Genetic Characterization of the Mutator System in Maize: Behavior and Regulation of Mu Transposons in a Minimal Line

INVESTIGATIONS

Genetic Characterization of the Mutator System in Maize: Behavior and Regulation of Mu Transposons in a Minimal Line

D. Lisch, P. Chomet and M. Freeling
Department of Plant Biology, University of California, Berkeley, California 94720

Most Mutator lines of maize harbor several different classes of Mu transposons, each of which may be present in high copy number. The regulatory element is also often found in high copy number, and it is this element's behavior that is presumed to cause the non-Mendelian inheritance of Mutator activity. Using a very simple Mutator line, we demonstrate that MuDR-1, a regulator of the Mutator system, can functionally replace standard non-Mendelian Mutator activity and that MuDR-1 is associated with the loss of methylation of the termini of another Mu transposon. Further, we show that Mu transposons can transpose duplicatively, that reinsertion tends to be into unlinked sites, and that MuDR-1 frequently suffers deletions. Changes in chromosomal position and the mode of sexual transmission are shown to be associated with changes in the frequency of MuDR-1 duplication and with the activity of MuDR-1 as monitored by the excision frequency of a reporter transposon of the Mu family, Mu1. Our data are derived from a Minimal Mutator Line in which there are relatively few Mu transposons, including one MuDR-1 regulator and as few as one Mu1 reporter. The seemingly enigmatic results that have been obtained using more complicated Mu genotypes are reinterpreted using simple Mendelian principles. We have borrowed a gap-repair model from Drosophila biologists to explain both duplications and deletions of MuDR-1.

This article has been cited by other articles:

M. L. Robbins, R. S. Sekhon, R. Meeley, and S. Chopra
A Mutator Transposon Insertion Is Associated With Ectopic Expression of a Tandemly Repeated Multicopy Myb Gene pericarp color1 of Maize
Genetics, April 1, 2008; 178(4): 1859 - 1874.
[Abstract] [Full Text] [PDF]

J. Li, T.-J. Wen, and P. S. Schnable
Role of RAD51 in the Repair of MuDR-Induced Double-Strand Breaks in Maize (Zea mays L.)
Genetics, January 1, 2008; 178(1): 57 - 66.
[Abstract] [Full Text] [PDF]

W. Yu, J. C. Lamb, F. Han, and J. A. Birchler
Cytological Visualization of DNA Transposons and Their Transposition Pattern in Somatic Cells of Maize
Genetics, January 1, 2007; 175(1): 31 - 39.
[Abstract] [Full Text] [PDF]

S. J. Emrich, L. Li, T.-J. Wen, M. D. Yandeau-Nelson, Y. Fu, L. Guo, H.-H. Chou, S. Aluru, D. A. Ashlock, and P. S. Schnable
Nearly Identical Paralogs: Implications for Maize (Zea mays L.) Genome Evolution
Genetics, January 1, 2007; 175(1): 429 - 439.
[Abstract] [Full Text] [PDF]

S. Moon, K.-H. Jung, D.-e. Lee, W.-Z. Jiang, H. J. Koh, M.-H. Heu, D. S. Lee, H. S. Suh, and G. An
Identification of Active Transposon dTok, a Member of the hAT Family, in Rice
Plant Cell Physiol., November 1, 2006; 47(11): 1473 - 1483.
[Abstract] [Full Text] [PDF]

M. R. Woodhouse, M. Freeling, and D. Lisch
The mop1 (mediator of paramutation1) Mutant Progressively Reactivates One of the Two Genes Encoded by the MuDR Transposon in Maize
Genetics, January 1, 2006; 172(1): 579 - 592.
[Abstract] [Full Text] [PDF]

S.-N. Hashida, T. Uchiyama, C. Martin, Y. Kishima, Y. Sano, and T. Mikami
The Temperature-Dependent Change in Methylation of the Antirrhinum Transposon Tam3 Is Controlled by the Activity of Its Transposase
PLANT CELL, January 1, 2006; 18(1): 104 - 118.
[Abstract] [Full Text] [PDF]

M. D. Yandeau-Nelson, Q. Zhou, H. Yao, X. Xu, B. J. Nikolau, and P. S. Schnable
MuDR Transposase Increases the Frequency of Meiotic Crossovers in the Vicinity of a Mu Insertion in the Maize a1 Gene
Genetics, February 1, 2005; 169(2): 917 - 929.
[Abstract] [Full Text] [PDF]

Z. Xu, X. Yan, S. Maurais, H. Fu, D. G. O'Brien, J. Mottinger, and H. K. Dooner
Jittery, a Mutator Distant Relative with a Paradoxical Mobile Behavior: Excision without Reinsertion
PLANT CELL, May 1, 2004; 16(5): 1105 - 1114.
[Abstract] [Full Text] [PDF]

R. K. Slotkin, M. Freeling, and D. Lisch
Mu killer Causes the Heritable Inactivation of the Mutator Family of Transposable Elements in Zea mays
Genetics, October 1, 2003; 165(2): 781 - 797.
[Abstract] [Full Text] [PDF]

B. P. May, H. Liu, E. Vollbrecht, L. Senior, P. D. Rabinowicz, D. Roh, X. Pan, L. Stein, M. Freeling, D. Alexander, et al.
Maize-targeted mutagenesis: A knockout resource for maize
PNAS, September 30, 2003; 100(20): 11541 - 11546.
[Abstract] [Full Text] [PDF]

F. Chalvet, C. Grimaldi, F. Kaper, T. Langin, and M.-J. Daboussi
Hop, an Active Mutator-like Element in the Genome of the Fungus Fusarium oxysporum
Mol. Biol. Evol., August 1, 2003; 20(8): 1362 - 1375.
[Abstract] [Full Text] [PDF]

D. Lisch, C. C. Carey, J. E. Dorweiler, and V. L. Chandler
A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing
PNAS, April 30, 2002; 99(9): 6130 - 6135.
[Abstract] [Full Text] [PDF]

D. Liu, R. Wang, M. Galli, and N. M. Crawford
Somatic and Germinal Excision Activities of the Arabidopsis Transposon Tag1 Are Controlled by Distinct Regulatory Sequences within Tag1
PLANT CELL, August 1, 2001; 13(8): 1851 - 1863.
[Abstract] [Full Text] [PDF]

M. N. Raizada, G.-L. Nan, and V. Walbot
Somatic and Germinal Mobility of the RescueMu Transposon in Transgenic Maize
PLANT CELL, July 1, 2001; 13(7): 1587 - 1608.
[Abstract] [Full Text] [PDF]

T. Singer, C. Yordan, and R. A. Martienssen
Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1)
Genes & Dev., March 1, 2001; 15(5): 591 - 602.
[Abstract] [Full Text]

G. N. Rudenko and V. Walbot
Expression and Post-Transcriptional Regulation of Maize Transposable Element MuDR and Its Derivatives
PLANT CELL, March 1, 2001; 13(3): 553 - 570.
[Abstract] [Full Text]

Z. Yu, S. I. Wright, and T. E. Bureau
Mutator-like Elements in Arabidopsis thaliana: Structure, Diversity and Evolution
Genetics, December 1, 2000; 156(4): 2019 - 2031.
[Abstract] [Full Text] [PDF]

M. N. Raizada and V. Walbot
The Late Developmental Pattern of Mu Transposon Excision Is Conferred by a Cauliflower Mosaic Virus 35S -Driven MURA cDNA in Transgenic Maize
PLANT CELL, January 1, 2000; 12(1): 5 - 22.
[Abstract] [Full Text] [PDF]

L. Girard and M. Freeling
Mutator-Suppressible Alleles of rough sheath1 and liguleless3 in
Genetics, January 1, 2000; 154(1): 437 - 446.
[Abstract] [Full Text]

X. Yan, I. M. Martínez-Férez, S. Kavchok, and H. K. Dooner
Origination of Ds Elements From Ac Elements in Maize: Evidence for Rare Repair Synthesis at the Site of Ac Excision
Genetics, August 1, 1999; 152(4): 1733 - 1740.
[Abstract] [Full Text]

A. van Houwelingen, E. Souer, J. Mol, and R. Koes
Epigenetic Interactions among Three dTph1 Transposons in Two Homologous Chromosomes Activate a New Excision–Repair Mechanism in Petunia
PLANT CELL, July 1, 1999; 11(7): 1319 - 1336.
[Abstract] [Full Text]

D. Lisch, L. Girard, M. Donlin, and M. Freeling
Functional Analysis of Deletion Derivatives of the Maize Transposon MuDR Delineates Roles for the MURA and MURB Proteins
Genetics, January 1, 1999; 151(1): 331 - 341.
[Abstract] [Full Text]

M. de la Luz Gutierrez-Nava, C. A. Warren, P. Leon, and V. Walbot
Transcriptionally Active MuDR, the Regulatory Element of the Mutator Transposable Element Family of Zea mays, Is Present in Some Accessions of the Mexican land race Zapalote chico
Genetics, May 1, 1998; 149(1): 329 - 346.
[Abstract] [Full Text] [PDF]

J. Walsh, C. A. Waters, and M. Freeling
The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary
Genes & Dev., January 15, 1998; 12(2): 208 - 218.
[Abstract] [Full Text] [PDF]

Characterization of the Germinal and Somatic Activity of the Arabidopsis Transposable Element Tag1
Genetics, January 1, 1998; 148(1): 445 - 456.

G. Muehlbauer, J. Fowler, and M Freeling
Sectors expressing the homeobox gene liguleless3 implicate a time-dependent mechanism for cell fate acquisition along the proximal-distal axis of the maize leaf
Development, January 12, 1997; 124(24): 5097 - 5106.
[Abstract] [PDF]

D. Lisch, C. C. Carey, J. E. Dorweiler, and V. L. Chandler
A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing
PNAS, April 30, 2002; 99(9): 6130 - 6135.
[Abstract] [Full Text] [PDF]

M. Cowperthwaite, W. Park, Z. Xu, X. Yan, S. C. Maurais, and H. K. Dooner
Use of the Transposon Ac as a Gene-Searching Engine in the Maize Genome
PLANT CELL, March 1, 2002; 14(3): 713 - 726.
[Abstract] [Full Text] [PDF]

				J. Li, T.-J. Wen, and P. S. Schnable Role of RAD51 in the Repair of MuDR-Induced Double-Strand Breaks in Maize (Zea mays L.) Genetics, January 1, 2008; 178(1): 57 - 66. [Abstract] [Full Text] [PDF]

				W. Yu, J. C. Lamb, F. Han, and J. A. Birchler Cytological Visualization of DNA Transposons and Their Transposition Pattern in Somatic Cells of Maize Genetics, January 1, 2007; 175(1): 31 - 39. [Abstract] [Full Text] [PDF]

				S. J. Emrich, L. Li, T.-J. Wen, M. D. Yandeau-Nelson, Y. Fu, L. Guo, H.-H. Chou, S. Aluru, D. A. Ashlock, and P. S. Schnable Nearly Identical Paralogs: Implications for Maize (Zea mays L.) Genome Evolution Genetics, January 1, 2007; 175(1): 429 - 439. [Abstract] [Full Text] [PDF]

				S. Moon, K.-H. Jung, D.-e. Lee, W.-Z. Jiang, H. J. Koh, M.-H. Heu, D. S. Lee, H. S. Suh, and G. An Identification of Active Transposon dTok, a Member of the hAT Family, in Rice Plant Cell Physiol., November 1, 2006; 47(11): 1473 - 1483. [Abstract] [Full Text] [PDF]

				M. R. Woodhouse, M. Freeling, and D. Lisch The mop1 (mediator of paramutation1) Mutant Progressively Reactivates One of the Two Genes Encoded by the MuDR Transposon in Maize Genetics, January 1, 2006; 172(1): 579 - 592. [Abstract] [Full Text] [PDF]

				S.-N. Hashida, T. Uchiyama, C. Martin, Y. Kishima, Y. Sano, and T. Mikami The Temperature-Dependent Change in Methylation of the Antirrhinum Transposon Tam3 Is Controlled by the Activity of Its Transposase PLANT CELL, January 1, 2006; 18(1): 104 - 118. [Abstract] [Full Text] [PDF]

				M. D. Yandeau-Nelson, Q. Zhou, H. Yao, X. Xu, B. J. Nikolau, and P. S. Schnable MuDR Transposase Increases the Frequency of Meiotic Crossovers in the Vicinity of a Mu Insertion in the Maize a1 Gene Genetics, February 1, 2005; 169(2): 917 - 929. [Abstract] [Full Text] [PDF]

				Z. Xu, X. Yan, S. Maurais, H. Fu, D. G. O'Brien, J. Mottinger, and H. K. Dooner Jittery, a Mutator Distant Relative with a Paradoxical Mobile Behavior: Excision without Reinsertion PLANT CELL, May 1, 2004; 16(5): 1105 - 1114. [Abstract] [Full Text] [PDF]

				R. K. Slotkin, M. Freeling, and D. Lisch Mu killer Causes the Heritable Inactivation of the Mutator Family of Transposable Elements in Zea mays Genetics, October 1, 2003; 165(2): 781 - 797. [Abstract] [Full Text] [PDF]

				B. P. May, H. Liu, E. Vollbrecht, L. Senior, P. D. Rabinowicz, D. Roh, X. Pan, L. Stein, M. Freeling, D. Alexander, et al. Maize-targeted mutagenesis: A knockout resource for maize PNAS, September 30, 2003; 100(20): 11541 - 11546. [Abstract] [Full Text] [PDF]

				F. Chalvet, C. Grimaldi, F. Kaper, T. Langin, and M.-J. Daboussi Hop, an Active Mutator-like Element in the Genome of the Fungus Fusarium oxysporum Mol. Biol. Evol., August 1, 2003; 20(8): 1362 - 1375. [Abstract] [Full Text] [PDF]

				D. Lisch, C. C. Carey, J. E. Dorweiler, and V. L. Chandler A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing PNAS, April 30, 2002; 99(9): 6130 - 6135. [Abstract] [Full Text] [PDF]

				D. Liu, R. Wang, M. Galli, and N. M. Crawford Somatic and Germinal Excision Activities of the Arabidopsis Transposon Tag1 Are Controlled by Distinct Regulatory Sequences within Tag1 PLANT CELL, August 1, 2001; 13(8): 1851 - 1863. [Abstract] [Full Text] [PDF]

				M. N. Raizada, G.-L. Nan, and V. Walbot Somatic and Germinal Mobility of the RescueMu Transposon in Transgenic Maize PLANT CELL, July 1, 2001; 13(7): 1587 - 1608. [Abstract] [Full Text] [PDF]

				T. Singer, C. Yordan, and R. A. Martienssen Robertson's Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1) Genes & Dev., March 1, 2001; 15(5): 591 - 602. [Abstract] [Full Text]

				G. N. Rudenko and V. Walbot Expression and Post-Transcriptional Regulation of Maize Transposable Element MuDR and Its Derivatives PLANT CELL, March 1, 2001; 13(3): 553 - 570. [Abstract] [Full Text]

				Z. Yu, S. I. Wright, and T. E. Bureau Mutator-like Elements in Arabidopsis thaliana: Structure, Diversity and Evolution Genetics, December 1, 2000; 156(4): 2019 - 2031. [Abstract] [Full Text] [PDF]

				M. N. Raizada and V. Walbot The Late Developmental Pattern of Mu Transposon Excision Is Conferred by a Cauliflower Mosaic Virus 35S -Driven MURA cDNA in Transgenic Maize PLANT CELL, January 1, 2000; 12(1): 5 - 22. [Abstract] [Full Text] [PDF]

				L. Girard and M. Freeling Mutator-Suppressible Alleles of rough sheath1 and liguleless3 in Genetics, January 1, 2000; 154(1): 437 - 446. [Abstract] [Full Text]

				X. Yan, I. M. Martínez-Férez, S. Kavchok, and H. K. Dooner Origination of Ds Elements From Ac Elements in Maize: Evidence for Rare Repair Synthesis at the Site of Ac Excision Genetics, August 1, 1999; 152(4): 1733 - 1740. [Abstract] [Full Text]

				A. van Houwelingen, E. Souer, J. Mol, and R. Koes Epigenetic Interactions among Three dTph1 Transposons in Two Homologous Chromosomes Activate a New Excision–Repair Mechanism in Petunia PLANT CELL, July 1, 1999; 11(7): 1319 - 1336. [Abstract] [Full Text]

				D. Lisch, L. Girard, M. Donlin, and M. Freeling Functional Analysis of Deletion Derivatives of the Maize Transposon MuDR Delineates Roles for the MURA and MURB Proteins Genetics, January 1, 1999; 151(1): 331 - 341. [Abstract] [Full Text]

				M. de la Luz Gutierrez-Nava, C. A. Warren, P. Leon, and V. Walbot Transcriptionally Active MuDR, the Regulatory Element of the Mutator Transposable Element Family of Zea mays, Is Present in Some Accessions of the Mexican land race Zapalote chico Genetics, May 1, 1998; 149(1): 329 - 346. [Abstract] [Full Text] [PDF]

				J. Walsh, C. A. Waters, and M. Freeling The maize gene liguleless2 encodes a basic leucine zipper protein involved in the establishment of the leaf blade-sheath boundary Genes & Dev., January 15, 1998; 12(2): 208 - 218. [Abstract] [Full Text] [PDF]

				Characterization of the Germinal and Somatic Activity of the Arabidopsis Transposable Element Tag1 Genetics, January 1, 1998; 148(1): 445 - 456.

				G. Muehlbauer, J. Fowler, and M Freeling Sectors expressing the homeobox gene liguleless3 implicate a time-dependent mechanism for cell fate acquisition along the proximal-distal axis of the maize leaf Development, January 12, 1997; 124(24): 5097 - 5106. [Abstract] [PDF]

				M. Cowperthwaite, W. Park, Z. Xu, X. Yan, S. C. Maurais, and H. K. Dooner Use of the Transposon Ac as a Gene-Searching Engine in the Maize Genome PLANT CELL, March 1, 2002; 14(3): 713 - 726. [Abstract] [Full Text] [PDF]