Ty3/gypsy-like retrotransposon knockout of a 2-methyl-6-phytyl-1,4- benzoquinone methyltransferase is non-lethal, uncovers a cryptic paralogous mutation, and produces novel tocopherol (vitamin E) profiles in sunflower

Theoretical and Applied Genetics

Volumn 113, Issue 5, 2006, Pages 783-799

  Tang, Shunxue ^a   Hass, Catherine G ^b   Knapp, Steven J ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; GROWTH KINETICS; MUTAGENESIS; PLANTS (BOTANY); VITAMINS;

HOMOZYGOTES; MUTANTS; PLANT GROWTH; TOCOPHEROL;

ENZYMES;

HELIANTHUS; HELIANTHUS ANNUUS;

EID: 33747713373     PISSN: 00405752     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00122-006-0321-3     Document Type: Article

References (71)

1. Baack EJ, Whitney KD, Rieseberg LH (2005) Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species. New Phytol 167:321-333
2. Bennetzen JL (2000) Mechanisms and rates of genome expansion and contraction in flowering plants. Genetica 115:251-269 29-36
3. Bennetzen JL (2002) Transposable element contributions to plant gene and genome evolution. Plant Mol Biol 42:251-269
4. Bergmüller E, Porfirova S, Dörmann P (2003) Characterization of an Arabidopsis mutant deficient in γ-tocopherol methyltransferase. Plant Mol Biol 52:1181-1190
5. Bowen NJ, McDonald JF (2001) Drosophila euchromatic LTR-retrotransposons are much younger than the host species in which they reside. Genome Res 11:1527-1540
6. Brown JWS (1996) Arabidopsis intron mutations and pre-mRNA splicing. Plant J 10:771-780
7. Cheng S, Fockler C, Barnes W, Higuchi R (1994) Effective amplification of long targets from cloned inserts and human genomic DNA. Proc Natl Acad Sci USA 91:5695-5699
8. Cheng Z, Sattler S, Maeda H, Sakuragi Y, Bryant DA, DellaPenna D (2003) Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15:2343-2356
9. Collakova E, DellaPenna D (2001) Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp PCC 6803 and Arabidopsis. Plant Physiol 127:1113-1124
10. Comai L, Young K, Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Henikoff S (2004) Efficient discovery of DNA polymorphisms in natural populations by Ecotilling. Plant J 37:778-86
11. Comai L, Henikoff S (2006) TILLING: practical single-nucleotide mutation discovery. Plant J 45:684-94
12. Cook W, Miles D (1992) Nuclear mutations affecting plastoquinone accumulation in maize. Photosynth Res 31:99-111
13. Cui X, Hsiac AP, Liu F, Ashlockd DA, Wise RP, Schnable PS (2003) Alternative transcription initiation sites and polyadenylation sites are recruited during Mu suppression at the rf2a locus of maize. Genetics 163:685-698
14. Demurin Y (1993) Genetic variability of tocopherol composition in sunflower seeds. Helia 16:59-62
15. Demurin Y, Skoric D, Karlovic D (1996) Genetic variability of tocopherol composition in sunflower seeds as a basis of breeding for improved oil quality. Plant Breed 115:33-36
16. Demurin Y, Efimenko SG, Peretyagina TM (2004) Genetic identification of tocopherol mutations in sunflower. Helia 27:113-116
17. Dolde D, Vlahakis C, Hazebroek J (1999) Tocopherols in breeding lines and effects of plant location, fatty acid composition, and temperature during development. J Am Oil Chem Soc 76:349-355
18. Emanuelsson O, Nielsen H, von Heijne G (1999) ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci 8:978-984
19. Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nature Rev Genetics 3:329-341
20. Fick GN, Zimmer DE, Kinman ML (1974) Registration of six sunflower parental lines. Crop Sci 14:912
21. Grandbastein AM, Spielman A, Caboche M (1989) Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature 337:376-380
22. Grandbastein AM (1998). Activation of plant retrotransposons under stress conditions. Trends Plant Sci. 3:181-187
23. Greene EA, Codomo CA, Taylor NE, Henikoff JG, Till BJ, Reynolds SH, Enns LC, Burtner C, Johnson JE, Odden AR, Comai L, Henikoff S (2003) Spectrum of chemically induced mutations from a large-scale reverse-genetic screen in Arabidopsis. Genetics 164:731-40
24. Grusak MA, DellaPenna D (1999) Improving the nutrient composition of plants to enhance human nutrition and health. Annu Rev Plant Physiol Plant Mol Biol 50:133-161
25. Hass CG, Leonard SW, Miller JF, Slabaugh MB, Traber MG, Knapp SJ (2003) Genetics of tocopherol (vitamin E) composition mutants in sunflower. In: Abstract of Plant and Animal Genome Conference XI, San Diego, CA, USA, Jan 11-15, 2003 (http://wwwintl-pagorg/11/ abstracts/P7b_P821_XI.html)
26. Hass CG, Tang S, Leonard S, Traber M, Miller JF, Knapp SJ (2006) Three non-allelic epistatically interacting methyltransferase mutations produce novel tocopherol (vitamin E) profiles in sunflower. Theor Appl Genet (in press)
27. Hoffmann GR (1980) Genetic effects of dimethyl sulfate, diethyl sulfate, and related compounds. Mutat Res 75:63-129
28. Jiang N, Feschotte C, Zhang X, Wessler SR (2004) Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). Curr Opin Plant Biol 7:115-119
29. Johns MA, Mottinger J, Freeling M (1985) A low copy number, copia-like transposon in maize. EMBO J 4:1093-1102
30. Joshi C, Chiang V (1998) Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol Biol 37:663-674
31. Kagan R, Clarke S (1994) Widespread occurrence of three sequence motifs in diverse S-adenosylmethionine-dependent methyltransferases suggests a common structure for these enzymes. Arch Biochem Biophys 310:417-427
32. Kamal-Eldin A, Andersson R (1997) A multivariate study of the correlation between tocopherols composition content and fatty acid composition in vegetable oils. J Am Oil Chem Soc 74:375-380
33. Lal SK, Choi J-H, Shaw JR, Hannah LC (1999) A splice site mutant of maize activates cryptic splice sites, elicits intron inclusion and exon exclusion, and permits branch point elucidation. Plant Physiol 121:411-418
34. Lal SK, Giroux MJ, Brendel V, Vallejos CE, Hannah LC (2003) The maize genome contains a helitron insertion. Plant Cell 15:381-391
35. Lal SK, Hannah LC (2005) Plant genomes: massive changes of the maize genome are caused by Helitrons. Heredity 95:421-2
36. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174-181
37. Ma J, Devos KM, Bennetzen JL (2004) Analyses of LTR-retrotransposon structures reveal recent and rapid genomic DNA loss in rice. Genome Res 14:860-869
38. Marchler-Bauer A, Bryant SH (2004) CD-Search: protein domain annotations on the fly. Nucleic Acids Res 32:W327-W331
39. Marillonnet S, Wessler SR (1997) Retrotransposon insertion into the maize waxy gene results in tissue-specific RNA processing. Plant Cell 9:967-78
40. Marillonnet S, Wessler SR (1998) Extreme structural heterogeneity among the members of a maize retrotransposon family. Genetics 150:1245-56
41. Michelmore RW, Paran I, Kesseli V (1991) Identification of markers linked to disease resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828-9832
42. Miller JF (1997) Registration of cms HA89 (PEF1) cytoplasmic male-sterile, RPEF1 restorer, and two nuclear male-sterile (NMS373 and 377) sunflower genetic stocks. Crop Sci 37:1984
43. Motohashi R, Ito T, Kobayashi M, Taji T, Nagata N, Asami T, Yoshida S, Yamaguchi-Shinozaki K, Shinozaki K (2003) Functional analysis of the 37 kDa inner envelope membrane polypeptide in chloroplast biogenesis using a Ds-tagged Arabidopsis pale-green mutant. Plant J 34:719-731
44. Perez-Vich B, Berry ST, Velasco L, Fernandez-Martinez JM, Gandhi S, Freeman C, Heesacker A, Knapp SJ, Leon AJ (2005) Molecular mapping of nuclear male sterility genes in sunflower. Crop Sci 45:1851-1857
45. Porfirova S, Bergmüller E, Tropf S, Lemke R, Dormann P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis. Proc Natl Acad Sci USA 99:12495-12500
46. Purugganan MD, Wessler SR (1994) Molecular evolution of magellan, a maize Ty3/gypsy-like retrotransposon. Proc Natl Acad Sci USA 91:11674-11678
47. Roath WW, Miller JF, Gulya TJ (1981) Registration of RHA 801 sunflower germplasm. Crop Sci 21:479
48. Rocheford TR, Wong JC, Egesel CO, Lambert RJ (2002) Enhancement of vitamin E levels in corn. J Am Coll Nutr 21:191S-198S
49. Rozas J, Sanchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496-2497
50. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765-768
51. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nature Genet 20:43-45
52. Santini S, Cavallini A, Natali L, Minelli S, Maggini F, Cionini PG (2002) Ty1/copia- and Ty3/ gypsy-like DNA sequences in Helianthus species. Chromosoma 111:192-120
53. Sattler SE, Cahoon EB, Coughlan SJ, DellaPenna D (2003) Characterization of tocopherol cyclases from higher plants and cyanobacteria: evolutionary implications for tocopherol synthesis and function. Plant Physiol 132:2184-2195
54. Sattler SE, Gillilanda LU, Magallanes-Lundbacka M, Pollard M, DellaPenna D (2004) Vitamin E is essential for seed longevity and for preventing lipid peroxidation during germination. Plant Cell 16:1419-1432
55. Sheppard AJ, Pennington JAT, Weihrauch JL (1993) Analysis and distribution of vitamin E in vegetable oils and foods. In: Packer L, Fuch J (eds) Vitamin E in health and disease. Marcel-Dekker, New York, pp 9-31
56. Shintani DK, DellaPenna D (1998) Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098-2100
57. Shintani DK, Cheng Z, DellaPenna D (2002) The role of 2-methyl-6-phytylbenzoquinone methyltransferase in determining tocopherol composition in Synechocystis sp. PCC6803. FEBS Lett. 511:1-5
58. Song SU, Gerasimova T, Kurkulos M, Boeke JD, Corces VG (1994) An env-like protein encoded by a Drosophila retroelement: evidence that gypsy is an infectious retrovirus. Genes Dev 8:2046-2057
59. Tang S, Yu JK, Slabaugh MB, Shintani DK, Knapp SJ (2002) Simple sequence repeat map of the sunflower genome. Theor Appl Genet 105:1124-1136
60. Tang S, Kishore VK, Knapp SJ (2003) PCR-multiplexes for a genome-wide framework of simple sequence repeat marker loci in cultivated sunflower. Theor Appl Genet 107:6-19
61. Tang S, Hass CG, Knapp SJ (2005) Candidate genes for mutations causing changes in tocopherol composition in sunflower. In: Abstract of Plant and Animal Genome Conference XIII, San Diego, CA, USA, Jan 15-19, 2005 (http:// www.intl-pag.org/13/abstracts/PAG13_W071.html)
62. Tatusova TA, Madden TL (1999) Blast 2 sequences - a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett 174:247-250
63. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680
64. Till BJ, Reynolds SH, Greene EA, Codomo CA, Enns LC, Johnson JE, Burtner C, Odden AR, Young K, Taylor NE, Henikoff JG, Comai L, Henikoff S (2003) Large-scale discovery of induced point mutations with high-throughput TILLING. Genome Res 13:524-30
65. Van Eenennaam AL, Lincoln K, Durrett TP, Valentin HE, Shewmaker CK, Thorne GM, Jiang J, Baszis SR, Levering CK, Aasen ED, Hao M, Stein JC, Norris SR, Last RL (2003) Engineering vitamin E content: from Arabidopsis mutant to soy oil. Plant Cell 15:3007-3019
66. Varagona MJ, Purugganan M, Wessler SR (1992) Alternative splicing induced by insertion of retrotransposons into the maize waxy gene. Plant Cell 4:811-820
67. Velasco L, Domínguez J, Fernández-Martínez JM (2004a) Registration of T589 and T2100 sunflower germplasms with modified tocopherol profiles. Crop Sci 44:362-363
68. Velasco L, Pérez-Vich B, Fernández-Martínez JM (2004b) Novel variation for the tocopherol profile in a sunflower created by mutagenesis and recombination. Plant Breed 123:490-492
69. Weil CF, Marillonnet S, Burr B, Wessler SR (1992) Changes in state of the Wx-m5 allele of maize are due to intragenic transposition of Ds. Genetics 130:75-85
70. Wong JC, Lambert RT, Tadmor Y, Rocheford TR (2003) QTL associated with accumulation of tocopherols in maize. Crop Sci 43:2257-2266
71. Yu JK, Tang S, Slabaugh MB, Heesacker A, Cole G, Herring M, Soper J, Han F, Chu WC, Webb DM, Thompson L, Edwards KJ, Berry S, Leon AJ, Olungu C, Maes N, Knapp SJ (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Sci 43:367-387