Anatomical Changes during Chestnut (Castanea mollissima BL.) Gall Development Stages Induced by the Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae)
Abstract
:1. Introduction
2. Results
2.1. Observations of Gall Morphological Characteristics
2.2. Microscopic Observations of Galls
2.2.1. Anatomical Observations with Stereomicroscope
2.2.2. Paraffin Section Safranin O/Fast Green, Periodic Acid–Schiff, and Reactive Oxygen Species Accumulation Stainings
Safranin O/Fast Green and Periodic Acid–Schiff Stainings
Staining for Reactive Oxygen Species Accumulation
2.2.3. Scanning Electron Microscopy (SEM)
3. Discussion
3.1. External Morphological Characteristics of Chestnut Galls and Development of GWDK
3.2. Microscopic Observation of Internal Gall Structure
3.3. Effects of Gall on Host Organ Structure
4. Materials and Methods
4.1. Materials
4.2. Methods
4.2.1. Observations of Gall Morphology
4.2.2. Observations of Gall Structure
4.2.3. Staining for Reactive Oxygen Species (ROS) Accumulation in Frozen Sections
4.2.4. Scanning Electron Microscope (SEM) Observations
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Reale, L.; Tedeschini, E.; Rondoni, G.; Ricci, C.; Bin, F.; Frenguelli, G.; Ferranti, F. Histological investigation on gall development induced by a worldwide invasive pest, Dryocosmus kuriphilus, on Castanea sativa. Plant Biosyst.-Int. J. Deal. All Asp. Plant Biol. 2016, 150, 35–42. [Google Scholar]
- Mani, M.S. Ecology of Plant Galls; Springer: Dordrecht, The Netherlands, 1964. [Google Scholar]
- Stone, G.N.; Schönrogge, K. The adaptive significance of insect gall morphology. Trends Ecol. Evol. 2003, 18, 512–522. [Google Scholar] [CrossRef]
- Price, P.W.; Fernandes, G.W.; Waring, G.L. Adaptive nature of insect galls. Environ. Entomol. 1987, 16, 15–24. [Google Scholar] [CrossRef]
- Jara-Chiquito, J.L.; Pujade-Villar, J.; Ferreira, B.G.; Álvarez, R. Histological changes induced by the cynipid wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae) in leaves of the chestnut Castanea sativa (Fagaceae): Mechanisms of galling impact on host vigor. Arthropod-Plant Interact. 2021, 15, 223–233. [Google Scholar] [CrossRef]
- Zhou, J.Y.; Liu, L.; Mao, A.N. Analysis on the influence of cultivation factors on the occurrence of chestnut blight. Jiangsu For. Technol. 1998, 4, 45–48. [Google Scholar]
- Harper, L.J.; Schönrogge, K.; Lim, K.Y.; Francis, P.; Lichtenstein, C.P. Cynipid galls: Insect-induced modifications of plant development create novel plant organs. Plant Cell Environ. 2004, 27, 327–335. [Google Scholar] [CrossRef]
- Wang, S.F.; Tang, Z.Z.; Yan, Y. Development and structure of wasp gall of Quadrastichus erythrinae. For. Sci. 2015, 51, 165–170. [Google Scholar]
- Cambier, S.; Ginis, O.; Moreau, S. Gall wasp transcriptomes unravel potential efectors involved in molecular dialogues with oak and rose. Front. Physiol. 2019, 10, 9–26. [Google Scholar] [CrossRef]
- Isaias, R.; Ferreira, B.; Alvarenga, D.; Barbosa, L.; Salminen, J.; Steinbauer, M. Functional compartmentalisation of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Austral Entomol. 2018, 57, 238–246. [Google Scholar] [CrossRef]
- Otake, A. Chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae): Analyses of records on cell contents inside galls and on emergence of wasps and parasitoids outside galls. Appl. Entomol. Zool. 1989, 24, 193–201. [Google Scholar] [CrossRef]
- Kajiura, M. The breeding of new varieties of Japanese chestnut resistant to chestnut gall wasp (Dryocosmus kuriphilus Yasumatsu. In Proceedings of the 14th International Horticultural Congress, The Hague-Scheveningen, The Netherlands, 29 August–6 September 1955; pp. 1243–1249. [Google Scholar]
- Hartley, S.E. The chemical composition of plant galls: Are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 1998, 113, 492–501. [Google Scholar] [CrossRef] [PubMed]
- Morris, D.C.; Schwarz, M.P.; Cooper, S.J.; Mound, L.A. Phylogenetics of Australian Acacia thrips: The evolution of behaviour and ecology. Mol. Phylogenetics Evol. 2002, 25, 278–292. [Google Scholar] [CrossRef] [PubMed]
- Van Veen, F.J.F.; Muller, C.B.; Adriaanse, I.C.T.; Godfray, H.C.J. Spatial heterogeneity in risk of secondary parasitism in a natural population of an aphid parasitoid. J. Anim. Ecol. 2002, 71, 463–469. [Google Scholar] [CrossRef]
- Vårdal, H. From Parasitoids to Gall Inducers and Inquilines: Morphological Evolution in Cynipoid Wasps. PhD Thesis, Acta Universitatis Upsaliensis, Uppsala, Sweden, 2004. [Google Scholar]
- Nakagaki, S.; Sekiguchi, K. Biology and control of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu, with special reference to the difference between the gall wasp on the susceptible varieties of chestnut trees and that on the resistant varieties. Bull. Ibaraki-Ken Hortic. Exp. Stn. 1976, 6, 33–64. [Google Scholar]
- Kato, K.; Hijii, N. Ovipositional traits of the chestnut gall wasp, Dryocosmus kuriphilus(Hymenoptera: Cynipidae). Entomol. Sci. 2001, 4, 295–299. [Google Scholar]
- Liang, G.H.; Deng, C.Y.; Ling, L. Relationship between leaf characteristics of Quadrastichus erythrinae and its resistance to Quadrastichus erythrinae. J. Trop. Crops 2012, 33, 545–550. [Google Scholar]
- Ding, Y.Z.; Bi, S.D.; Fang, G.F. Study on the relationship between the gall formation, development and occurrence amount of galls in chestnut galls. J. Appl. Ecol. 2004, 15, 108–110. [Google Scholar]
- Wang, G.Y. Biology of Gall Causing and Its Influence on the Growth and Development of Host Plants in Chestnut Gall Wasp; Zhejiang A & F University: Hangzhou, China, 2010. [Google Scholar]
- Guo, S.J.; Qu, A.J.; Sun, W. Preliminary study on Parasitoids of chestnut gall wasp. For. Sci. 1997, 3, 242–246. [Google Scholar]
- Chun, F.J.; Zhi, Q.L. The peculiar insect galls. Kunchong Zhishi 2004, 41, 603–606. [Google Scholar]
- Yang, M.M. The evolution and biology of Gall insect. Classif. Evol. Semin. Trib. Insect 1999, 4, 113–125. [Google Scholar]
- Crespi, B.; Worobey, M. Comparative analysis of gall morphology in Australian gall thrips: The evolution of extended phenotypes. Evolution 1998, 52, 1686–1696. [Google Scholar] [CrossRef]
- Hawkins, B.A.; Lawton, J.H. Species richness for parasitoids of British phytophagous insects. Nature 1987, 326, 788–790. [Google Scholar] [CrossRef]
- Ma, S.M.; Yu, H.; Li, C.C. Plant gall. Insect Knowl. 2008, 45, 330–335. [Google Scholar]
- Ferreira, B.G.; Dos Santos Isaias, R.M. Floral-like destiny induced by a galling Cecidomyiidae on the axillary buds of Marcetia taxifolia (Melastomataceae). Flora-Morphol. Distrib. Funct. Ecol. Plants 2014, 209, 391–400. [Google Scholar] [CrossRef]
- Oliveira, D.C.; Isaias, R.M.S.; Fernandes, G.W.; Ferreira, B.G.; Carneiro, R.G.S.; Fuzaro, L. Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J. Insect Physiol. 2016, 84, 103–113. [Google Scholar] [CrossRef]
- Ferreira, B.G.; Álvarez, R.; Bragança, G.P.; Alvarenga, D.R.; Pérez-Hidalgo, N.; Isaias, R.M. Feeding and other gall facets: Patterns and determinants in gall structure. Bot. Rev. 2019, 85, 78–106. [Google Scholar] [CrossRef]
- Nobrega, L.P.; Silva, J.B.; De Luna, B.N.; Ferreira, B.G. Modulation of anatomical adaptations of leaves of Avicennia schaueriana (Acanthaceae) by a galling Meunieriella (Cecidomyiidae). Flora 2021, 274, 151750. [Google Scholar] [CrossRef]
- Warmund, M.R. Dryocosmus kuriphilus-induced chestnut galls and their inhabitants. HortScience 2013, 48, 969–974. [Google Scholar] [CrossRef]
- Cooper, W.R.; Rieske, L.K. Gall structure affects ecological associations of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Environ. Entomol. 2010, 39, 787–797. [Google Scholar] [CrossRef]
- Ferreira, B.G.; Álvarez, R.; Avritzer, S.C.; Isaias, R.M. Revisiting the histological patterns of storage tissues: Beyond the limits of gall-inducing taxa. Botany 2017, 95, 173–184. [Google Scholar] [CrossRef]
- Lin, H.T.; Xi, Y.F.; Chen, S.J. A review of enzymatic browning in fruit during storage. J. Fuzhou Univ. 2002, 30, 696–703. [Google Scholar]
- Zhang, X.; Dong, F.C.; Song, C.P. Oxidative burst and H2O2 signal transduction in plant cells. Plant Physiol. Commun. 2000, 36, 376–381. [Google Scholar]
- Mandal, S.; Mitra, A.; Mallick, N. Biochemical characterization of oxidative burst during interaction between Solanum lycopersicum and Fusarium oxysporum f. sp. lycopersici. Physiol. Mol. Plant Pathol. 2008, 72, 56–61. [Google Scholar] [CrossRef]
- Doke, N. Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol. Plant Pathol. 1983, 23, 345–357. [Google Scholar] [CrossRef]
- Bragança, G.P.P.; Freitas, M.D.S.C.; Isaias, R.M.D.S. The influence of gall position over xylem features in leaflets of Inga ingoides (Rich.) Willd.(Fabaceae: Caesalpinioideae). Trees 2021, 35, 199–209. [Google Scholar] [CrossRef]
- Hu, Q.Q.; Huang, J.H.; Ling, X.J. Observation of gall structure and development of Asphondylia sp. leaf gall mosquitoes. J. Trop. Crops 2012, 33, 2035–2039. [Google Scholar]
- Zhu, C.; Wang, W.; Chen, Y.; Zhao, Y.; Zhang, S.; Shi, F.; Nieuwenhuizen, N.J. Transcriptomics and antioxidant analysis of two chinese chestnut (Castanea mollissima BL.) varieties provides new insights into the mechanisms of resistance to gall wasp Dryocosmus kuriphilus infestation). Front. Plant Sci. 2022, 13, 874434. [Google Scholar] [CrossRef]
- Bai, X.; Zhang, S.; Wang, W.; Chen, Y.; Zhao, Y.; Shi, F.; Zhu, C. Genetic Relationships of 118 Castanea Specific Germplasms and Construction of Their Molecular ID Based on Morphological Characteristics and SSR Markers. Plants 2023, 12, 1438. [Google Scholar] [CrossRef]
- Matsui, S.; Torikata, H. Studies on the resistance of chestnut trees to chestnut gall wasp. II. The resistance of trees to gall wasp and the histochemistry of the chestnut buds. Engei Gakkai Zasshi J. Jpn. Soc. Hortic. Sci. 1970, 39, 44–54. [Google Scholar] [CrossRef]
- Álvarez, R.; Encina, A.; Hidalgo, N.P. Histological aspects of three Pistacia terebinthus galls induced by three different aphids: Paracletus cimiciformis, Forda marginata and Forda formicaria. Plant Sci. 2009, 176, 303–314. [Google Scholar] [CrossRef]
- Pan, L.L.; Zhu, C.; Mei, Y. Comparison of fungal fluorescence staining and PAS staining in pathological diagnosis of pulmonary cryptococcosis. Chin. J. Mycol. 2023, 18, 229–231. [Google Scholar]
- Borowiec, N.; Thaon, M.; Brancaccio, L.; Warot, S.; Vercken, E.; Fauvergue, X.; Malausa, J.C. Classical biological control against the chestnut gall wasp ‘Dryocosmus kuriphilus’ (Hymenoptera, Cynipidae) in France. Plant Prot. Q. 2014, 29, 7–10. [Google Scholar]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wang, C.; Wang, W.; Zhang, S.; Chen, Y.; Zhao, Y.; Zhu, C. Anatomical Changes during Chestnut (Castanea mollissima BL.) Gall Development Stages Induced by the Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Plants 2024, 13, 1766. https://doi.org/10.3390/plants13131766
Wang C, Wang W, Zhang S, Chen Y, Zhao Y, Zhu C. Anatomical Changes during Chestnut (Castanea mollissima BL.) Gall Development Stages Induced by the Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Plants. 2024; 13(13):1766. https://doi.org/10.3390/plants13131766
Chicago/Turabian StyleWang, Cheng, Wu Wang, Shijie Zhang, Yu Chen, Yuqiang Zhao, and Cancan Zhu. 2024. "Anatomical Changes during Chestnut (Castanea mollissima BL.) Gall Development Stages Induced by the Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae)" Plants 13, no. 13: 1766. https://doi.org/10.3390/plants13131766
APA StyleWang, C., Wang, W., Zhang, S., Chen, Y., Zhao, Y., & Zhu, C. (2024). Anatomical Changes during Chestnut (Castanea mollissima BL.) Gall Development Stages Induced by the Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Plants, 13(13), 1766. https://doi.org/10.3390/plants13131766