{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T00:56:53Z","timestamp":1760057813004,"version":"build-2065373602"},"reference-count":45,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2025,2,26]],"date-time":"2025-02-26T00:00:00Z","timestamp":1740528000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Pistacia palaestina hosts several Fordini gall-forming aphid species, which manipulate its anatomy and metabolism, creating galls that provide nutrients and protection. This study compared the extended metabolic profiles of P. palaestina leaves and galls induced by Baizongia pistaciae, Paracletus cimiciformis, and Geoica spp. GC\u2013MS analysis of ethyl acetate (EtOAc) and methanol (MeOH) extracts revealed a high abundance of shikimic acid and quinic acid isomers, along with diverse hydrocarbons, lipids, terpenoids, phenolics, and carbohydrates, each showing distinct distributions across gall types. Paracletus\u00a0cimiciformis galls closely resembled intact leaves, exhibiting limited metabolic disruption. In contrast, the larger, more complex galls of Baizongia and Geoica underwent profound metabolic modifications. These aphids manipulate host metabolism, leading to triterpenoid and phenolics accumulation, which likely fortifies gall structure and enhances chemical defense. The considerable variation among individual trees suggests that specific host plant templates significantly influence the metabolic profile of the galls.<\/jats:p>","DOI":"10.3390\/plants14050721","type":"journal-article","created":{"date-parts":[[2025,2,27]],"date-time":"2025-02-27T08:04:44Z","timestamp":1740643484000},"page":"721","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Association Between Gall Structural and Metabolic Complexity: Evidence from Pistacia palaestina"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3225-3067","authenticated-orcid":false,"given":"Daniela","family":"Batovska","sequence":"first","affiliation":[{"name":"Institute of Chemical Engineering, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., Bl. 103, 1113 Sofia, Bulgaria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mirena","family":"Chakarova","sequence":"additional","affiliation":[{"name":"Institute of Chemical Engineering, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., Bl. 103, 1113 Sofia, Bulgaria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Monica","family":"Dines","sequence":"additional","affiliation":[{"name":"Department of Evolutionary and Environmental Biology, University of Haifa, Haifa 3498838, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0276-4170","authenticated-orcid":false,"given":"Ivayla","family":"Dincheva","sequence":"additional","affiliation":[{"name":"Department of Agrobiotechnologies, Agrobioinstitute, Agricultural Academy, 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3964-6039","authenticated-orcid":false,"given":"Ilian","family":"Badjakov","sequence":"additional","affiliation":[{"name":"Department of Agrobiotechnologies, Agrobioinstitute, Agricultural Academy, 8 Dragan Tsankov Blvd., 1164 Sofia, Bulgaria"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Moshe","family":"Inbar","sequence":"additional","affiliation":[{"name":"Department of Evolutionary and Environmental Biology, University of Haifa, Haifa 3498838, Israel"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,2,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"109","DOI":"10.2307\/3545732","article-title":"Phloem-Feeding Specialists Sharing a Host Tree: Resource Partitioning Minimizes Interference Competition among Galling Aphid Species","volume":"73","author":"Inbar","year":"1995","journal-title":"Oikos"},{"key":"ref_2","first-page":"591","article-title":"Aphid-Induced Galls on Pistacia in the Natural Mediterranean Forest of Israel: Which, Where, and How Many?","volume":"41","author":"Wool","year":"2013","journal-title":"Israel J. Zool."},{"key":"ref_3","first-page":"1359","article-title":"The Mechanism of Plant Gall Induction by Insects: Revealing Clues, Facts, and Consequences in a Cross-Kingdom Complex Interaction","volume":"67","year":"2019","journal-title":"Rev. Biol. Trop."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1836","DOI":"10.1016\/j.cub.2021.01.104","article-title":"A Novel Family of Secreted Insect Proteins Linked to Plant Gall Development","volume":"31","author":"Korgaonkar","year":"2021","journal-title":"Curr. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1016\/j.ympev.2004.01.006","article-title":"The Evolution of Host Plant Manipulation by Insects: Molecular and Ecological Evidence from Gall-Forming Aphids on Pistacia","volume":"32","author":"Inbar","year":"2004","journal-title":"Mol. Phylogenet. Evol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Rost\u00e1s, M., Maag, D., Ikegami, M., and Inbar, M. (2013). Gall Volatiles Defend Aphids Against a Browsing Mammal. BMC Evol. Biol., 13.","DOI":"10.1186\/1471-2148-13-193"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1021\/jf034773t","article-title":"Composition of the Essential Oil of Leaves, Galls, and Ripe and Unripe Fruits of Jordanian Pistacia palaestina Boiss","volume":"52","author":"Flamini","year":"2004","journal-title":"J. Agric. Food Chem."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1007\/s10886-014-0462-9","article-title":"The Mono- and Sesquiterpene Content of Aphid-Induced Galls on Pistacia palaestina is Not a Simple Reflection of Their Composition in Intact Leaves","volume":"40","author":"Rand","year":"2014","journal-title":"J. Chem. Ecol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1016\/0031-9422(79)80046-1","article-title":"Triterpenes from the Galls of Pistacia palestina","volume":"18","author":"Caputo","year":"1979","journal-title":"Phytochemistry"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1007\/s10886-016-0817-5","article-title":"Differences in Monoterpene Biosynthesis and Accumulation in Pistacia palaestina Leaves and Aphid-Induced Galls","volume":"43","author":"Rand","year":"2017","journal-title":"J. Chem. Ecol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1093\/jxb\/erab289","article-title":"Transcriptional Up-Regulation of Host-Specific Terpene Metabolism in Aphid-Induced Galls of Pistacia palaestina","volume":"73","author":"Bar","year":"2022","journal-title":"J. Exp. Bot."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e23702","DOI":"10.1002\/chir.23702","article-title":"Chiral Chemopolymorphism in the Monoterpenes of Pistacia palaestina Leaves and Galls","volume":"36","author":"Bar","year":"2024","journal-title":"Chirality"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1007\/s11829-009-9081-8","article-title":"Anti-Insect Effects of the Gall Wall of Baizongia pistaciae [L.], a Gall-Inducing Aphid on Pistacia palaestina Boiss","volume":"4","author":"Martinez","year":"2010","journal-title":"Arthropod Plant Interact."},{"key":"ref_14","first-page":"287","article-title":"The Potential of Visual and Olfactory Signals in Gall Defence","volume":"86","author":"Inbar","year":"2024","journal-title":"Indian J. Entomol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2008","DOI":"10.4161\/psb.6.12.18031","article-title":"Distinct Antimicrobial Activities in Aphid Galls on Pistacia atlantica","volume":"6","author":"Gerchman","year":"2011","journal-title":"Plant Signal. Behav."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/j.biopha.2017.10.111","article-title":"The Relevance of Folkloric Usage of Plant Galls as Medicines: Finding the Scientific Rationale","volume":"97","author":"Patel","year":"2018","journal-title":"Biomed. Pharmacother."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"285","DOI":"10.14450\/2318-9312.v35.e3.a2023.pp285-331","article-title":"A Review of the Phytochemical Properties and Pharmacological Uses of the Genus Pistacia L. (Anacardiaceae)","volume":"35","author":"Crutcher","year":"2023","journal-title":"Infarma"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Xiong, W., Liao, L., Ni, Y., Gao, H., Yang, J., and Guo, Y. (2023). The Effects of Epicuticular Wax on Anthracnose Resistance of Sorghum bicolor. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24043070"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Mamgain, J., Mujib, A., Bansal, Y., Gulzar, B., Zafar, N., Syeed, R., Alsughayyir, A., and Dewir, Y.H. (2023). Elicitation Induced \u03b1-Amyrin Synthesis in Tylophora indica In Vitro Cultures and Comparative Phytochemical Analyses of In Vivo and Micropropagated Plants. Plants, 13.","DOI":"10.3390\/plants13010122"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"115193","DOI":"10.1016\/j.fct.2024.115193","article-title":"Exploring the Therapeutic Potential of Lupeol: A Review of its Mechanisms, Clinical Applications, and Advances in Bioavailability Enhancement","volume":"196","author":"Luo","year":"2025","journal-title":"Food Chem. Toxicol."},{"key":"ref_21","first-page":"103","article-title":"Fatty Acid Composition of Stems, Leaves, Flowers, and Seeds of Some Medicinal Plants","volume":"100","author":"Kokten","year":"2023","journal-title":"Riv. Ital. Sostanze Grasse"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Podell, S., and Gribskov, M. (2004). Predicting N-Terminal Myristoylation Sites in Plant Proteins. BMC Genom., 5.","DOI":"10.1186\/1471-2164-5-37"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Hamrouni, H., Othman, K.B., Benmoussa, H., Idoudi, S., Najjaa, H., Neffati, M., and Elfalleh, W. (2023). Chemical Composition and Diversity in Medicinal Plants. Chem. Biodivers., 20.","DOI":"10.1002\/cbdv.202300265"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"22572","DOI":"10.1074\/jbc.M116.754689","article-title":"Identification of the Plant Ribokinase and Discovery of a Role for Arabidopsis Ribokinase in Nucleoside Metabolism","volume":"291","author":"Riggs","year":"2016","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Campos-Garc\u00eda, T., Hern\u00e1ndez-Soltero, M.F., Hern\u00e1ndez-Fern\u00e1ndez, O.B., V\u00e1zquez-Mart\u00ednez, J., and Garc\u00eda-Morales, S. (2025). Selenium Nanoparticles Induce Differential Shoot\/Root Response of Capsicum annuum Seedlings Revealed by Non-Targeted Metabolomic Analysis. Plant Nano Biol., 11.","DOI":"10.1016\/j.plana.2025.100139"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1619","DOI":"10.1111\/ppl.13353","article-title":"Myo-Inositol Transport and Metabolism Participate in Salt Tolerance of Halophyte Ice Plant Seedlings","volume":"172","author":"Li","year":"2021","journal-title":"Physiol. Plant."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Cui, Y.N., Yan, S.J., Zhang, Y.N., Wang, R., Song, L.L., Ma, Y., Guo, H., and Yang, P.Z. (2024). Physiological, Metabolome and Gene Expression Analyses Reveal the Accumulation and Biosynthesis Pathways of Soluble Sugars and Amino Acids in Sweet Sorghum under Osmotic Stresses. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25168942"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/B978-0-12-819483-6.00012-6","article-title":"Chapter 12\u2014Triterpenoids: Structural Diversity, Biosynthetic Pathway, and Bioactivity","volume":"Volume 67","year":"2020","journal-title":"Studies in Natural Products Chemistry"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Kurzfeld-Zexer, L., and Inbar, M. (2021). Gall-Forming Aphids Are Protected (and Benefit) from Defoliating Caterpillars: The Role of Plant-Mediated Mechanisms. BMC Ecol. Evol., 21.","DOI":"10.1186\/s12862-021-01861-2"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Parra-Rivero, O., Barros, M.P., Prado, M.D.M., Gil, J.V., Hornero-M\u00e9ndez, D., Zacar\u00edas, L., Rodrigo, M.J., Lim\u00f3n, M.C., and Avalos, J. (2020). Neurosporaxanthin Overproduction by Fusarium fujikuroi and Evaluation of Its Antioxidant Properties. Antioxidants, 9.","DOI":"10.3390\/antiox9060528"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Sandmann, G. (2019). Antioxidant Protection from UV- and Light-Stress Related to Carotenoid Structures. Antioxidants, 8.","DOI":"10.3390\/antiox8070219"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Wro\u0144ska, N., Szlaur, M., Zawadzka, K., and Lisowska, K. (2022). The Synergistic Effect of Triterpenoids and Flavonoids\u2014New Approaches for Treating Bacterial Infections?. Molecules, 27.","DOI":"10.3390\/molecules27030847"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/j.plaphy.2017.07.024","article-title":"Role of Phenolic Compounds During Antioxidative Responses of Winter Triticale to Aphid and Beetle Attack","volume":"118","author":"Czerniewicz","year":"2017","journal-title":"Plant Physiol. Biochem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.bse.2014.02.016","article-title":"The Role of Phenolics in the Control of Auxin in galls of Piptadenia gonoacantha (Mart.) MacBr (Fabaceae: Mimosoideae)","volume":"55","author":"Bedetti","year":"2014","journal-title":"Biochem. Syst. Ecol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Lone, R., Shuab, R., and Kamili, A. (2020). Role of Phenolic Compounds in Plant-Defensive Mechanisms. Plant Phenolics in Sustainable Agriculture, Springer.","DOI":"10.1007\/978-981-15-4890-1"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Ferreira, B.G., Oliveira, D.C., Moreira, A.S., Faria, A.P., Guedes, L.M., Fran\u00e7a, M.G., \u00c1lvarez, R., and Isaias, R.M. (2018). Antioxidant Metabolism in Galls Due to the Extended Phenotypes of the Associated Organisms. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0205364"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Bae, J., Kim, N., Shin, Y., Kim, S.-Y., and Kim, Y.-J. (2020). Activity of Catechins and Their Applications. Biomed. Dermatol., 4.","DOI":"10.1186\/s41702-020-0057-8"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"139","DOI":"10.4103\/2221-1691.374230","article-title":"Natural Sources, Biosynthesis, Biological Functions, and Molecular Mechanisms of Shikimic Acid and Its Derivatives","volume":"13","author":"Gandhi","year":"2023","journal-title":"Asian Pac. J. Trop. Biomed."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1007\/s11295-008-0150-4","article-title":"Phenotypic Plasticity and Gene Diversity in Pistacia lentiscus L. Along Environmental Gradients in Israel","volume":"4","author":"Nahum","year":"2008","journal-title":"Tree Genet. Genomes"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Schultz, J.C., Edger, P.P., Body, M.J., and Appel, H.M.A. (2019). Galling Insect Activates Plant Reproductive Programs During Gall Development. Sci. Rep., 9.","DOI":"10.1038\/s41598-018-38475-6"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1111\/plb.12475","article-title":"Contribution of Gall Microscopic Structure to Taxonomy of Gallicolous Aphids on Pistacia","volume":"18","author":"Martinez","year":"2016","journal-title":"Plant Biol."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Batovska, D., and Inbar, M. (2024). Beyond the Nut: Pistacia Leaves as Natural Food Preservatives. Foods, 13.","DOI":"10.3390\/foods13193138"},{"key":"ref_43","unstructured":"(2008). NIST Standard Reference Database 1A: NIST\/EPA\/NIH Mass Spectral Library (NIST 08) and NIST Mass Spectral Search Program (Version 20f) Manual (Standard No. NIST08)."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1007\/s11306-010-0198-7","article-title":"Decision Tree-Supported Substructure Prediction of Metabolites from GC-MS Profiles","volume":"6","author":"Hummel","year":"2010","journal-title":"J. Metabolomics"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Dincheva, I., Badjakov, I., Georgiev, V., Semerdjieva, I., Vrancheva, R., Ivanov, I., and Pavlov, A. (2025). Comprehensive GC-MS Characterization and Histochemical Assessment of Various Parts of Three Colchicum Species from Bulgarian Flora. Plants, 14.","DOI":"10.3390\/plants14020270"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/14\/5\/721\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T16:43:35Z","timestamp":1760028215000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/14\/5\/721"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,2,26]]},"references-count":45,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,3]]}},"alternative-id":["plants14050721"],"URL":"https:\/\/doi.org\/10.3390\/plants14050721","relation":{},"ISSN":["2223-7747"],"issn-type":[{"type":"electronic","value":"2223-7747"}],"subject":[],"published":{"date-parts":[[2025,2,26]]}}}