A deletion in an indole synthase gene is responsible for the DIMBOA-deficient phenotype of<i>bxbx</i> maize

Melanson, Denise; Chilton, Mary-Dell; Masters-Moore, David; Chilton, William Scott

doi:10.1073/pnas.94.24.13345

Cited by 48 publications

(34 citation statements)

References 55 publications

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“…Interestingly, the bx1 single mutant can accumulate up to up to 20% of wild-type BX levels after caterpillar infestation (N. Veyrat, personal communication). Furthermore, treatment of the bx1 single mutant with indole can rescue DIMBOA production (Frey et al, 1997;Melanson et al, 1997). Hence, IGL has the potential to complement the bx1 mutation and contribute to in planta BX biosynthesis during expression of JA-dependent defense.…”

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confidence: 99%

“…In rye (Secale cereale) and wild barley (Hordeum vulgare), 2,4-dihydroxy-2H-1,4-benzoxazin-3(4H)-one (DIBOA) is the dominant BX, whereas the methoxy derivative DIMBOA is more prevalent in maize and wheat (Triticum aestivum; Niemeyer, 2009). The BENZOXAZINELESS1 (Bx1) gene mediates thefirst dedicated step in the BX pathway and encodes a close homolog of the Trp synthetase a-subunit, which catalyzes the formation of indole from indole-3-glycerole phosphate (Frey et al, 1997;Melanson et al, 1997). This compound is subsequently oxidized by four cytochrome P450 monooxygenases, BX2 to BX5, into DIBOA (Frey et al, 1997), which can then be glucosidated by the glucosyltransferases BX8 and BX9 (von Rad et al, 2001).…”

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Benzoxazinoid Metabolites Regulate Innate Immunity against Aphids and Fungi in Maize

et al. 2011

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Benzoxazinoids (BXs), such as 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one (DIMBOA), are secondary metabolites in grasses. The first step in BX biosynthesis converts indole-3-glycerol phosphate into indole. In maize (Zea mays), this reaction is catalyzed by either BENZOXAZINELESS1 (BX1) or INDOLE GLYCEROL PHOSPHATE LYASE (IGL). The Bx1 gene is under developmental control and is mainly responsible for BX production, whereas the Igl gene is inducible by stress signals, such as wounding, herbivory, or jasmonates. To determine the role of BXs in defense against aphids and fungi, we compared basal resistance between Bx1 wild-type and bx1 mutant lines in the igl mutant background, thereby preventing BX production from IGL. Compared to Bx1 wild-type plants, BX-deficient bx1 mutant plants allowed better development of the cereal aphid Rhopalosiphum padi, and were affected in penetration resistance against the fungus Setosphaeria turtica. At stages preceding major tissue disruption, R. padi and S. turtica elicited increased accumulation of DIMBOA-glucoside, DIMBOA, and 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one-glucoside (HDMBOA-glc), which was most pronounced in apoplastic leaf extracts. Treatment with the defense elicitor chitosan similarly enhanced apoplastic accumulation of DIMBOA and HDMBOA-glc, but repressed transcription of genes controlling BX biosynthesis downstream of BX1. This repression was also obtained after treatment with the BX precursor indole and DIMBOA, but not with HDMBOA-glc. Furthermore, BX-deficient bx1 mutant lines deposited less chitosan-induced callose than Bx1 wild-type lines, whereas apoplast infiltration with DIMBOA, but not HDMBOA-glc, mimicked chitosan-induced callose. Hence, DIMBOA functions as a defense regulatory signal in maize innate immunity, which acts in addition to its well-characterized activity as a biocidal defense metabolite.

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Benzoxazinoid Metabolites Regulate Innate Immunity against Aphids and Fungi in Maize

et al. 2011

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“…An especially elegant example is found in grass species, which have evolved a novel form of the Trp synthase a-subunit (indole synthase or indole-3-glycerolphosphate lyase) that produces indole in the first committing step of defensive cyclic hydroxamic acid biosynthesis (Frey et al, 1997;Melanson et al, 1997;Gierl and Frey, 2001). This evolutionary protein engineering created an enzyme that diverts indole away from amino acid production and toward specialized metabolism.…”

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A feedback insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato

Ning

Moghe²,

Leong³

et al. 2015

Plant Physiol.

177

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Acylsugars are insecticidal specialized metabolites produced in the glandular trichomes of plants in the Solanaceae family. In the tomato clade of the Solanum genus, acylsugars consist of aliphatic acids of different chain lengths esterified to sucrose, or less frequently to glucose. Through liquid chromatography-mass spectrometry screening of introgression lines, we previously identified a region of chromosome 8 in the Solanum pennellii LA0716 genome (IL8-1/8-1-1) that causes the cultivated tomato Solanum lycopersicum to shift from producing acylsucroses with abundant 3-methylbutanoic acid acyl chains derived from leucine metabolism to 2-methylpropanoic acid acyl chains derived from valine metabolism. We describe multiple lines of evidence implicating a trichome-expressed gene from this region as playing a role in this shift. S. lycopersicum M82 SlIPMS3 (Solyc08g014230) encodes a functional end product inhibition-insensitive version of the committing enzyme of leucine biosynthesis, isopropylmalate synthase, missing the carboxyl-terminal 160 amino acids. In contrast, the S. pennellii LA0716 IPMS3 allele found in IL8-1/8-1-1 encodes a nonfunctional truncated IPMS protein. M82 transformed with an SlIPMS3 RNA interference construct exhibited an acylsugar profile similar to that of IL8-1-1, whereas the expression of SlIPMS3 in IL8-1-1 partially restored the M82 acylsugar phenotype. These IPMS3 alleles are polymorphic in 14 S. pennellii accessions spread throughout the geographical range of occurrence for this species and are associated with acylsugars containing varying amounts of 2-methylpropanoic acid and 3-methylbutanoic acid acyl chains.

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“…The biosynthetic pathway of Bxs branches off from that of tryptophan at indole-3-glycerol phosphate (5)(6)(7)(8). Previously, we isolated five genes responsible for the Bx biosynthesis, TaBx1-TaBx5, from hexaploid wheat (9,10).…”

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Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaploid wheat

Nomura

Ishihara

Yanagita

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

127

144

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Hexaploid wheat (Triticum aestivum) accumulates benzoxazinones (Bxs) as defensive compounds. Previously, we found that five Bx biosynthetic genes, TaBx1-TaBx5, are located on each of the three genomes (A, B, and D) of hexaploid wheat. In this study, we isolated three homoeologous cDNAs of each TaBx gene to estimate the contribution of individual homoeologous TaBx genes to the biosynthesis of Bxs in hexaploid wheat. We analyzed their transcript levels by homoeolog-or genome-specific quantitative RT-PCR and the catalytic properties of their translation products by kinetic analyses using recombinant TaBX enzymes. The three homoeologs were transcribed differentially, and the ratio of the individual homoeologous transcripts to total homoeologous transcripts also varied with the tissue, i.e., shoots or roots, as well as with the developmental stage. Moreover, the translation products of the three homoeologs had different catalytic properties. Some TaBx homoeologs were efficiently transcribed, but the translation products showed only weak enzymatic activities, which inferred their weak contribution to Bx biosynthesis. Considering the transcript levels and the catalytic properties collectively, we concluded that the homoeologs on the B genome generally contributed the most to the Bx biosynthesis in hexaploid wheat, especially in shoots. In tetraploid wheat and the three diploid progenitors of hexaploid wheat, the respective transcript levels of the TaBx homoeologs were similar in ratio to those observed in hexaploid wheat. This result indicates that the genomic bias in the transcription of the TaBx genes in hexaploid wheat originated in the diploid progenitors and has been retained through the polyploidization.biosynthetic genes ͉ homoeolog ͉ polyploidization

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A deletion in an indole synthase gene is responsible for the DIMBOA-deficient phenotype ofbxbx maize

Cited by 48 publications

References 55 publications

Benzoxazinoid Metabolites Regulate Innate Immunity against Aphids and Fungi in Maize

Benzoxazinoid Metabolites Regulate Innate Immunity against Aphids and Fungi in Maize

A feedback insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato

Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaploid wheat

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