Abstract
A large percentage of crop loss is due to insect damage, especially caterpillar damage. Plant chitinases are considered excellent candidates to combat these insects since they can degrade chitin in peritrophic matrix (PM), an important protective structure in caterpillar midgut. Compared to chemical insecticides, chitinases could improve host plant resistance and be both economically and environmentally advantageous. The focus of this research was to find chitinase candidates that could improve plant resistance by effectively limiting caterpillar damage. Five classes of endochitinase (I-V) genes were characterized in the maize genome, and we isolated and cloned four chitinase genes (chitinase A, chitinase B, chitinase I, and PRm3) present in two maize (Zea mays L.) inbred lines Mp708 and Tx601, with different levels of resistance to caterpillar pests. We also investigated the expression of these maize chitinases in response to fall armyworm (Spodoptera frugiperda, FAW) attack. The results indicated that both chitinase transcript abundance and enzymatic activity increased in response to FAW feeding and mechanical wounding. Furthermore, chitinases retained activity inside the caterpillar midgut and enzymatic activity was detected in the food bolus and frass. When examined under scanning electron microscopy, PMs from Tx601-fed caterpillars showed structural damage when compared to diet controls. Analysis of chitinase transcript abundance after caterpillar feeding and proteomic analysis of maize leaf trichomes in the two inbreds implicated chitinase PRm3 found in Tx601 as a potential insecticidal protein.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Code Availability
Not applicable.
References
Adang MJ, Spence KD (1981) Surface morphology of peritrophic membrane formation in the cabbage looper. Trichoplusia Ni Cell Tissue Res 218:141–147. https://doi.org/10.1007/bf00210100
Aranda E, Sanchez J, Peferoen M, Guereca L, Bravo A (1996) Interactions of Bacillus thuringiensis crystal proteins with the midgut epithelial cells of Spodoptera frugiperda (Lepidoptera: Noctuidae). J Invertebr Pathol 68:203–212. https://doi.org/10.1006/jipa.1996.0087
Beintema JJ (1994) Structural features of plant chitinases and chitin-binding proteins. FEBS Lett 350:159–163
Bekesiova B, Hraska S, Libantova J, Moravcikova J, Matusikova I (2008) Heavy-metal stress induced accumulation of chitinase isoforms in plants. Mol Biol Rep 35:579–588. https://doi.org/10.1007/s11033-007-9127-x
Bernardi D et al (2015) Cross-Resistance between Cry1 Proteins in Fall Armyworm (Spodoptera frugiperda) May Affect the Durability of Current Pyramided Bt Maize Hybrids in Brazil. PLoS One 10:e0140130. https://doi.org/10.1371/journal.pone.0140130
Bohorova N et al (2001) Novel synthetic Bacillus thuringiensiscry1B gene and the cry1B-cry1Ab translational fusion confer resistance to southwestern corn borer, sugarcane borer and fall armyworm in transgenic tropical maize. Theoret Appl Genet 103:817–826. https://doi.org/10.1007/s001220100686
Bokonon-Ganta A, Bernal JS, Pietrantonio PV, SÉTamou M (2003) Survivorship and development of fall armyworm, Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), on conventional and transgenic maize cultivars expressing Bacillus thuringiensis Cry9C and Cry1A(b) endotoxins. Int J Pest Manag 49:169
Bolognesi R, Arakane Y, Muthukrishnan S, Kramer KJ, Terra WR, Ferreira C (2005) Sequences of cDNAs and expression of genes encoding chitin synthase and chitinase in the midgut of Spodoptera frugiperda. Insect Biochem Mol Biol 35:1249–1259. https://doi.org/10.1016/j.ibmb.2005.06.006
Bosak EJ (2011) Using a developmental comparison to decipher priming of induced defenses in maize and its effects on a generalist herbivore. The Pennsylvania State University
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 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brandt CR, Adang MJ, Spence KD (1978) The peritrophic membrane: Ultrastructural analysis and function as a mechanical barrier to microbial infection in Orgyia pseudotsugata. J Invertebr Pathol 32:12–24
Broadway R et al (1998) Novel Chitinolytic Enzymes with Biological Activity Against Herbivorous Insects. J Chem Ecol 24:985–998. https://doi.org/10.1023/a:1022346301626
Brooks TD, Bushman BS, Williams WP, McMullen MD, Buckley PM (2007) Genetic basis of resistance to fall armyworm (Lepidoptera: Noctuidae) and southwestern corn borer (Lepidoptera: Crambidae) leaf-feeding damage in maize. J Econ Entomol 100:1470–1475
Brooks TD, Willcox MC, Williams WP, Buckley PM (2005) Quantitative Trait Loci Conferring Resistance to Fall Armyworm and Southwestern Corn Borer Leaf Feeding Damage This paper is a joint contribution of USDA-ARS and the Mississippi Agricultural and Forestry Experiment Station and is published as journal no. J10582 of the Miss. Agric. and Forestry Exp. Stn Crop Sci 45:2430–2434. https://doi.org/10.2135/cropsci2004.0656
Chang YM, Luthe DS, Davis FM, Williams WP (2000) Influence of whorl region from resistant and susceptible corn genotypes on fall armyworm (Lepidoptera: Noctuidae) growth and development. J Econ Entomol 93:477–483
Chaudet MM, Naumann TA, Price NPJ, Rose DR (2014) Crystallographic structure of ChitA, a glycoside hydrolase family 19, plant class IV chitinase from Zea mays. Protein Sci : A Publication of the Protein Society 23:586–593. https://doi.org/10.1002/pro.2437
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/10.2307/40065405
Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci U S A 102:19237–19242. https://doi.org/10.1073/pnas.0509026102
Chuang WP, Herde M, Ray S, Castano-Duque L, Howe GA, Luthe DS (2014) Caterpillar attack triggers accumulation of the toxic maize protein RIP2. New Phytol 201:928–939. https://doi.org/10.1111/nph.12581
Clarke HRG, Lawrence SD, Flaskerud J, Korhnak TE, Gordon MP, Davis JM (1998) Chitinase accumulates systemically in wounded poplar trees. Physiol Plant 103:154–161. https://doi.org/10.1034/j.1399-3054.1998.1030202.x
Cohen-Kupiec R, Chet I (1998) The molecular biology of chitin digestion. Curr Opin Biotechnol 9:270–277
Corrado G et al (2008) The Chitinase A from the baculovirus AcMNPV enhances resistance to both fungi and herbivorous pests in tobacco. Transgenic Res 17:557–571. https://doi.org/10.1007/s11248-007-9129-4
Didierjean L, Frendo P, Nasser W, Genot G, Marivet J, Burkard G (1996) Heavy-metal-responsive genes in maize: identification and comparison of their expression upon various forms of abiotic stress. Planta 199:1–8
Donaldson JR, Nanduri B, Burgess SC, Lawrence ML (2009) Comparative Proteomic Analysis of Listeria monocytogenes Strains F2365 and EGD. Appl Environ Microbiol 75:366–373. https://doi.org/10.1128/aem.01847-08
Dow J (1992) pH gradients in Lepidopteran midgut. J Exp Biol 172:355–375
Eckardt NA (2008) Chitin signaling in plants: insights into the perception of fungal pathogens and rhizobacterial symbionts. Plant Cell 20:241–243. https://doi.org/10.1105/tpc.108.058784
Elle E, Hare JD (2000) No Benefit of Glandular Trichome Production in Natural Populations of Datura wrightii? Oecologia 123:57–65. https://doi.org/10.2307/4222591
Fescemyer HW, Sandoya GV, Gill TA, Ozkan S, Marden JH, Luthe DS (2013) Maize toxin degrades peritrophic matrix proteins and stimulates compensatory transcriptome responses in fall armyworm midgut. Insect Biochem Mol Biol 43:280–291. https://doi.org/10.1016/j.ibmb.2012.12.008
Finn RD et al (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230. https://doi.org/10.1093/nar/gkt1223
Flach J, Pilet PE, Jolles P (1992) What’s new in chitinase research? Experientia 48:701–716
Flagel L et al (2018) Mutational disruption of the ABCC2 gene in fall armyworm, Spodoptera frugiperda, confers resistance to the Cry1Fa and Cry1A.105 insecticidal proteins. Sci Rep 8:7255. https://doi.org/10.1038/s41598-018-25491-9
Freeling M, Lane B (1994) The Maize Leaf. In: Freeling M, Walbot V (eds) The Maize Handbook. Springer Lab Manuals. Springer, New York, pp 17–28. https://doi.org/10.1007/978-1-4612-2694-9_3
Gomez Ramirez M, Rojas Avelizapa LI, Rojas Avelizapa NG, Cruz Camarillo R (2004) Colloidal chitin stained with Remazol Brilliant Blue R, a useful substrate to select chitinolytic microorganisms and to evaluate chitinases. J Microbiol Methods 56:213–219. https://doi.org/10.1016/j.mimet.2003.10.011
Gongora CE, Wang S, Barbehenn RV, Broadway RM (2001) Chitinolytic Enzymes from Streptomyces Albidoflavus Expressed in Tomato Plants: Effects on Trichoplusia Ni Entomologia Experimentalis Et Applicata 99:193–204. https://doi.org/10.1046/j.1570-7458.2001.00817.x
Gooday GW (1999) Aggressive and Defensive Roles for Chitinases Exs 87:157–169
Gopalakrishnan B, Muthukrishnan S, Kramer KJ (1995) Baculovirus-mediated expression of a Manduca sexta chitinase gene: Properties of the recombinant protein. Insect Biochem Mol Biol 25:255–265. https://doi.org/10.1016/0965-1748(94)00070-X
Graham LS, Sticklen MB (1994) Plant Chitinases Canadian Journal of Botany 72:1057–1083. https://doi.org/10.1139/b94-132
Grover A (2012) Plant Chitinases: Genetic Diversity and Physiological Roles. Crit Rev Plant Sci 31:57–73. https://doi.org/10.1080/07352689.2011.616043
Gutierrez-Moreno R, Mota-Sanchez D, Blanco CA, Whalon ME, Teran-Santofimio H, Rodriguez-Maciel JC, DiFonzo C (2019) Field-Evolved Resistance of the Fall Armyworm (Lepidoptera: Noctuidae) to Synthetic Insecticides in Puerto Rico and Mexico. J Econ Entomol 112:792–802. https://doi.org/10.1093/jee/toy372
Hall BG (2013) Building Phylogenetic Trees from Molecular Data with MEGA. Mol Biol Evol. https://doi.org/10.1093/molbev/mst012
Hamel F, Boivin R, Tremblay C, Bellemare G (1997) Structural and Evolutionary Relationships Among Chitinases of Flowering Plants. J Mol Evol 44:614–624. https://doi.org/10.1007/pl00006184
Hamid R, Khan MA, Ahmad M, Ahmad MM, Abdin MZ, Musarrat J, Javed S (2013) Chitinases: An update. J Pharm Bioallied Sci 5:21–29. https://doi.org/10.4103/0975-7406.106559
Harrison RL, Puttler B, Popham HJR (2008) Genomic sequence analysis of a fast-killing isolate of Spodoptera frugiperda multiple nucleopolyhedrovirus. J Gen Virol 89:775–790. https://doi.org/10.1099/vir.0.83566-0
Hawkins LK et al (2015) Characterization of the Maize Chitinase Genes and Their Effect on Aspergillus flavus and Aflatoxin Accumulation Resistance. PLoS ONE 10:e0126185. https://doi.org/10.1371/journal.pone.0126185
Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54:285–302. https://doi.org/10.1146/annurev.ento.54.110807.090559
Henrissat B (1999) Classification of chitinases modules. In: Chitin and Chitinases. Springer, pp 137–156
Herrera-Estrella A, Chet I (1999) Chitinases in biological control. In: Chitin and Chitinases. Springer, pp 171–184
Hoffmann WA, Poorter H (2002) Avoiding bias in calculations of relative growth rate. Ann Bot 90:37–42. https://doi.org/10.1093/aob/mcf140
Holeski LM, Chase-Alone R, Kelly JK (2010) The genetics of phenotypic plasticity in plant defense: trichome production in Mimulus guttatus. Am Nat 175:391–400. https://doi.org/10.1086/651300
Horikoshi RJ et al (2016) Effective Dominance of Resistance of Spodoptera Frugiperda to Bt Maize and Cotton Varieties: Implications for Resistance Management Scientific Reports 6:34864. https://doi.org/10.1038/srep34864
http://www.nature.com/articles/srep34864#supplementary-information
Huang F (2020) Resistance of the fall armyworm, Spodoptera frugiperda, to transgenic Bacillus thuringiensis Cry1F corn in the America: lessons and implications for Bt corn IRM in China Insect Science doi:https://doi.org/10.1111/1744-7917.12826
Huber M, Cabib E, Miller LH (1991) Malaria parasite chitinase and penetration of the mosquito peritrophic membrane. Proc Natl Acad Sci 88:2807–2810. https://doi.org/10.1073/pnas.88.7.2807
Hunter S et al (2012) InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 40:D306-312. https://doi.org/10.1093/nar/gkr948
Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81:802–806
Huynh QK, Hironaka CM, Levine EB, Smith CE, Borgmeyer JR, Shah DM (1992) Antifungal proteins from plants. Purification, Molecular Cloning, and Antifungal Properties of Chitinases from Maize Seed J Biol Chem 267:6635–6640
Iseli B, Armand S, Boller T, Neuhaus JM, Henrissat B (1996) Plant chitinases use two different hydrolytic mechanisms. FEBS Lett 382:186–188
Johnson HB (1975) Plant Pubescence: an Ecological Perspective Botanical Review 41:233–258. https://doi.org/10.2307/4353882
Kesari P, Patil DN, Kumar P, Tomar S, Sharma AK (2015) Structural and functional evolution of chitinase-like proteins from plants. Proteomics 15:1693–1705. https://doi.org/10.1002/pmic.201400421
Koga D, Mitsutomi M Fau - Kono M, Kono M Fau - Matsumiya M, Matsumiya M (1999) Biochemistry of chitinases. In: Chitin and Chitinases. vol 1023–294X (Print). Springer, pp 111–123
Kramer KJ, Muthukrishnan S (1997) Insect chitinases: molecular biology and potential use as biopesticides. Insect Biochem Mol Biol 27:887–900
LaLonde SM Transforming variables for normality and linearity—when, how, why and why not’s. In: SAS Conference Proceedings NESUG, 2005. pp 11–14
Lawrence S, Novak N (2006) Expression of Poplar Chitinase in Tomato Leads to Inhibition of Development in Colorado Potato Beetle. Biotechnol Lett 28:593–599. https://doi.org/10.1007/s10529-006-0022-7
Lehane MJ (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–550. https://doi.org/10.1146/annurev.ento.42.1.525
Levin DA (1973) The Role of Trichomes in Plant Defense. Q Rev Biol 48:3–15. https://doi.org/10.1086/407484
Li Q, Wang F, Zhou Y, Xiao X (2005) Putative exposed aromatic and hydroxyl residues on the surface of the N-terminal domains of Chi1 from Aeromonas caviae CB101 are essential for chitin binding and hydrolysis. Applied Environ Microbiol 71:7559–7561. https://doi.org/10.1128/AEM.71.11.7559-7561.2005
Lin Z, Wu D, Luo A, Zhang W (1992) Chitinases from Seeds of Zea mays and Coix lachryma-jobi L. Purification and Some Properties Process Biochemistry 27:83–88. https://doi.org/10.1016/0032-9592(92)80014-T
Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy). Nucleic Acids Res 42:D490–D495. https://doi.org/10.1093/nar/gkt1178
Luthe DS et al (2011) Aboveground to belowground herbivore defense signaling in maize: a two-way street? Plant Signal Behav 6:126–129
Martinez C, Echeverri C, Florez J, Gaitan A, Gongora C (2012) In vitro production of two chitinolytic proteins with an inhibiting effect on the insect coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae) and the fungus Hemileia vastatrix the most limiting pests of coffee crops. AMB Express 2:22
Mason CJ et al (2019) Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome. Proc Natl Acad Sci U S A 116:15991–15996. https://doi.org/10.1073/pnas.1908748116
McMullen M, Frey M, Degenhardt J (2009) Genetics and Biochemistry of Insect Resistance in Maize. In: Bennetzen J, Hake S (eds) Handbook of Maize: Its Biology. Springer, New York, pp 271–289. https://doi.org/10.1007/978-0-387-79418-1_14
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
Mohan S, Ma PW, Williams WP, Luthe DS (2008) A naturally occurring plant cysteine protease possesses remarkable toxicity against insect pests and synergizes Bacillus thuringiensis toxin. PLoS ONE 3:e1786. https://doi.org/10.1371/journal.pone.0001786
Molano J, Polacheck I, Duran A, Cabib E (1979) An endochitinase from wheat germ. Activity on Nascent and Preformed Chitin J Biol Chem 254:4901–4907
Monaco MK et al (2014) Gramene 2013: comparative plant genomics resources. Nucleic Acids Res 42:D1193-1199. https://doi.org/10.1093/nar/gkt1110
Osborne JW (2010) Improving your data transformations: Applying the Box-Cox transformation Practical Assessment. Research, and Evaluation 15:1–9. https://doi.org/10.7275/qbpc-gk17
Oyeleye A, Normi YM (2018) Chitinase: diversity, limitations, and trends in engineering for suitable applications Biosci Rep 38 10.1042/BSR20180323
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 99:13319–13323. https://doi.org/10.1073/pnas.202224899
Pechan T et al (2000) A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell 12:1031–1040
Pechanova O, Pechan T, Ozkan S, McCarthy FM, Williams WP, Luthe DS (2010) Proteome profile of the developing maize (Zea mays L.) rachis. Proteomics 10:3051–3055. https://doi.org/10.1002/pmic.200900833
Pechanova O, Pechan T, Williams WP, Luthe DS (2011) Proteomic analysis of the maize rachis: potential roles of constitutive and induced proteins in resistance to Aspergillus flavus infection and aflatoxin accumulation. Proteomics 11:114–127. https://doi.org/10.1002/pmic.201000368
Pechanova O, Stone WD, Monroe W, Nebeker TE, Klepzig KD, Yuceer C (2008) Global and comparative protein profiles of the pronotum of the southern pine beetle. Dendroctonus Frontalis Insect Mol Biol 17:261–277. https://doi.org/10.1111/j.1365-2583.2008.00801.x
Peethambaran B, Hawkins L, Windham GL, Williams WP, Luthe DS (2010) Anti-fungal activity of maize silk proteins and role of chitinases in Aspergillus flavus resistance. Toxin Reviews 29:27–39. https://doi.org/10.3109/15569540903402874
Pegg GF, Young DH (1982) Purification and characterization of chitinase enzymes from healthy and Verticillium albo-atrum-infected tomato plants, and from V. albo-atrum. Physiol Plant Pathol 21:389–409. https://doi.org/10.1016/0048-4059(82)90074-1
Peiffer M, Felton GW (2005) The host plant as a factor in the synthesis and secretion of salivary glucose oxidase in larval Helicoverpa zea. Arch Insect Biochem Physiol 58:106–113. https://doi.org/10.1002/arch.20034
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
Plymale R, Grove MJ, Cox-Foster D, Ostiguy N, Hoover K (2008) Plant-mediated alteration of the peritrophic matrix and baculovirus infection in lepidopteran larvae. J Insect Physiol 54:737–749. https://doi.org/10.1016/j.jinsphys.2008.02.005
Poethig RS (1990) Phase change and the regulation of shoot morphogenesis in plants. Science 250:923–930. https://doi.org/10.1126/science.250.4983.923
Ray S et al (2016) Turnabout Is Fair Play: Herbivory-Induced Plant Chitinases Excreted in Fall Armyworm Frass Suppress Herbivore Defenses in Maize. Plant Physiol 171:694–706. https://doi.org/10.1104/pp.15.01854
Regev A et al (1996) Synergistic activity of a Bacillus thuringiensis delta-endotoxin and a bacterial endochitinase against Spodoptera littoralis larvae. Appl Environ Microbiol 62:3581–3586
Ritchie SW, Hanway JJ, Service ISUCE (1984) How a Corn Plant Develops. Iowa State University of Science and Technology, Cooperative Extension Service
Robertus JD, Monzingo AF (1999) The structure and action of chitinases. In: Chitin and Chitinases. vol 1023–294X (Print). Springer, pp 125–135
Schaeffer ML et al. (2011) MaizeGDB: curation and outreach go hand-in-hand Database 2011 doi:https://doi.org/10.1093/database/bar022
Schnable PS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Sci 326:1112–1115. https://doi.org/10.1126/science.1178534
Sekhon RS, Lin H, Childs KL, Hansey CN, Buell CR, de Leon N, Kaeppler SM (2011) Genome-wide atlas of transcription during maize development. Plant J 66:553–563. https://doi.org/10.1111/j.1365-313X.2011.04527.x
Serna L, Martin C (2006) Trichomes: different regulatory networks lead to convergent structures. Trends Plant Sci 11:274–280. https://doi.org/10.1016/j.tplants.2006.04.008
Sharma N, Sharma K, Gaur R, Gupta V (2011) Role of chitinase in plant defense Asian. J Biochem 6:29–37. https://doi.org/10.3923/ajb.2011.29.37
Shivaji R et al (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
Shoresh M, Harman GE (2008) Genome-wide identification, expression and chromosomal location of the genes encoding chitinolytic enzymes in Zea mays. Mol Genet Genomics 280:173–185. https://doi.org/10.1007/s00438-008-0354-1
Storer NP, Babcock JM, Schlenz M, Meade T, Thompson GD, Bing JW, Huckaba RM (2010) Discovery and characterization of field resistance to Bt maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico. J Econ Entomol 103:1031–1038
Storer NP, Kubiszak ME, Ed King J, Thompson GD, Santos AC (2012) Status of resistance to Bt maize in Spodoptera frugiperda: lessons from Puerto Rico. J Invertebr Pathol 110:294–300. https://doi.org/10.1016/j.jip.2012.04.007
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 Mol Biol Evol 30:2725–2729 doi:https://doi.org/10.1093/molbev/mst197
Tellam RL, Wijffels G, Willadsen P (1999) Peritrophic Matrix Proteins Insect Biochem Mol Biol 29:87–101
Thompson SE, Smith M, Wilkinson MC, Peek K (2001) Identification and characterization of a chitinase antigen from Pseudomonas aeruginosa strain 385. Appl Environ Microbiol 67:4001–4008. https://doi.org/10.1128/aem.67.9.4001-4008.2001
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 doi:https://doi.org/10.1007/s00425-012-1651-9
Tiffin P (2004) Comparative evolutionary histories of chitinase genes in the Genus zea and Family poaceae. Genetics 167:1331–1340. https://doi.org/10.1534/genetics.104.026856
Tronsmo A, Harman GE (1993) Detection and quantification of N-acetyl-beta-D-glucosaminidase, chitobiosidase, and endochitinase in solutions and on gels. Anal Biochem 208:74–79. https://doi.org/10.1006/abio.1993.1010
van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162. https://doi.org/10.1146/annurev.phyto.44.070505.143425
Virla EG, Álvarez A, Loto F, Pera LM, Baigorí M (2008) Fall Armyworm Strains (Lepidoptera: Noctuidae) in Argentina, Their Associate Host Plants and Response to Different Mortality Factors in Laboratory. Florida Entomologist 91:63–69. https://doi.org/10.1653/0015-4040(2008)091[0063:FASLNI]2.0.CO;2
Wagner GJ (1991) Secreting Glandular Trichomes: More than Just Hairs. Plant Physiol 96:675–679. https://doi.org/10.1104/pp.96.3.675
Werker E (2000) Trichome diversity and development. In: Advances in Botanical Research, vol Volume 31. Academic Press, pp 1–35. doi:https://doi.org/10.1016/S0065-2296(00)31005-9
Wessler S, Bennetzen J, Dawe R, Jiang N, SanMiguel P, Freeman B (2009) Maize Transposable Element Database. http://maizetedb.org/~maize/. http://maizetedb.org/~maize/
White F, Kramer K, Johnson L, Muthukrishnan S (1997) Chitinases for insect control Advances in insect control, the role of transgenic plants CRC Press, Boca Raton ISBN:978–970
Williams W, Buckley P, Davis F (2000) Vegetative Phase Change in Maize and Its Association with Resistance to Fall Armyworm Maydica (italy) 45:215–219
Williams WP, Davis FM, Windham GL (1990) Registration of Mp708 Germplasm Line of Maize. Crop Sci 30:757–757. https://doi.org/10.2135/cropsci1990.0011183X003000030082x
Wu S, Kriz AL, Widholm JM (1994) Molecular analysis of two cDNA clones encoding acidic class I chitinase in maize. Plant Physiol 105:1097–1105
Yoshida Y, Sano R, Wada T, Takabayashi J, Okada K (2009) Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Dev 136:1039–1048. https://doi.org/10.1242/dev.030585
Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X (2012) Genome-wide identification and analysis of the TIFY gene family in grape. PLoS ONE 7:e44465. https://doi.org/10.1371/journal.pone.0044465
Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad spectrum defenses against multiple herbivores. Plant Physiol 146:852–858. https://doi.org/10.1104/pp.107.112177
Zhu YC, Blanco CA, Portilla M, Adamczyk J, Luttrell R, Huang F (2015) Evidence of multiple/cross resistance to Bt and organophosphate insecticides in Puerto Rico population of the fall armyworm. Spodoptera Frugiperda Pesticide Biochemistry and Physiology 122:15–21. https://doi.org/10.1016/j.pestbp.2015.01.007
Acknowledgements
Special thanks to M. Peiffer and Penn State Microscopy facility (University Park, PA, U.S.A.) for their technical support.
Funding
This study was funded by the Pennsylvania State University.
Author information
Authors and Affiliations
Contributions
Yang Han and Dawn Luthe contributed to the study conception and design. Material preparation, data collection and analysis were performed by Yang Han. Proteomic analysis of trichomes was carried out by Erin Taylor. The first draft of the manuscript was written by Yang Han and Dawn Luthe commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no conflicts of interest to declare that are relevant to the content of this article.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Han, Y., Taylor, E.B. & Luthe, D. Maize Endochitinase Expression in Response to Fall Armyworm Herbivory. J Chem Ecol 47, 689–706 (2021). https://doi.org/10.1007/s10886-021-01284-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-021-01284-9