Abstract
Brazil is the world’s largest producer of soybeans, and the crop is one of the most important contributors to the economy. Soybeans often suffer damage from insect pests, such as Anticarsia gemmatalis, which also attacks other crops. Genotypes of soybeans have been used to decipher the resistance mechanisms by evaluating the activity of defense compounds such as protease inhibitors (PIs) and flavonols. However, the genetic determinants of resistance have not been thoroughly investigated. This study used the response of resistant and susceptible genotypes of soybean to evaluate genes and proteins responsive to caterpillar attack and involved in the biosynthesis of methylated and glycosylated flavonols. Rutin and isorhamnetin rutinoside were produced constitutively in the resistant genotypes IAC 17 and IAC 100. Following insect attack, genes encoding flavonol synthase and methyltransferases were highly upregulated in IAC 17. Some herbivory defense responses appear constitutive, while others were induced or JA-independent, as verified for flavonol levels. Salicylic acid levels were higher in IAC 17 and IAC 100. Proteins not yet characterized for their involvement in plant–insect interactions, such as transmembrane receptors and transcription factors, were upregulated in the resistant genotype IAC 17. It appears constitutive flavonol biosynthesis in both IAC 17 and IAC 100 was inherited from the PI229358 parent, making the two genotypes good genetic sources to study flavonol biosynthesis and their relationship with insect resistance.
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Aryal UK, Krochko JE, Ross ARS (2012) Identification of phosphoproteins in Arabidopsis thaliana leaves using polyethylene glycol fractionation, immobilized metal-ion affinity chromatography, two-dimensional gel electrophoresis and mass spectrometry. J Proteome Res 11:425–437. https://doi.org/10.1021/pr200917t
Axelrod B, Cheesbrough TM, Laakso S (1981) Lipoxygenase from soybeans. In: Lowenstein JM (ed) Methods in enzymology 71. Academic Press, New York
Bacalhau FB, Dourado PM, Horikoshi RJ, Carvalho RA, Semeão A, Martinelli S, Berger GU, Head GP, Salvadori JR, Bernardi O (2020) Performance of genetically modified soybean expressing the Cry1A.105, Cry2Ab2, and Cry1Ac proteins against key Lepidopteran pests in Brazil. J Econ Entomol 113:2883–2889. https://doi.org/10.1093/jee/toaa236
Bernardi O, Malvestiti GS, Dourado PM, Oliveira WS, Martinelli S, Berger GU, Omoto C (2012) Assessment of the high-dose concept and level of control provided by MON 87701 × MON 89788 soybean against Anticarsia gemmatalis and Pseudoplusia includens (Lepidoptera: Noctuidae) in Brazil. Pest Manag Sci 68:1083–1091. https://doi.org/10.1002/ps.3271
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1006/abio.1976.9999.PMID942051
Canassa VF, Baldin ELL, Bentivenha JPF, Pannuti LER, Lourenção AL (2017) Characterization of antixenosis to Dichelops melacanthus (Hemiptera: Pentatomidae) in soybean genotypes. International Journal of Pest Management 63:112–118. https://doi.org/10.1080/09670874.2016.1227884
Cenci A, Rouard M (2017) Evolutionary analyses of GRAS transcription factors in angiosperms. Front Plant Sci 8:1–15. https://doi.org/10.3389/fpls.2017.00273
Chang HX, Hartman GL (2017) characterization of insect resistance loci in the USDA soybean germplasm collection using genome-wide association studies. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.00670
Chen JY, Dai XF (2010) Cloning and characterization of the Gossypium hirsutum major latex protein gene and functional analysis in Arabidopsis thaliana. Planta 23:861–873. https://doi.org/10.1007/s00425-009-1092-2
Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol 143:1954–1967. https://doi.org/10.1104/pp.106.095588
Coelho M, Godoy AF, Baptista YA, Bentivenha JPF, Lourenção AL, Baldin ELL, Catchot AL (2020) Assessing soybean genotypes for resistance to Helicoverpa armigera (Lepidoptera: Noctuidae). J Economic Entomol 113:471–481. https://doi.org/10.1093/jee/toz269
Coutinho FS, Santos DS, Lima LL, Vital CE, Santos LA, Pimenta MR, Silva JC, Ramos JRLS, Metha A, Fontes EPB, Ramos HJO (2019) Mechanism of the drought tolerance of a transgenic soybean overexpressing the molecular chaperone BiP Physiol. Mol Biol Plants 1:1–16. https://doi.org/10.1007/s12298-019-00643-x
Da Silva FF, De Almeida OMG, Brumano MHN et al (2007) Lipoxygenase-induced defense of soybean varieties to the attack of the velvetbean caterpillar (Anticarsia gemmatalis Hübner). J Pest Sci 80:241–247. https://doi.org/10.1007/s10340-007-0179-4
Da Silva D, Hoffmann-Campo C, De Freitas BA, De Freitas BR, De Oliveira M, Moscardi F (2012) Biological characteristics of Anticarsia gemmatalis (Lepidoptera: Noctuidae) for three consecutive generations under different temperatures: Understanding the possible impact of global warming on a soybean pest. Bull Entomol Res 102:285–292. https://doi.org/10.1017/S0007485311000642
Dakora FD, Phillips DA (1996) Diverse functions of isoflavonoids in legumes transcend anti-microbial definitions of phytoalexins. Physiol Mol Plant Pathol 49:1–20. https://doi.org/10.1006/pmpp.1996.0035
Decker D, Kleczkowski LA (2019) UDP-sugar producing pyrophosphorylases: distinct and essential enzymes with overlapping substrate specificities, providing de novo precursors for glycosylation reactions. Front Plant Sci 9:1822. https://doi.org/10.3389/fpls.2018.01822
Fan R, Wang H, Wang Y, Yu D (2012) Proteomic analysis of soybean defense response induced by cotton worm (Prodenia litura, fabricius) feeding. Proteome Science 10:1–11. https://doi.org/10.1186/1477-5956-10-16
Farmer EE, Ryan CA (1992) Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134. https://doi.org/10.1105/tpc.4.2.129
Faustino VA, Gouveia AS, Coutinho FS, Júnior NRS, Barros RA, Cabrera YM, Vital CE, Loriato VAP, Martins LGC, Fontes EPB, Ramos HJO, Oliveira MGA (2021) Soybean plants under simultaneous signals of drought and Anticarsia gemmatalis herbivory trigger gene expression and metabolic pathways reducing larval survival. Environ Exp Botany. https://doi.org/10.1016/j.envexpbot.2021.104594
Feng Y, Zhang S, Li J, Pei R, Tian L, Qi J, Azam M, Agyenim-Boateng KG, Shaibu AS, Liu Y, Zhu Z, Li B, Sun J (2023) Dual-function C2H2-type zinc-finger transcription factor GmZFP7 contributes to isoflavone accumulation in soybean. New Phytol 237:1794–1809. https://doi.org/10.1111/nph.18610
Fernandes FO, Rosa APA, Abreu JA, Christ LM, Belarmino LC, Martins JFS (2020) Performance of soybean cultivars in integrated pest management in lowland agroecosystem. Revista Brasileira De Ciências Agrárias 15(e5726):2020
Fugi CGQ, Lourenção AL, Parra JRP (2005) Biology of Anticarsia gemmatalis on soybean genotypes with different degrees of resistance to insects. Scientia Agricola 62:31–35. https://doi.org/10.1590/S0103-90162005000100006
Gatehouse JA (2011) Prospects for using proteinase inhibitors to protect transgenic plants against attack by herbivorous insects. Curr Protein Peptide Sci 12:409–416. https://doi.org/10.2174/138920311796391142
Gill RS, Gupta K, Taggar GK, Taggar MS (2010) Role of oxidative enzymes in plant defenses against herbivory. Acta Phytopathologica Et Entomologica Hungarica 45:277–290. https://doi.org/10.1556/APhyt.45.2010.2.4
Goel MK, Khanna P, Kishore J (2010) Understanding survival analysis: Kaplan-Meier estimate. Int J Ayurveda Res 1:274–278. https://doi.org/10.4103/0974-7788.76794
Gomez JD, Vital CE, Oliveira MGA, Ramos HJO (2018) Broad range flavonoid profiling by LC/MS of soybean genotypes contrasting for resistance to Anticarsia gemmatalis (Lepidoptera: Noctuidae). PLoS ONE 13:1–24. https://doi.org/10.1371/journal.pone.0205010
Gomez JD, Pinheiro VJM, Silva JC, Romero JV, Meriño-Cabrera Y, Coutinho FS, Lourenção AL, Serrão JE, Vital CE, Fontes EPB, Oliveira MGA, Ramos HJO (2020) Leaf metabolic profiles of two soybean genotypes differentially affect the survival and the digestibility of Anticarsia gemmatalis caterpillars. Plant Physiol Biochem 155:196–212. https://doi.org/10.1016/j.plaphy.2020.07.010
Ha J, Kang YG, Lee T, Kim M, Yoon MY, Lee E, Yang X, Kim D, Kim YJ, Lee TR, Kim MY, Lee SH (2019) Comprehensive RNA sequencing and co-expression network analysis to complete the biosynthetic pathway of coumestrol, a phytoestrogen. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-018-38219-6
Horikoshi RJ, Bernardi O, Godoy DN, Semeão AA, Willse A, Corazza GO, Ruthes E, Fernandes DS, Sosa-Gómez DR, Bueno AF, Omoto C, Berger GU, Corrêa AS, Martinelli S, Dourado PM, Head G (2021) Resistance status of lepidopteran soybean pests following large-scale use of MON 87701 × MON 89788 soybean in Brazil. Sci Rep 29:21323. https://doi.org/10.1038/s41598-021-00770-0
Hou M, Zhang Y, Mu G et al (2020) Molecular cloning and expression characterization of flavonol synthase genes in peanut (Arachis hypogaea). Sci Rep 10:17717. https://doi.org/10.1038/s41598-020-74763-w
Jing M, Ma H, Li H, Guo B, Zhang X, Ye W, Wang Y (2015) Differential regulation of defense-related proteins in soybean during compatible and incompatible interactions between Phytophthora sojae and soybean by comparative proteomic analysis. Plant Cell Rep 34:1263–1280. https://doi.org/10.1007/s00299-015-1786-9
Jones AM, Thomas V, Bennett MH, Mansfield J, Grant M (2006) Modifications to the Arabidopsis defense proteome occur prior to significant transcriptional change in response to inoculation with Pseudomonas syringae. Plant Physiol 142:1603–1620. https://doi.org/10.1038/s41598-018-38219-6
Kerchev PL, Fenton B, Foyer CH, Hancock RD (2011) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant, Cell Environ 35:441–453. https://doi.org/10.1111/j.1365-3040.2011.02399.x
Lee K, Kang H (2016) Emerging roles of RNA-binding proteins in plant growth, development, and stress responses. Mol Cells 39:179–185. https://doi.org/10.14348/molcells.2016.2359
Leubner-Metzger G, Meins FJR, Datta SK, Muthukrishnan S (1999) Functions and regulation of plant beta-1,3-glucanases (PR-2), Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 49–76
Lima LL, Mesquita R, Balbi BP, Coutinho FS, Silva C, Carmo FMS, Vital CE, Mehta A, Loureiro ME, Fontes EPB, Barros EG, Ramos HJO (2019) Proteomic and metabolomic analysis of a drought tolerant soybean cultivar from Brazilian savanna. Crop Breeding Genetics Genomics. https://doi.org/10.20900/cbgg20190022
Liu X, Lam E (1994) Two binding sites for the plant transcription factor ASF-1 can respond to auxin treatments in transgenic tobacco. J Biol Chem 269:668–675
Liu H, Su B, Zhang H, Gong J, Zhang B, Liu Y, Du L (2019) Identification and functional analysis of a flavonol synthase gene from grape hyacinth. Molecules 24:1–15. https://doi.org/10.3390/molecules24081579
Lourenção AL, Costa AS, Miranda, MAC (1989) Sources of resistance to insect pests and virus vectors in the soybean germplasm tested at IAC. In: World Soybean Research Conference IV. Proceedings. A.J. Pascale (ed.). Buenos Aires, Argentina, pp1578–1580.
Maffei ME, Mithöfer A, Boland W (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68:2946–2959. https://doi.org/10.1016/j.phytochem.2007.07.016
Mantzoukas S, Eliopoulos PA (2020) Endophytic entomopathogenic fungi: a valuable biological control tool against plant pests. Applied Sci 40:1–13. https://doi.org/10.3390/app10010360
Marques LH, Santos AC, Castro BA, Moscardini VF, Rossetto J, Silva OAN, Zobiole LHS, Valverde-Garcia P, Babcock JM, Storer NP, Rule DM, Fernandes AO (2017) Field evaluation of soybean transgenic event DAS-81419-2 expressing Cry1F and Cry1Ac proteins for the control of secondary lepidopteran pests in Brazil. Crop Prot 96:109–115. https://doi.org/10.1016/j.cropro.2017.02.014
Matos NFC, Zanuncio JC, Cruz I, Torres JB (2002) Nymphal development of Podisus nigrispinus (Heteroptera, Pentatomidae) preying on larvae of Anticarsia gemmatalis (Lepidoptera, Noctuidae) fed with resistant and susceptible soybeans. Revista Brasileira De Entomologia 46:237–241. https://doi.org/10.1590/S0085-56262002000300002
Melo BP, Fraga OT, Silva JCF, Ferreira DO, Brustolini OJB, Carpinetti PA, Machado JPB, Reis PAB, Fontes EPB (2018) Revisiting the Soybean GmNAC Superfamily. Front Plant Sci 9:1864. https://doi.org/10.3389/fpls.2018.01864
Meng Y, Zhang Q, Zhang M, Gu B, Huang G, Wang Q et al (2015) The protein disulfide isomerase 1 of Phytophthora parasitica (PpPDI1) is associated with the haustoria-like structures and contributes to plant infection. Front Plant Sci 6:1–10. https://doi.org/10.3389/fpls.2015.00632
Moraes MCB, Laumann R, Sujii ER, Pires C, Borges M (2005) Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi. Entomol Exp Appl 115:227–237. https://doi.org/10.1111/j.1570-7458.2005.00290.x
Morris JS, Caldo KM, Liang S, Facchini P (2020) PR10/Bet v 1-like proteins as novel contributors to plant biochemical diversity. ChemBioChem. https://doi.org/10.1002/cbic.202000354
Oerke EC (2006) Crop losses to pests. J Agric Sci 144:31–43. https://doi.org/10.1017/S0021859605005708
Ondzighi CA, Christopher DA, Cho EJ, Chang SC, Staehelin LA (2008) Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20:2205–2220. https://doi.org/10.1105/tpc.108.058339
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2013) Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. J Exp Bot 64:445–458. https://doi.org/10.1093/jxb/ers354
Paixão GP, Lourenção AL, Silva CR, Cordeiro G, Barros RA, Oliveira JA, Visôtto LE, Oliveira MGA (2016) Active response of soybean to defoliator Anticarsia gemmatalis Hübner: strategies to overcome protease inhibitor production. Idesia (arica) 34:69–75. https://doi.org/10.4067/S0718-34292016005000010
Quezada EH, García GX, Arthikala MK, Melappa G, Lara M, Nanjareddy K (2019) Cysteine-rich receptor-like kinase gene family identification in the phaseolus genome and comparative analysis of their expression profiles specific to Mycorrhizal and Rhizobial Symbiosis. Genes 10:1–21. https://doi.org/10.3390/genes10010059
Radauer C, Lackner P, Breiteneder H (2008) The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol Biol 8:1–19. https://doi.org/10.1186/1471-2148-8-286
Rojo E, Solano R, Sanchez-Serrano J (2003) Interactions between signaling compounds involved in plant defense. J Plant Growth Regul 22:82–98. https://doi.org/10.1007/s00344-003-0027-6
Schlick-Souza EU, Baldin ELL, Morando R, Lourenção AL (2018) Antixenosis to Chrysodeixis includens (Lepidoptera: Noctuidae) among soybean genotypes. Bragantia 77:124–133. https://doi.org/10.1590/1678-4499.2016449
Shi J, Li W, Gao Y, Wang B, Li Y, Song Z (2017) Enhanced rutin accumulation in tobacco leaves by overexpressing the NtFLS2 gene. Biosci Biotechnol Biochem 81:1721–1725. https://doi.org/10.1080/09168451.2017.1353401
Shivaji R, Camas A, Ankala A, Engelberth J, Tumlinson JH, Williams WP, Wilkinson PR, Luthe DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191. https://doi.org/10.1007/s10886-010-9752-z
Souza ES, Silva JPGF, Baldin ELL, Pierozzi CG, Cunha LS, Canassa VF, Lourenção AL (2015) Response of soybean genotypes challenged by a stink bug complex (Hemiptera: Pentatomidae). J Econ Entomol 109:898–906. https://doi.org/10.1093/jee/tov341
Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochem Biophys Acta 1577:1–9. https://doi.org/10.1016/S0167-4781(02)00417-7
Tang D, Wnag G, Zhou JM (2017) Receptor kinases in plant-pathogen interactions: more than pattern recognition. Plant Cell Adv Publ 29:618–637. https://doi.org/10.1105/tpc.16.00891
Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C (2005) Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J 44:100–113. https://doi.org/10.1111/j.1365-313X.2005.02513.x
Treutter D (2008) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591. https://doi.org/10.1055/s-2005-873009
Valle GE, Lourenção AL, Pinheiro JB (2012) Adult attractiveness and oviposition preference of Bemisia tabaci biotype B in soybean genotypes with different trichome density. J Pest Sci 85:431–442. https://doi.org/10.1007/s10340-012-0443-0
Vasconcelos ES, Reis MS, Cruz CD, Sediyama T, Scapim CA (2010) Adaptability and stability of semilate and late maturing soybean genotypes in Minas Gerais state. Acta Scientiarum-Agronomy 32:411–415. https://doi.org/10.4025/actasciagron.v32i3.8249
Verhage A, Van Wees SCM, Pieterse CMJ (2010) Plant immunity: it’s the hormones talking, but what do they say? Plant Physiol 154:536–540. https://doi.org/10.1104/pp.110.161570
Wang Y, Yang L, Chen X, Ye T, Bao Z, Liu R, Wu Y, Chan Z (2016) Major latex protein-like protein 43 (MLP43) functions as a positive regulator during abscisic acid responses and confers drought tolerance in Arabidopsis thaliana. J Exp Bot 67:421–434. https://doi.org/10.1093/jxb/erv477
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behavior 7:1306–1320. https://doi.org/10.4161/psb.21663
Wilkinson B, Gilbert HF (2005) Protein disulfide isomerase. Methods Enzymol 290:26
Zeng W, Sun Z, Cai Z, Chen H, Lai Z, Yang S, Tang X (2017) Proteomic analysis by iTRAQ-MRM of soybean resistance to Lamprosema Indicate. BMC Genomics 18:1–22. https://doi.org/10.1186/s12864-017-3825-0
Zhang YL, Tessaro MJ, Lassner M, Li X (2003) Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15:2647–2653. https://doi.org/10.1105/tpc.014894
Vick BA, Zimmerman DC (1987) The Lipoxygenase Pathway. In: Stumpf PK, Mudd JB, Nes WD (eds) The Metabolism, Structure, and Function of Plant Lipids. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-5263-1_71
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The authors would like to thank NuBioMol (Center for Analyses of Biomolecules-UFV, Brazil) for the infrastructure and technical assistance. This study was supported by the National Institute of Science and Technology in Plant–Pest Interaction (INCT-IPP), Instituto Agronômico de Campinas (IAC), the Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
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Pinheiro, V.J.M., Gómez, J.D., Gouveia, A.S. et al. Gene expression, proteomic, and metabolic profiles of Brazilian soybean genotypes reveal a possible mechanism of resistance to the velvet bean caterpillar Anticarsia gemmatalis. Arthropod-Plant Interactions 18, 15–32 (2024). https://doi.org/10.1007/s11829-023-10030-9
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DOI: https://doi.org/10.1007/s11829-023-10030-9