Análise das diferenças transcriptômicas entre dois clones de <i>Populus</i> seção <i>Aigeiros</i> após infestação por insetos

Autores

DOI:

https://doi.org/10.5902/1980509888195

Palavras-chave:

Seção Populus Aigeiros, Clones, Transcriptoma, Genes diferencialmente expressos, Resistência induzida

Resumo

A resistência a insetos é uma característica inerente das plantas e determinada por diferenças genotípicas entre as plantas. Neste estudo, determinamos diferenças nos padrões de expressão gênica entre dois clones de Populus seção Aigeiros após infestação de insetos e elucidamos o mecanismo de resistência induzido pela alimentação de insetos. Realizamos análise de expressão gênica diferencial (DEG) usando o sequenciamento de alto rendimento Illumina Hiseq 2000 de amostras de folhas das partes superior, média e inferior de Populus euramericana cv. 'Neva' ("P107") e P. deltoides 'Chuangxin' ("P17-2") infestados com o inseto. Selecionamos 3.462 DEGs por meio de uma comparação entre "P107" e "P17-2" (A vs. B). Com base na análise da ontologia genética, os DEGs identificados foram anotados funcionalmente, o que revelou 20, 23 e 22 categorias funcionais de "processo biológico", "componente celular" e "função molecular", com enriquecimento principalmente em "processo celular", "parte celular" e "funções de ligação", respectivamente. Após a alimentação dos insetos, as folhas danificadas de "P107" e "P17-2" mostraram diferentes graus de resistência, juntamente com expressões gênicas de defesa reguladas positivamente, redução do acúmulo de nutrientes e fotossíntese e aumento da biossíntese de metabólitos secundários. Este estudo fornece uma base molecular para a compreensão do mecanismo subjacente à resistência de insetos em plantas.

Downloads

Não há dados estatísticos.

Biografia do Autor

Li Guo, undefined

Doctor in Agriculture, Lecturer

College of Chemical Engineering and Biotechnology, Xingtai University, Xingtai, Hebei Province, China

Yanchao Wang, undefined

Doctor in Engineering, Professor

College of Chemical Engineering and Biotechnology, Xingtai University, Xingtai, Hebei Province, China

Lin Li, undefined

Doctor in Agriculture, Lecturer

College of Chemical Engineering and Biotechnology, Xingtai University, Xingtai, Hebei Province, China

Chengxu Wu, undefined

Doctor in Science, Lecturer

College of Forestry, Guizhou University, Guiyang, Guizhou Province, China

Zhen Zhang, undefined

Doctor in Science, Professor

Research Institute of Forest Ecology, Environment and Protection, CAF Key Lab of Forest Protection of State Forestry Administration, Chinese Academy of Forestry, Beijing, China

Yansheng Wu, undefined

Doctor in Science, Professor

College of Chemical Engineering and Biotechnology, Xingtai University, Xingtai, Hebei Province, China

Referências

AGATI, G., AZZARELLO, E., POLLASTRI, TATTINI, M., Flavonoids as antioxidants in plants: Location and functional significance. Plant Science., v. 196, p. 67-76, 2012. DOI: https://doi.org/10.1016/j.plantsci.2012.07.014

AMORE, A., KNOTT, B. C., SUPEKAR, N. T., SHAJAHAN, A., TAYLOR, L.E. Distinct roles of N- and O-glycans in cellulase activity and stability. Proceedings of the National Academy of Sciences., v. 114, n. 52, p. 13667-13672, 2017. DOI: https://doi.org/10.1073/pnas.1714249114

ANDERSON, M. A., VAN, H. R., WEST, J., BATEMAN, K., LEE, M., CHRISTELLER, J. T., MCDONALD, G., HEATH, R. L. Proteinase inhibitors from Nicotiana alata enhance plant resistance to insect pests. J Insect Physiol, v. 43, p. 833. 1997. DOI: https://doi.org/10.1016/S0022-1910(97)00026-7

BALDWIN, I. T. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci U S A., v. 95, p. 8113, 1998. DOI: https://doi.org/10.1073/pnas.95.14.8113

BALDWIN, J. T., SCHULTZ, J. C. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science., v. 221, n. 4607, p. 277-279, 1983. DOI: https://doi.org/10.1126/science.221.4607.277

BAO, S., LI, F., LI, Z., WU, T. The resistance of fourteen poplar species to Anoplophora glabripennis (Motsch.). Journal of Beijing Forestry University., v. 21, n. 4, p. 97–100, 1999.

BARBEHENN, R. V., JONES, C. P., YIP, L., TRAN, L., CONSTABEL, C. P. Limited impact of elevated levels of polyphenol oxidase on tree-feeding caterpillars: assessing individual plant defenses with transgenic poplar. Oecologia., v. 154, n. 1, p. 129-140, 2007. DOI: https://doi.org/10.1007/s00442-007-0822-z

BERNARDS, M. A., BASTRUPSPOHR, L. Induced Plant Resistance to Herbivory. Volume I: Phenylpropanoid metabolism induced by wounding and insect herbivory, p. 189-211, 2008, Springer, Dordrecht. DOI: https://doi.org/10.1007/978-1-4020-8182-8_9

BLODGETT, J. T., EYLES, A., BONELLO, P. Organ-dependent induction of systemic resistance and systemic susceptibility in Pinus nigra inoculated with Sphaeropsis sapinea and Diplodia scrobiculata. Tree Physiology., 27(4): 511-517, 2007. DOI: https://doi.org/10.1093/treephys/27.4.511

BOLTON, M. D. Primary metabolism and plant defense - fuel for the fire. Molecular Plant-Microbe Interactions., v. 22, n. 5, p. 487, 2009. DOI: https://doi.org/10.1094/MPMI-22-5-0487

BONELLO, P., GORDON, T. R., HERMS, D. A., WOOD, D. L., ERBILGIN, N. Nature and ecological implications of pathogen-induced systemic resistance in conifers: a novel hypothesis. Physiol Mol Plant Pathol., v. 68, n. 4, p. 95-104, 2006. DOI: https://doi.org/10.1016/j.pmpp.2006.12.002

BOULTER, D., GATEHOUSE, J. A., GATEHOUSE, A., HILDER, V. A. Genetic engineering of plants for insect resistance. Endeavour., v. 14, n. 4, p. 185-190, 1990. DOI: https://doi.org/10.1016/0160-9327(90)90042-P

BUER, C. S., IMIN, N., DJORDJEVIC, M. A. Flavonoids: new roles for old molecules. Journal of Integrative Plant Biology., v. 52, n. 001, p. 98-111, 2010. DOI: https://doi.org/10.1111/j.1744-7909.2010.00905.x

CAO, G., SOFIC, E., PRIOR, R. L. Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radic Biol Med., v. 22, n. 5, p. 749-760, 1997. DOI: https://doi.org/10.1016/S0891-5849(96)00351-6

CHEN, Q., JIANG X. H., TAN, Y., SHUANG, S., LIU, H. J., DAI, R., TE, M. E., ZHANG, Z. Q. Changes of alfalfa metabolites induced by feeding of thrips. Jiangsu Agricultural Sciences., v. 51, n. 3, p. 126-132, 2023.

CLARKE, H. R. G., LAWRENCE, S. D., FLASKERUD, J., KORHNAK, T. E., GORDON, M. P., DAVIS, J. M. Chitinase accumulates systemically in wounded poplar trees. Physiologia Plantarum., v. 103, n. 2, p. 154-161, 1998. DOI: https://doi.org/10.1034/j.1399-3054.1998.1030202.x

COSSU, R. M., GIORDANI, T., CAVALLIN, A., NATALI, L. High-throughput analysis of transcriptome variation during water deficit in a poplar hybrid: a general overview. Tree Genetics & Genomes., v. 10, n. 1, p. 53-66, 2014. DOI: https://doi.org/10.1007/s11295-013-0661-5

CUSHNIE, T., LAMB, A. J. Antimicrobial activity of flavonoids. International Journal of Antimicrobial Agents., v. 26, n. 5, p. 343-356, 2005. DOI: https://doi.org/10.1016/j.ijantimicag.2005.09.002

DING, C. J., ZHANG, W. X., GAO, M., HUANG, Q. J., CHU, Y. G., SU, X. H. Analysis of transcriptome differences among Populus deltoides with different growth potentials. Scientia Silvae Sinicae., v. 52, p. 47–58, 2016.

DORADO, F. J., MATSIAKH, I., lVARO C, OLAIZOLA, J., ROMERALO, C., JUAN, A. M., WITZELL, J., SOLLA, A. Methyl jasmonate spray for the protection of broad-leaf trees against oomycete and fungal pathogens. Journal of Plant Diseases and Protection, v.132, n. 2, p. 1-13, 2025. DOI: https://doi.org/10.1007/s41348-025-01061-w

EYLES, A., BONELLO, P., GANLEY, R., MOHAMMED, C. Induced resistance to pests and pathogens in trees. New Phytol., v. 185, p. 893–908, 2010. DOI: https://doi.org/10.1111/j.1469-8137.2009.03127.x

EYLES, A., DAVIES, N. W., MOHAMMED, C. Traumatic oil glands induced by pruning in the wound-associated phloem of Eucalyptus globulus: chemistry and histology. Trees., v. 18, n. 2, p. 204–210, 2003. DOI: https://doi.org/10.1007/s00468-003-0297-4

FACCHINI, P. J. Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annual Review of Plant Physiology & Plant Molecular Biology., v. 52, n. 52, p. 29–66, 2001. DOI: https://doi.org/10.1146/annurev.arplant.52.1.29

FANG, J., ZHAO, B. G. Resistance of diferent clones of Populus deltoides to Clostera anastomosis (Lepidoptera: Notodontidae) larvae and the relatedm echanisms. Acta Entomologica Sinica., v. 54, n. 9, p. 1042–1050, 2011.

FANG, S. Z. Silviculture of poplar plantation in China: A review. Chinese Journal of Applied Ecology., n.10, p. 2308-2316, 2008.

FANG, X., XIE, Y., YUAN, Y., LONG, Q., ZHANG, L., AID, G., ZHANG, W. The role of salicylic acid in plant defense responses against biotic stresses. Plant Hormones, v.1, n. 1, 2025. DOI:10.48130/ph-0025-0003. DOI: https://doi.org/10.48130/ph-0025-0003

FERRY, N., EDWARDS, M. G., GATEHOUSE, J. A., GATEHOUSE, A. M. Plant–insect interactions: molecular approaches to insect resistance. Current Opinion in Biotechnology., v. 15, n. 2, p. 155-161, 2004. DOI: https://doi.org/10.1016/j.copbio.2004.01.008

FOSTER, A. J., PELLETIER, G., TANGUAY, P., SEGUIN, A. Transcriptome analysis of poplar during leaf spot infection with Sphaerulina spp. PLoS One., 10: e0138162, 2015. DOI: https://doi.org/10.1371/journal.pone.0138162

GOZIA, O., CIOPRAGA, J., BENTIA, T., LUNGU, M., NITU, F. Antifungal properties of lectin and new chitinases from potato tubers. Comptes Rendus de l Académie des Sciences - Series III - Sciences de la Vie., v. 316, n. 8, p. 788-792, 1993.

GUO, L., ZHANG, S. F., LIU, F., KONG, X. B., ZHANG, Z. Effect of Micromelalopha sieversi (Staudinger) oviposition behavior on the transcriptome of two Populus section Aigeiros clones. Forests., 11(9), 1021; doi:10.3390/f11091021, 2020. DOI: https://doi.org/10.3390/f11091021

HAMANISHI, E. T., BARCHET, G. L., DAUWE, R., MANSFIELD, S. D., CAMPBELL, M. M. Poplar trees reconfigure the transcriptome and metabolome in response to drought in a genotype-and time-of-day-dependent manner. BMC Genom., v. 16, p. 1-16, 2015. DOI: https://doi.org/10.1186/s12864-015-1535-z

HAUKIOJA, E. Induction of defenses in trees. Annual Review of Entomology., 36(1): 25-42, 1991. DOI: https://doi.org/10.1146/annurev.ento.36.1.25

HOLLICK, J. B., Gordon, M. P., A poplar tree proteinase inhibitor-like gene promoter is responsive to wounding in transgenic tobacco. Plant Mol Biol., v. 22, p. 561–572, 1993. DOI: https://doi.org/10.1007/BF00047398

HU, Z. H., WEN, Z., SHEN, Y. B., FU, H. J., ZHANG, Z. Y. Activities of lipoxygenase and phenylalanine ammonia lyase in poplar leaves induced by insect herbivory and volatiles. Journal of Forestry Research., v. 20, n. 4, p. 372, 2009. DOI: https://doi.org/10.1007/s11676-009-0063-6

INOUE, K. Cytochrome P450 enzymes in biosyntheses of some plant secondary metabolites. Yakugaku Zasshi., v. 125, p. 31-49, 2005. DOI: https://doi.org/10.1248/yakushi.125.31

JANZ, D., BEHNKE, K., SCHNITZLER, J. P., KANAWATI, B., SCHMITT-KOPPLIN, P., POLLE, A. Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol., v. 10, p. 1-17, 2010. DOI: https://doi.org/10.1186/1471-2229-10-150

JONGSMA, M. A., BEEKWILDER, J. In Induced plant resistance to herbivory.Volume I: Plant protease inhibitors: functional evolution for defense, p. 235-251. Springer, Dordrecht, 2008. DOI: https://doi.org/10.1007/978-1-4020-8182-8_11

JWA, N. S., AGRAWAL, G. K., TAMOGAMI, S., YONEKURA, M., HAN, O., IWAHASHI, H., RAKWAL, R. Role of defense/stress-related marker genes, proteins and secondary metabolites in defining rice self-defense mechanisms. Plant Physiol Biochem., v. 44, p. 261–273, 2006. DOI: https://doi.org/10.1016/j.plaphy.2006.06.010

KANDASWAMI, C., MIDDLETON, E. Free radical scavenging and antioxidant activity of plant flavonoids. Advances in Experimental Medicine & Biology., v. 366, p. 351-376, 1994. DOI: https://doi.org/10.1007/978-1-4615-1833-4_25

KEELING, C. I., BOHLMANN, J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytologist., v. 170, n. 4, p. 657-675, 2006. DOI: https://doi.org/10.1111/j.1469-8137.2006.01716.x

KESSLER, A., BALDWIN, I. T. Plant responses to insect herbivory: the emerging molecular analysis. Ann Rev Plant Biol., v. 53, p. 299-328, 2002. DOI: https://doi.org/10.1146/annurev.arplant.53.100301.135207

KIM, J., PARK, H., Park, B. T., KIM, H. H. O-glycans and O-glycosylation sites of recombinant human GM-CSF derived from suspension-cultured rice cells, and their structural role. Biochemical and Biophysical Research Communications., v. 479, n. 2, p. 266-271, 2016. DOI: https://doi.org/10.1016/j.bbrc.2016.09.057

LAI, C. L., ZHANG, J., SHENTU, X. P., HAO P. Y., PANG, K., YU, X. P. Review of how secondary metabolites defend plants against herbivorous insects. Chinese Journal of Applied Entomology., v. 59, n. 5, p. 969-978, 2022.

LI, C. Z., LU, J. C., PAN, X. D., XIAO, Y. J., DENG, J. Y., ZHOU, G. X., LOU, Y. G. Herbivore-induced resistant rice volatiles enhance the direct and indirect resistance of the neighboring susceptible rice varieties to Nilaparvata lugens (Hemiptera: Delphacidae). Acta Entomologica Sinica., v. 66, n. 3, p. 351-359, 2023.

LI, D., JIA, Y.,ZHI, J. R., ZHANG, T. Effect of jasmonic acid and ethylene mediate faba bean defense responses to the activity and gene expression of the detoxifying enzyme in Frankliniella occidentalis. Entomological Research, v. 54,n.1, 2024. DOI:10.1111/1748-5967.12699. DOI: https://doi.org/10.1111/1748-5967.12699

LI, D. M., ZHOU, L. Y. Coevolution -- the relationship between insects and plants. Entomological Knowledge., v. 34, n. 1, p. 45-49, 1997.

LI, K. H., HU, J. J. An elite variety of Populus deltoids 'Chuangxin'. Scientia Silvae Sinicae., v. 52, n. 3, p. 130, 2016.

LIU, H., ZHANG, Y., CHEN, J. L. Feeding preference and adaptability of Spodoptera frugiperda(Lepidoptera:Noctuidae)on different wheat cultivars in relation to leaf biochemical contents. Acta Entomologica Sinica., v. 64, n. 2, p. 230-239, 2021.

MOSOLOV, V. V., VALUEVA, T. A. Proteinase inhibitors and their function in plants: a review. Appl Biochem Microbiol., v. 41, p. 227–261, 2005. DOI: https://doi.org/10.1007/s10438-005-0040-6

MUMM, R., HILKER, M. Direct and indirect chemical defence of pine against folivorous insects. Trends in Plant Science., v. 11, n. 7, p. 351-358, 2006. DOI: https://doi.org/10.1016/j.tplants.2006.05.007

NARVAES I D S , BRENA D A , LONGHI S J . Estrutura da regeneração natural em Floresta Ombrófila Mista na Floresta Nacional de São Francisco de Paula, RS. Ciência Florestal, v. 159, n. 4, p. 663-5, 2005. DOI:10.1176/appi.ajp.159.4.663. DOI: https://doi.org/10.5902/198050981871

NIJVELDT, R. J., ELS, V. N., EC, V. H. D., BOELENS, P. G., KLASKE, V. N., AM, V. L. P. Flavonoids: a review of probable mechanisms of action and potential applications. American Journal of Clinical Nutrition., n. 4, p. 418-425, 2001. DOI: https://doi.org/10.1093/ajcn/74.4.418

PALO, R.T. Distribution of birch (Betula SPP.), willow (Salix SPP.), and poplar (Populus SPP.) secondary metabolites and their potential role as chemical defense against herbivores. Journal of Chemical Ecology., v. 10, n. 3, p. 499-520, 1984. DOI: https://doi.org/10.1007/BF00988096

PHILIPPE, R. N., BOHLMANN, J. Poplar defense against insect herbivores. Revue Canadienne De Botanique., v. 85, p. 1111–1126, 2007. DOI: https://doi.org/10.1139/B07-109

PHILIPPE, R. N., RALPH, S. G., MANSFILED, S. D., BOHLMANN, J. Transcriptome profiles of hybrid poplar (Populus trichocarpa× deltoides) reveal rapid changes in undamaged, systemic sink leaves after simulated feeding by forest tent caterpillar (Malacosoma disstria). New Phytol., v. 188, n. 3, p. 787-802, 2010. DOI: https://doi.org/10.1111/j.1469-8137.2010.03392.x

R Core Team. R: A language and environment for statistical computing. In The R Project for Statistical Computing. The R Foundation, 2019. Available at: http://www.R-project.org/. Accessed in: 15 June 2024.

RASMANN, S., VOS, M. D., CASTEEL, C. L., TIAN, D., HALITSCHKE, R., SUN, J. Y., AGRAWAL, A. A., FELTON, G. W., Jander, G. Herbivory in the Previous Generation Primes Plants for Enhanced Insect Resistance. Plant Physiology., v. 158, n. 2, p. 854-863, 2012. DOI: https://doi.org/10.1104/pp.111.187831

RUUHOLA, T., YANG, S., OSSIPOV, V., HAUKIOJA, E. Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Epirrita autumnata. Oecologia., v. 154, n. 4, p. 725-730, 2008. DOI: https://doi.org/10.1007/s00442-007-0869-x

RYAN, C. A. Protease Inhibitors in plants: genes for improving defenses against insects and pathogens. Ann. Rev. Phytopathol., v. 28, p. 425–449, 1990. DOI: https://doi.org/10.1146/annurev.py.28.090190.002233

SELS, J., MATHYS, J., DE, C., BARBARA, M. A., CAMMUE, B. P. A., DE, B., MIGUEL, F. C. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiol Biochem., v. 46, p. 941–950, 2008. DOI: https://doi.org/10.1016/j.plaphy.2008.06.011

STRASSER, R. Challenges in O-glycan engineering of plants. Frontiers in Plant Science., v. 3, p. 218, 2012. DOI: https://doi.org/10.3389/fpls.2012.00218

SUN, Y. M., XU, Y. Q., YANG, L. Research on antioxidant activity of flavonoids from natural materials. Chain Oils and Fats., v. , p. 53-57, 2003.

TRAPNELL, C., WILLIAMS, B. A., PERTEA, G., MOETAZAVI, A., KWAN, G., BAREN, M. J. V., SALZBERG, S. L., WOLD, B. J., PACHTER, L. Transcript assembly and abundance estimation from RNA-Seq reveals thousands of new transcripts and switching among isoforms. Nat Biotechnol., v. 28, p. 511, 2010. DOI: https://doi.org/10.1038/nbt.1621

TSAI, C. J., KAYAL, W. E., HARDING, S. A. Populus, the new model system for investigating phenylpropanoid complexity. International Journal of Applied Science & Engineering., v. 4, n. 3, p. 221-233, 2006.

TUSKAN, G. A., DIFAZIO, S., JANSSIN, S., BOHLMANN, J., GRIGORIEV, I., HELLSTEN, U., PUTNAM, N., RALPH, S., ROMBAUTS, S., SALAMOV, A., et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science., v. 313, p. 1596–604, 2006.

VAN, LOON L., PIERPOINT, W., BOLLER, T., CONEJERO, V. Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep., v. 12, p. 245-264, 1994. DOI: https://doi.org/10.1007/BF02668748

VELASQUEZ, S. M., MARZOL, E., BORASSI, C., POL-FACHIN, L., RICARDI, M. M., MANGANO, S., JUAREZ, S. P. D., SALTER, J. D. S., DOROSE, J. G., MARCUS, S. E., et al. Low Sugar Is Not Always Good: Impact of Specific O-Glycan Defects on Tip Growth in Arabidopsis. Plant Physiology., v. 168, n. 3, p. 808-813, 2015. DOI: https://doi.org/10.1104/pp.114.255521

WANG, J., SONG, Y. Y., HU, L., YANG, M. Y., ZENG, R. S. Plant anti-herbivore defense priming: Concept, mechanisms and application. Chinese Journal of Applied Ecology., v. 29, n. 6, p. 2068-2078, 2018.

WANG, X. W., LV, W., ZHANG, Z. The Resistance of the poplar apecier to the harmful effect of Anoplophora nobilis G. Scientia Silvae Sinicae., v. 23, n. 1, p. 95-99, 1985.

WIKLUND, S., KARLSSON, M., ANTTI, H., JOHNELS, D., SJOSTROM, M., WINGSLE, G., EDLUND, U. A new metabonomic strategy for analysing the growth process of the poplar tree. Plant Biotechnology Journal., v. 3, n. 3, p. 353-362, 2005. DOI: https://doi.org/10.1111/j.1467-7652.2005.00129.x

WU, F., SHI, S. L., KANG, W. J., CHEN, X. M., A, Y., ZHANG, H. H., LI, Z. L. Effects of thrips feeding on secondary metabolites and defense enzymes of alfalfa cultivars. Grassland and Turf., v. 42, n. 6, p. 21-27, 2022.

XIA, L. Q., GUO, T. B., ZHAO, B. G. Research advance on control poplar pests. China Forestry Scinece and Technology., v. 15, n. 5, p. 8-10, 2001.

XING, F., ZHANG, L., GE, W., FAN, H., TIAN, C., MENG, F. Comparative transcriptome analysis reveals the importance of phenylpropanoid biosynthesis for the induced resistance of 84k poplar to anthracnose. BMC Genomics, v. 25, n. 1, 2024. DOI: 10.1186/s12864-024-10209-1. DOI: https://doi.org/10.1186/s12864-024-10209-1

YANG, G., GUAN, X., WANG-PRUSKI, G., WEI, H., YOU, M.S. Advance on induced plant defense genes against insect pests. J. Agric Biotechnol., v. 15, p. 157–166, 2007.

YANG, N. B., WU, S. R., SHEN, L. B., ZHANG, S. Z., YANG, B. P. A review on plant resistance to insect pests. Chinese Journal of Tropical Agriculture., n. 9, p. 61-68, 89, 2014.

YAN, S. C. Silicon Enhanced Italian Ryegrass (Lolium multiflorum) Production and induced defense responses against Fall Armyworm (Spodoptera frugiperda). Agronomy, n.14, 2024. DOI:10.3390/agronomy14122827. DOI: https://doi.org/10.3390/agronomy14122827

YU, Y. C., YANG, M. F., SHANG, S. H., LIU, J. F., YU, X. F. Effects of different insects feeding on tobacco signaling molecules and defense enzymes. Journal of Environmental Entomology., v. 43, n. 4, p. 967-977, 2021.

ZANGERL, A. R. Induced Responses to Herbivory. Plant Pathol., v. 24, n. 1, p. 122-123, 2010. DOI: https://doi.org/10.1046/j.1365-2311.1999.00178.x

ZENG, R. S., SU, Y. J., YE, M., XIE, L. J., CHEN, M., SONG, Y. Y. Plant induced defense and biochemical mechanisms. Journal of South Agricultural University., v. 29, n. 2, p. 1-6, 2008.

ZHANG, Q. W. A new variety of poplar with excellent pulp wood and ecological shelterbelt is Populus×euramericana CL.'74/76'. Scientia Silvae Sinicae., v. 3, p. 113, 1999.

ZHANG, W., CHU, Y., DING, C., ZHANG, B., HUANG, Q., HU, Z., HUANG, R., TIAN, Y., SU, X. Transcriptome sequencing of transgenic poplar (Populus× euramericana'Guariento') expressing multiple resistance genes. BMC Genet., v. 15, p. 1-17, 2014. DOI: https://doi.org/10.1186/1471-2156-15-S1-S7

ZHANG, W. H., LIU, G. J. A review on plant secondary substances in plant resistance to insect pests. Chinese Bulletin of Botany., v. 20, n. 5, p. 522-530, 2003.

ZHANG, X. F., LIU, Y., WANG, M., LI, X. P., LIANG, D. J., WU, Y. Research on Cryptorhynehus lapathi resistance of different poplar varieties. Liaoning Forstry Science and Technology., v. 3, p. 23-24, 2005.

ZHONG, L. Antimicrobial flavonoids from the twigs of Populus nigra x Populus deltoides. Natural Product Research., v. 26, n. 4, p. 307-313, 2012. DOI: https://doi.org/10.1080/14786411003675667

ZHOU, X. Y., YAN, L. Q., LV, Y. T., SUN, L. L., ZHU J. W., CAO C. W. Activities and gene expressions of phenylpropane metabolic enzymes in Populus simonii×P.nigra by herbivore induction of Lymantria dispar(Lepidoptera:Lymantriidae). Scientia Silvae Sinicae., n. 3, p. 108-116, 2021.

Downloads

Publicado

08-08-2025

Como Citar

Guo, L., Wang, Y., Li, L., Wu, C., Zhang, Z., & Wu, Y. (2025). Análise das diferenças transcriptômicas entre dois clones de <i>Populus</i> seção <i>Aigeiros</i> após infestação por insetos. Ciência Florestal, 35, e88195. https://doi.org/10.5902/1980509888195