Abstract
Gramineous plants, including the major agricultural crops wheat (Triticum aestivum L.), rye (Secale cereale L.) and maize (Zea mays L.), accumulate benzoxazinones (Bxs) as defensive compounds. Previously, we isolated cDNAs of the Bx biosynthetic genes in wheat, TaBx2–TaBx5, that encode the enzymes catalyzing the sequential hydroxylation of indole to Bxs. In this study we isolated a cDNA of TaBx1, which encodes the first enzyme of the Bx pathway of wheat. The level of identity (80%) in deduced amino-acid sequence between TaBx1 and the corresponding maize gene Bx1 was as high as those shown between TaBx2–TaBx5 and the corresponding maize genes Bx2–Bx5, respectively. Southern blot analysis using the TaBx1–TaBx5 cDNAs as probes was conducted with aneuploid lines of hexaploid wheat in order to determine sub-chromosomal locations of the five Bx biosynthetic genes in Triticeae species. In wheat, TaBx1 and TaBx2 co-existed in specific regions of chromosomes 4A, 4B and 4D, and TaBx3–TaBx5 were localized together in the distal regions of the short arms of chromosomes 5A, 5B and 5D. TaBx3 and TaBx5 were found to have duplicated loci in the long arm and the short arm of chromosome 5B, respectively. In rye, homoeoloci of TaBx1 and TaBx2 were located on chromosome 7R and those for TaBx3–TaBx5 were located on chromosome 5R. In barley, no Southern blot band was detected with any of the probes under the highly stringent hybridization conditions, suggesting that the non-Bx phenotype of barley is attributable to the loss of Bx biosynthetic genes.
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Abbreviations
- Bx:
-
benzoxazinone
- CS:
-
Chinese Spring
- CYP:
-
cytochrome P450 monooxygenase
- Dt:
-
ditelosomic
- EST:
-
expressed sequence tag
- FL:
-
fraction length
- Igl:
-
indole-3-glycerol phosphate lyase
- TSA:
-
tryptophan synthase alpha subunit
References
Barria BN, Copaja SV, Niemeyer HM (1992) Occurrence of DIBOA in wild Hordeum species and its relation to aphid resistance. Phytochemistry 31:89–91
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Devos KM, Gale MD (1997) Comparative genetics in the grass. Plant Mol Biol 35:3–15
Devos KM, Atkinson MD, Chinoy CN, Francis HA, Harcourt RL, Koebner RMD, Liu CJ, Masojć P, Xie DX, Gale MD (1993) Chromosomal rearrangements in the rye genome relative to that of wheat. Theor Appl Genet 85:673–680
Devos KM, Dubcovsky J, Dvořák J, Chinoy CN, Gale MD (1995) Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor Appl Genet 91:282–288
Driscoll CJ, Sears ER (1971) Individual addition of the chromosomes of 'Imperial' rye to wheat. Agron Abstr 1971:6
Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016
Endo TR, Gill BS (1996) The deletion stocks of common wheat. J Hered 87:295–307
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, Chomet P, Glawischnig E, Stettner C, Grün S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277:696–699
Frey M, Stettner C, Paré PW, Schmelz EA, Tumlinson JH, Gierl A (2000) An herbivore elicitor activates the gene for indole emission in maize. Proc Natl Acad Sci USA 97:14801–14806
Gierl A, Frey M (2001) Evolution of benzoxazinone biosynthesis and indole production in maize. Planta 213:493–498
Glawischnig E, Grün S, Frey M, Gierl A (1999) Cytochrome P450 monooxygenases of DIBOA biosynthesis: specificity and conservation among grasses. Phytochemistry 50:925–930
Huang S, Sirikhachornkit A, Faris JD, Su X, Gill BS, Haselkorn R, Gornicki P (2002) Phylogenetic analysis of the acetyl-CoA carboxylase and 3-phosphoglycerate kinase loci in wheat and other grasses. Plant Mol Biol 48:805–820
Kawahara T (ed) (1997) Catalog of Aegilops–Triticum germplasm preserved in Kyoto University. Plant Germ-Plasm Institute of the Faculty of Agriculture, Kyoto University, Kyoto, Japan
Kramer VC, Koziel MG (1995) Structure of a maize tryptophan synthase alpha subunit gene with pith enhanced expression. Plant Mol Biol 27:1183–1188
Leighton V, Niemeyer HM, Jonsson LMV (1994) Substrate specificity of a glucosyltransferase and an N-hydroxylase involved in the biosynthesis of cyclic hydroxamic acids in Gramineae. Phytochemistry 36:887–892
Liu CJ, Atkinson MD, Chinoy CN, Devos KM, Gale MD (1992) Nonhomoeologous translocations between group 4, 5 and 7 chromosomes within wheat and rye. Theor Appl Genet 83:305–312
Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155
Melanson D, Chilton M-D, Masters-Moore D, Chilton WS (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
Mickelson-Young L, Endo TR, Gill BS (1995) A cytogenetic ladder-map of the wheat homoeologous group-4 chromosomes. Theor Appl Genet 90:1007–1011
Nakagawa E, Amano T, Hirai N, Iwamura H (1995) Non-induced cyclic hydroxamic acids in wheat during juvenile stage of growth. Phytochemistry 38:1349–1354
Niemeyer HM (1988) Hydroxamic acids (4-hydroxy-1,4-benzoxazin-3-ones): defence chemicals in the Gramineae. Phytochemistry 27:3349–3358
Nomura T, Ishihara A, Imaishi H, Endo TR, Ohkawa H, Iwamura H (2002) Molecular characterization and chromosomal localization of cytochrome P450 genes involved in the biosynthesis of cyclic hydroxamic acids in hexaploid wheat. Mol Genet Genomics 267:210–217
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sears ER, Sears LMS (1978) The telocentric chromosomes of common wheat. In: Ramanujam S (ed) Proceedings of the 5th international wheat genetics symposium. Indian Society of Genetics and Plant Breeding, New Delhi, pp 389–407
Sicker D, Frey M, Schulz M, Gierl A (2000) Role of natural benzoxazinones in the survival strategy of plants. Int Rev Cytol 198:319–346
von Rad U, Hüttl R, Lottspeich F, Gierl A, Frey M (2001) Two glucosyltransferases are involved in detoxification of benzoxazinoids in maize. Plant J 28:633–642
Yang YF, Furuta Y, Nagata S, Watanabe W (1999) Tetra Chinese Spring with AABB genomes extracted from the hexaploid common wheat, Chinese Spring. Genes Genet Syst 74:67–70
Zhao J, Last RL (1995) Immunological characterization and chloroplast localization of the tryptophan biosynthetic enzymes of the flowering plant Arabidopsis thaliana. J Biol Chem 270:6081–6087
Acknowledgements
We express our sincere gratitude to Dr. Chihiro Tanaka, Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, for instrumental support in DNA sequencing. The authors are also grateful to Radioisotope Research Center, Kyoto University, for instrumental support in radioisotope experiments. This work was supported by a Grant-in-Aid for Scientific Research (No. 13003902) from the Ministry of Education, Science, Sports and Culture of Japan.
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T. Nomura is a member of the Japan Society for the Promotion of Science
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Nomura, T., Ishihara, A., Imaishi, H. et al. Rearrangement of the genes for the biosynthesis of benzoxazinones in the evolution of Triticeae species. Planta 217, 776–782 (2003). https://doi.org/10.1007/s00425-003-1040-5
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DOI: https://doi.org/10.1007/s00425-003-1040-5