Prolonged expression of the BX1 signature enzyme is associated with a recombination hotspot in the benzoxazinoid gene cluster in Zea mays

Journal of Experimental Botany

Volumn 66, Issue 13, 2015, Pages 3917-3930

  Zheng, Linlin ^a   McMullen, Michael D ^b   Bauer, Eva ^a   Schön, Chris Carolin ^a   Gierl, Alfons ^a   Frey, Monika ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Allele specific expression; biosynthetic cluster; cis element; defence; DIMBOA; QTL mapping; secondary metabolites

Indexed keywords

ZEA MAYS;

2,4-DIHYDROXY-7-METHOXY-1,4-BENZOXAZIN-3-ONE; BENZOXAZINE DERIVATIVE; MESSENGER RNA; PLANT PROTEIN;

ALLELE; BASE PAIRING; BIOSYNTHESIS; CHROMOSOMAL MAPPING; CROSS BREEDING; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; INBREEDING; MAIZE; METABOLISM; MULTIGENE FAMILY; PLANT CHROMOSOME; PLANT GENE; PROMOTER REGION; QUANTITATIVE TRAIT LOCUS; SEEDLING; TRANSGENIC PLANT;

ALLELES; BASE PAIRING; BENZOXAZINES; BIOSYNTHETIC PATHWAYS; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; CROSSES, GENETIC; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOTYPE; INBREEDING; MULTIGENE FAMILY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROMOTER REGIONS, GENETIC; QUANTITATIVE TRAIT LOCI; RECOMBINATION, GENETIC; RNA, MESSENGER; SEEDLINGS; TRANSCRIPTION, GENETIC; ZEA MAYS;

EID: 84938228955     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv192     Document Type: Article

References (60)

1. Basten CJ, Weir B, Zeng ZB. 1997. QTL Cartographer: a reference manual and tutorial for QTL mapping. Department of Statistics, North Carolina State University: Raleigh, NC. http://statgen.ncsu.edu/qtlcart/manual/.
2. Belele CL, Sidorenko L, Stam M, Bader R, Arteaga-Vazquez MA, Chandler VL. 2013. Specific tandem repeats are sufficient for paramutation-induced trans-generational silencing. PLoS Genetics 9, e1003773.
3. Betsiashvili M, Ahern KR, and Jander G. 2015. Two Rhopalosiphum maidis (corn leaf aphid) resistance loci in maize inbred line Mo17 have additive effect. Journal of Experimental Botany 66, 571-578.
4. Brzeska K, Brzeski J, Smith J, Chandler VL. 2010. Transgenic expression of CBBP, a CXC domain protein, establishes paramutation in maize. Proceedings of the National Academy of Sciences, USA 107, 5516-5521.
5. Butrón A, Chen YC, Rottinghaus GE, McMullen MD. 2010. Genetic variation at bx1 controls DIMBOA content in maize. Theoretical and Applied Genetics 120, 721-734.
6. Campos F, Atkinson J, Arnason JT, Philogene BJR, Morand P, Werstiuk NH, Timmins G. 1989. Toxicokinetics of 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) in the European corn borer, Ostrinia nubilalis (Hübner). Journal of Chemical Ecology 15, 1989-2001.
7. Cardinal AJ, Lee M, Guthrie WD, Bing J, Austin DF, Leldboom LR, Senior ML. 2006. Mapping of factors for resistance to leaf-blade feeding by European corn borer (Ostrinia nubilalis) in maize. Maydica 51, 93-102.
8. Christensen AH, Quail PH. 1996. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Research 5, 213-218.
9. Clark RM, Wagler TN, Quijada P, Doebley J. 2006. A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nature Genetics 38, 594-597.
10. Dafoe NJ, Thomas JD, Shirk PD, Legaspi ME, Vaughan MM, Huffaker A, Teal PE, Schmelz EA. 2013. European corn borer (Ostrinia nubilalis) induced responses enhance susceptibility in maize. PLoS One 8, e73394.
11. Dooner HK, He L. 2008. Maize genome structure variation: interplay between retrotransposon polymorphisms and genic recombination. The Plant Cell 20, 249-258.
12. Dooner HK, Weck E, Adams S, Ralston E, Favreau M, English J. 1985. A molecular genetic analysis of insertions in the bronze locus in maize. Molecular and General Genetics 200, 240-246.
13. Eichten SR, Swanson-Wagner RA, Schnable JC, et al. 2011. Heritable epigenetic variation among maize inbreds. PLoS Genetics 7, e1002372.
14. Field B, Osbourn A. 2012. Order in the playground. Formation of plant gene clusters in dynamic chromosomal regions. Mobile Genetic Elements 2, 46-50.
15. Frame BR, Shou H, Chikwamba RK, et al. 2002. Agrobacterium tumefaciens-mediated transformation of maize embryos using a standard binary vector system. Plant Physiology 129, 13-22.
16. Frey M, Chomet P, Glawischnig E, et al. 1997. Analysis of a chemical plant defense mechanism in grasses. Science 277, 696-699.
17. Frey M, Huber K, Park WJ, Sicker D, Lindberg P, Meeley RB, Simmons CR, Yalpani N, Gierl A. 2003. A 2-oxoglutarate-dependent dioxygenase is integrated in DIMBOA-biosynthesis. Phytochemistry 62, 371-376.
18. 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.
19. Gierl A, Frey M. 2001. Evolution of benzoxazinone biosynthesis and indole production in maize. Planta 213, 493-498.
20. Goodstadt L, Ponting CP. 2011. Is the control of recombination conserved among diverse eukaryotes? Heredity 106, 710-711.
21. Grombacher AW, Russell WA, Guthrie WD. 1989. Resistance to firstgeneration European corn borer (Lepidoptera: Pyralidae) and DIMBOA concentration in midwhorl leaves of the BS9 maize synthetic. Journal of the Kansas Entomological Society 62, 103-107.
22. Grün S, Frey M, Gierl A. 2005. Evolution of the indole alkaloid biosynthesis in the genus Hordeum: distribution of gramine and DIBOA and isolation of the benzoxazinoid biosynthesis genes from Hordeum lechleri. Phytochemistry 66, 1264-1272.
23. Hawkins JS, Delgado V, Feng L, Carlise M, Dooner HK, Bennetzen JL. 2014. Variation in allelic expression associated with a recombination hotspot in Zea mays. The Plant Journal 79, 375-384.
24. Herms DA, Mattson WJ. 1992. The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283-335.
25. Huffaker A, Pearce G, Veyrat N, et al. 2013. Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proceedings of the National Academy of Sciences, USA 110, 5707-5712.
26. Jampatong C, McMullen MD, Barry BD, Darrah LL, Byrne PF, Kross H. 2002. Quantitative loci for first-and second-generation European corn borer resistance derived from the maize inbred Mo47. Crop Science 42, 584-593.
27. Jansen RC, Stam P. 1994. High resolution mapping of quantitative traits into multiple loci via interval mapping. Genetics 136, 1447-1455.
28. Jonczyk R, Schmidt H, Osterrieder A, et al. 2008. Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiology 146, 1053-1063.
29. King AJ, Brown GD, Gilday AD, Larson TR, Graham IA. 2014. Production of bioactive diterpenoids in the Euphorbiaceae depends on evolutionarily conserved gene clusters. The Plant Cell 26, 3286-3298.
30. Klun JA, Guthrie WD, Hallauer AR, Russell WA. 1970. Genetic nature of the concentration of 2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one and resistance to the European corn borer in a diallel set of eleven maize inbreds. Crop Science 10, 87-90.
31. Kurtz S, Narechania A, Stein JC, Ware D. 2008. A new method to compute K-mer frequencies and its application to annotate large repetitive plant genomes. BMC Genomics 9, 517.
32. Lee M, Sharopova N, Beavis WD, Grant D, Katt M, Blair D, Hallauer A. 2002. Expanding the genetic map of maize with the intermated B73×Mo17 (IBM) population. Plant Molecular Biology 48, 453-461.
33. Liu, K., M. Goodman, S. Muse, J.S. Smith, E. Buckler, Doebley J. 2003. Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites. Genetics 165, 2117-2128.
34. Long BJ, Dunn GM, Routley DG. 1975. Relationship of hydroxamic acid content in maize and resistance to northern corn leaf blight. Crop Science 15, 333-335.
35. Long BJ, Dunn GM, Bowman JS, Routley DG. 1977. Relationship of hydroxamic acid content in corn and resistance to the corn leaf aphid. Crop Science 17, 55-58.
36. Monaco MK, Taner ZS, Palitha DD, et al. 2013. Maize metabolic network construction and transcriptome analysis. Plant Genome 6, doi:10.3835/plantgenome2012.09.0025.
37. Meihls LN, 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. The Plant Cell 25, 2341-2355.
38. Niemeyer HM. 1988. Hydroxamic acids (4-hydroxy-1,4-benzoxazin-3-ones), defence chemicals in the Gramineae. Phytochemistry 27, 3349-3358.
39. Niemeyer HM. 2009. Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. Journal of Agricultural and Food Chemistry 57, 1677-1696.
40. Nomura T, Ishihara A, Imaishi H, Ohkawa H, Endo TR, and Iwamura H. 2003. Rearrangement of the genes for the biosynthesis of benzoxazinones in the evolution of Triticeae species. Planta 217, 776-782.
41. Nomura T, Nasuda S, Kawaura K, Ogihara Y, Kato N, Sato F, Kojima T, Toyoda A, Iwamura H, Endo TR. 2008. Structures of the three homoeologous loci of wheat benzoxazinone biosynthetic genes TaBx3 and TaBx4 and characterization of their promoter sequences. Theoretical and Applied Genetics 116, 373-381.
42. Nützmann HW, Osbourn A. 2014. Gene clustering in plant specialized metabolism. Current Opinion in Biotechnology 26, 91-99.
43. Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H. 2009. OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice. Journal of Biological Chemistry 284, 26510-26518.
44. Osbourn A. 2010. Gene clusters for secondary metabolic pathways: an emerging theme in plant biology. Plant Physiology 154, 531-535.
45. Salvi S, Sponza G, Morgante M, et al. 2007. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proceedings of the National Academy of Sciences, USA 104, 11376-11381.
46. Schaeffer ML, Harper LC, Gardiner JM, Andorf CM, Campbell DA, Cannon EK, Sen TZ, Lawrence CJ. 2011. MaizeGDB: curation and outreach go hand-in-hand. Database 2011 : Bar022.
47. Schnable PS, Ware D, Fulton RS, et al. 2009. The B73 maize genome: complexity, diversity, and dynamics. Science 326, 1112-1115.
48. Schullehner K, Dick R, Vitzthum F, Schwab W, Brandt W, Frey M, Gierl A. 2008. Benzoxazinoid biosynthesis in dicot plants. Phytochemistry 69, 2668-2677.
49. Sicker D, Frey M, Schulz M, Gierl A. 2000. Role of natural benzoxazinones in the survival strategy of plants. International Review of Cytology 198, 319-346.
50. Stam M, Belele C, Dorweiler JE, Chandler VL. 2002. Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes & Development 16, 1906-1918.
51. Takos AM, Rook F. 2012. Why biosynthetic genes for chemical defense compounds cluster. Trends in Plant Science 17, 383-387.
52. Virtanen AI, Hietala PK. 1955. 2(3)-Benzoxazolinone, an anti-fusarium factor in rye seedlings. Acta Chemica Scandinavica 09, 1543.
53. von Rad U, Hüttl R, Lottspeich F, Gierl A, Frey M. 2001. Two glucosyltransferases are involved in detoxification of benzoxazinoids in maize. The Plant Journal 28, 633-642.
54. Wahlroos Ö, Virtanen A. 1959. Precursors of 6-methoxybenzoxazolinone in maize and wheat plants, their isolation and some of their properties. Acta Chemica Scandinavica 13, 1906-1908.
55. Wegel E, Koumproglou R, Shaw and Osbourn A. 2009. Cell typespecific chromatin decondensation of a metabolic gene cluster in oats. The Plant Cell 21, 3926-3936
56. Yao H, Zhou Q, Li J, Smith H, Yandeau M, Nikolau BJ, Schnable PS. 2002. Molecular characterization of meiotic recombination across the 140-kb multigenic a1-sh2 interval of maize. Proceedings of the National Academy of Sciences, USA 99, 6157-6162.
57. Yu J, Holland JB, McMullen MD, Buckler ES. 2008. Genetic design and statistical power of nested association mapping in maize. Genetics 178, 539-551.
58. Zeng ZB. 1994. Precision mapping of quantitative trait loci. Genetics 136, 1457-1468.
59. Zhao ZY, Gu W, Cai T, Tagliani LA, Hondred DA, Bond D, Krell S, Rudert ML, Bruce WB, Pierce DA. 1998. Molecular analysis of T0 plants transformed by Agrobacterium and comparison of Agrobacteriummediated transformation with bombardment transformation in maize. Maize Genetics Cooperation Newsletter 72, 34-37.
60. Züst T, Joseph B, Shimizu KK, Kliebenstein DJ, Turnbull LA. 2011. Using knockout mutants to reveal the growth costs of defensive traits. Proceedings of the Royal Society B: Biological Sciences 278, 2598-2526.