Indole-3-glycerolphosphate synthase, a branchpoint for the biosynthesis of tryptophan, indole, and benzoxazinoids in maize.

Zea mays benzoxazinoid indole indole-3-glycerolphosphate synthase maize metabolic channeling tryptophan

Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
04 2021
Historique:
revised: 22 12 2020
received: 23 10 2020
accepted: 07 01 2021
pubmed: 19 1 2021
medline: 19 8 2021
entrez: 18 1 2021
Statut: ppublish

Résumé

The maize (Zea mays) genome encodes three indole-3-glycerolphosphate synthase enzymes (IGPS1, 2, and 3) catalyzing the conversion of 1-(2-carboxyphenylamino)-l-deoxyribulose-5-phosphate to indole-3-glycerolphosphate. Three further maize enzymes (BX1, benzoxazinoneless 1; TSA, tryptophan synthase alpha subunit; and IGL, indole glycerolphosphate lyase) convert indole-3-glycerolphosphate to indole, which is released as a volatile defense signaling compound and also serves as a precursor for the biosynthesis of tryptophan and defense-related benzoxazinoids. Phylogenetic analyses showed that IGPS2 is similar to enzymes found in both monocots and dicots, whereas maize IGPS1 and IGPS3 are in monocot-specific clades. Fusions of yellow fluorescent protein with maize IGPS enzymes and indole-3-glycerolphosphate lyases were all localized in chloroplasts. In bimolecular fluorescence complementation assays, IGPS1 interacted strongly with BX1 and IGL, IGPS2 interacted primarily with TSA, and IGPS3 interacted equally with all three indole-3-glycerolphosphate lyases. Whereas IGPS1 and IGPS3 expression was induced by insect feeding, IGPS2 expression was not. Transposon insertions in IGPS1 and IGPS3 reduced the abundance of both benzoxazinoids and free indole. Spodoptera exigua (beet armyworm) larvae show improved growth on igps1 mutant maize plants. Together, these results suggest that IGPS1 and IGPS3 function mainly in the biosynthesis of defensive metabolites, whereas IGPS2 may be involved in the biosynthesis of tryptophan. This metabolic channeling is similar to, though less exclusive than, that proposed for the three maize indole-3-glycerolphosphate lyases.

Identifiants

pubmed: 33458870
doi: 10.1111/tpj.15163
doi:

Substances chimiques

Benzoxazines 0
Indoles 0
indole 8724FJW4M5
Tryptophan 8DUH1N11BX
Indole-3-Glycerol-Phosphate Synthase EC 4.1.1.48

Types de publication

Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

245-257

Informations de copyright

© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Ahmad, S., Veyrat, N., Gordon-Weeks, R. et al. (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol. 157, 317-327.
Benton, H.P., Want, E.J. & Ebbels, T.M. (2010) Correction of mass calibration gaps in liquid chromatography-mass spectrometry metabolomics data. Bioinformatics, 26, 2488-2489.
Bethke, G., Unthan, T., Uhrig, J.F., Poschl, Y., Gust, A.A., Scheel, D. & Lee, J. (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc. Natl Acad. Sci. USA, 106, 8067-8072.
Betsiashvili, M., Ahern, K.R. & Jander, G. (2015) Additive effects of two quantitative trait loci that confer Rhopalosiphum maidis (corn leaf aphid) resistance in maize inbred line Mo17. J. Exp. Bot. 66, 571-578.
Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114-2120.
Brändén, C.-I. (1991) The TIM barrel-the most frequently occurring folding motif in proteins. Curr. Opin. Struct. Biol. 1, 978-983.
Bui, H., Greenhalgh, R., Ruckert, A., Gill, G.S., Lee, S., Ramirez, R.A. & Clark, R.M. (2018) Generalist and specialist mite herbivores induce similar defense responses in maize and barley but differ in susceptibility to benzoxazinoids. Front. Plant Sci. 9, 1222.
Chambers, M.C., Maclean, B., Burke, R. et al. (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat. Biotechnol. 30, 918-920.
Chan, Y.H. (2017) The complex role of sequence and structure in the stability and function of the TIM barrel proteins. PhD thesis in Biochemistry and Molecular Pharmacology. Worcester, USA: University of Massachusetts Medical School, 1-148. https://doi.org/10.13028/M2J09H.
DeBlasio, S.L., Rebelo, A.R., Parks, K., Gray, S.M. & Heck, M.C. (2018) Disruption of chloroplast function through downregulation of phytoene desaturase enhances the systemic accumulation of an aphid-borne, phloem-restricted virus. Mol. Plant Microbe Interact. 31, 1095-1110.
Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M. & Gingeras, T.R. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15-21.
Dutartre, L., Hilliou, F. & Feyereisen, R. (2012) Phylogenomics of the benzoxazinoid biosynthetic pathway of Poaceae: gene duplications and origin of the Bx cluster. BMC Evol. Biol. 12, 64.
Erb, M., Veyrat, N., Robert, C.A., Xu, H., Frey, M., Ton, J. & Turlings, T.C. (2015) Indole is an essential herbivore-induced volatile priming signal in maize. Nat. Commun. 6, 6273.
Farber, G.K. & Petsko, G.A. (1990) The evolution of alpha/beta barrel enzymes. Trends Biochem. Sci. 15, 228-234.
Frey, M., Chomet, P., Glawischnig, E. et al. (1997) Analysis of a chemical plant defense mechanism in grasses. Science, 277, 696-699.
Frey, M., Kliem, R., Saedler, H. & Gierl, A. (1995) Expression of a cytochrome P450 gene family in maize. Mol. Gen. Genet. 246, 100-109.
Frey, M., Schullehner, K., Dick, R., Fiesselmann, A. & Gierl, A. (2009) Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants. Phytochemistry, 70, 1645-1651.
Frey, M., Stettner, C., Pare, P.W., Schmelz, E.A., Tumlinson, J.H. & Gierl, A. (2000) An herbivore elicitor activates the gene for indole emission in maize. Proc. Natl Acad. Sci. USA, 97, 14801-14806.
Glawischnig, E., Grun, S., Frey, M. & Gierl, A. (1999) Cytochrome P450 monooxygenases of DIBOA biosynthesis: specificity and conservation among grasses. Phytochemistry, 50, 925-930.
Hamilton, R.H. (1964) A corn mutant deficient in 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one with an altered tolerance of atrazine. Weeds, 12, 27-30.
Howe, G.A. & Jander, G.J. (2008) Plant Immunity to Insect Herbivores. Annual Review of Plant Biology, 59 (1), 41-66. http://dx.doi.org/10.1146/annurev.arplant.59.032607.092825.
Jones, D.T., Taylor, W.R. & Thornton, J.M. (1992) The rapid generation of mutation data matrices from protein sequences. Comput. Appl. Biosci. 8, 275-282.
Karimi, S., Ahl, D., Vagesjo, E., Holm, L., Phillipson, M., Jonsson, H. & Roos, S. (2016) In vivo and in vitro detection of luminescent and fluorescent Lactobacillus reuteri and application of red fluorescent mCherry for assessing plasmid persistence. PLoS One, 11, e0151969.
Köllner, T.G., Schnee, C., Gershenzon, J. & Degenhardt, J. (2004) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions. Phytochemistry, 65, 1895-1902.
Kong, L., Wu, J., Lu, L., Xu, Y. & Zhou, X. (2014) Interaction between Rice stripe virus disease-specific protein and host PsbP enhances virus symptoms. Mol. Plant, 7, 691-708.
Kremling, K.A.G., Chen, S.Y., Su, M.H., Lepak, N.K., Romay, M.C., Swarts, K.L., Lu, F., Lorant, A., Bradbury, P.J. & Buckler, E.S. (2018) Dysregulation of expression correlates with rare-allele burden and fitness loss in maize. Nature, 555, 520-523.
Kriechbaumer, V., Weigang, L., Fiesselmann, A., Letzel, T., Frey, M., Gierl, A. & Glawischnig, E. (2008) Characterisation of the tryptophan synthase alpha subunit in maize. BMC Plant Biol. 8, 44.
Kuhl, C., Tautenhahn, R., Bottcher, C., Larson, T.R. & Neumann, S. (2012) CAMERA: an integrated strategy for compound spectra extraction and annotation of liquid chromatography/mass spectrometry data sets. Anal. Chem. 84, 283-289.
Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549.
Li, J., Chen, S., Zhu, L. & Last, R.L. (1995a) Isolation of cDNAs encoding the tryptophan pathway enzyme indole-3-glycerol phosphate synthase from Arabidopsis thaliana. Plant Physiol. 108, 877-878.
Li, J., Zhao, J., Rose, A.B., Schmidt, R. & Last, R.L. (1995b) Arabidopsis phosphoribosylanthranilate isomerase: molecular genetic analysis of triplicate tryptophan pathway genes. Plant Cell, 7, 447-461.
Maag, D., Köhler, A., Robert, C.A., Frey, M., Wolfender, J.L., Turlings, T.C., Glauser, G. & Erb, M. (2016) Highly localized and persistent induction of Bx1-dependent herbivore resistance factors in maize. Plant J. 88, 976-991.
Marcon, C., Altrogge, L. & Win, Y.N. et al. (2020) BonnMu: a sequence-indexed resource of transposon-induced maize mutations for functional genomics studies. Plant Physiol. epub ahead of print. 10.1104/pp.20.00478.
Martin, D., Tholl, D., Gershenzon, J. & Bohlmann, J. (2002) Methyl Jasmonate Induces Traumatic Resin Ducts, Terpenoid Resin Biosynthesis, and Terpenoid Accumulation in Developing Xylem of Norway Spruce Stems. Plant Physiology, 129 (3), 1003-1018. http://dx.doi.org/10.1104/pp.011001.
McCarty, D.R., Settles, A.M., Suzuki, M. et al. (2005) Steady-state transposon mutagenesis in inbred maize. Plant J. 44, 52-61.
McMullen, M., Frey, M. & Degenhardt, J. (2009a) Genetics and biochemistry of insect resistance in maize. In Handbook of Maize: its Biology (Bennetzen, J.L. and Hake, S., eds). New York: Springer, p. 587.
McMullen, M.D., Kresovich, S., Villeda, H.S. et al. (2009b) Genetic properties of the maize nested association mapping population. Science, 325, 737-740.
Meihls, L.N., Handrick, V., Glauser, G. et al. (2013) Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell, 25, 2341-2355.
Meihls, L.N., Kaur, H. & Jander, G. (2012) Natural variation in maize defense against insect herbivores. Cold Spring Harbor Symp. Quant. Biol. 77, 269-283.
Melanson, D., Chilton, M.D., Masters-Moore, D. & Chilton, W.S. (1997) A deletion in an indole synthase gene is responsible for the DIMBOA-deficient phenotype of bxbx maize. Proc. Natl Acad. Sci. USA, 94, 13345-13350.
Nagano, N., Orengo, C.A. & Thornton, J.M. (2002) One Fold with Many Functions: The Evolutionary Relationships between TIM Barrel Families Based on their Sequences, Structures and Functions. Journal of Molecular Biology, 321 (5), 741-765. http://dx.doi.org/10.1016/s0022-2836(02)00649-6.
Nelson, B.K., Cai, X. & Nebenfuhr, A. (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136.
Niemeyer, H.M. (2009) Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. J. Agric. Food Chem. 57, 1677-1696.
Reichman, P. & Dissmeyer, N. (2017) In Vivo Reporters for Protein Half-Life. In: Plant Germline Development: Methods and Protocols. Methods in Molecular Biology Schmidt, A. (ed), 1669 New York: Springer.
Richter, A., Schaff, C., Zhang, Z. et al. (2016) Characterization of the (herbivore-induced) biosynthetic pathways of the volatile homoterpenes 3,8-dimethyl-1,4,7-nonatriene (DMNT) and 4,8,12-trimethyltrideca-1,3,7,11-tetraene, in Zea mays. Plant Cell, 28, 2651-2665.
Richter, A., Seidl-Adams, I., Kollner, T.G., Schaff, C., Tumlinson, J.H. & Degenhardt, J. (2015) A small, differentially regulated family of farnesyl diphosphate synthases in maize (Zea mays) provides farnesyl diphosphate for the biosynthesis of herbivore-induced sesquiterpenes. Planta, 241, 1351-1361.
Rose, A.B. & Last, R.L. (1994) Molecular genetics of amino acid, nucleotide, and vitamin biosynthesis. Cold Spring Harbor Monograph Archive, 27, 835-879.
Settles, A.M., Holding, D.R., Tan, B.C. et al. (2007) Sequence-indexed mutations in maize using the UniformMu transposon-tagging population. BMC Genom., 8, 116.
Singh, M. & Widholm, J.M. (1974) Measurement of 5 enzymes which convert chorismate to tryptophan in wheat plants (Triticum aestivum cv Kalyansona). Physiol. Plant. 32, 240-246.
Springer, N.M., Anderson, S.N., Andorf, C.M. et al. (2018) The W22 genome: a foundation for maize functional genomics and transposon biology. Nat. Genet. 50, 1282-1288.
Springer, P.S., Zimmer, E.A. & Bennetzen, J.L. (1989) Genomic organization of the ribosomal DNA of sorghum and its close relatives. Theoretical And Applied Genetics, 77, 844-850. http://dx.doi.org/10.1007/bf00268337.
Stettner, C. (1998) DIMBOA-Biosynthese in Mais: Isolierung und funktionelle Charakterisierung des Bx1-Gens. PhD thesis in Genetics, Munich, Germany: Technische Universität München, pp. 1-95.
Tamiru, A., Bruce, T.J.A., Richter, A., Woodcock, C.M., Midega, C.A.O., Degenhardt, J., Kelemu, S., Pickett, J.A. & Khan, Z.R. (2017) A maize landrace that emits defense volatiles in response to herbivore eggs possesses a strongly inducible terpene synthase gene. Ecol. Evol. 7, 2835-2845.
Tautenhahn, R., Bottcher, C. & Neumann, S. (2008) Highly sensitive feature detection for high resolution LC/MS. BMC Bioinformatics, 9, 504.
Tautenhahn, R., Patti, G.J., Rinehart, D. & Siuzdak, G. (2012) XCMS Online: a web-based platform to process untargeted metabolomic data. Anal. Chem. 84, 5035-5039.
Tzin, V., Fernandez-Pozo, N., Richter, A. et al. (2015) Dynamic maize responses to aphid feeding are revealed by a time series of transcriptomic and metabolomic assays. Plant Physiol. 169, 1727-1743.
Tzin, V., Hojo, Y., Strickler, S.R. et al. (2017) Rapid defense responses in maize leaves induced by Spodoptera exigua caterpillar feeding. J. Exp. Bot. 68, 4709-4723.
Vogel, H.J. & Bonner, D.M. (1956) Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218, 97-106.
Wierenga, R.K. (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett. 492, 193-198.
Williams-Carrier, R., Stiffler, N., Belcher, S., Kroeger, T., Stern, D.B., Monde, R.A., Coalter, R. & Barkan, A. (2010) Use of Illumina sequencing to identify transposon insertions underlying mutant phenotypes in high-copy Mutator lines of maize. Plant J. 63, 167-177.
Wilmanns, M., Hyde, C.C., Davies, D.R., Kirschner, K. & Jansonius, J.N. (1991) Structural conservation in parallel beta/alpha-barrel enzymes that catalyze three sequential reactions in the pathway of tryptophan biosynthesis. Biochemistry, 30, 9161-9169.
Wisecaver, J.H., Borowsky, A.T., Tzin, V., Jander, G., Kliebenstein, D.J. & Rokas, A. (2017) A global coexpression network approach for connecting genes to specialized metabolic pathways in plants. Plant Cell, 29, 944-959.
Wouters, F.C., Blanchette, B., Gershenzon, J. & Vassao, D.G. (2016) Plant defense and herbivore counter-defense: benzoxazinoids and insect herbivores. Phytochem. Rev. 15, 1127-1151.
Wright, A.D., Moehlenkamp, C.A., Perrot, G.H., Neuffer, M.G. & Cone, K.C. (1992) The maize auxotrophic mutant orange pericarp is defective in duplicate genes for tryptophan synthase beta. Plant Cell, 4, 711-719.
Yang, X., Baliji, S., Buchmann, R.C., Wang, H., Lindbo, J.A., Sunter, G. & Bisaro, D.M. (2007) Functional modulation of the geminivirus AL2 transcription factor and silencing suppressor by self-interaction. J. Virol. 81, 11972-11981.
Yanofsky, C., Horn, V., Bonner, M. & Stasiowski, S. (1971) Polarity and enzyme functions in mutants of the first three genes of the tryptophan operon of Escherichia coli. Genetics, 69, 409-433.
Zhang, R., Wang, B., Ouyang, J., Li, J. & Wang, Y. (2008) Arabidopsis indole synthase, a homolog of tryptophan synthase alpha, is an enzyme involved in the Trp-independent indole-containing metabolite biosynthesis. J. Integr. Plant Biol. 50, 1070-1077.

Auteurs

Annett Richter (A)

Boyce Thompson Institute, Ithaca, NY, USA.

Adrian F Powell (AF)

Boyce Thompson Institute, Ithaca, NY, USA.

Mahdieh Mirzaei (M)

Boyce Thompson Institute, Ithaca, NY, USA.

Lucy J Wang (LJ)

Boyce Thompson Institute, Ithaca, NY, USA.

Navid Movahed (N)

Boyce Thompson Institute, Ithaca, NY, USA.

Julia K Miller (JK)

Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA.

Miguel A Piñeros (MA)

Robert W. Holley Center for Agriculture and Health, USDA-ARS, Ithaca, NY, USA.

Georg Jander (G)

Boyce Thompson Institute, Ithaca, NY, USA.

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