ADVANCES IN THE STUDY OF MITE GALLOGENESIS AND ITS COMPARISON WITH THE DEVELOPMENT OF INSECT-INDUCED GALLS

About authors:

Saint-Petersburg State University, Saint-Petersburg, Russia

Zoological Institute, Russian Academy of Sciences, Saint-Petersburg, Russia; Saint-Petersburg State University, Saint-Petersburg, Russia

Ondokuz Mayis University, Samsun, Turkiye

Acknowledgments:

The authors thank Gregory T. Sullivan of the University of Queensland for language editing assistance. The authors are also grateful to two reviewers for critical comments on the original version of the article.

This study was financially supported by the Russian Foundation for Basic Research (grant № 21-54-46003 СТ_а), the Scientific and Technological Research Council of Turkiye (TUBITAK, grant № 220N174) and the Zoological Institute of the Russian Academy of Sciences (project № 122031100263-1).

Annotation:

The present article reviews the main parasite–host model systems that have been used in recent studies in the molecular genetic analysis and in the investigation of the morpho-functional traits of mite gallogenesis on the leaves of angiosperms. The aforementioned works focused on the development of galls with a chamber, while other types of mite galls, including the most simply organized (erinea), remain virtually unstudied. Our article discusses the possible role of endosymbiotic bacteria in the induction of mite gallogenesis, as well as changes in the adaxial-abaxial polarity of the leaf and the expression of host plant genes during gallogenesis. The need for additional testing of the hypothesis regarding the participation of bacteria of the genera Wolbachia and Rhodococcus in the induction of gallogenesis is demonstrated. We have revealed certain convergent similarities in the gallogeneses induced by the grape phylloxera and by the gall mites. In particular, in both instances, the nutritive tissue is formed, the primary gall-inducing stimulus is produced by the feeding of females on young leaves, and the gall formations are accompanied by the abaxialization of the leaf. A review of the literature suggests that the Hearn’s hypothesis about the similarity of arthropod gallogenesis with the somatic embryogenesis of plants, as well as Wolpert’s embryological concept of the positional information in its classical form, are not appropriate for the modeling of gallogenesis. Finally, a new impetus for the study of gallogenesis could be provided by the studies that investigate the link between the genetic heterogeneity of different zones of the leaf blade and the developmental patterns of galls formed in these zones under the influence of plant parasites.

DOI: 10.21684/0132-8077-2024-32-1-43-57

Bibliography:

Álvarez, R., Ferreira, B. G., López, B., Martínez, J.-J.I., Boso, S. and Martínez, M.-C. 2021. Histological study of leaf galls induced by phylloxera in Vitis (Vitaceae) leaves. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 91 (1): 117–122. https://doi.org/10.1007/S40011-020-01206-X  

Anand, P. P. and Ramani, N. 2021a. Enzymatic characterization of the saliva of the eriophyid mite, Aceria pongamiae Keifer1966 (Acari: Eriophyidae) and the bacterial endobiome of the galls induced on Pongamia pinnata (L.) Pierre (Fabaceae). Naturwissenschaften, 108 (4): 33. https://doi.org/10.1007/s00114-021-01743-z

Anand, P. P. and Ramani, N. 2021b. Dynamics of limited neoplastic growth on Pongamia pinnata (L.) (Fabaceae) leaf, induced by Aceria pongamiae (Acari: Eriophyidae). BMC Plant Biology, 21: 1. https://doi.org/10.1186/s12870-020-02777-7

Arduin, M., Fernandes, G. W. and Kraus, J. E. 2005. Morphogenesis of galls induced by Baccharopelma dracunculifoliae (Hemiptera: Psyllidae) on Baccharis dracunculifolia (Asteraceae) leaves. Brazilian Journal of Biology, 65 (4): 559–571. https://doi.org/10.1590/s1519-69842005000400002

Bhatia, N., Runions, A. and Tsiantis, M. 2021. Leaf shape diversity: from genetic modules to computational models. Annual Review of Plant Biology, 72: 325–356. https://doi.org/10.1146/annurev-arplant-080720-101613

Bing, X.-L., Xia, C.-B., Ye, Q.-T., Gong, X., Cui, J.-R., Peng, C.-W. and Hong, X.-Y. 2023. Wolbachia manipulates reproduction of spider mites by influencing herbivore salivary proteins. Pest Management Science, 79 (1): 315–323. https://doi.org/10.1002/ps.7201

Cambier, S., Ginis, O., Moreau, S. J. M., Gayral, P., Hearn, J., Stone, G. N., Giron, D., Huguet, E. and Drezen, J.-M. 2019. Gall wasp transcriptomes unravel potential effectors involved in molecular dialogues with oak and rose. Frontiers in Physiology, 10: 926. https://doi.org/10.3389/fphys.2019.00926

Chetverikov, P. E. 2016. Generic delimitation between Fragariocoptes and Sierraphytoptus (Acari: Eriophyoidea: Phytoptidae) and a supplementary description of Fragariocoptes gansuensis with remarks on searching for mummified eriophyoid mites in herbaria under UV light. Zootaxa, 4066 (3): 271–290. https://doi.org/10.11646/zootaxa.4066.3.4

Chetverikov, P. E., Vishnyakov, A. E., Dodueva, I. E., Osipova, M.A., Sukhareva, S. I. and Shavarda, A.L. 2015. Gallogenesis induced by eriophyoid mites (Acariformes: Eriophyoidea). Entomological Review, 95 (8): 1137–1143. https://doi.org/10.1134/S0013873815080217

Chetverikov, P. E., Craemer, C., Cyrković, T., Klimov, P. B., Petanović, R. U., Romanovich, A. E., Sukhareva, S. I., Zukoff, S. N., Bolton, S. and Amrine, J. 2021. Molecular phylogeny of the phytoparasitic mite family Phytoptidae (Acariformes: Eriophyoidea) identified the female genitalic anatomy as a major macroevolutionary factor and revealed multiple origins of gall induction. Experimental and Applied Acarology, 83 (1): 31–68. https://doi.org/10.1007/s10493-020-00571-6

Conklin, P. A., Johnston, R., Conlon, B. R., Shimizu, R. and Scanlon, M. J. 2020. Plant homeodomain proteins provide a mechanism for how leaves grow wide. Development, 147 (20): dev193623. https://doi.org/10.1242/dev.193623

Corvalho-Fernandes, S. P., Ascendino, S., Maia, V. C. and Couri, M. S. 2016. Diversity of insect galls associated with coastal shrub vegetation in Rio de Janeiro, Brazil. Anais de Academia Brasileira de Ciências, 88 (3): 1407–1418. https://doi.org/10.1590/0001-3765201620150658

de Araújo, W. S., de Freitas, É. V. D., Kollár, J., Pessoa, R. O., Corgosinho, P. H. C., Valério, H. M., Falcão, L. A. D., Fagundes, M., Pimenta, M. A. S., de Faria, M. L., Martins, W. P. and Borges, M. A. Z. 2019. Host specialization in plant-galling interactions: contrasting mites and insects. Diversity, 11 (10): 180. https://doi.org/10.3390/d11100180

de Lillo, E. and Monfreda, R. 2004. ‘Salivary secretions’ of eriophyoids (Acari: Eriophyoidea): first results of an experimental model. Experimental and Applied Acarology, 34 (3–4): 291–306. https://doi.org/10.1007/s10493-004-0267-6 

de Lillo, E., Pozzebon, A., Valenzano, D. and Duso, C. 2018. An intimate relationship between eriophyoid mites and their host plants—a review. Frontiers in Plant Science, 9: 1786. https://doi.org/10.3389/fpls.2018.01786

Desnitskiy, A. G. and Chetverikov, P. E. 2022. Induction of leaf galls by four-legged mites (Eriophyoidea) as a problem of developmental biology. Russian Journal of Development Biology, 53 (1): 6–14. https://doi.org/10.1134/S1062360422010039

Desnitskiy, A. G., Chetverikov, P. E., Ivanova, L. A., Kuzmin, I .V., Ozman-Sullivan, S. K. and Sukhareva, S. I. 2023. Molecular aspects of gall formation induced by mites and insects. Life, 13: 1347. https://doi.org/10.3390/life13061347

Du, F., Guan, C. and Jiao, Y. 2018. Molecular mechanisms of leaf morphogenesis. Molecular Plant, 11 (9): 1117–1134. https://doi.org/10.1016/j.molp.2018.06.006

Elhiti, M. and Stasolla, C. 2022. Transduction of signals during somatic embryogenesis. Plants, 11: 178. https://doi.org/10.3390/plants11020178

Espírito-Santo, M. M. and Fernandes, G. W. 2007. How many species of gall-inducing insects are there on Earth, and where are they? Annals of the Entomological Society of America, 100 (2): 95–99. https://doi.org/10.1603/0013-8746(2007)100[95:HMSOGI]2.0.CO;2

Ferreira, B. G., Álvarez, R., Avritzer, S. C. and Isaias, R. M. S. 2017. Revisiting the histological patterns of storage tissues: beyond the limits of gallinducing taxa. Botany, 95 (2): 173–184. https://doi.org/10.1139/cjb-2016-0189

Ferreira, B. G., Álvarez, R., Bragança, G. P., Alvarenga, D. R., Pérez-Hidalgo, N. and Isaias, R. M. S. 2019. Feeding and other gall facets: patterns and determinants in gall structure. The Botanical Review, 85 (1): 78–106. https://doi.org/10.1007/s12229-019-09207-w

Freitas, M. S. C., Ferreira, B. G., Braganca, G. P. P., Boanares, D. and Isaias, R. M. S. 2023. Can the galling Eriophyidae (Trombidiformes) manipulate leaf structural and histochemical profiles over environmental stressors? Australian Journal of Botany, 71 (3): 146–156. https://doi.org/10.1071/BT22091

Gätjens-Boniche, O. 2019. The mechanism of plant gall induction by insects: revealing clues, facts, and consequences in a cross-kingdom complex interaction. Revista de Biologia Tropical, 67 (6): 1359–1382. https://doi.org/10.15517/rbt.v67i6.33984

Gätjens-Boniche, O., Jimenez-Madrigal, J. P., Whetten, R. W., Valenzuela-Diaz, S., AlemánGutiérrez, A., Hanson, P. E. and Pinto-Tomás A. A. 2023. Microbiome and plant cell transformation trigger insect gall induction in cassava. Frontiers in Plant Science, 14: 1237966. https://doi.org/10.3389/fpls.2023.1237966

Giron, D., Huguet, E., Stone, G. N. and Body, M. 2016. Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. Journal of Insect Physiology, 84: 70–89. https://doi.org/10.1016/j.jinsphys.2015.12.009

Guedes, L. M., Gavilán, E. and Aguilera, N. 2023. Do different gall induction organs and leaf microsites determine different structural profiles?: The case of Ophelimus migdanorum (Hymenoptera: Eulophidae) galls on Eucalyptus globulus (Myrtaceaae). South African Journal of Botany, 152: 11–18. https://doi.org/10.1016/j.sajb.2022.11.030

Guiguet, A., Ohshima, I., Takeda, S., Laurans, F., Lopez-Vaamonde, C. and Giron, D. 2019. Origin of gall-inducing from leaf-mining in Caloptilia micromoths (Lepidoptera, Gracillariidae). Scientific Reports, 9 (1): 6794. https://doi.org/10.1038/s41598-019-43213-7

Gupta, R. S., Patel, S., Saini, N. and Chen, S. 2020. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. International Journal of Systematic and Evolutionary Microbiology, 70(11): 5753–5798.  https://doi.org/10.1099/ijsem.0.004475

Hardy, N. B. and Cook, L. G. 2010. Gall-induction in insects: evolutionary dead-end or speciation driver? BMC Evolutionary Biology, 10: 257. https://doi.org/10.1186/1471-2148-10-257

Harris, M. O. and Pitzschke, A. 2020. Plants make galls to accommodate foreigners: some are friends, most are foes. New Phytologist, 225 (5): 1852–1872. https://doi.org/10.1111/nph.16340

Hearn, J., Blaxter, M., Schönrogge, K., Nieves-Aldrey, J.-L., Pujade-Villar, J., Huguet, E., Drezen, J.M., Shorthouse, J. D. and Stone, G. M. 2019. Genomic dissection of an extended phenotype: oak galling by a cynipid gall wasp. PLOS Genetics, 15 (11): e1008398. https://doi.org/10.1371/journal.pgen.1008398

Hesse, M. 1971 Über Mehrkernigkeit und Polyploidisierung der Nährgewebe einiger Milbengallen. Österreichische Botanische Zeitschrift, 119 (1-3): 74–93. https://doi.org/10.1007/BF01373110

Horstman, A., Bemer, M. and Boutilier, K. 2017. A transcriptional view on somatic embryogenesis. Regeneration, 4: 201–216. https://doi.org/10.1002/reg2.91

Isaias, R. M. S., Carneiro, R. G. S., Oliveira, D. C. and Santos, J. C. 2013. Illustrated and annotated checklist of Brazilian gall morphotypes. Neotropical Entomology, 42 (3): 230–239. https://doi.org/10.1007/s13744-013-0115-7

Jones, C. G., Lawton, J. H. and Shachak, M. 1994. Organisms as ecosystem engineers. Oikos, 69 (3): 373–386. https://doi.org/10.2307/3545850

Kaiser, W., Huguet, E., Casas, J., Commin, C. and Giron, D. 2010. Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proceedings of the Royal Society B, 277 (1692): 2311–2319. https://doi.org/10.1098/rspb.2010.0214

Kane, N. A., Jones, C. S. and Vuorisalo, T. 1997. Development of galls on leaves of Alnus glutinosa and Alnus incana (Betulaceae) caused by the eriophyid mite Eriophyes laevis (Nalepa). International Journal of Plant Sciences, 1589 (1): 13–23. https://doi.org/10.1086/297409

Kendall, J. 1930. The structure and development of certain eriophyid galls. Zeitschrift für Parasitenkunde, 2 (4): 477–501. https://doi.org/10.1007/BF02119368

Khan, F. S., Li, Z., Shi, P., Zhang, D., Htwe, Y. M., Yu, Q. and Wang, Y. 2023. Transcriptional regulations and hormonal signaling during somatic embryogenesis in the coconut tree: an insight. Forests, 14 (9):1800. https://doi.org/10.3390/f14091800

Kierzkowski, D., Runions, A., Vuolo, F., Strauss, S., Lymbouridou, R., Routier-Kierzkowska, A.-L., Wilson-Sánchez, D., Jenke, H., Galinha, C., Mosca, G., Zhang, Z., Canales, C., Dello Ioio, R., Huijser, P., Smith, R. S. and Tsiantis, M. 2019. A growth-based framework for leaf shape development and diversity. Cell, 177 (6): 1405–1418. https://doi.org/10.1016/j.cell.2019.05.011

Kishor, P. B. K., Hima Kumari, P., Sunita, M. S. L. and Sreenivasulu, N. 2015. Role of proline in cell wall synthesis and plant development and its implications in plant ontogeny. Frontiers in Plant Science, 6: 544. https://doi.org/10.3389/fpls.2015.00544

Klimov, P. B., Chetverikov, P. E., Dodueva, I. E., Vishnyakov, A. E., Bolton, S. J., Paponova, S. S., Lutova, L. A. and Tolstikov, A. V. 2022. Symbiotic bacteria of the gall-inducing mite Fragariocoptes setiger (Eriophyoidea) and phylogenomic resolution of the eriophyoid position among Acari. Scientific Reports, 12 (1): 3811. https://doi.org/10.1038/s41598-022-07535-3

Korgaonkar, A., Han, C., Lemire, A. L., Siwanowicz, I., Bennouna, D., Kopec, R. E., Andolfatto, P., Shigenobu, S. and Stern, D. L. 2021. A novel family of secreted insect proteins linked to plant gall development. Current Biology, 31 (9): 1836–1849. https://doi.org/10.1016/j.cub.2021.01.104

Lamb, K. P. 1953. Tomato gall mites from Morocco. Bulletin of Entomological Research, 44 (3): 401–404. https://doi.org/10.1017/S0007485300025499

Lu, Q., Chen, H., Zhang, J. Wang, W., Cui, Y. and Liu, J. 2023. A study on the effect of host plants on Chinese gallnut morphogenesis. PLoS ONE, 18 (3): e0283464. https://doi.org/10.1371/journal.pone.0283464

Lv, Z., Zhao, W., Kong, S., Li, L. and Lin, S. 2023. Overview of molecular mechanisms of plant leaf development: a systematic review. Frontiers in Plant Science, 14: 1293424. https://doi.org/10.3389/fpls.2023.1293424

Ma, Y., Yan, C., Li, H., Wu, W., Liu, Y., Wang, Y., Chen, Q. and Ma, H. 2017. Bioinformatics prediction and evolution analysis of arabinogalactan proteins in the plant kingdom. Frontiers in Plant Science, 8: 66. https://doi.org/10.3389/fpls.2017.00066

Mani, M. S. 1964. Ecology of Plant Galls. W. Junk Publishers, the Hague. 434 pp.

Manuela, D. and Xu, M. 2020. Patterning a leaf by establishing polarities. Frontiers in Plant Science, 11: 568730. https://doi.org/10.3389/fpls.2020.568730

Martinez, C. C., Li, S., Woodhouse, M. R., Sugimoto, K. and Sinha, N. R. 2021. Spatial transcriptional signatures define margin morphogenesis along the proximal–distal and medio-lateral axes in tomato (Solanum lycopersicum) leaves. Plant Cell, 33 (1): 44–65. https://doi.org/10.1093/plcell/koaa012

Martinson, E. O., Werren, J. H. and Egan, S. P. 2022. Tissue-specific gene expression shows a cynipid wasp repurposes oak host gene networks to create a complex and novel parasite-specific organ. Molecular Ecology, 31 (11): 3228–3240. https://doi.org/10.1111/mec.16159

Mashiguchi, K., Asami, T. and Suzuki, Y. 2009. Genome-wide identification, structure and expression studies, and mutant collection of 22 early nodulinlike protein genes in Arabidopsis. Bioscience, Biotechnology, and Biochemistry, 73 (11): 2452–2459. https://doi.org/10.1271/bbb.90407

Méndez-Hernández, H. A., Ledezma-Rodríguez, M., Avilez-Montalvo, R. N., Juárez-Gómez, Y. L., Skeete, A., Avilez-Montalvo, J., De-la-Peña, C. and Loyola-Vargas, V. M. 2019. Signaling overview of plant somatic embryogenesis. Frontiers in Plant Science, 10: 77. https://doi.org/10.3389/fpls.2019.00077

Miller, D. G. III and Raman, A. 2019. Host-plant relations of gall-inducing insects. Annals of the Entomological Society of America, 112 (1): 1–19. https://doi.org/10.1093/aesa/say034

Nabity, P. D., Haus, M. J., Berenbaum, M. R. and DeLucia, E. H. 2013. Leaf-galling phylloxera on grapes reprograms host metabolism and morphology. Proceedings of the National Academy of Sciences of the United States of America, 110 (41): 16663–16668. https://doi.org/10.1073/pnas.1220219110

Paponova, S. S., Chetverikov, P. E., Pautov, A. A., Yakovleva, O. V., Zukoff, S. N., Vishnyakov, A. E., Sukhareva, S. I., Krylova, E. G., Dodueva, I. E. and Lutova, L. A. 2018. Gall mite Fragariocoptes setiger (Eriophyoidea) changes leaf developmental program and regulates gene expression in the leaf tissues of Fragaria viridis (Rosaceae). Annals of Applied Biology, 172 (1): 33–46. https://doi.org/10.1111/aab.12399

Perrimon, N. and Bernfield, M. 2001. Cellular functions of proteoglycans—an overview. Seminars in Cell and Developmental Biology, 12: 65–67. https://doi.org/10.1006/scdb.2000.0237

Petanović, R. and Kielkiewicz, M. 2010. Plant–eriophyoid mite interactions: cellular biochemistry and metabolic responses induced in mite-injured plants. Part I. Experimental and Applied Acarology, 51 (13): 61–80. https://doi.org/10.1007/s10493-010-9351-2

Raman, A. 2011. Morphogenesis of insect-induced plant galls: facts and questions. Flora, 206 (6): 517–533. https://doi.org/10.1016/j.flora.2010.08.004

Raman, A. 2021. Gall-inducing insects and plants: the induction conundrum. Current Science, 120 (1): 66–78. https://doi.org/10.18520/cs/v120/i1/66-78 Rohfritsch, O. 2010. Genesis and development of dipterocecidia. Atti della Accademia Nazionale Italiana di Entomologia, Rendiconti, 58: 55–66.

Rohfritsch, O. and Shorthouse, J. D. 1982. Insect galls. In: G. Kahl and J. S. Schell (Eds.). Molecular Biology of Plant Tumors. Academic Press, New York, pp. 131–152.

Ronquist, F., Nieves-Aldrey, J.-L., Buffington, M. L., Liu, Z., Liljeblad, J. and Nylander, J. A. A. 2015. Phylogeny, evolution and classification of gall wasps: the plot thickens. PLoS ONE, 10 (5): e0123301. https://doi.org/10.1371/journal.pone.0123301

Rose, R. J. 2019. Somatic embryogenesis in the Medicago truncatula model: cellular and molecular mechanisms. Frontiers in Plant Science, 10: 267. https://doi.org/10.3389/fpls.2019.00267

Schleifer, K. H., Kilpper-Bälz, R. and Devriese, L. A. 1984. Staphylococcus arlettae sp. nov., S. equorum sp. nov. and S. k1oosii sp. nov.: three new coagulase-negative, novobiocin-resistant species from animals. Systematic and Applied Microbiology, 5 (4): 501–509. https://doi.org/10.1016/S0723-2020(84)80007-7

Schultz, J. C., Edger, P. P., Body, M. J. A. and Appel, H. M. 2019. A galling insect activates plant reproductive programs during gall development. Scientific Reports, 9 (1): 1833. https://doi.org/10.1038/s41598-018-38475-6

Seifert, G. J. and Roberts, K. 2007. The biology of arabinogalactan proteins. Annual Review of Plant Biology, 58: 137–161. https://doi.org/10.1146/annurev.arplant.58.032806.103801

Showalter, A. M. 2001. Arabinogalactan-proteins: structure, expression and function. Cellular and Molecular Life Sciences, 58 (10): 1399–1417. https://doi.org/10.1007/PL00000784

Sinnott, E. W. 1960. Plant Morphogenesis. McGrowHill Book Co., New York, Toronto, London. 550 pp.

Stern, D. L. and Han, C. 2022. Gene structure-based homology search identifies highly divergent putative effector gene family. Genome Biology and Evolution, 14 (6): evac069. https://doi.org/10.1093/gbe/evac069

Steward, F. C., Mapes, M. O. and Smith, J. 1958. Growth and organized development of cultured cells. I. Growth and division of freely suspended cells. American Journal of Botany, 45(9): 693–703. https://doi.org/10.2307/2439507

Stone, G. N., Schönrogge, K. 2003. The adaptive significance of insect gall morphology. Trends in Ecology and Evolution, 18 (10): 512–522. https://doi.org/10.1016/S0169-5347(03)00247-7

Strauss, S., Runions, A., Lane, B., Eschweiler, D., Bajpai, N, Trozzi, N., Routier-Kierzkowska, A.-L., Yoshida, S., Rodrigues da Silveira, S., Vijayan, A., Rachele Tofanelli, R., Majda, M., Echevin, E., Le Gloanec, C., Bertrand-Rakusova, H., Adibi, M., Schneitz, K., Bassel, G. W., Kierzkowski, D., Stegmaier, J., Tsiantis, M. and Smith, R. S. 2022. Using positional information to provide context for biological image analysis with MorphoGraphX 2.0. eLife, 11: e72601. https://doi.org/10.7554/eLife.72601

Takeda, S., Yoza, M., Amano, T., Ohshima, I., Hirano, T., Sato, M. H., Sakamoto, T. and Kimura, S. 2019. Comparative transcriptome analysis of galls from four different host plants suggests the molecular mechanism of gall development. PLoS One, 14 (10): e0223686. https://doi.org/10.1371/journal.pone.0223686

Takeda, S., Hirano, T., Ohshima, I. and Sato, M. H. 2021. Recent progress regarding the molecular aspects of insect gall formation. International Journal of Molecular Sciences, 22 (17): 9424. https://doi.org/10.3390/ijms22179424

Teixeira, C. T., Kuster, V. C., Carneiro, R. G. S., Cardoso, J. C. F. and Isaias, R. M. S. 2022. Anatomical profiles validate gall morphospecies under similar morphotypes. Journal of Plant Research, 135 (4): 593–608.  https://doi.org/10.1007/s10265-022-01397-6

Vargesson, N. 2020. Positional information—a concept underpinning our understanding of biology. Developmental Dynamics, 249 (3): 298–312. https://doi.org/10.1002/dvdy.116

Wells, B. W. 1921. Evolution of zoocecidia. Botanical Gazette, 71 (5): 358–377. https://www.jstor.org/stable/2470294

Westphal, E. 1982. Modification du pH vacuolaire des cellules épidermiques foliaires de Solanum dulcamara soumises á l’action d’un acarien cécidogène. Canadian Journal of Botany, 60 (12): 2882–2888. https://doi.org/10.1139/b82-348

Westphal, E. 1992. Cecidogenesis and resistance phenomena in mite-induced galls. In: J. Shorthouse and O. Rohfritsch (Eds.). Biology of Insect-Induced Galls. Oxford University Press, New York, pp. 141–156.

Westphal, E., Bronner, R. and Le Ret, M. 1981. Changes in leaves of susceptible and resistant Solanum dulcamara infested by the gall mite Eriophyes cladophthirus (Acarina, Eriophyoidea). Canadian Journal of Botany, 59 (5): 875–882. https://doi.org/10.1139/b81-122

Westphal, E. and Manson, D. C. M. 1996. Feeding effects on host plants: gall formation and other distortions. In: E. E. Lindquist, M. W. Sabelis and J. Bruin (Eds.). Eriophyoid Mites—Their Biology, Natural Enemies and Control. Elsevier, Amsterdam, pp. 231–242. https://doi.org/10.1016/S15724379(96)80014-5

Wolpert, L. 1969. Positional information and the spatial pattern of cellular differentiation. Journal of Theoretical Biology, 25 (1): 1–47. https://doi.org/10.1016/s0022-5193(69)80016-0

Wolpert, L. 1978. Pattern formation in biological development. Scientific American, 239 (4): 154–165. https://doi.org/10.1038/scientificamerican1078154

Wu, W., Du, K., Kang, X. and Wei, H. 2021. The diverse roles of cytokinins in regulating leaf development. Horticulture Research, 8 (1): 118. https://doi.org/10.1038/s41438-021-00558-3

Yamaguchi, T., Nukazuka, A., Tsukaya, H. 2012. Leaf adaxial–abaxial polarity specification and lamina outgrowth: evolution and development. Plant and Cell Physiology, 53 (7): 1180–1194. https://doi.org/10.1093/pcp/pcs074

Yang, M., Li, H., Qiao. H., Guo, K., Xu, R., Wei, H., Wei, J., Liu, S. and Xu, C. 2023. Integrated transcriptome and metabolome dynamic analysis of galls induced by the gall mite Aceria pallida on Lycium barbarum reveals the molecular mechanism underlying gall formation and development. International Journal of Molecular Sciences, 24(12): 9839. https://doi.org/10.3390/ijms24129839

Zhang, H., Guiguet, A., Dubreuil, G., Kisiala, A., Andreas, P., Neil Emery, R. J., Huguet, E., Body, M. and Giron, D. 2017. Dynamics and origin of cytokinins involved in plant manipulation by a leafmining insect. Insect Science, 24 (6): 1065–1078. https://doi.org/10.1111/1744-7917.12500

Zimmerman, J. L. 1993. Somatic embryogenesis: A model for early development in higher plants. Plant Cell, 5 (10): 1411–1423. https://doi.org/10.1105/tpc.5.10.1411