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Evaluation of physiological and morphological responses of Salix alba and Salix babylonica to witches’ broom gall

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Abstract

The gall formation in Salix species is caused by Candidatus phytoplasma trifolii. The present study was designed with the aim of evaluation of the morphological and physiological response of two species of Salix alba and Salix babylonica to gallers in the witches’ broom structure. The morphological responses of Salix species to gallers, denoted as biotic stress, were represented by growth suppression of leaves and shoots. Accordingly, the leaf area and shoot internodes significantly decreased, in comparison with healthy plants. The biotic stress can induce oxidative stress, which was observed in the present study with a high accumulation of H2O2 in galled tissues. High accumulation of H2O2 in the infected tissue damaged chlorophyll a and proteins. Even though Salix species induced the antioxidants catalase, peroxidase, proline, anthocyanins and phenols to scavenge reactive oxygen species (ROS), high accumulation of H2O2 was observed in galled tissues. Altogether, regardless of activation of antioxidants in response to galls-induced oxidative stress, ROS accumulation damaged photosynthetic apparatus and proteins.

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References

  • Aebi, H. (1984). Catalase in vitro. In Methods in enzymology (Vol. 105, pp. 121–126). Elsevier.

  • Askari Seyahooei, M., Hemmati, C., Faghihi, M. M., & Bagheri, A. (2017). First report of a ‘Candidatus Phytoplasma trifolii’-related strain associated with Suaeda aegyptiaca and its potential vector in Iran. Australasian Plant Disease Notes, 12, 1–4.

    Article  CAS  Google Scholar 

  • Azimi, M., Mehrabi-Koushki, M., & Farokhinejad, R. (2018). Association of two groups of phytoplasma with various symptoms in some wooden and herbaceous plants. Journal of Phytopathology, 166, 273–282.

    Article  CAS  Google Scholar 

  • Bajraktari, D., Bauer, B., & Zeneli, L. (2022). Antioxidant capacity of Salix alba (Fam. Salicaceae) and influence of heavy metal accumulation. Horticulturae, 8, 642.

  • Barna, B., & Pogány, M. (2001). Antioxidant enzymes and membrane lipid composition of disease resistant tomato plants regenerated from crown galls. Acta Physiologiae Plantarum, 23, 273–277.

    Article  CAS  Google Scholar 

  • Bates, L. S., Waldren, R. P., & Teare, I. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39, 205–207.

    Article  CAS  Google Scholar 

  • Bohlmann, H., & Sobczak, M. (2014). The plant cell wall in the feeding sites of cyst nematodes. Frontiers in Plant Science, 5, 89.

    Article  PubMed  PubMed Central  Google Scholar 

  • Baldacci-Cresp, F., Maucourt, M., Deborde, C., Pierre, O., Moing, A., Brouquisse, R., Favery, B., & Frendo, P. (2015). Maturation of nematode-induced galls in Medicago truncatula is related to water status and primary metabolism modifications. Plant Science, 232, 77–85.

    Article  CAS  PubMed  Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Britton, M. T., Escobar, M. A., & Dandekar, A. M. (2008). The oncogenes of Agrobacterium tumefaciens and Agrobacterium rhizogenes. Tzfira, T., & Citovsky, V. (Eds.), Agrobacterium: from biology to biotechnology, pp. 523–563. Springer Science & Business Media.

  • Cambier, S., Ginis, O., Moreau, S. J., Gayral, P., Hearn, J., Stone, G. N., Giron, D., Huguet, E., & Drezen, J.-M. (2019). Gall wasp transcriptomes unravel potential effectors involved in molecular dialogues with oak and rose. Frontiers in Physiology, 10, 926.

    Article  PubMed  PubMed Central  Google Scholar 

  • Carneiro, R., Castro, A., & Isaias, R. (2014). Unique histochemical gradients in a photosynthesis-deficient plant gall. South African Journal of Botany, 92, 97–104.

    Article  CAS  Google Scholar 

  • Connor, E. F., Bartlett, L., O’Toole, S., Byrd, S., Biskar, K., & Orozco, J. (2012). The mechanism of gall induction makes galls red. Arthropod-Plant Interactions, 6, 489–495.

    Article  Google Scholar 

  • Deng, L., Hu, J., Yao, Y., Wang, T., Liao, L., Xiong, B., Wang, X., Sun, G., Zhang, M., He, J., He, S., & Wang, Z. (2024). Defense response of ‘Cuimili’plum/‘Maotao’to Agrobacterium tumefaciens: A combined physiological and transcriptomic analysis. Scientia Horticulturae, 325, 112678.

    Article  CAS  Google Scholar 

  • Favery, B., Dubreuil, G., Chen, M.-S., Giron, D., & Abad, P. (2020). Gall-inducing parasites: Convergent and conserved strategies of plant manipulation by insects and nematodes. Annual Review of Phytopathology, 58, 1–22.

    Article  CAS  PubMed  Google Scholar 

  • Favery, B., Quentin, M., Jaubert-Possamai, S., & Abad, P. (2016). Gall-forming root-knot nematodes hijack key plant cellular functions to induce multinucleate and hypertrophied feeding cells. Journal of Insect Physiology, 84, 60–69.

    Article  CAS  PubMed  Google Scholar 

  • Fernandes, G., & Waring, G. (1987). Adaptive nature of insect galls. Environmental Entomology, 16, 15–24.

    Article  Google Scholar 

  • Ferreira, B. G., Álvarez, R., Bragança, G. P., Alvarenga, D. R., Pérez-Hidalgo, N., & Isaias, R. M. (2019). Feeding and other gall facets: patterns and determinants in gall structure. The Botanical Review, 85, 78–106.

    Article  Google Scholar 

  • Flurkey, W. H., & Jen, J. J. (1980). Purification of peach polyphenol oxidase in the presence of added protease inhibitors Journal of Food Biochemistry, 4, 29–41.

  • Foyer, C. H., & Shigeoka, S. (2011). Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiology, 155, 93–100.

    Article  CAS  PubMed  Google Scholar 

  • Gailite, A., Andersone, U., & Ievinsh, G. (2005). Arthropod-induced neoplastic formations on trees change photosynthetic pigment levels and oxidative enzyme activities. Journal of Plant Interactions, 1, 61–67.

    Article  CAS  Google Scholar 

  • Ghayeb Zamharir, M. (2018a). Association of ‘Candidatus Phytoplasma trifolii’related strain with white willow proliferation in Iran. Australasian Plant Disease Notes, 13, 17.

    Article  Google Scholar 

  • Ghayeb Zamharir, M. (2018b). Association of ‘Candidatus Phytoplasma trifolii’related strain with white willow proliferation in Iran. Australasian Plant Disease Notes, 13, 1–4.

    Article  Google Scholar 

  • Ghayeb Zamharir, M., & Taheri, P. (2017). ‘Candidatus Phytoplasma solani’related strain associated with Babylon willow witches’ broom in central provinces of Iran. Australasian Plant Disease Notes, 12, 1–3.

    Article  Google Scholar 

  • Gheysen, G., & Mitchum, M. G. (2019). Phytoparasitic nematode control of plant hormone pathways. Plant Physiology, 179, 1212–1226.

    Article  CAS  PubMed  Google Scholar 

  • Grieve, C., & Grattan, S. (1983). Rapid assay for determination of water soluble quaternary ammonium compounds. Plant and Soil, 70, 303–307.

    Article  CAS  Google Scholar 

  • Guedes, L. M., Sanhueza, C., Torres, S., Figueroa, C., Gavilán, E., Pérez, C. I., & Aguilera, N. (2022). Gallinducing Eriophyes tiliae stimulates the metabolism of Tilia platyphyllos leaves towards oxidative protection. Plant Physiology and Biochemistry 195, 25–36.

  • Harris, M., Freeman, T., Rohfritsch, O., Anderson, K., Payne, S., & Moore, J. (2006). Virulent Hessian fly (Diptera: Cecidomyiidae) larvae induce a nutritive tissue during compatible interactions with wheat. Annals of the Entomological Society of America, 99, 305–316.

    Article  Google Scholar 

  • Harris, M. O., & Pitzschke, A. (2020). Plants make galls to accommodate foreigners: Some are friends, most are foes. New Phytologist, 225, 1852–1872.

    Article  PubMed  Google Scholar 

  • Hossain, M. A., Kumar, V., Burritt, D. J., Fujita, M., & Mäkelä, P. (2019). Osmoprotectant-mediated abiotic stress tolerance in plants. In Proline Metabolism and Its Functions in Development and Stress Tolerance, pp. 41–72. Springer Nature.

  • Hosseinifard, M., Stefaniak, S., Ghorbani Javid, M., Soltani, E., Wojtyla, Ł, & Garnczarska, M. (2022). Contribution of exogenous proline to abiotic stresses tolerance in plants: A review. International Journal of Molecular Sciences, 23, 5186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, M.-Y., Huang, W.-D., Chou, H.-M., Chen, C.-C., Chang, Y.-T., & Yang, C.-M. (2014a). Herbivorous insects alter the chlorophyll metabolism of galls on host plants. Journal of Asia-Pacific Entomology, 17, 431–434.

    Article  CAS  Google Scholar 

  • Huang, M.-Y., Lin, K.-H., Yang, M.-M., Chou, H.-M., Yang, C.-M., & Chang, Y.-T. (2011). Chlorophyll fluorescence, spectral properties, and pigment composition of galls on leaves of Machilus thunbergii. International Journal of Plant Sciences, 172, 323–329.

    Article  CAS  Google Scholar 

  • Huang, M. Y., Huang, W. D., Chou, H. M., Lin, K. H., Chen, C. C., Chen, P. J., Chang, Y. T., & Yang, C. M. (2014b). Leaf-derived cecidomyiid galls are sinks in Machilus thunbergii (Lauraceae) leaves. Physiologia Plantarum, 152, 475–485.

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim, M. H., Jaafar, H. Z., Rahmat, A., & Rahman, Z. A. (2010). The relationship between phenolics and flavonoids production with total non structural carbohydrate and photosynthetic rate in Labisia pumila Benth. under high CO2 and nitrogen fertilization. Molecules, 16, 162–174.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kerpen, L., Niccolini, L., Licausi, F., van Dongen, J. T., & Weits, D. A. (2019). Hypoxic conditions in crown galls induce plant anaerobic responses that support tumor proliferation. Frontiers in Plant Science, 10, 56.

    Article  PubMed  PubMed Central  Google Scholar 

  • Khadhair, A.-H., & Hiruki, C. (1995). The molecular genetic relatedness of willow witches’-broom phytoplasma to the clover proliferation group. Proceedings of the Japan Academy, Series B, 71, 145–147.

    Article  Google Scholar 

  • Khajuria, C., Wang, H., Liu, X., Wheeler, S., Reese, J. C., El Bouhssini, M., Whitworth, R. J., & Chen, M.-S. (2013). Mobilization of lipids and fortification of cell wall and cuticle are important in host defense against Hessian fly. BMC Genomics, 14, 1–16.

    Article  Google Scholar 

  • Kmieć, K., Kot, I., Rubinowska, K., Górska-Drabik, E., Golan, K., & Sytykiewicz, H. (2022). The variation of selected physiological parameters in elm leaves (Ulmus glabra Huds.) infested by gall inducing aphids. Plants, 11, 244.

  • Kot, I., Sempruch, C., Rubinowska, K., & Michałek, W. (2020). Effect of Neuroterus quercusbaccarum (L.) galls on physiological and biochemical response of Quercus robur leaves. Bulletin of Entomological Research, 110, 34–43.

    Article  CAS  PubMed  Google Scholar 

  • Kume, A., Akitsu, T., & Nasahara, K. N. (2018). Why is chlorophyll b only used in light-harvesting systems? Journal of Plant Research, 131, 961–972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzovkina, Y. A., & Vietto, L. (2014). An update on the cultivar registration of Populus and Salix (Salicaceae). Skvortsovia, 1, 133–148.

    Google Scholar 

  • Lichtenthaler, H. K., & Wellburn, A. R. (1983). Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.

    Book  Google Scholar 

  • Liu, X., Bai, J., Huang, L., Zhu, L., Liu, X., Weng, N., Reese, J. C., Harris, M., Stuart, J. J., & Chen, M.-S. (2007). Gene expression of different wheat genotypes during attack by virulent and avirulent Hessian fly (Mayetiola destructor) larvae. Journal of Chemical Ecology, 33, 2171–2194.

    Article  CAS  PubMed  Google Scholar 

  • Maejima, K., Oshima, K., & Namba, S. (2014). Exploring the phytoplasmas, plant pathogenic bacteria. Journal of General Plant Pathology, 80, 210–221.

    Article  CAS  Google Scholar 

  • Meinhardt, L. W., Rincones, J., Bailey, B. A., Aime, M. C., Griffith, G. W., Zhang, D., & Pereira, G. A. (2008). Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao: What’s new from this old foe? Molecular Plant Pathology, 9(5), 577–588.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcone, C. (2014). Molecular biology and pathogenicity of phytoplasmas. Annals of Applied Biology, 165(2), 199–221.

    Article  CAS  Google Scholar 

  • Meikle, R. D., (1984). Willows and poplars of Great Britain and Ireland. Botanical Society of the British Isles.

  • Mukherjee, S., Lokesh, G., Aruna, A., Sharma, S., & Sahay, A. (2016). Studies on the foliar biochemical changes in the gall (Trioza fletcheri minor) infested tasar food plants Terminalia arjuna and Terminalia tomentosa. Journal of Entomology and Zoology Studies, 4, 154–158.

    Google Scholar 

  • Murata, N., Takahashi, S., Nishiyama, Y., & Allakhverdiev, S. I. (2007). Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1767, 414–421.

  • Nyman, T., Widmer, A., & Roininen, H. (2000). Evolution of gall morphology and host-plant relationships in willow-feeding sawflies (Hymenoptera: Tenthredinidae). Evolution, 54, 526–533.

    CAS  PubMed  Google Scholar 

  • Oliveira, D., Isaias, R., Fernandes, G., Ferreira, B., Carneiro, R., & Fuzaro, L. (2016). Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. Journal of Insect Physiology, 84, 103–113.

    Article  CAS  PubMed  Google Scholar 

  • Pandey, S., Fartyal, D., Agarwal, A., Shukla, T., James, D., Kaul, T., Negi, Y. K., Arora, S., & Reddy, M. K. (2017). Abiotic stress tolerance in plants: Myriad roles of ascorbate peroxidase. Frontiers in Plant Science, 8, 581.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pandey, S., & Singh, H. (2011). A simple, cost-effective method for leaf area estimation. Journal of Botany, 2011, 1–6.

    Article  Google Scholar 

  • Patankar, R., Starr, G., Mortazavi, B., Oberbauer, S. F., & Rosenblum, A. (2013). The effects of mite galling on the ecophysiology of two arctic willows. Arctic, Antarctic, and Alpine Research, 45, 99–106.

    Article  Google Scholar 

  • Plewa, M. J., Smith, S. R., & Wagner, E. D. (1991). Diethyldithiocarbamate suppresses the plant activation of aromatic amines into mutagens by inhibiting tobacco cell peroxidase. Mutation Research/fundamental and Molecular Mechanisms of Mutagenesis, 247, 57–64.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Salehi-Eskandari, B., Gahrouei, M. S., Boyd, R. S., Rajakaruna, N., & Ghasemi, R. (2022). Physiological responses to lead and PEG-simulated drought stress in metallicolous and non-metallicolous Matthiola (Brassicaceae) species from Iran. South African Journal of Botany, 150, 1011–1021.

    Article  CAS  Google Scholar 

  • Samsone, I., Andersone, U., & Ievinsh, G. (2011). Gall midge Rhabdophaga rosaria-induced rosette galls on Salix: Morphology, photochemistry of photosynthesis and defense enzyme activity. Environmental and Experimental Biology, 9, 29–36.

    Google Scholar 

  • Samsone, I., Andersone, U., & Ievinsh, G. (2012). Variable effect of arthropod-induced galls on photochemistry of photosynthesis, oxidative enzyme activity and ethylene production in tree leaf tissues. Environmental and Experimental Biology, 10, 15–26.

    Google Scholar 

  • Schultz, J. C., Edger, P. P., Body, M. J., & Appel, H. M. (2019). A galling insect activates plant reproductive programs during gall development. Scientific Reports, 9, 1–17.

    Article  CAS  Google Scholar 

  • Sergiev, I., Alexieva, V., & Karanov, E. (1997). Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Compt Rend Acad Bulg Sci, 51, 121–124.

    Google Scholar 

  • Shahryari, F., & Allahverdipour, T. (2018). “Candidatus Phytoplasma trifolii” related strain affecting Salix babylonica in Iran. Australasian Plant Disease Notes, 13, 1–3.

    Article  CAS  Google Scholar 

  • Sherin, G., Aswathi, K. R., & Puthur, J. T. (2022). Photosynthetic functions in plants subjected to stresses are positively influenced by priming. Plant Stress, 4, 100079.

  • Singh, M., Kumar, J., Singh, S., Singh, V. P., & Prasad, S. M. (2015). Roles of osmoprotectants in improving salinity and drought tolerance in plants: A review. Reviews in Environmental Science and Bio/technology, 14, 407–426.

    Article  CAS  Google Scholar 

  • Stone, G. N., & Schönrogge, K. (2003a). The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18, 512–522.

    Article  Google Scholar 

  • Stone, G. N., & Schönrogge, K. (2003b). The adaptive significance of insect gall morphology. Trends in Ecology & Evolution, 18, 512–522.

    Article  Google Scholar 

  • Takeda, S., Yoza, M., Amano, T., Ohshima, I., Hirano, T., Sato, M. H., Sakamoto, T., & Kimura, S. (2019). Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development. PLoS ONE, 14, e0223686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawfeek, N., Mahmoud, M. F., Hamdan, D. I., Sobeh, M., Farrag, N., Wink, M., & El-Shazly, A. M. (2021). Phytochemistry, pharmacology and medicinal uses of plants of the genus Salix: An updated review. Frontiers in Pharmacology, 12, 593856.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science, 151(1), 59–66.

    Article  CAS  Google Scholar 

  • Velioglu, Y., Mazza, G., Gao, L., & Oomah, B. (1998). Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. Journal of Agricultural and Food Chemistry, 46, 4113–4117.

    Article  CAS  Google Scholar 

  • Wanger, G. (1979). Content and vacuole/extra vacuole distribution of neutral sugars, free amino acids, and anthocyanins in protoplasts. Plant Physiology, 64, 88–93.

    Article  Google Scholar 

  • Weinstein, S. B., & Kuris, A. M. (2016). Independent origins of parasitism in Animalia. Biology Letters, 12, 20160324.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xue, C., Zhiguo, L., Li, D., Jiaodi, B., Mengjun, L., Zhihui, Z., Zihui, J., Weilin, G., & Jin, Z. (2018). Changing host photosynthetic, carbohydrate, and energy metabolisms play important roles in phytoplasma infection. Phytopathology, 108, 1067–1077.

    Article  CAS  PubMed  Google Scholar 

  • Yang, C., Yang, M., Huang, M., Hsu, J., & Jane, W. (2007). Life time deficiency of photosynthetic pigment-protein complexes CP1, A1, AB1, and AB2 in two cecidomyiid galls derived from Machilus thunbergii leaves. Photosynthetica, 45, 589–593.

    Article  CAS  Google Scholar 

  • Yang, X. H., Li, X. M., & Zhu, D. H. (2020). Alteration of free amino acid concentrations in insect galls induced by Andricus mukaigawae (Hymenoptera; Cynipidae). Ecological Entomology, 45, 945–954.

    Article  Google Scholar 

  • Yang, J., Song, J., & Jeong, B. R. (2022). Lighting from top and side enhances photosynthesis and plant performance by improving light usage efficiency. International Journal of Molecular Sciences, 23(5), 2448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, W., Jia, M., Zhang, G., Sun, J., Li, Q., Wang, X., Hua, J., & Luo, S. (2021). Up-regulation of phenylpropanoid biosynthesis system in peach species by peach aphids produces anthocyanins that protect the aphids against UVB and UVC radiation. Tree Physiology, 41(3), 428–443.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the Graduate School of University of Payame Noor for providing research facilities. We also thank our colleague, Mrs Z.Nasirian Jazi for contributing to the intellectual foundations for this research project.

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  1. Department of Biology, Payame Noor University, Tehran, Iran

    Behrooz Salehi-Eskandari & Shahla Kazemi Renani

  2. Department of Biology, Faculty of Science, Behbahan Khatam Alanbia University of Technology, Behbahan, Iran

    Shokoofeh Hajihashemi

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Salehi-Eskandari, B., Kazemi Renani, S. & Hajihashemi, S. Evaluation of physiological and morphological responses of Salix alba and Salix babylonica to witches’ broom gall. Eur J Plant Pathol (2024). https://doi.org/10.1007/s10658-024-02833-0

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