Artvin Coruh University Journal of Forestry Faculty
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Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları

Year 2023, Volume: 24 Issue: 2, 151 - 159, 15.10.2023

Serap MUTUN

https://doi.org/10.17474/artvinofd.1313775

Abstract

Dünyada yaşamın ilk ortaya çıkmasından bu yana pek çok farklı yaşam formu hem birbirleri ile hem de cansız çevre faktörleriyle etkileşim içinde bulunmuşlar ve evrimleşerek çeşitlenmişlerdir. Bu etkileşimler arasında en dikkat çekici olanlarından biri bitkiler ile gal oluşturan böcekler arasında görülür. Özellikle gal arıları (Hymenoptera, Cynipidae) oldukça karmaşık gal yapıları ile adaptif radyasyonun en güzel örneklerinden birini sergiler. Sıra dışı bitki yapıları olan gallerin oluşabilmesi için herbivor böcek, bitkinin savunma bariyerlerini tek tek geçerek konak genomunu yeniden programlar ve onun öz kaynaklarını kendi lehine kullanır. Gal oluşum sürecinde hücre proliferasyonunun başlatılması sonrasında konak için tamamen yeni ve olağan dışı yapıların oluşumuna kadar bir dizi gen, molekül ve metabolik yol ve yolak kullanılır. Son yıllarda yapılan moleküler çalışmalarda artış olsa da gal oluşumu, moleküler mekanizmalar ve gal komünitelerindeki evrimsel ilişkiler henüz yeni yeni aydınlatılmaya başlanmıştır. Bu derleme çalışmasında gal oluşumu, meşe gal arıları (Cynipidae, Cynipini) temel alınarak morfolojik ve güncel moleküler bilgiler ışığında kısaca özetlenmeye çalışılmıştır.

Keywords

Cynipidae, efektör molekül, Gal arıları, Gal komünitesi, Omiks

References

  • Abe Y (1994) The karotype in the chestnut Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Applied Entomological Zoology, 29(2): 299-300.
  • Abe Y (1995) Relationships between the Gall Wasp, Trichagalma serratae (Ashmead) (Hymenoptera: Cynipidae), and two moth species, Andrioplecta pulverula (Meyrick) (Lepidoptera: Tortricidae) and Characoma ruficirra (Hampson) (Lepidoptera: Noctuidae). Applied Entomology and Zoology, 30: 83-89.
  • Azmaz M, Katılmış Y (2017) Updated species list of Cynipidae (Hymenoptera) from Turkey. Zootaxa, 4303(3): 361–378.
  • Azmaz M, Katılmış Y (2020a) A new species of herb Gall Wasp (Cynipidae, Aulacideini, Aulacidea) from Turkey. Zootaxa, 4747(2): 378–390.
  • Azmaz M, Katılmış Y (2020b) A new species of Cynips (Cynipidae: Cynipini) from Turkey. Zoology in the Middle East, 66: 232–239.
  • Azmaz M, Katılmış Y (2021a) Three new species of herb Gall Wasps (Hymenoptera: Cynipidae) from Turkey. European Journal of Taxonomy, 757: 152–168.
  • Azmaz M, Katılmış Y (2021) Two new oak Gall Wasp species (Hymenoptera: Cynipidae, Cynipini) from Quercus pontica (Fagaceae) in Turkey. Zootaxa, 5016 (3): 382–394.
  • Azmaz M, Kılınçarslan Aksoy Ö, Katılmış Y, Mammadov R (2020) Investigation of the antioxidant activity and phenolic compounds of Andricus quer custozae Gall and Host Plant (Quercus infectoria). IJSM, 7(2): 77-87.
  • Azmaz M (2021) Quercus infectoria Oliv. (Mazı Meşesi) köklerinde oluşan mazılar (Hymenoptera: Cynipidae): İki yeni kayıt. Turkish Journal of Forestry, 22(2): 91–96.
  • Bonall R, Vargas-Osuna E, Mena JD, Aparicio JM, Santoro M, Martín A (2018) Looking for variable molecular markers in the chestnut Gall Wasp Dryocosmus kuriphilus: First comparison across genes. Scientific Reports, 8: 1-9.
  • Buffington ML, Forshage M, Liljeblad J, Tang C-T, van Noort S (2020) World Cynipoidea (Hymenoptera): A key to higher-level groups. Insect Systematics and Diversity, 4(4): 1–69.
  • Bunnefeld L, Hearn J, Stone GN, Lohse K (2018) Whole-genome data reveal the complex history of a diverse ecological community. PNAS, 115(28): 1-9.
  • Cambier S, Ginins O, Moreau SJM, Gayral P, Hearn J, Stone GN, Huguet E, Drezen J-M (2019) Gall Wasp transcriptomes unravel potential effectors involved in molecular dialogues with oak and rose. Frontiers in Physiology, 10: 926-943.
  • Carneiro RG, Isaias RMS (2015) Gradients of metabolic accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking-insects. AOB Plants, 7, plv086. DOI: 10.1093/aobpla/plv086. Cook JM, Rokas A, Pagel M, Stone GN (2002) Evolutionary shifts between host oak sections and host- plant organs in Andricus Gall Wasps. Evolution, 56(9): 1821-1830.
  • Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how? American Midland Naturalist, 110: 225-234.
  • Csóka G, Stone GN, Melika G (2005) Biology, Ecology and Evolution of Gall-inducing Cynipidae. Biology, Ecology and Evolution of Gall-Inducing Arthropods Publisher: Science Publishers Eds: Raman A., Schaefer C.W., Withers T.W.s: 573-642.
  • Czeczuga B (1977) Carotenoids in leaves and their galls. Marcellia, 40: 177-180.
  • Demirel M, Azmaz M, Katılmış Y (2022) A new species of oak Gall Wasp (Hymenoptera: Cynipidae, Cynipini) from Turkey. Zootaxa, 5087(4): 583–590.
  • Demirel M, Tataroğlu M, Katılmış Y (2023) Cynipidae (Hymenoptera, Cynipoidea) fauna of Burdur province (Türkiye). Zootaxa, 5296 (3): 362–380.
  • Egan SP, Hood GR, Martinson EO, Ott JR (2018) Cynipid Gall Wasps. Current Biology, 28: 1-5.
  • Eleftherianos I, Atri J, Accetta J, Castillo JC (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Frontiers in Physiology, 4: 1-10.
  • Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. International Journal of Molecular Sciences, 14: 10242–10297.
  • Giron D, Huguet E, Stone GN, Body M (2015) 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.
  • Harper LJ, Schönrogge K, Lim KY, Francis P, Lichtenstein CP (2004) Cynipid galls: insect- induced modifications of plant development create novel plant organs. Plant, Cell, and Environment, 27: 327-335.
  • Hayward A, Stone GN (2005) Oak Gall Wasp communities: evolution and ecology. Basic and Applied Ecology, 6: 435- 443.
  • Hayward A, Stone GN (2005) Comparative phylogeography across two trophic levels: the Oak Gall Wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans. Molecular Ecology, 15: 479-489.
  • Hearn J, Blaxter M, Schönrogge K, Nieves-Aldrey J-L, Pujade-Villar J, Huguet E, Drezen J-M, Shorthouse JD, Stone GN (2019) Genomic dissection of an extended phenotype: oak galling by a cynipid Gall Wasp. PLoS Genetics, 15(1): e1008398.
  • Hogenhout SA, Bos JIB (2011) Effector proteins that modulate plant–insect interactions. Current Opinion in Plant Biology, 14: 422-428.
  • Isaias RMS, Ferreira BG, Alvarenga DR, Barbosa LR, Salminen JP, Steinbauer MJ (2018) Functional compartmentalization of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Austral Entomology, 57(2): 238-246.
  • Jones D (1983) The influence of host density and gall shape on the survivorship of Diastrophus kinkaidii Gill (Hymenoptera: Cynipidae). Canadian Journal of Zoology, 61: 2138-2142.
  • Kuster VC, Rezende UC, Cardoso JCF, Isaias RMS, Oliveira DC (2020) How Galling Organisms Manipulate the Secondary Metabolites in the Host Plant Tissues? A Histochemical Overview in Neotropical Gall Systems. In: Mérillon JM, Ramawat KG, editors. Co-Evolution of Secondary Metabolites, Springer International Publishing.
  • Kinsey AC (1922) Studies of some new and described Cynipidae (Hymenoptera). Indiana University Studies, 9: 1-141.
  • Laine AL (2009) Role of coevolution in generating biological diversity: Spatially divergent selection trajectories. Journal of Experimental Botany, 60: 2957-2970.
  • Liljeblad J, Ronquist F (1998) A phylogenetic analysis of higher-level Gall Wasp relationships (Hymenoptera: Cynipidae). Systematic Entomology, 23: 229-252.
  • Liu X, Bai, J, Huang L, Zhu L, Liu X, Weng N, Reese JC, Harris M, Stuart JJ, 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.
  • Lobato-Vila I, Bae J, Roca-Cusachs M, Kang M, Jung S, Melika G, Pénzes Z, Pujade-Villar J (2022) Global phylogeny of the inquilinous Gall Wasp tribe Synergini (Hymenoptera: Cynipoidea: Cynipidae): first insights and establishment of a new cynipid tribe. Zoological Journal of the Linnean Society, 195(4): 1338–1354.
  • Manos PS, Doyle JJ, Nixon KC (1999) Phylogeny, biogeography, and the processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Molecular Phylogenetics and Evolution, 12: 333-349.
  • Martinson E, Werren J, Egan S (2022) Tissue-specific gene expression shows cynipid wasps repurpose host gene networks to create complex and novel parasite-specific organs on Oaks. Molecular Ecology, 31: 3228-3240.
  • Melika G, Pujade-Villar J, Bellido D, López G (1999) Current state of knowledge of heterogony in Cynipidae (Hymenoptera, Cynipoidea). Sessió Conjunta d’Entomologia, 11, 87-107.
  • Melika G (2006) Gall wasps of Ukraine: Cynipidae. Vestnik Zoologii, Supplement, 21 (1–2): 1–300+301–644.
  • Melika G, Ros-Farre P, Pujade-Villar J (2001) Synonymy of two genera (Fioriella and Plagiotrochus) of cynipid Gall Wasps and the description of the sexual generation of Plagiotrochus razeti Barbotin (Hymenoptera: Cynipidae, Cynipinae). Folia Entomologica Hungaricae, 62: 115-125.
  • Nabity PD (2016) Insect-induced plant phenotypes: revealing mechanisms through comparative genomics of galling insects and their hosts. American Journal of Botany, 103(6): 979-981.
  • Nogueira RM, Costa EC, Silva JS, Isaias RM (2018) Structural and histochemical profile of Lopesia sp. Rübsaamen 1908 pinnula galls on Mimosa tenuiflora (Willd.) Poir. in a Caatinga environment. Hoehnea, 45(2): 314-322.
  • Oates CN, Denby KJ, Myburg AA, Slippers B, Naidoo S (2016) Insect gallers and their plant hosts: from omics data to systems biology. International Journal of Molecular Sciences, 17: 1891- 1905.
  • Patterson JT (1928) Functionless males in two species of Neuroterus. Biological Bulletin of Marine Biology Laboratory, 54(2): 196-200.
  • Price P, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environmental Entomology, 16: 15-24.
  • Price P (2005) Adaptive radiation of gall-inducing insects. Basics Ecological Applications, 6: 413-421.
  • Quicke DLJ (1997) Parasitic Wasps. Chapman&Hall, Cambridge University Press, 470 p, London.
  • Raman A, Schaefer C W, Withers TM (2005) Biology, ecology, and evolution of gall-inducing arthropods. Enfield: Science Publishers, 1: 1-34. Rokas A, Melika G, Abe Y, Nieves-Aldrey JL, Cook JM, Stone GN (2003) Lifecycle closure, lineage sorting, and hybridization revealed in a phylogenetic analysis of European Oak Gallwasps (Hymenoptera: Cynipidae: Cynipini) using mitochondrial sequence data. Molecular Phylogenetics and Evolution, 26: 36-45.
  • Ronquist F (1999) Phylogeny, classification, and evolution of the Cynipoidea (Hymenoptera). Zoologica Scripta, 28: 139-164.
  • Ronquist F, Nieves-Aldrey J-L, Buffington ML, Liu Z, Liljeblad J, Nylander JAA (2015) Phylogeny, evolution, and classification of Gall Wasps: The plot thickens. Plos One, 10(5): e0123301.
  • Schultz JC, Stone GN (2022) A tale of two tissues: probing gene expression in a complex insect-induced gall. Molecular Ecology, 31: 3031-3034.
  • Schönrogge K, Harper LJ, Lichtenstein CP (2000) The protein content of tissues in Cynipid galls (Hymenoptera: Cynipidae): similarities between cynipid galls and seeds. Plant Cell Environment, 23: 215-222.
  • Shorthouse JD, Wool D, Raman A (2005) Gall-inducing Insects- Nature’s Most Sophisticated Herbivores. Basic and Applied Ecology, 6: 407-411.
  • Stone GN, Cook JM (1998) The structure of Cynipid Oak Galls: patterns in evolution of an extended phenotype. Proceedings of the Royal Society of London B, 265: 979-988.
  • Stone GN, Schönrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of Oak Gall Wasps (Hymenoptera: Cynipidae). Annual Review of Entomology, 47: 633-668.
  • Stone GN, Schrönrogge K (2003) The Adaptive Significance of Insect Gall Morphology Trends in Ecology & Evolution 18: 512-522.
  • Stone GN, van der Ham RW, Brewer JG (2008) Fossil oak galls preserve ancient multitrophic interactions. Proceedings of the Royal Society B, 275: 2213-2219.
  • Stuart JDG (2015) Insect effectors and gene-for-gene interactions with host plants. Current Opinion in Insect Science, 9: 56-61.
  • Su Q, Zhou X, Zhang Y (2013) Symbiont-mediated functions in insect hosts. Communicative&Integrative Biology, 6(3): e23804-1-e23804-7.
  • Tataroğlu M, Katılmış Y (2022) First record of Barbotinia oraniensis (Barbotin, 1964) (Hymenoptera: Cynipidae) from Turkey. Turkish Journal of Forestry, 23(2): 103–105.

Arm race between plant and ınsects: gall wasps and gall formation

Year 2023, Volume: 24 Issue: 2, 151 - 159, 15.10.2023

Serap MUTUN

https://doi.org/10.17474/artvinofd.1313775

Abstract

Since the emergence of life on Earth, numerous different life forms have interacted with both each other and their environment and evolved over time. One of the most remarkable interactions is observed between plants and gall forming insects, where gall wasps (Hymenoptera, Cynipidae) represent one of the most significant examples of adaptive radiation through inducing very complicated gall structures. For the formation of these extraordinary gall structures, herbivorous insects bypass the plant's defense barriers and reprogram the host genome, utilizing its resources for their own benefit. Through gall formation, a series of genes, molecules, metabolic pathways, and routes are utilized, starting from the initiation of cell proliferation to the formation of entirely new and extraordinary structures for the host. While there has been an increase in molecular studies in recent years, gall formation, molecular mechanisms, and evolutionary relationships within gall communities have not been completely understood yet. This review aims to provide a brief summary of gall formation based on oak gall wasps (Cynipidae, Cynipini), incorporating morphological and current molecular information.

Keywords

Cynipidae, effector molecule, gall wasps, gall communities, omics

References

  • Abe Y (1994) The karotype in the chestnut Gall Wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Applied Entomological Zoology, 29(2): 299-300.
  • Abe Y (1995) Relationships between the Gall Wasp, Trichagalma serratae (Ashmead) (Hymenoptera: Cynipidae), and two moth species, Andrioplecta pulverula (Meyrick) (Lepidoptera: Tortricidae) and Characoma ruficirra (Hampson) (Lepidoptera: Noctuidae). Applied Entomology and Zoology, 30: 83-89.
  • Azmaz M, Katılmış Y (2017) Updated species list of Cynipidae (Hymenoptera) from Turkey. Zootaxa, 4303(3): 361–378.
  • Azmaz M, Katılmış Y (2020a) A new species of herb Gall Wasp (Cynipidae, Aulacideini, Aulacidea) from Turkey. Zootaxa, 4747(2): 378–390.
  • Azmaz M, Katılmış Y (2020b) A new species of Cynips (Cynipidae: Cynipini) from Turkey. Zoology in the Middle East, 66: 232–239.
  • Azmaz M, Katılmış Y (2021a) Three new species of herb Gall Wasps (Hymenoptera: Cynipidae) from Turkey. European Journal of Taxonomy, 757: 152–168.
  • Azmaz M, Katılmış Y (2021) Two new oak Gall Wasp species (Hymenoptera: Cynipidae, Cynipini) from Quercus pontica (Fagaceae) in Turkey. Zootaxa, 5016 (3): 382–394.
  • Azmaz M, Kılınçarslan Aksoy Ö, Katılmış Y, Mammadov R (2020) Investigation of the antioxidant activity and phenolic compounds of Andricus quer custozae Gall and Host Plant (Quercus infectoria). IJSM, 7(2): 77-87.
  • Azmaz M (2021) Quercus infectoria Oliv. (Mazı Meşesi) köklerinde oluşan mazılar (Hymenoptera: Cynipidae): İki yeni kayıt. Turkish Journal of Forestry, 22(2): 91–96.
  • Bonall R, Vargas-Osuna E, Mena JD, Aparicio JM, Santoro M, Martín A (2018) Looking for variable molecular markers in the chestnut Gall Wasp Dryocosmus kuriphilus: First comparison across genes. Scientific Reports, 8: 1-9.
  • Buffington ML, Forshage M, Liljeblad J, Tang C-T, van Noort S (2020) World Cynipoidea (Hymenoptera): A key to higher-level groups. Insect Systematics and Diversity, 4(4): 1–69.
  • Bunnefeld L, Hearn J, Stone GN, Lohse K (2018) Whole-genome data reveal the complex history of a diverse ecological community. PNAS, 115(28): 1-9.
  • Cambier S, Ginins O, Moreau SJM, Gayral P, Hearn J, Stone GN, Huguet E, Drezen J-M (2019) Gall Wasp transcriptomes unravel potential effectors involved in molecular dialogues with oak and rose. Frontiers in Physiology, 10: 926-943.
  • Carneiro RG, Isaias RMS (2015) Gradients of metabolic accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking-insects. AOB Plants, 7, plv086. DOI: 10.1093/aobpla/plv086. Cook JM, Rokas A, Pagel M, Stone GN (2002) Evolutionary shifts between host oak sections and host- plant organs in Andricus Gall Wasps. Evolution, 56(9): 1821-1830.
  • Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how? American Midland Naturalist, 110: 225-234.
  • Csóka G, Stone GN, Melika G (2005) Biology, Ecology and Evolution of Gall-inducing Cynipidae. Biology, Ecology and Evolution of Gall-Inducing Arthropods Publisher: Science Publishers Eds: Raman A., Schaefer C.W., Withers T.W.s: 573-642.
  • Czeczuga B (1977) Carotenoids in leaves and their galls. Marcellia, 40: 177-180.
  • Demirel M, Azmaz M, Katılmış Y (2022) A new species of oak Gall Wasp (Hymenoptera: Cynipidae, Cynipini) from Turkey. Zootaxa, 5087(4): 583–590.
  • Demirel M, Tataroğlu M, Katılmış Y (2023) Cynipidae (Hymenoptera, Cynipoidea) fauna of Burdur province (Türkiye). Zootaxa, 5296 (3): 362–380.
  • Egan SP, Hood GR, Martinson EO, Ott JR (2018) Cynipid Gall Wasps. Current Biology, 28: 1-5.
  • Eleftherianos I, Atri J, Accetta J, Castillo JC (2013) Endosymbiotic bacteria in insects: guardians of the immune system? Frontiers in Physiology, 4: 1-10.
  • Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. International Journal of Molecular Sciences, 14: 10242–10297.
  • Giron D, Huguet E, Stone GN, Body M (2015) 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.
  • Harper LJ, Schönrogge K, Lim KY, Francis P, Lichtenstein CP (2004) Cynipid galls: insect- induced modifications of plant development create novel plant organs. Plant, Cell, and Environment, 27: 327-335.
  • Hayward A, Stone GN (2005) Oak Gall Wasp communities: evolution and ecology. Basic and Applied Ecology, 6: 435- 443.
  • Hayward A, Stone GN (2005) Comparative phylogeography across two trophic levels: the Oak Gall Wasp Andricus kollari and its chalcid parasitoid Megastigmus stigmatizans. Molecular Ecology, 15: 479-489.
  • Hearn J, Blaxter M, Schönrogge K, Nieves-Aldrey J-L, Pujade-Villar J, Huguet E, Drezen J-M, Shorthouse JD, Stone GN (2019) Genomic dissection of an extended phenotype: oak galling by a cynipid Gall Wasp. PLoS Genetics, 15(1): e1008398.
  • Hogenhout SA, Bos JIB (2011) Effector proteins that modulate plant–insect interactions. Current Opinion in Plant Biology, 14: 422-428.
  • Isaias RMS, Ferreira BG, Alvarenga DR, Barbosa LR, Salminen JP, Steinbauer MJ (2018) Functional compartmentalization of nutrients and phenolics in the tissues of galls induced by Leptocybe invasa (Hymenoptera: Eulophidae) on Eucalyptus camaldulensis (Myrtaceae). Austral Entomology, 57(2): 238-246.
  • Jones D (1983) The influence of host density and gall shape on the survivorship of Diastrophus kinkaidii Gill (Hymenoptera: Cynipidae). Canadian Journal of Zoology, 61: 2138-2142.
  • Kuster VC, Rezende UC, Cardoso JCF, Isaias RMS, Oliveira DC (2020) How Galling Organisms Manipulate the Secondary Metabolites in the Host Plant Tissues? A Histochemical Overview in Neotropical Gall Systems. In: Mérillon JM, Ramawat KG, editors. Co-Evolution of Secondary Metabolites, Springer International Publishing.
  • Kinsey AC (1922) Studies of some new and described Cynipidae (Hymenoptera). Indiana University Studies, 9: 1-141.
  • Laine AL (2009) Role of coevolution in generating biological diversity: Spatially divergent selection trajectories. Journal of Experimental Botany, 60: 2957-2970.
  • Liljeblad J, Ronquist F (1998) A phylogenetic analysis of higher-level Gall Wasp relationships (Hymenoptera: Cynipidae). Systematic Entomology, 23: 229-252.
  • Liu X, Bai, J, Huang L, Zhu L, Liu X, Weng N, Reese JC, Harris M, Stuart JJ, 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.
  • Lobato-Vila I, Bae J, Roca-Cusachs M, Kang M, Jung S, Melika G, Pénzes Z, Pujade-Villar J (2022) Global phylogeny of the inquilinous Gall Wasp tribe Synergini (Hymenoptera: Cynipoidea: Cynipidae): first insights and establishment of a new cynipid tribe. Zoological Journal of the Linnean Society, 195(4): 1338–1354.
  • Manos PS, Doyle JJ, Nixon KC (1999) Phylogeny, biogeography, and the processes of molecular differentiation in Quercus subgenus Quercus (Fagaceae). Molecular Phylogenetics and Evolution, 12: 333-349.
  • Martinson E, Werren J, Egan S (2022) Tissue-specific gene expression shows cynipid wasps repurpose host gene networks to create complex and novel parasite-specific organs on Oaks. Molecular Ecology, 31: 3228-3240.
  • Melika G, Pujade-Villar J, Bellido D, López G (1999) Current state of knowledge of heterogony in Cynipidae (Hymenoptera, Cynipoidea). Sessió Conjunta d’Entomologia, 11, 87-107.
  • Melika G (2006) Gall wasps of Ukraine: Cynipidae. Vestnik Zoologii, Supplement, 21 (1–2): 1–300+301–644.
  • Melika G, Ros-Farre P, Pujade-Villar J (2001) Synonymy of two genera (Fioriella and Plagiotrochus) of cynipid Gall Wasps and the description of the sexual generation of Plagiotrochus razeti Barbotin (Hymenoptera: Cynipidae, Cynipinae). Folia Entomologica Hungaricae, 62: 115-125.
  • Nabity PD (2016) Insect-induced plant phenotypes: revealing mechanisms through comparative genomics of galling insects and their hosts. American Journal of Botany, 103(6): 979-981.
  • Nogueira RM, Costa EC, Silva JS, Isaias RM (2018) Structural and histochemical profile of Lopesia sp. Rübsaamen 1908 pinnula galls on Mimosa tenuiflora (Willd.) Poir. in a Caatinga environment. Hoehnea, 45(2): 314-322.
  • Oates CN, Denby KJ, Myburg AA, Slippers B, Naidoo S (2016) Insect gallers and their plant hosts: from omics data to systems biology. International Journal of Molecular Sciences, 17: 1891- 1905.
  • Patterson JT (1928) Functionless males in two species of Neuroterus. Biological Bulletin of Marine Biology Laboratory, 54(2): 196-200.
  • Price P, Fernandes GW, Waring GL (1987) Adaptive nature of insect galls. Environmental Entomology, 16: 15-24.
  • Price P (2005) Adaptive radiation of gall-inducing insects. Basics Ecological Applications, 6: 413-421.
  • Quicke DLJ (1997) Parasitic Wasps. Chapman&Hall, Cambridge University Press, 470 p, London.
  • Raman A, Schaefer C W, Withers TM (2005) Biology, ecology, and evolution of gall-inducing arthropods. Enfield: Science Publishers, 1: 1-34. Rokas A, Melika G, Abe Y, Nieves-Aldrey JL, Cook JM, Stone GN (2003) Lifecycle closure, lineage sorting, and hybridization revealed in a phylogenetic analysis of European Oak Gallwasps (Hymenoptera: Cynipidae: Cynipini) using mitochondrial sequence data. Molecular Phylogenetics and Evolution, 26: 36-45.
  • Ronquist F (1999) Phylogeny, classification, and evolution of the Cynipoidea (Hymenoptera). Zoologica Scripta, 28: 139-164.
  • Ronquist F, Nieves-Aldrey J-L, Buffington ML, Liu Z, Liljeblad J, Nylander JAA (2015) Phylogeny, evolution, and classification of Gall Wasps: The plot thickens. Plos One, 10(5): e0123301.
  • Schultz JC, Stone GN (2022) A tale of two tissues: probing gene expression in a complex insect-induced gall. Molecular Ecology, 31: 3031-3034.
  • Schönrogge K, Harper LJ, Lichtenstein CP (2000) The protein content of tissues in Cynipid galls (Hymenoptera: Cynipidae): similarities between cynipid galls and seeds. Plant Cell Environment, 23: 215-222.
  • Shorthouse JD, Wool D, Raman A (2005) Gall-inducing Insects- Nature’s Most Sophisticated Herbivores. Basic and Applied Ecology, 6: 407-411.
  • Stone GN, Cook JM (1998) The structure of Cynipid Oak Galls: patterns in evolution of an extended phenotype. Proceedings of the Royal Society of London B, 265: 979-988.
  • Stone GN, Schönrogge K, Atkinson RJ, Bellido D, Pujade-Villar J (2002) The population biology of Oak Gall Wasps (Hymenoptera: Cynipidae). Annual Review of Entomology, 47: 633-668.
  • Stone GN, Schrönrogge K (2003) The Adaptive Significance of Insect Gall Morphology Trends in Ecology & Evolution 18: 512-522.
  • Stone GN, van der Ham RW, Brewer JG (2008) Fossil oak galls preserve ancient multitrophic interactions. Proceedings of the Royal Society B, 275: 2213-2219.
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Details

Primary Language Turkish
Subjects Entomology
Journal Section Review
Authors

Serap MUTUN
BOLU ABANT İZZET BAYSAL ÜNİVERSİTESİ
0000-0002-0838-3857
Türkiye

Publication Date October 15, 2023
Acceptance Date September 5, 2023
Published in Issue Year 2023Volume: 24 Issue: 2

Cite

APA
MUTUN, S. (2023). Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları. Artvin Çoruh Üniversitesi Orman Fakültesi Dergisi, 24(2), 151-159. https://doi.org/10.17474/artvinofd.1313775
MLA
MUTUN, Serap. “Bitki Ve böcekler arasındaki Bilek güreşi: Gal oluşumu Ve Gal arıları”. Artvin Çoruh Üniversitesi Orman Fakültesi Dergisi, vol. 24, no. 2, 2023, pp. 151-9, doi:10.17474/artvinofd.1313775.
Chicago
MUTUN, Serap. “Bitki Ve böcekler arasındaki Bilek güreşi: Gal oluşumu Ve Gal arıları”. Artvin Çoruh Üniversitesi Orman Fakültesi Dergisi 24, no. 2 (October 2023): 151-59. https://doi.org/10.17474/artvinofd.1313775.
EndNote
MUTUN S (October 1, 2023) Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları. Artvin Çoruh Üniversitesi Orman Fakültesi Dergisi 24 2 151–159.
ISNAD
MUTUN, Serap. “Bitki Ve böcekler arasındaki Bilek güreşi: Gal oluşumu Ve Gal arıları”. Artvin Çoruh Üniversitesi Orman Fakültesi Dergisi 24/2 (October 2023), 151-159. https://doi.org/10.17474/artvinofd.1313775.
AMA
MUTUN S. Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları. ACUJFF. October 2023;24(2):151-159. doi:10.17474/artvinofd.1313775
Vancouver
MUTUN S. Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları. ACUJFF. 2023;24(2):151-9.
IEEE
S. MUTUN, “Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları”, ACUJFF, vol. 24, no. 2, pp. 151–159, 2023, doi: 10.17474/artvinofd.1313775.
JAMA
MUTUN S. Bitki ve böcekler arasındaki bilek güreşi: gal oluşumu ve gal arıları. ACUJFF. 2023;24:151–159.
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Artvin Coruh University Journal of Forestry Faculty is licensed under a Creative Commons Attribution 4.0 International License.