Arabidopsis PTD Is Required for Type I Crossover Formation and Affects Recombination Frequency in Two Different Chromosomal Regions

Pingli Lu; Asela J. Wijeratne; Zhengjia Wang; Gregory P. Copenhaver; Hong Ma

doi:10.1016/j.jgg.2014.02.001

Volume 41 Issue 3

Mar. 2014

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Article Navigation > Journal of Genetics and Genomics > 2014 > 41(3): 165-175

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Arabidopsis PTD Is Required for Type I Crossover Formation and Affects Recombination Frequency in Two Different Chromosomal Regions

doi: 10.1016/j.jgg.2014.02.001

a
Institute of Plant Biology, Institute of Genetics, School of Life Sciences, Fudan University, Shanghai 200433, China
b
Department of Biology and the Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16802, USA
c
School of Forestry and Biotechnology, Zhejiang A&F University, Linan 311300, China
d
Department of Biology and the Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
e
Lineberger Comprehensive Cancer Center, University of North Carolina School of Medicine, Chapel Hill, NC 27599-3280, USA

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Corresponding author: E-mail address: pinglilu@fudan.edu.cn (Pingli Lu); E-mail address: hongma@fudan.edu.cn (Hong Ma)
Received Date: 2013-10-21
Accepted Date: 2014-02-17
Rev Recd Date: 2014-02-17

Available Online: 2014-02-22

Publish Date: 2014-03-20

Abstract

Abstract

In eukaryotes, crossovers together with sister chromatid cohesion maintain physical association between homologous chromosomes, ensuring accurate chromosome segregation during meiosis I and resulting in exchange of genetic information between homologues. The Arabidopsis PTD (Parting Dancers) gene affects the level of meiotic crossover formation, but its functional relationships with other core meiotic genes, such as AtSPO11-1, AtRAD51, and AtMSH4, are unclear; whether PTD has other functions in meiosis is also unknown. To further analyze PTD function and to test for epistatic relationships, we compared the meiotic chromosome behaviors of Atspo11-1 ptd and Atrad51 ptd double mutants with the relevant single mutants. The results suggest that PTD functions downstream of AtSPO11-1 and AtRAD51 in the meiotic recombination pathway. Furthermore, we found that meiotic defects in rck ptd and Atmsh4 ptd double mutants showed similar meiotic phenotypes to those of the relevant single mutants, providing genetic evidences for roles of PTD and RCK in the type I crossovers pathway. Moreover, we employed a pollen tetrad-based fluorescence method and found that the meiotic crossover frequencies in two genetic intervals were significantly reduced from 6.63% and 22.26% in wild-type to 1.14% and 6.36%, respectively, in the ptd-2 mutant. These results revealed new aspects ofPTD function in meiotic crossover formation.
- Meiosis,
- Crossover,
- Recombination frequency

Current address: Molecular and Cellular Imaging Center (MCIC), Ohio State University/OARDC, Wooster, OH 44691, USA.

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References(44)

References

[1]	Börner, G.V., Kleckner, N., Hunter, N. Crossover/noncrossover differentiation, synaptonemal complex formation and regulatory surveillance at the leptotene/zygotene transition of meiosis Cell, 117 (2004),pp. 29-45
[2]	Barlow, A., Hulten, M. Crossing over analysis at pachytene in man Eur. J. Hum. Genet., 6 (1998),pp. 350-358
[3]	Berchowitz, L.E., Francis, K.E., Bey, A.L. et al. PLoS Genet., 3 (2007),p. e132
[4]	Bishop, D.K., Zickler, D. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis Cell, 117 (2004),pp. 9-15
[5]	Celerin, M., Merino, S.T., Stone, J.E. et al. Multiple roles of SPO11 in meiotic chromosome behavior EMBO J., 19 (2000),pp. 2739-2750
[6]	Chen, C., Zhang, W., Timofejeva, L. et al. Plant J., 43 (2005),pp. 321-334
[7]	Copenhaver, G.P., Housworth, E.A., Stahl, F.W. Genetics, 160 (2002),pp. 1631-1639
[8]	Dernburg, A.F., McDonald, K., Moulder, G. et al. Cell, 94 (1998),pp. 387-398
[9]	Deyhle, F., Sarkar, A.K., Tucker, E.J. et al. WUSCHEL regulates cell differentiation during anther development Dev. Biol., 302 (2007),pp. 154-159
[10]	Esposito, M.S., Esposito, R.E. Genetics, 61 (1969),pp. 79-89
[11]	Felsenstein, J. The evolutionary advantage of recombination Genetics, 78 (1974),pp. 737-756
[12]	Francis, K.E., Lam, S.Y., Copenhaver, G.P. Plant Physiol., 142 (2006),pp. 1004-1013
[13]	Francis, K.E., Lam, S.Y., Harrison, B.D. et al. Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 3913-3918
[14]	Grelon, M., Vezon, D., Gendrot, G. et al. EMBO J., 20 (2001),pp. 589-600
[15]	Hamant, O., Ma, H., Cande, W.Z. Genetics of meiotic prophase I in plants Annu. Rev. Plant Biol., 57 (2006),pp. 267-302
[16]	Handel, M.A., Schimenti, J.C. Genetics of mammalian meiosis: regulation, dynamics and impact on fertility Nat. Rev. Genet., 11 (2010),pp. 124-136
[17]	Higgins, J.D., Armstrong, S.J., Franklin, F.C. et al. Genes Dev., 18 (2004),pp. 2557-2570
[18]	Higgins, J.D., Buckling, E.F., Franklin, F.C. et al. Plant J., 54 (2008),pp. 152-162
[19]	Hoffmann, E.R., Borts, R.H. Meiotic recombination intermediates and mismatch repair proteins Cytogenet. Genome Res., 107 (2004),pp. 232-248
[20]	Hollingsworth, N., Brill, S. The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions Genes Dev., 18 (2004),pp. 117-125
[21]	Keeney, S. Mechanism and control of meiotic recombination initiation Curr. Top. Dev. Biol., 52 (2001),pp. 1-53
[22]	Keeney, S., Baudat, F., Angeles, M. et al. Genomics, 61 (1999),pp. 170-182
[23]	Li, W., Chen, C., Markmann-Mulisch, U. et al. Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 10596-10601
[24]	Lichten, M. Meiotic recombination: breaking the genome to save it Curr. Biol., 11 (2001),pp. R253-R256
[25]	Ma, H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants Annu. Rev. Plant Biol., 56 (2005),pp. 393-434
[26]	Ma, H. Arabidopsis Book, 4 (2006),p. e0095
[27]	Macaisne, N., Vignard, J., Mercier, R. SHOC1 and PTD form an XPF-ERCC1-like complex that is required for formation of class I crossovers J. Cell Sci., 124 (2011),pp. 2687-2691
[28]	Macaisne, N., Novatchkova, M., Peirera, L. et al. SHOC1, an XPF endonuclease-related protein, is essential for the formation of class I meiotic crossovers Curr. Biol., 18 (2008),pp. 1432-1437
[29]	Malik, S.B., Ramesh, M.A., Hulstrand, A.M. et al. Mol. Biol. Evol., 24 (2007),pp. 2827-2841
[30]	Mazina, O.M., Mazin, A.V., Nakagawa, T. et al. Cell, 117 (2004),pp. 47-56
[31]	McKim, A.K.S., Green-Marroquin, B.L., Sekelsky, J.J. et al. Meiotic synapsis in the absence of recombination Science, 279 (1998),pp. 876-878
[32]	Mercier, R., Jolivet, S., Vezon, D. et al. Curr. Biol., 15 (2005),pp. 692-701
[33]	Nakagawa, T., Ogawa, H. EMBO J., 18 (1999),pp. 5714-5723
[34]	Osman, F., Dixon, J., Doe, C.L. et al. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis Mol. Cell, 12 (2003),pp. 761-774
[35]	Perkins, D.D. Genetics, 34 (1949),pp. 607-626
[36]	Preuss, D., Rhee, S.Y., Davis, R.W. Science, 264 (1994),pp. 1458-1460
[37]	Romanienko, P.J., Camerini-Otero, R.D. Genomics, 61 (1999),pp. 156-169
[38]	Ross, K.J., Fransz, P., Jones, G.H. Chromosome Res., 4 (1996),pp. 507-516
[39]	Stacey, N.J., Kuromori, T., Azumi, Y. et al. Plant J., 48 (2006),pp. 206-216
[40]	Szostak, J., Orr-Weaver, T., Rothstein, R. et al. The double-strand-break repair model for recombination Cell, 33 (1983),pp. 25-35
[41]	Twell, D., Yamaguchi, J., McCormick, S. Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis Development, 109 (1990),pp. 705-713
[42]	Wijeratne, A.J., Chen, C., Zhang, W. et al. Mol. Biol. Cell, 17 (2006),pp. 1331-1343
[43]	Zalevsky, J., MacQueen, A.J., Duffy, J.B. et al. Genetics, 153 (1999),pp. 1271-1283
[44]	Zickler, D., Kleckner, N. Meiotic chromosomes: integrating structure and function Annu. Rev. Genet., 33 (1999),pp. 603-607