Abstract
Fall armyworm (FAW) Spodoptera frugiperda (J.E. Smith) is becoming an invasive pest globally, and it causes significant yield losses in sorghum (Sorghum bicolor (L.) Moench) and maize (Zea mays L.). In this study, we demonstrated that sorghum and maize flavonoids affect survival of FAW larvae. Larvae reared on an artificial diet supplemented with sorghum flavonoids showed significant mortality and decreased body weight. When sprayed on leaves of susceptible maize lines, flavonoid extract effectively reduced the growth and increased the mortality of FAW larvae. As FAW is a major pest of maize, we further investigated the larval mortality when reared on maize lines overproducing flavonoids compared to their near-isogenic wild-type lines. The detached leaf assays showed significantly high mortality of larvae that were fed on flavonoid producer lines compared to wild type. The peritrophic membrane that protects the midgut was severely damaged in larvae fed on leaves of flavonoid producer lines compared to wild type. The effectiveness of the flavonoids as feeding deterrents by endogenous expression and exogenous application demonstrates the eco-friendly potential for the management of FAW larvae.
Similar content being viewed by others
References
Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from chewing insects - the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86. https://doi.org/10.1016/j.pbi.2015.05.029
Babu SR, Kalyan RK, Joshi S, Balai CM, Mahla MK, Rokadia P (2019) Report of an exotic invasive pest the fall armyworm, Spodoptera frugiperda (J.E. Smith) on maize in Southern Rajasthan. J Entomol Zool Stud 7:1296–1300. https://www.entomoljournal.com/archives/?year=2019&vol=7&issue=3&ArticleId=5357
Balla A, Bhaskar M, Bagade P, Rawal N (2019) Yield losses in maize (Zea mays) due to fall armyworm infestation and potential IoT-based interventions for its control. J Entomol Zool Stud 7:920–927. https://www.entomoljournal.com/archives/?year=2019&vol=7&issue=5&ArticleId=5789
Barbehenn RV (2001) Roles of peritrophic membranes in protecting herbivorous insects from ingested plant allelochemicals. Arch Insect Biochem Physiol 47:86–99. https://doi.org/10.1002/arch.1039
Barbehenn RV (2002) Gut-based antioxidant enzymes in a polyphagous and a graminivorous grasshopper. J Chem Ecol 28:1329–1347. https://doi.org/10.1023/A:1016288201110
Barbehenn RV, Constabel PC (2011) Tannins in plant-herbivore interactions. Phytochemistry 72:1551–1565. https://doi.org/10.1016/j.phytochem.2011.01.040
Barbehenn RV, Stannard J (2004) Antioxidant defense of the midgut epithelium by the peritrophic envelope in caterpillars. J Insect Physiol 50:783–790. https://doi.org/10.1016/j.jinsphys.2004.05.012
Barbeta BL, Marshall AT, Gillon AD, Craik DJ, Anderson MA (2008) Plant cyclotides disrupt epithelial cells in the midgut of lepidopteran larvae. Proc Natl Acad Sci U S A 105:1221–1225. https://doi.org/10.1073/pnas.0710338104
Bilbo TR, Reay-Jones FPF, Greene JK (2020) Evaluation of insecticide thresholds in late-planted bt and non-bt corn for management of fall armyworm (Lepidoptera: Noctuidae). J Econ Entomol 113:814–823. https://doi.org/10.1093/jee/toz364
Bizuneh GK (2021) The chemical diversity and biological activities of phytoalexins. Adv Tradit Med 21:31–43. https://doi.org/10.1007/s13596-020-00442-w
Boddu J, Jiang C, Sangar V, Olson T, Peterson T, Chopra S (2006) Comparative structural and functional characterization of sorghum and maize duplications containing orthologous myb transcription regulators of 3-deoxyflavonoid biosynthesis. Plant Mol Biol 60:185–199. https://doi.org/10.1007/s11103-005-3568-1
Böttger A, Vothknecht U, Bolle C, Wolf A (2018) Lessons on caffeine. Cannabis & Co. Springer, Cham, pp 171–178. https://doi.org/10.1007/978-3-319-99546
Brookes G, Barfoot P (2020) GM crop technology use 1996–2018: farm income and production impacts. GM Crops Food 11:242–261. https://doi.org/10.1080/21645698.2020.1779574
Chatterjee D, Wittmeyer K, Lee T-f, Cui J, Yennawar NH, Yennawar HP, Meyers BC, Chopra S (2021) Maize unstable factor for orange1 is essential for endosperm development and carbohydrate accumulation. Plant Physiol 186:1932–1950. https://doi.org/10.1093/plphys/kiab183
Chopra S, Athma P, Peterson T (1996) Alleles of the maize P gene with distinct tissue specificities encode Myb-homologous proteins with C-terminal replacements. Plant Cell 8:1149–1158. https://doi.org/10.1105/tpc.8.7.1149
Chopra S, Brendel V, Zhang J, Axtell JD, Peterson T (1999) Molecular characterization of a mutable pigmentation phenotype and isolation of the first active transposable element from Sorghum bicolor. Proc Natl Acad Sci USA 96:15330–15335. https://doi.org/10.1073/pnas.96.26.15330
Chopra S, Gevens A, Svabek C, Wood KV, Peterson T, Nicholson RL (2002) Excision of the candystripe1 transposon from a hyper-mutable y1-cs allele shows that the sorghum y1 gene controls the biosynthesis of both 3-deoxyanthocyanidin phytoalexins and phlobaphene pigments. Physiol Mol Plant Pathol 60:321–330. https://doi.org/10.1006/pmpp.2002.0411
Chopra S, Cocciolone SM, Bushman S, Sangar V, McMullen MD, Peterson T (2003) The maize unstable factor for orange1 is a dominant epigenetic modifier of a tissue specifically silent allele of pericarp color1. Genetics 163:1135–1146. https://doi.org/10.1093/genetics/163.3.1135
Choy KW, Murugan D, Leong X-F, Abas R, Alias A, Mustafa MR (2019) Flavonoids as natural anti-inflammatory agents targeting nuclear factor-kappa B (NFκB) signaling in cardiovascular diseases: a mini review. Front Pharmacol 10:1295. https://doi.org/10.3389/fphar.2019.01295
Cloutier M, Chatterjee D, Elango D, Cui J, Bruns MA, Chopra S (2021) Sorghum root flavonoid chemistry, cultivar, and frost stress effects on rhizosphere bacteria and fungi. Phytobiomes J 5:39–50. https://doi.org/10.1094/PBIOMES-01-20-0013-FI
Davis FM, Ng SS, Williams WP (1992) Visual rating scales for screening whorl-stage corn for resistance to fall armyworm. Miss Agric for Exp Stn Res Bull 186:1–9
Day R et al (2017) Fall armyworm: impacts and implications for Africa. Outlooks Pest Manag 28:196–201. https://doi.org/10.1564/v28_oct_02
De Groote H, Kimenju SC, Munyua B, Palmas S, Kassie M, Bruce A (2020) Spread and impact of fall armyworm (Spodoptera frugiperda JE Smith) in maize production areas of Kenya. Agric Ecosyst Environ 292:106804. https://doi.org/10.1016/j.agee.2019.106804
De Lange ES et al (2020) Spodoptera frugiperda caterpillars suppress herbivore-induced volatile emissions in maize. J Chem Ecol 46:344–360. https://doi.org/10.1007/s10886-020-01153-x
Deole S, Paul N (2018) First report of fall army worm, Spodoptera frugiperda (J.E. Smith), their nature of damage and biology on maize crop at Raipur Chhattisgarh. J Entomol Zool Stud 6:219–221. https://www.entomoljournal.com/archives/?year=2018&vol=6:issue=6:ArticleId=4446.
Dias MC, Pinto DCGA, Silva AMS (2021) Plant flavonoids: chemical characteristics and biological activity. Molecules 26:5377. https://doi.org/10.3390/molecules26175377
Diaz Napal GN, Palacios SM (2015) Bioinsecticidal effect of the flavonoids pinocembrin and quercetin against Spodoptera frugiperda. J Pest Sci 88:629–635. https://doi.org/10.1007/s10340-014-0641-z
Ding Y et al (2020) Genetic elucidation of interconnected antibiotic pathways mediating maize innate immunity. Nat Plants 6:1375–1388. https://doi.org/10.1038/s41477-020-00787-9
Douglas AE (2015) Multiorganismal insects: diversity and function of resident microorganisms. Annu Rev Entomol 60:17–34. https://doi.org/10.1146/annurev-ento-010814-020822
Dudek B, Warskulat A-C, Schneider B (2016) The occurrence of flavonoids and related compounds in flower sections of Papaver nudicaule. Plants (basel) 5:28. https://doi.org/10.3390/plants5020028
Engel P, Moran NA (2013) The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025
Ganiger P, Yeshwanth HM, Muralimohan K, Vinay N, Kumar A, Chandrashekara K (2018) Occurrence of the new invasive pest, fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), in the maize fields of Karnataka, India. Curr Sci 115:621–623. https://doi.org/10.18520/cs/v115/i4/621-623
Goergen G, Kumar PL, Sankung SB, Togola A, Tamò M (2016) First report of outbreaks of the fall armyworm Spodoptera frugiperda (J E Smith) (Lepidoptera, Noctuidae), a new alien invasive pest in west and central Africa. PLoS ONE 11:e0165632. https://doi.org/10.1371/journal.pone.0165632
Goławska S, Sprawka I, Łukasik I, Goławski A (2014) Are naringenin and quercetin useful chemicals in pest-management strategies? J Pest Sci 87:173–180. https://doi.org/10.1007/s10340-013-0535-5
Górniak I, Bartoszewski R, Króliczewski J (2019) Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem Rev 18:241–272. https://doi.org/10.1007/s11101-018-9591-z
Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553. https://doi.org/10.1016/0092-8674(94)90117-1
Grotewold E et al (1998) Engineering secondary metabolism in maize cells by ectopic expression of transcription factors. Plant Cell 10:721–740. https://doi.org/10.2307/3870660
Hardke JT, Leonard BR, Huang F, Jackson RE (2011) Damage and survivorship of fall armyworm (Lepidoptera: Noctuidae) on transgenic field corn expressing Bacillus thuringiensis Cry proteins. Crop Prot 30(2):168–172. https://doi.org/10.1016/j.cropro.2010.10.005
Harper MS, Hopkins TL, Czapla TH (1998) Effect of wheat germ agglutinin on formation and structure of the peritrophic membrane in European corn borer (Ostrinia nubilalis) larvae. Tissue Cell 30:166–176. https://doi.org/10.1016/S0040-8166(98)80065-7
Hopkins TL, Harper MS (2001) Lepidopteran peritrophic membranes and effects of dietary wheat germ agglutinin on their formation and structure. Arch Insect Biochem Physiol 47:100–109. https://doi.org/10.1002/arch.1040
Hruska AJ (2019) Fall armyworm (Spodoptera frugiperda) management by smallholders. CAB Rev 14(043):1–11. https://doi.org/10.1079/PAVSNNR201914043
Huang J, Chen L, Xue B, Liu Q, Ou S, Wang Y, Peng X (2016) Different flavonoids can shape unique gut microbiota profile in vitro. J Food Sci 81:H2273-2279. https://doi.org/10.1111/1750-3841.13411
Ibraheem F, Gaffoor I, Chopra S (2010) Flavonoid phytoalexin-dependent resistance to anthracnose leaf blight requires a functional yellow seed1 in Sorghum bicolor. Genetics 184:915–926. https://doi.org/10.1534/genetics.109.111831
Ibraheem F, Gaffoor I, Tan Q, Shyu CR, Chopra S (2015) A sorghum MYB transcription factor induces 3-deoxyanthocyanidins and enhances resistance against leaf blights in maize. Molecules 20:2388–2404. https://doi.org/10.3390/molecules20022388
Isah T (2019) Stress and defense responses in plant secondary metabolites production. Biol Res 52:39. https://doi.org/10.1186/s40659-019-0246-3
Iwashina T (2003) Flavonoid function and activity to plants and other organisms. Biol Sci Space 17:24–44. https://doi.org/10.2187/bss.17.24
Jing DP, Guo JF, Jiang YY, Zhao JZ, Sethi A, He KL, Wang ZY (2020) Initial detections and spread of invasive Spodoptera frugiperda in China and comparisons with other noctuid larvae in cornfields using molecular techniques. Insect Sci 27:780–790. https://doi.org/10.1111/1744-7917.12700
Kariyat RR et al (2019) Sorghum 3-deoxyanthocyanidin flavonoids confer resistance against corn leaf aphid. J Chem Ecol 45:502–514. https://doi.org/10.1007/s10886-019-01062-8
Kim D-H, Jung E-A, Sohng I-S, Han J-A, Kim T-H, Han MJ (1998) Intestinal bacterial metabolism of flavonoids and its relation to some biological activities. Arch Pharm Res 21:17–23. https://doi.org/10.1007/BF03216747
Krishnan N, Sehnal F (2006) Compartmentalization of oxidative stress and antioxidant defense in the larval gut of Spodoptera littoralis. Arch Insect Biochem Physiol 63:1–10. https://doi.org/10.1002/arch.20135
Kumela T, Simiyu J, Sisay B, Likhayo P, Mendesil E, Gohole L, Tefera T (2019) Farmers’ knowledge, perceptions, and management practices of the new invasive pest, fall armyworm (Spodoptera frugiperda) in Ethiopia and Kenya international. Int J Pest Manag 65:1–9. https://doi.org/10.1080/09670874.2017.1423129
Lee J, Kim S-L, Lee S, Chung MJ, Park YI (2014) Immunostimulating activity of maysin isolated from corn silk in murine RAW 264.7 macrophages. BMB Rep 47:382–387. https://doi.org/10.5483/BMBRep.2014.47.7.191
Lerro CC et al (2015) Organophosphate insecticide use and cancer incidence among spouses of pesticide applicators in the agricultural health study. Occup Environ Med 72:736–744. https://doi.org/10.1136/oemed-2014-102798
Lev-Yadun S, Halpern M (2019) Extended phenotype in action. Two possible roles for silica needles in plants: not just injuring herbivores but also inserting pathogens into their tissues. Plant Signal Behav 14:1609858. https://doi.org/10.1080/15592324.2019.1609858
Li XJ et al (2020) Prediction of migratory routes of the invasive fall armyworm in eastern China using a trajectory analytical approach. Pest Manag Sci 76:454–463. https://doi.org/10.1002/ps.5530
Lima AF, Do Prado Ribeiro L, Gonçalves GLP, Maimone NM, Gissi DS, De Lira SP, Vendramim JD (2021) Searching for bioactive compounds from Solanaceae: lethal and sublethal toxicity to Spodoptera frugiperda and untargeted metabolomics approaches. J Pest Sci 95:1317–1329. https://doi.org/10.1007/s10340-021-01453-5
Lo SC, Weiergang I, Bonham C, Hipskind J, Wood K, Nicholson RL (1996) Phytoalexin accumulation in sorghum: identification of a methyl ether of luteolinidin. Physiol Mol Plant Pathol 49:21–31. https://doi.org/10.1006/pmpp.1996.0036
Luginbill P (1928) The fall armyworm. USDA Tech Bull No. 34, London
Mason CJ, Couture JJ, Raffa KF (2014) Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia 175:901–910. https://doi.org/10.1007/s00442-014-2950-6
Mason CJ et al (2019) Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome. Proc Natl Acad Sci USA 116:15991–15996. https://doi.org/10.1073/pnas.1908748116
Mason CJ, Hoover K, Felton GW (2021) Effects of maize (Zea mays) genotypes and microbial sources in shaping fall armyworm (Spodoptera frugiperda) gut bacterial communities. Sci Rep 11:4429. https://doi.org/10.1038/s41598-021-83497-2
Michereff MFF et al (2019) Variability in herbivore-induced defence signalling across different maize genotypes impacts significantly on natural enemy foraging behaviour. J Pest Sci 92:723–736. https://doi.org/10.1007/s10340-018-1033-6
Mohan S, Ma PW, Pechan T, Bassford ER, Williams WP, Luthe DS (2006) Degradation of the S. frugiperda peritrophic matrix by an inducible maize cysteine protease. J Insect Physiol 52:21–28. https://doi.org/10.1016/j.jinsphys.2005.08.011
Molina-Ochoa J, Hamm JJ, Lezama-Gutiérrez R, López-Edwards M, González-Ramírez M, Pescador-Rubio A (2001) A survey of fall armyworm (Lepidoptera: Noctuidae) Parasitoids in the Mexican States of Michoacán, Colima, Jalisco, and Tamaulipas. Fla Entomol 84:31–36. https://doi.org/10.2307/3496659
Montezano DG, Specht A, Sosa-Gómez DR, Roque-Specht VF, Sousa-Silva JC, Paula-Moraes SD, Peterson JA, Hunt TE (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. Afr Entomol 26(2):286–300
Morohashi K et al (2012) A genome-wide regulatory framework identifies maize pericarp color1 controlled genes. Plant Cell 24:2745–2764. https://doi.org/10.1105/tpc.112.098004
Nagoshi RN, Goergen G, Tounou KA, Agboka K, Koffi D, Meagher RL (2018) Analysis of strain distribution, migratory potential, and invasion history of fall armyworm populations in northern Sub-Saharan Africa. Sci Rep 8:3710. https://doi.org/10.1038/s41598-018-21954-1
Nagoshi RN, Htain NN, Boughton D, Zhang L, Xiao Y, Nagoshi BY, Mota-Sanchez D (2020) Southeastern Asia fall armyworms are closely related to populations in Africa and India, consistent with common origin and recent migration. Sci Rep 10:1421. https://doi.org/10.1038/s41598-020-58249-3
Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: The urgent need for a new concept in agriculture. Front Pub Health 4:148–148. https://doi.org/10.3389/fpubh.2016.00148
Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA (2001) Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr 74:418–425. https://doi.org/10.1093/ajcn/74.4.418
Noonan J, Williams WP, Shan X (2017) Investigation of antimicrobial peptide genes associated with fungus and insect resistance in maize. Int J Mol Sci 18:1938. https://doi.org/10.3390/ijms18091938
Nuessly GS, Webb SE. Insect management for sweet corn. Gainesville; 2017. https://doi.org/10.32473/edis-ig158-2005
Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, van Loon JJA, Dicke M (2014) Modulation of flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor: role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. J Exp Bot 65:2203–2217. https://doi.org/10.1093/jxb/eru096
Palmer NA, Basu S, Heng-Moss T, Bradshaw JD, Sarath G, Louis J (2019) Fall armyworm (Spodoptera frugiperda Smith) feeding elicits differential defense responses in upland and lowland switchgrass. PLoS ONE 14:e0218352. https://doi.org/10.1371/journal.pone.0218352
Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. J Nutr Sci 5:e47–e47. https://doi.org/10.1017/jns.2016.41
Pannuti LE, Baldin EL, Hunt TE, Paula-Moraes SV (2016) On-plant larval movement and feeding behavior of fall armyworm (Lepidoptera: Noctuidae) on reproductive corn stages. Environ Entomol 45:192–200. https://doi.org/10.1093/ee/nvv159
Pechan T, Cohen A, Williams WP, Luthe DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the peritrophic matrix of caterpillars. Proc Natl Acad Sci USA 99:13319–13323. https://doi.org/10.1073/pnas.202224899
Peiffer M, Tooker JF, Luthe DS, Felton GW (2009) Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–656. https://doi.org/10.1111/j.1469-8137.2009.03002.x
Perić-Mataruga V, Lazarević J, Vlahović M, Mrdaković M, Ilijin L (2006) Note: histology of the midgut and peritrophic membrane inLymantria dispar caterpillars fed on leaves of Quercus cerris or Robinia pseudoacacia. Phytoparasitica 34:49–53. https://doi.org/10.1007/BF02981338
Phambala K, Tembo Y, Kasambala T, Kabambe VH, Stevenson PC, Belmain SR (2020) Bioactivity of common pesticidal plants on fall armyworm larvae (Spodoptera frugiperda). Plants (basel) 9(1):112. https://doi.org/10.3390/plants9010112
Poloni A, Schirawski J (2014) Red card for pathogens: phytoalexins in sorghum and maize. Molecules 19:9114–9133. https://doi.org/10.3390/molecules19079114
Reed H. Corn growth stages. https://extension.psu.edu/corn-growth-stages. (2020). Accessed 17 June 2020
Riddick EW (2021) Potential of quercetin to reduce herbivory without disrupting natural enemies and pollinators. Agriculture 11:476. https://doi.org/10.3390/agriculture11060476
Rojas JC, Kolomiets MV, Bernal JS (2018) Nonsensical choices? fall armyworm moths choose seemingly best or worst hosts for their larvae, but neonate larvae make their own choices. PLoS ONE 13:e0197628. https://doi.org/10.1371/journal.pone.0197628
Rwomushana I, Bateman M, Beale T, Beseh P, Cameron K, Chiluba M, Clottey V, Davis T, Day R, Early R, Godwin J, Gonzalez-Moreno P, Kansiime M, Kenis M, Makale F, Mugambi I, Murphy S, Nunda W, Phiri N, Pratt C, Tambo J (2018) Fall armyworm: impacts and implication for Africa. evidence note update. CAB International. https://www.invasive-species.org/wp-content/uploads/sites/2/2019/02/FAW-Evidence-Note-October-2018.pdf
Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177:67–80. https://doi.org/10.1016/S0300-483X(02)00196-8
Sharma M, Cortes-Cruz M, Ahern KR, McMullen M, Brutnell TP, Chopra S (2011) Identification of the pr1 gene product completes the anthocyanin biosynthesis pathway of maize. Genetics 188:69–79. https://doi.org/10.1534/genetics.110.126136
Sharma M, Chai C, Morohashi K, Grotewold E, Snook ME, Chopra S (2012) Expression of flavonoid 3’-hydroxylase is controlled by P1, the regulator of 3-deoxyflavonoid biosynthesis in maize. BMC Plant Biol 12:196. https://doi.org/10.1186/1471-2229-12-196
Simmonds MSJ (2003) Flavonoid–insect interactions: recent advances in our knowledge. Phytochemistry 64:21–30. https://doi.org/10.1016/S0031-9422(03)00293-0
Singh S, Kariyat RR (2020) Exposure to polyphenol-rich purple corn pericarp extract restricts fall armyworm (Spodoptera frugiperda) growth. Plant Signal Behav 15:1784545. https://doi.org/10.1080/15592324.2020.1784545
Singh S, Kaur I, Kariyat R (2021) The multifunctional roles of polyphenols in plant-herbivore interactions. Int J Mol Sci 22(3):1442. https://doi.org/10.3390/ijms22031442
Sisay B, Tefera T, Wakgari M, Ayalew G, Mendesil E (2019) The efficacy of selected synthetic insecticides and botanicals against fall armyworm, Spodoptera frugiperda, in maize. Insects 10(2):45. https://doi.org/10.3390/insects10020045
Snyder BA, Nicholson RL (1990) Synthesis of phytoalexins in sorghum as a site-specific response to fungal ingress. Science 248:1637. https://doi.org/10.1126/science.248.4963.1637
Sparks AN (1979) A review of the biology of the fall armyworm. Fla Entomol 62:82–87. https://doi.org/10.2307/3494083
Speranza S, Knechtl R, Witlaczil R, Schönlechner R (2021) Reversed-phase HPLC characterization and quantification and antioxidant capacity of the phenolic acids and flavonoids extracted from eight varieties of sorghum grown in Austria. Front Plant Sci 12:769151. https://doi.org/10.3389/fpls.2021.769151
Styles ED, Ceska O (1977) The genetic control of flavonoid synthesis in maize. Can J Genet Cytol 19:289–302. https://doi.org/10.1139/g77-032
Styles E, Ceska O (1989) Pericarp flavonoids in genetic strains of Zea mays. Maydica 34:227–237
Summers CB, Felton GW (1996) Peritrophic envelope as a functional antioxidant. Arch Insect Biochem Physiol 32:131–142. https://doi.org/10.1002/(SICI)1520-6327(1996)32:1%3c131::AID-ARCH8%3e3.0.CO;2-2
Tayal M, Somavat P, Rodriguez I, Thomas T, Christoffersen B, Kariyat R (2020) Polyphenol-rich purple corn pericarp extract adversely impacts herbivore growth and development. Insects 11:98. https://doi.org/10.3390/insects11020098
Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic matrix proteins. Insect Biochem Mol Biol 29:87–101. https://doi.org/10.1016/S0965-1748(98)00123-4
Tian D, Tooker J, Peiffer M, Chung SH, Felton GW (2012) Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236:1053–1066. https://doi.org/10.1007/s00425-012-1651-9
Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol (stuttg) 7:581–591. https://doi.org/10.1055/s-2005-873009
Venkateswarlu U, Johnson M, Narasimhulu R, Muralikrishna T (2018) Occurrence of the fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae), a new pest on bajra and sorghum in the fields of agricultural research station, Ananthapuramu, Andhra Pradesh India. J Entomol Zool Stud 6(6):811–813. https://www.entomoljournal.com/archives/?year=2018&vol=6&issue=6&ArticleId=4541
War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320. https://doi.org/10.4161/psb.21663
War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC (2018) Plant defence against herbivory and insect adaptations. AoB Plants 10:ply037. https://doi.org/10.1093/aobpla/ply037
Westbrook JK, Nagoshi RN, Meagher RL, Fleischer SJ, Jairam S (2016) Modeling seasonal migration of fall armyworm moths. Int J Biometeorol 60:255–267. https://doi.org/10.1007/s00484-015-1022-x
Wharton PS, Nicholson RL (2000) Temporal synthesis and radiolabelling of the sorghum 3-deoxyanthocyanidin phytoalexins and the anthocyanin, cyanidin 3-dimalonyl glucoside. New Phytol 145:457–469. https://doi.org/10.1046/j.1469-8137.2000.00600.x
Wiseman BR, Snook ME, Isenhour DJ, Mihm JA, Widstrom NW (1992) Relationship between growth of corn earworm and fall armyworm larvae (Lepidoptera: Noctuidae) and maysin concentration in corn silks. J Econ Entom 85:2473–2477. https://doi.org/10.1093/jee/85.6.2473
Wittmeyer K, Cui J, Chatterjee D, Lee TF, Tan Q, Xue W, Jiao Y, Wang PH, Gaffoor I, Ware D, Meyers BC, Chopra S (2018) The dominant and poorly penetrant phenotypes of maize Unstable factor for orange1 are caused by dna methylation changes at a linked transposon. Plant Cell 30:3006–3023. https://doi.org/10.1105/tpc.18.00546
Yang F, Qureshi JA, Leonard BR, Head GP, Niu Y, Huang F (2013) Susceptibility of Louisiana and Florida populations of Spodoptera frugiperda (Lepidoptera: Noctuidae) to pyramided Bt corn containing Genuity®Vt Double Pro™ and Smartstax™ Traits. Fla Entomol 96:714–723. https://doi.org/10.1653/024.096.0303
Acknowledgements
We thank the staff of Penn State Russel E. Larson farm, Plant Science greenhouse, and Microscopy Core Facilities for their assistance.
Funding
This work was supported by USDA/NIFA awards 2019-70006-30442 to SC, JB, and GWF, 2020-67013-31918 to SC and GWF, AES awards 4780 and 4613 to SC, NESARE GNE19-195-33243 graduate student grant award to DC. DC was partially supported by an International Fellowship from ICAR, India, and a graduate assistantship from Plant Science Department, Penn State University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that there is no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed while conducting this research.
Additional information
Communicated by Antonio Biondi.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chatterjee, D., Lesko, T., Peiffer, M. et al. Sorghum and maize flavonoids are detrimental to growth and survival of fall armyworm Spodoptera frugiperda. J Pest Sci 96, 1551–1567 (2023). https://doi.org/10.1007/s10340-022-01535-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-022-01535-y