tree phloem composition and affects oviposition behavior of its vector Cacopsylla picta. Chemoecology, 31, 31-45.

[25]

Grunseich, J.M. Thompson, M.N. Aguirre, N.M. and Helms, A.M. (2020) The role of plant-associated microbes in mediating host-plant selection by insect herbivores. Plants, 9, 6.

[26]

Hammerbacher, A. Schmidt, A. Wadke, N. Wright, L.P. Schneider, B. Bohlmann, J. et al. (2013) A common fungal associate of the spruce bark beetle metabolizes the stilbene defenses of Norway spruce. Plant Physiology, 162, 1324-1336.

[27]

Heil, M. (2016) Host manipulation by parasites: cases, patterns, and remaining doubts. Frontiers in Ecology and Evolution, 4, 80.

[28]

Hemmati, C. and Nikooei, M. (2019) Phytoplasma infection could affect chemical composition of Artemisia sieberi. The Plant Pathology Journal, 35, 274-279.

[29]

Hogenhout, S.A. Oshima, K. Ammar, E.D. Kakizawa, S. Kingdom, H.N. and Namba, S. (2008) Phytoplasmas: bacteria that manipulate plants and insects. Molecular Plant Pathology, 9, 403-423.

[30]

Horneck, D.A. and Miller, R.O. (1998) Determination of total nitrogen in plant tissue. In Handbook and Reference Methods for Plant Analysis (ed. Y.P. Kalra), pp. 75-83. CRC Press, New York, US.

[31]

Kiprovski, B. Đalović, I. Adamović, D. Mitrović, P. Marjanović-Jeromela, A. Malenčić, Đ. et al. (2018) Biochemical changes in Oenothera biennis plants infected by “Candidatus Phytoplasma solani.” Journal of Plant Pathology, 100, 209-214.

[32]

Labaude, S. Rigaud, T. and Cézilly, F. (2015) Host manipulation in the face of environmental changes: ecological consequences. International Journal for Parasitology: Parasites and Wildlife, 4, 442-451.

[33]

Lee, I.M. Polashock, J. Bottner-Parker, K.D. Bagadia, P.G. Rodriguez-Saona, C. Zhao, Y. et al. (2014) New subgroup 16SrIII-Y phytoplasmas associated with false-blossom diseased cranberry (Vaccinium macrocarpon) plants and with known and potential insect vectors in New Jersey. European Journal of Plant Pathology, 139, 399-406.

[34]

Lepka, P. Stitt, M. Moll, E. and Seemüller, E. (1999) Effect of phytoplasmal infection on concentration and translocation of carbohydrates and amino acids in periwinkle and tobacco. Physiological and Molecular Plant Pathology, 55, 59-68.

[35]

Lu, Y.T. Li, M.Y. Cheng, K.T. Tan, C.M. Su, L.W. Lin, W.Y. et al. (2014) Transgenic plants that express the phytoplasma effector SAP11 show altered phosphate starvation and defense responses. Plant Physiology, 164, 1456-1469.

[36]

MacLean, A.M. Sugio, A. Makarova, O.V. Findlay, K.C. Grieve, V.M. Tóth, R. et al. (2011) Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiology, 157, 831-841.

[37]

MacLean, A.M. Orlovskis, Z. Kowitwanich, K. Zdziarska, A.M. Angenent, G.C. Immink, R.G.H. et al. (2014) Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLoS Biology, 12, e1001835.

[38]

Mason, C.J. Couture, J.J. and Raffa, K.F. (2014) Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia, 175, 901-910.

[39]

Mattson, W.J. (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics, 11, 119-161.

[40]

Mauck, K.E. De Moraes, C.M. and Mescher, M.C. (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences USA, 107, 3600-3605.

[41]

Mauck, K.E. Smyers, E. De Moraes, C.M. and Mescher, M.C. (2015) Virus infection influences host plant interactions with non-vector herbivores and predators. Functional Ecology, 29, 662-673.

[42]

Meyer, R.S. DuVal, A.E. and Jensen, H.R. (2012) Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytologist, 196, 29-48.

[43]

Moreira, X. Abdala-Roberts, L. Gols, R. and Francisco, M. (2018) Plant domestication decreases both constitutive and induced chemical defences by direct selection against defensive traits. Scientific Reports, 8, 12678.

[44]

Pella, E. (1990) Elemental organic analysis. Part 1, Historical developments. American Laboratory, 22, 116-125.

[45]

Polashock, J.J. Caruso, F.L. Averill, A.L. and Schilder, A.C. (2017) Compendium of Blueberry, Cranberry, and Lingonberry Diseases and Pests (2nd Edition). American Phytopathological Society (APS) Press, Minnesota, USA.

[46]

Pradit, N. Mescher, M.C. De Moraes, C.M. and Rodriguez-Saona, C. (2020) Phytoplasma infection of cranberry affects development and oviposition, but not host-plant selection, of the insect vector Limotettix vaccinii. Journal of Chemical Ecology, 46, 722-734.

[47]

Pradit, N. Mescher, M.C. Wang, Y. Vorsa, N. and Rodriguez-Saona, C. (2019a) Phytoplasma infection of cranberries benefits non-vector phytophagous insects. Frontiers in Ecology and Evolution, 7, 181.

[48]

Pradit, N. Rodriguez-Saona, C. Kawash, J. and Polashock, J. (2019b) Phytoplasma infection influences gene expression in American cranberry. Frontiers in Ecology and Evolution, 7, 178.

[49]

Queiroz, R.B. Donkersley, P. Silva, F.N. Al-Mahmmoli, I.H. Al-Sadi, A.M. Carvalho, C.M. et al. (2016) Invasive mutualisms between a plant pathogen and insect vectors in the Middle East and Brazil. Royal Society Open Science, 3, 160557.

[50]

R Core Team. (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

[51]

Raiesi, T. and Golmohammadi, M. (2020) Changes in nutrient concentrations and biochemical characteristics of Mexican lime (Citrus aurantifolia) infected by phytoplasma. Journal of General Plant Pathology, 86, 486-493.

[52]

Rasband, W.S. (2020) ImageJ, US National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/.

[53]

Rodriguez-Saona, C. Polashock, J.J. Kyryczenko-Roth, V. Holdcraft, R. Jimenez-Gonzalez, G. De Moraes, C.M. et al. (2021) Application of plant defense elicitors fails to enhance herbivore resistance or mitigate phytoplasma infection in cranberries. Frontiers in Plant Science, 12, 700242.

[54]

Rodriguez-Saona, C.R. Polashock, J. and Malo, E.A. (2013) Jasmonate-mediated induced volatiles in the American cranberry, Vaccinium macrocarpon: from gene expression to organismal interactions. Frontiers in Plant Science, 4, 115.

[55]

Rodriguez-Saona, C. Vorsa, N. Singh, A.P. Johnson-Cicalese, J. Szendrei, Z. Mescher, M.C. et al. (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. Journal of Experimental Botany, 62, 2633-2644.

[56]

Royer, M. Larbat, R. Le Bot, J. Adamowicz, S. and Robin, C. (2013) Is the C:N ratio a reliable indicator of C allocation to primary and defence-related metabolisms in tomato? Phytochemistry, 88, 25-33.

[57]

Salazar-Mendoza, P. Miyagusuku-Cruzado, G. Giusti, M.M. and Rodriguez-Saona, C. (2024) Genotypic variation and potential mechanisms of resistance against multiple insect herbivores in cranberries. Journal of Chemical Ecology, https://doi.org/10.1007/s10886-024-01522-w.

[58]

Sugio, A. MacLean, A.M. and Hogenhout, S.A. (2014) The small phytoplasma virulence effector SAP11 contains distinct domains required for nuclear targeting and CIN-TCP binding and destabilization. New Phytologist, 202, 838-848.

[59]

Sugio, A. Kingdom, H.N. MacLean, A.M. Grieve, V.M. and Hogenhout, S.A. (2011a) Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proceedings of the National Academy of Sciences USA, 108, E1254-E1263.

[60]

Sugio, A. MacLean, A.M. Kingdom, H.N. Grieve, V.M. Manimekalai, R. and Hogenhout, S.A. (2011b) Diverse targets of phytoplasma effectors: from plant development to defense against insects. Annual Review of Phytopathology, 49, 175-195.

[61]

Tamborindeguy, C. Huot, O.B. Ibanez, F. and Levy, J. (2017) The influence of bacteria on multitrophic interactions among plants, psyllids, and pathogen. Insect Science, 24, 961-974.

[62]

Trickle, C. Holland, L. and Guédot, C. (2023) Distribution and diversity of the cranberry false blossom phytoplasma and leafhopper populations. In 2023 WI Cranberry School Proceedings, Vol 31 (ed. C. Guédot), pp. 24-28. Wisconsin State Cranberry Growers Association, Wisconsin, Madison.

[63]

Venkataravanappa, V. Kodandaram, M.H. Manjunath, M. Chauhan, N.S. Nagendran, K. Tiwari, S.K. et al. (2022) Molecular characterization of phytoplasma strains associated with brinjal little leaf and screening of cultivated and wild relatives of eggplant cultivars for disease resistance. European Journal of Plant Pathology, 162, 433-453.

[64]

Vorsa, N. and Johnson-Cicalese, J. (2012) American cranberry. Fruit Breeding. Handbook of Plant Breeding (eds. M.L. Badenes & D.H Byrne), pp. 191-223. Springer, Massachusetts, USA.

[65]

Weintraub, P.G. and Beanland, L. (2006) Insect vectors of phytoplasmas. Annual Review of Entomology, 51, 91-111.

[66]

Whitehead, S.R. Turcotte, M.M. and Poveda, K. (2017) Domestication impacts on plant-herbivore interactions: a meta-analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20160034.

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2024 The Author(s). Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

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