INSECT-INDUCED FOLIAR GALLS: A CROSS-TALK AMONG PHYTOHORMONES FOR TISSUE GROWTH AND ENDOGENOUS DEFENSE
DOI:
https://doi.org/10.53808/KUS.SI.2023.ICES.A109-lsKeywords:
Foliar gall, phytohormone gradients, plant-herbivore co-evolutionAbstract
Insect-induced gall tissue has a unique ability to influence its hosts' phenotypic expression. When plants are stressed by insects, phytochemical manipulations in galling tissue strengthen the plant's resilience to subsequent herbivore attacks, and as a result, the damaged plant tissue regenerates and rejuvenates. Gall tissue development and differentiation are initiated by changes in and modulation of a variety of phytohormones in the affected galling sites. Such hormonal changes ultimately boost the plant's ability to respond to herbivore invasions. In this study, the insect-induced gall tissues of three model plants—mature and immature galls and non-gall tissue—were evaluated for five phytohormone gradients. Phytohormone gradients are continually altered and compared from non-differentiated (non-gall) tissue to moderately (immature gall) and highly (mature gall) developed tissue. The results indicate that phytohormones serve a dual role in stimulating the plant's endogenous defense and promoting tissue growth, pointing to a complex chemogenesis process in galling tissue associated with developing neoplasm and plant defensive responses. Tissue abnormalities in galls are thought to have resulted from the herbivore's interactions with the plant on which it infests. Insects' ovipositing fluids or oral discharge may have also contributed to the accumulation of phytohormones in the stressed and wounded tissue. Foliar galls are thus a sign of manifestation of insects' adaptation since the herbivore and their hosts are likely to co-evolve in the context of chemical adaptation.
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References
Abrahamson, W. G., & McCrea, K. D. (1986). Nutrient and biomass allocation in Solidago altissima: effects of two stem gallmakers, fertilization, and ramet isolation. Oecologia, 174-180.
Agrawal, A. A., & Konno, K. (2009). Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu. Rev. Ecol. Evol. Syst., 40, 311-331.
Akitt, D. B., Brown, A. W., & Potter, J. W. (1980). Role of ethylene in the response of tomato plants susceptible and resistant to Meloidogyne incognita. Phytopathology, 70(2), 94-97.
Anand, A., Uppalapati, S. R., Ryu, C. M., Allen, S. N., Kang, L., Tang, Y., & Mysore, K. S. (2008). Salicylic acid and systemic acquired resistance play a role in attenuating crown gall disease caused by Agrobacterium tumefaciens. Plant Physiology, 146(2), 703.
KOST, C., & Heil, M. (2006). Herbivore‐induced plant volatiles induce an indirect defense in neighbouring plants. Journal of Ecology, 94(3), 619-628.
Bari, R., & Jones, J. D. (2009). Role of plant hormones in plant defense responses. Plant molecular biology, 69, 473-488.
Byers, J. A., Brewer, J. W., & Denna, D. W. (1973). Plant growth hormones in pinyon insect galls (Doctoral dissertation, Colorado State University).
Davies, P. J. (Ed.). (2004). Plant hormones: biosynthesis, signal transduction, action! Springer Science & Business Media.
Dicke, M., & Van Poecke, R. (2002). Signalling in plant-insect interactions: signal transduction in direct and indirect plant defense. In Plant signal transduction (pp. 289-316). Oxford University Press.
Dorchin, N., Hoffmann, J. H., Stirk, W. A., NOVÁK, O., Strnad, M., & van Staden, J. (2009). Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae. Physiological Entomology, 34(4), 359-369.
Erb, M., Meldau, S., & Howe, G. A. (2012). Role of phytohormones in insect-specific plant reactions. Trends in plant science, 17(5), 250-259.
Fay, P. A., Hartnett, D. C., & Knapp, A. K. (1993). Increased photosynthesis and water potentials in Silphium integrifolium galled by cynipid wasps. Oecologia, 93, 114-120.
Bak, S., & Fürstenberg-Hägg, J. (2013). Zagrobelny, MikaPlant Defense against Insect Herbivores. International Journal of Molecular Science, 14(5), 10242-10297.
Gatehouse, J. A. (2002). Plant resistance towards insect herbivores: a dynamic interaction. New phytologist, 156(2), 145-169.
Ghosh, D. (2006). Bark is the hallmark. Resonance, 11(3), 41-50.
Goethals, K., Vereecke, D., Jaziri, M., Van Montagu, M., & Holsters, M. (2001). Leafy gall formation by Rhodococcus fascians. Annual review of phytopathology, 39(1), 27-52.
Hartley, S. E. (1998). The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia, 113, 492-501.
Hartley, S. E. (1999). Are gall insects large rhizobia? Oikos, 84(2), 333-342.
Hartley, S. E., & Lawton, J. H. (1992). Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. Journal of Animal Ecology, 113-119.
Howe, G. A., & Jander, G. (2008). Plant immunity to insect herbivores. Annu. Rev. Plant Biol., 59, 41-66.
Jameson, P. E. (2000). Cytokinins and auxins in plant-pathogen interactions–An overview. Plant Growth Regulation, 32, 369-380.
Kessler, A., & Baldwin, I. T. (2002). Plant responses to insect herbivory: the emerging molecular analysis. Annual review of plant biology, 53(1), 299-328.
Kim, J. S., Kim, Y. O., Ryu, H. J., Kwak, Y. S., Lee, J. Y., & Kang, H. (2003). Isolation of stress-related genes of rubber particles and latex in fig tree (Ficus carica) and their expressions by abiotic stress or plant hormone treatments. Plant and cell physiology, 44(4), 412-414.
Larson, K. C., & Whitham, T. G. (1991). Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions. Oecologia, 88, 15-21.
Lee, C. W., Efetova, M., Engelmann, J. C., Kramell, R., Wasternack, C., Ludwig-Muller, J., ... & Deeken, R. (2009). Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana. The Plant Cell, 21(9), 2948-2962.
Mani MS .(1964).Zoocecidia.In Ecology of Plant Galls9: 149-195.
Mello, M. O., & Silva-Filho, M. C. (2002). Plant-insect interactions: an evolutionary arms race between two distinct defense mechanisms. Brazilian Journal of Plant Physiology, 14, 71-81.
Melnyk, C. W. (2017). Connecting the plant vasculature to friend or foe. New Phytologist, 213(4), 1611-1617.
Meyer, J. (1987). Plant galls and gall inducers. Gebrüder Borntraeger.
Miles, P. W. (1999). Aphid saliva. Biological reviews, 74(1), 41-85.
Minelli, A. (2018). Plant evolutionary developmental biology: the evolvability of the phenotype. Cambridge University Press.
Moran, P. J., & Thompson, G. A. (2001). Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant physiology, 125(2), 1074-1085.
Morkunas, I., Mai, V. C., & Gabryś, B. (2011). Phytohormonal signaling in plant responses to aphid feeding. Acta Physiologiae Plantarum, 33, 2057-2073.
Mani, M. S. (1964). Ecology of plant galls. Dr. W. Junk Publisher, The Hague, 434, 45.
Orlovskis, Z., & Hogenhout, S. A. (2016). A bacterial parasite effector mediates insect vector attraction in host plants independently of developmental changes. Frontiers in plant science, 7, 885.
Pfunder, M., & Roy, B. A. (2000). Pollinator‐mediated interactions between a pathogenic fungus, Uromyces pisi (Pucciniaceae), and its host plant, Euphorbia cyparissias (Euphorbiaceae). American Journal of Botany, 87(1), 48-55.
Price, P. W., & Clancy, K. M. (1986). Interactions among three trophic levels: gall size and parasitoid attack. Ecology, 67(6), 1593-1600.
Rehill, B. J., & Schultz, J. C. (2001). Hormaphis hamamelidis and gall size: a test of the plant vigor hypothesis. Oikos, 95(1), 94-104.
Robert-Seilaniantz, A., Navarro, L., Bari, R., & Jones, J. D. (2007). Pathological hormone imbalances. Current opinion in plant biology, 10(4), 372-379.
Schmelz, E. A., Alborn, H. T., Engelberth, J., & Tumlinson, J. H. (2003). Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiology, 133(1), 295-306.
Shorthouse, J. D., & Rohfritsch, O. (1992). Biology of insect-induced galls. Oxford University Press.
Silva, É. A. S., Saboia, G., Jorge, N. C., Hoffmann, C., dos Santos Isaias, R. M., Soares, G. L., & Zini, C. A. (2017). Development of a HS-SPME-GC/MS protocol assisted by chemometric tools to study herbivore-induced volatiles in Myrcia splendens. Talanta, 175, 9-20.
Tanaka, Y., Okada, K., Asami, T., & Suzuki, Y. (2013). Phytohormones in Japanese mugwort gall induction by a gall-inducing gall midge. Bioscience, Biotechnology, and Biochemistry, 77(9), 1942-1948.
Tiku, A. R. (2021). Direct and indirect defense against insects. Plant-Pest Interactions: From Molecular Mechanisms to Chemical Ecology: Chemical Ecology, 157-192.
Tooker, J. F., & De Moraes, C. M. (2009). A gall-inducing caterpillar species increases essential fatty acid content of its host plant without concomitant increases in phytohormone levels. Molecular plant-microbe interactions, 22(5), 551-559.
Tooker, J. F., & De Moraes, C. M. (2011). Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod-Plant Interactions, 5, 115-124.
Tooker, J. F., & Helms, A. M. (2014). Phytohormone dynamics associated with gall insects, and their potential role in the evolution of the gall-inducing habit. Journal of Chemical Ecology, 40, 742-753.
Turlings, T. C., McCall, P. J., Alborn, H. T., & Tumlinson, J. H. (1993). An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. Journal of Chemical Ecology, 19, 411-425.
Ullah, A., Manghwar, H., Shaban, M., Khan, A. H., Akbar, A., Ali, U., ... & Fahad, S. (2018). Phytohormones enhanced drought tolerance in plants: a coping strategy. Environmental Science and Pollution Research, 25, 33103-33118.
Chandan, R. K., Kumar, R., Swain, D. M., Ghosh, S., Bhagat, P. K., Patel, S., ... & Jha, G. (2020). A novel cross talk of AtRAV1, an ethylene responsive transcription factor with MAP kinases imparts broad spectrum disease resistance in plants. BioRxiv, 2020-01.
Veselov, D., Langhans, M., Hartung, W., Aloni, R., Feussner, I., Götz, C., ... & Ullrich, C. I. (2003). Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta, 216, 512-522.
Vidhyasekaran, P., & Vidhyasekaran, P. (2015). Salicylic acid signaling in plant innate immunity. Plant hormone signaling systems in plant innate immunity, 27-122.
War, A. R., Paulraj, M. G., Ahmad, T., Buhroo, A. A., Hussain, B., Ignacimuthu, S., & Sharma, H. C. (2012). Mechanisms of plant defense against insect herbivores. Plant signaling & behavior, 7(10), 1306-1320.
Weiler, E. W., & Spanier, K. (1981). Phytohormones in the formation of crown gall tumors. Planta, 153, 326-337.
Weis, A. E., Walton, R., & Crego, C. L. (1988). Reactive plant tissue sites and the population biology of gall makers. Annual Review of Entomology, 33(1), 467-486.
Winde, I., & Wittstock, U. (2011). Insect herbivore counteradaptations to the plant glucosinolate–myrosinase system. Phytochemistry, 72(13), 1566-1575.
Wu, J., & Baldwin, I. T. (2010). New insights into plant responses to the attack from insect herbivores. Annual review of genetics, 44, 1-24.
Yamaguchi, H., Tanaka, H., Hasegawa, M., Tokuda, M., Asami, T., & Suzuki, Y. (2012). Phytohormones and willow gall induction by a gall‐inducing sawfly. New Phytologist, 196(2), 586-595.
Zander, M., La Camera, S., Lamotte, O., Métraux, J. P., & Gatz, C. (2010). Arabidopsis thaliana class‐II TGA transcription factors are essential activators of jasmonic acid/ethylene‐induced defense responses. The Plant Journal, 61(2), 200-210.
Zhang, C. X., He, M. X., Cao, Y., Liu, J., Gao, F., Wang, W. B., & Wang, Y. (2015). Fungus-insect gall of Phlebopus portentosus. Mycologia, 107(1), 12-20.
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