Resistance of Georgian Hazelnut (Corylus L.) to Brown Marmorated Stink Bug – Halyomorpha halys (Stål)

محورهای موضوعی : Hazelnut

Natalia Kharabadze ¹ , Nino Tsiklauri ² , Medea Burjanadze ³ , Nona Chkhaidze ⁴

1 - Vasil Gulisashvili Forest Institute, Agricultural University of Georgia, Tbilisi, 0159 Georgia
2 - Sergi Durmishidze Institute of Biochemistry and Biotechnology, Agricultural University of Georgia, Tbilisi, 0159, Georgia
3 - Vasil Gulisashvili Forest Institute, Agricultural University of Georgia, Tbilisi, 0159 Georgia
4 - Department of Botany and Plant Physiology, Agricultural University of Georgia, Tbilisi, 0159 Georgia

تاریخ دریافت : 1401/02/22 تاریخ پذیرش : 1401/07/09 تاریخ انتشار : 1401/12/10

کلید واژه: Resistance, Phenology, lignin, Hazelnut, Halyomorpha halys,

چکیده مقاله :

Brown Marmorated Stink Bug (BMSB), Halyomorpha halys (Hemiptera: Pentatomidae) (Stal, 1855) is an invasive, highly polyphagous, severe agricultural pest, that reduces the availability, quality, and value of hazelnut production. The most important method against H. halys is the use of resistant hazelnut varieties. The purpose of our work is to investigate the potential of hazelnut resistance to H. halys. Research objects are Georgian commercial varieties Berdznula (Corylus avellana) and Tita (Corylus pontica) in the condition of West Georgia. Hazelnut fruit shell thickness, qualitative and quantitative lignin contents and H. halys stylet length were determined by microscopic and biochemical methods, also H. halys and nut phenologies, and the degree of nut damage were evaluated according to the number of healthy kernels. It was demonstrated that overwintered insects and individuals of all ages of the first- and second-generation damage hazelnut fruit before the shell ripens, which is synchronized with the early stages of hazelnut fruit development. H. halys cannot damage the fruit after lignification of the pericarp. Lignin content and damage intensity are inversely proportional to each other according to Pearson's correlation. Hazelnut resistance depends on the synchronous development of H. halys and hazelnut phenopases, and also on the time and quantity of lignin biosynthesis in hazelnut pericarp. According to the above-mentioned resistance markers, Berdznula is more resistant than Tita. Research results contribute to maintaining a healthy environment, sustainable crop production, and food security.

منابع و مأخذ:

Acebes, A. L. (2016). Host plant effects on the biology, behavior and ecology of brown marmorated stink bug,

Halyomorpha Halys (STÅL) (Hemiptera: Pentatomidae). PhD Dissertation, Virginia Polytechnic Institute and State University.

Ayeni AO, Adeeyo OA, Oresegun OM, Oladimeji TE (2015) Compositional analysis of lignocellulosic materials: Evaluation of an economically viable method suitable for woody and non-woody biomass. American Journal of Engineering Research. 14-19

Bakken AJ, Schoof SC, Bickerton M, Kamminga KL, Jenrette JC, Malone S, Abney MA, Herbert DA, Reisig D, Kuhar TP, Walgenbach JF (2015) Occurrence of brown marmorated stink bug (Hemiptera: Pentatomidae) onwild hosts in nonmanaged woodlands and soybean fields in North Carolina and Virginia. Environmental Entomology. 44, 1011-1021. https:// doi:10. 1093/ee/nvv092  

Bergmann EK, Bernhard M, Bernon G, Bickerton M, Gill S, Gonzales C, Hamilton GC, Hedstrom Kamminga C, KC, Koplinka-Loehr (2015) Stop H. halys. http://www.stopH.halys.org/where-is-H.halys/host-plant. Accessed11. 24, 2019

Bernays E (1992) Interaction of insects and plants. Science Progress. pp. 300. 247-271. http://www.jstor.org/stable/43421301

Boudet A (2000) Lignins and lignification. In: Selected issues. Plant Physiology and Biochemistry, https://doi:10.1016/s0981-9428(00)00166-2.

CABI datasheet. https:// www. cabi. org/isc /datasheet/27377 . Accessed 24 November 2019.

Dowd PF, Sattler SE (2015) Helicoverpa zea (Lepidoptera: Noctuidae) and Spodoptera frugiperda (Lepidoptera: Noctuidae) Responses to Sorghum bicolor (Poales: Poaceae) Tissues from Lowered Lignin Lines. Journal of Insect Sciences. 15, 1–4. https:// doi. org/ 10.1093 /jisesa/ieu162.

EPPO Global Database. https://gd .eppo.int/ taxon/HALYHA. Accessed. 24 November 2019.

Evert RF, K Esau (2006) Esau's plant anatomy. In: Meristems, cells, and tissues of the plant body: Their structure, function, and development. Wiley-Interscience. 624.

FAOSTAT database. http:// www.fao. org/faostat /en/#data/QC. Accessed 13 September 2018.

Frary A, Ӧztürk SC, Balık HI, Balık SK, Kızılcı G, Doğanlar S, Frary A (2019) Analysis of European Hazelnut (Corylus Avellana) Reveals Loci for Cultivar Improvement and the Effects of Domestication and Selection on Nut and Kernel Traits." Molecular Genetics and Genomics. https://doi.org/10.1007/s00438-018-1527-1

Funayama K (2006) A new rearing method using carrots as food for the brown-marmorated stink bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae). Applied Entomology and Zoology. 415-418.

Gagnidze IR, Nakhutsrishvili G, Maier G (2005) Vascular Plants of Georgia: a nomenclatural Checklist. Georgian Academy of Sciences. pp. 243.

Geonuts Information about Georgian hazelnut (2014) https://geonuts.org/georgian-hazelnut/ Accessed 22 March 202.

Giacometti R, Jacobi V, Kronberg F, Panagos C, Edison AS, Zavala JA (2020) Digestive activity and organc compounds of Nezara viridula watery saliva induce defensive soybean seed responces. Scientific Reports. https://doi. org/10. 1038/ s41598 -020-72540-3 

Hano C, Addi M, Bensaddek L, Crônier D, Baltora-Rosset S, Doussot J, Lamblin F (2005) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta. 975-989. https://doi:10.1007/s00425-005-0156-1

Hedstrom CS, Shearer PW, Miller JC, Walton VM (2014) The Effects of Kernel Feeding by Halyomorpha halys (Hemiptera: Pentatomidae) on Commercial Hazelnuts. Journal of Economic Entomology. 107, 1858–65.

Hoebeke ER, Carter EM (2003) Halyomorpha halys (Sta˚l) (Heteroptera: Pentatomidae): a 10 polyphagous plant pest from

Asia newly detected in North America." Procidings of the Entomological Socciety of Washington. 105, 225–237.

Holstein N, Tamer S, Weigend M (2018) The Nutty World of Hazel Names – a Critical Taxonomic Checklist of the Genus Corylus (Betulaceae). European Journal of Taxonomy.no. 409. https://doi.org/10.5852/ejt.2018.409

International Nut and Dried Fruit Council. https://www.nutfruit.org/industry/statistics. Accessed 23 October 2019.

Jakeli E, & Nikolaishvili A (2019) The results of bio ecological study of brown marmorated stink bug-Halyomorpha halys (Stal) in the conditions of Western Georgia. Georgian Academy of Agricultural Sciences. In: 1^ed. 70-75.

Japaridze l (1958) Workshop on Chemistry microscopic plants. Moscow: Soviet science. [In Russian].

Javakhishvili Sh (1988) Georgia weather characterization by months. Education, Tbilisi. pp, 157. 63-80. [In Georgian].

Jesús LR, Kamiyama MT, Hernandez G, Nay J, Hoddle MS (2017) Assessment of Feeding Acceptance and Injury of Kerman Pistachios, Pistacia Vera, by Brown Marmorated Stink Bug (Hemiptera: Pentatomidae). Journal of Insect Science. 17(5). https://doi.org/10.1093/jisesa/iex084

Jones JR, Lambdin PL (2009) New County and State Records for Tennessee of an Exotic Pest, Halyomorpha halys (Hemiptera: Pentatomidae), with Potential Economic and Ecological Implications. Florida Entomologist. 92(1), 177-178. https://doi:10.1653/024.092.0132

Joseph SV, Nita M, Leskey TC, Bergh JC (2015) Temporal Effects on the Incidence and Severity of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) Feeding Injury to Peaches and Apples during the Fruiting Period in Virginia. Journal of Economic Entomology. 108(2), 592-599. https://doi:10.1093/jee/tou059

Karpun NN, Protsenko V E (2016) Brown Marmorated Stink Bug (Halyomorpha halys Stål) occurred in humid subtropical regions of Russia and Abkhazia. https:// www.vniisubtrop .ru/ novosti /769-mramornyj-klop-halyomorpha-halys-st-l-poyavilsya-vo-vlazhnykh-subtropikakh-rossii-i-abkhazii.html. Federal State Budgetary Institution of Science. Accessed 12 May 2022

Kharabadze N (2019) Natural Enemies as Potential Biological Agents for the Control of Brown Marmorated Stink Bug (H. halys) - Halyomorpha halys in Georgia. International conference on Brown Marmorated Stink Bug (H. halys)-Phytosanitary Regulator Framework. Tbilisi, Republic of Georgia. 11-14 March. Tbilisi.

Khomizurashvili T (1978) fruits, Nuts and Subtropical Crops. Georgian Fruits Volume IV. 934. [In Georgian].

Kutateladze R, Kochlamazashvili L, Kandashvili S (2013) Export potential of Georgian hazelnut. Technology Transfer and Innovations 2nd Annual Conference & Networking. Prague. 130–133.

Lauvergeat V, Lacomme C, Lacombe E, Lasserre E, Roby D, Grima-Pettenati J (2001) Two cinnamoyl-CoA reductase (CCR) genes from Arabidopsis thaliana are differentially expressed during development and in response to infection with pathogenic bacteria.  Phytochemistry. 57(7) 1187-1195. https://doi:10.1016/s0031-9422 (01) 00053-x.

Lee Doo-Hyung, Short BD, Shimat VJ, Bergh JC, Leskey TC (2013) Review of the Biology, Ecology, and Management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environmental Entomology. 42(4) 627-641. https://doi:10.1603/EN13006

Leskey TC, Hamilton G C, Nielsen AL, Polk DF, Rodriguez-Saona CJ, Bergh CD, Herbert A, et al. 2012a. Pest Status of the Brown Marmorated Stink Bug, Halyomorpha Halys in the USA. Outlooks on Pest Management 23(5), 218–26. https://doi.org/10.1564/23oct07

Leskey, TC, Short BD, Butler BR, Wright SE (2012b) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Journal of Entomology. https://doi:10.1155/2012/535062

Lin SY, Dence CW (1992) The determination of lignin. In: Methods in Lignin Chemistry, by C.W. Dence. 33-61. Heidelberg: Springer-Verlag.

Liu Q, Luo L, Zheng L (2018) Lignins: Biosynthesis and Biological Functions in Plants. International Journal of Molecular Sciences. 19(2), 335. https://doi.org/10.3390/ijms19020335

Maghlakelidze E, Bobokashvil Z, Maghradze D (2017) Biological and agronomical characteristics of local and introduced plum (Prunus domestica L.) cultivars in Georgia. International Journal of Horticultural Science and Technology. 4(2), 157-166. 

Mamedov ZM (2018) Brown marmorated sting bug (Halyomorpha halys Stal.) the pest of orchard, forest and decorative trees in Azerbaijan. Bulletin of Georgian Academy of Agricultural Sciences. 184, 88-89. https:// dspace. nplg. gov.ge/bitstream/1234/286197/1/Saqartvelos_Soflis_Meurneobis_Mecnierebata_Akademiis_Moambe_2018_N2.pdf. [In Russian].

McPherson JE, McPherson RM (2000) Stink bugs of economic importance in America north of Mexico. Edited by Boca

Raton. Florida: CRC Press. https:// doi:10. 1201/9781420042429.bmatt

Meskhi N (2017) Monitoring and control strategy of Brown marmorated stink bug (Halyomorpha halys) in Georgia Halyomorpha halys- Global Challenge International Experience for Best Sollution. Tbilisi, Republic of Georgia. 7 September, Tbilisi.

Meskhi N (2019) State Control Program of Brown Marmorated Stink Bug (BMSB) - Halyomorpha halys in Georgia. International Conference Brown Marmorated Stink Bug (BMSB) - Halyomorpha halys Phytosanitary Regulatory Framework. Tbilisi, Republic of Georgia 11-14 March, Tbilisi.

Mirotadze M (2011) Determination of the optimal regime of drying of some nuts (hazelnuts) industrial species Ph.D Dissertation, Agricultural Unversity of Georgia. https:// dspace.nplg.gov.ge/handle/1234/166244 [In Georgian].

Moura JC, Bonine CA, Viana JD, Dornelas MC, Mazzafera P (2010) Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants. Journal of Integrative Plant Biology. 52(4), 360-376. https://doi:10.1111/j.1744-7909

Moura-Sobczak J, Souza U, Mazzafera P (2011) Drought stress and changes in the lignin content and composition in Eucalyptus. BMC Proceedings, 5(Suppl 7). https:// doi:10. 1186/1753-6561-5-s7-p103

Murvanidze M, Krawczyk G, Inasaridze N, Dekanoidze L, Samsonadze N, Macharashvili M, Shengelaia S(2018) Preliminary data on the biology of brown marmorated stink bug Halyomorpha halys (Hemiptera, Pentatomidae) in Georgia. Turkish Journal of Zoology. 42(6) 617-624. https://doi:10.3906/zoo-1802-34

National Environmental Agency of Georgia. https://nea.gov.ge . Accessed 21 February 2021.

Neimirovets VV (2018) Brown marmorated stink bug Halyomorpha halys (Heteroptera: Pentatomidae): morphology, biology, distribution and threats to agriculture in the Russian Federation. Vestnik. 4, https://doi: 10.31993/2308-6459-2018-1(95)-11-16

Niva CC, Takeda M (2003) Effects of Photoperiod, Temperature and Melatonin on Nymphal Development, Polyphenism and Reproduction in Halyomorpha Halys (Heteroptera: Pentatomidae). Zoological Science 20(8), 963–70. https://doi.org/10.2108/zsj.20.963

Osakabe K, Tsao CC, Li L, Popko JL, Umezawa T, Carraway DT, Chiang VL (1999) Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proceedings of the National Academy of Sciences. 96(16) 8955-8960. https:// doi: 10.1073/pnas.96.16.8955

Peiffer M, Felton GW (2014) Insights into the Saliva of the Brown Marmorated Stink Bug Halyomorpha halys (Hemiptera: Pentatomidae). PLoS ONE. 9(2), e88483. https:// doi.org/ 10.1371/ journal. pone.0088483.

Peterson JA, Ode PJ, Oliveira-Hofman C, Harwood JD (2016) Integration of Plant Defense Traits with Biological Control of Arthropod Pests: Challenges and Opportunities. Frontiers in Plant Science. https://doi:10.3389/fpls.2016.01794

Rahman MM, Lim UT (2017) Evaluation of mature soybean pods as a food source for two pod-sucking bugs, Riptortus pedestris (Hemiptera: Alydidae) and Halyomorpha halys (Hemiptera: Pentatomidae). PloS One. 12(4). https:// doi: 10.1371 /journal.pone.0176187. 

Rijal J, Sudan G (2018) Characterizing Brown Marmorated Stink Bug Injury in Almond, a New Host Crop in California.

Insects 9(4), 126. https:// doi.org/ 10.3390/ insects9040126.  

Sathe TV, Bhoje PM (2000) Biological Pest Control. Daya Publishing House, Delhi. pp. 122. 10-15.

Shatilova I, Mchedlishvili N, Rukhadze L, Kvavadze E (2011) The History of the Flora and Vegetation of Georgia (South Caucasus). Georgian National Museum, Institute of Paleobiology.

Sichinava N (2005) Biological and economic characteristics of hazelnut spread in Samegrelo and scientific basis of its production. Tbilisi, 64. [In Georgian].

Skillman VP, Wiman NG, Lee JC (2018) Nutrient declines in overwintering Halyomorpha halys populations." Entomologia Experimentalis Et Applicata. 166(9), 778-789. https://doi: 10. 1111/eea.12708.

Solar A, Stampar F (2011) Characterization of selected hazelnut cultivars: phenology, growing and yielding capacity, market quality and nutraceutical value. Journal of the Science of Food and Agriculture. 91(7), 1205-1212. https://doi:10.1002/jsfa.4300

Ullah S, Li Z, Zuberi A, Arifeen MZ,  Baig MM (2019) Biomarkers of pyrethroid toxicity in fish. Environmental Chemistry Letters 1-29. https://doi:10.1007/s10311-018-00852-y  

Will T, Steckbauer K, Hardt M, Bel AJ (2012) Aphid Gel Saliva: Sheath Structure, Protein Composition and Secretory

Dependence on Stylet-Tip Milieu. PLoS ONE. 7(10). https://doi:10.1371/journal.pone.0046903

Yang Y, Nanxiang W, Wang C (2018) Toxicity of the Pyrethroid Bifenthrin Insecticide." Environmental Chemistry Letters. 16(4), 1377–91. https://doi.org/10.1007/s10311-018-0765-0