5.9
CiteScore
5.9
Impact Factor
Volume 48 Issue 6
Jun.  2021
Turn off MathJax
Article Contents

OsMLH1 interacts with OsMLH3 to regulate synapsis and interference-sensitive crossover formation during meiosis in rice

doi: 10.1016/j.jgg.2021.04.011
Funds:

We thank Prof. Jiankang Zhu for providing the CRISPR-Cas9 single target system. We thank Prof. Yaoguang Liu for providing the CRISPR-Cas9 multi-target system. We thank Prof. Wanqi Liang for providing the antibody against REC8. This work was supported by the National Natural Science Foundation of China (31630054, 31425018, 31821005) and Program for Chinese Outstanding Talents in Agricultural Scientific Research.

  • Received Date: 2021-04-15
  • Accepted Date: 2021-04-27
  • Rev Recd Date: 2021-04-25
  • Publish Date: 2021-06-20
  • Meiotic recombination is essential for reciprocal exchange of genetic information between homologous chromosomes and their subsequent proper segregation in sexually reproducing organisms. MLH1 and MLH3 belong to meiosis-specific members of the MutL-homolog family, which are required for normal level of crossovers (COs) in some eukaryotes. However, their functions in plants need to be further elucidated. Here, we report the identification of OsMLH1 and reveal its functions during meiosis in rice. Using CRISPR-Cas9 approach, two independent mutants, Osmlh1-1 and Osmlh1-2, are generated and exhibited significantly reduced male fertility. In Osmlh1-1, the clearance of PAIR2 is delayed and partial ZEP1 proteins are not loaded into the chromosomes, which might be due to the deficient in resolution of interlocks at late zygotene. Thus, OsMLH1 is required for the assembly of synapsis complex. In Osmlh1-1, CO number is dropped by ~53% and the distribution of residual COs is consistent with predicted Poisson distribution, indicating that OsMLH1 is essential for the formation of interference-sensitive COs (class I COs). OsMLH1 interacts with OsMLH3 through their C-terminal domains. Mutation in OsMLH3 also affects the pollen fertility. Thus, our experiments reveal that the conserved heterodimer MutLγ (OsMLH1-OsMLH3) is essential for the formation of class I COs in rice.

  • loading
  • Argueso, J.L., Wanat, J., Gemici, Z., Alani, E., 2004. Competing crossover pathways act during meiosis in Saccharomyces cerevisiae. Genetics 168, 1805-1816.
    Bishop, D.K., Zickler, D., 2004. Early decision; meiotic crossover interference prior to stable strand exchange and synapsis. Cell 117, 9-15.
    Chelysheva, L., Grandont, L., Vrielynck, N., le Guin, S., Mercier, R., Grelon, M., 2010. An easy protocol for studying chromatin and recombination protein dynamics during Arabidopsis thaliana meiosis: immunodetection of cohesins, histones and MLH1. Cytogenet. Genome Res. 129, 143-153.
    Chelysheva, L., Vezon, D., Chambon, A., Gendrot, G., Pereira, L., Lemhemdi, A., Vrielynck, N., Le Guin, S., Novatchkova, M., Grelon, M., 2012. The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet. 8, e1002799.
    Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R., Tang, X., Zhou, J.M., 2008. Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146, 368-376.
    Colas, I., Macaulay, M., Higgins, J.D., Phillips, D., Barakate, A., Posch, M., Armstrong, S.J., Franklin, F.C., Halpin, C., Waugh, R., et al., 2016. A spontaneous mutation in Mutl-homolog 3 (HvMlh3) affects synapsis and crossover resolution in the barley desynaptic mutant des10. New Phytol. 212, 693-707.
    Deng, L., Li, L., Zhang, S., Shen, J., Li, S., Hu, S., Peng, Q., Xiao, J., Wu, C., 2017. Suppressor of rid1 (SID1) shares common targets with RID1 on florigen genes to initiate floral transition in rice. PLoS Genet. 13, e1006642.
    Dion, E., Li, L., Jean, M., Belzile, F., 2007. An Arabidopsis mlh1 mutant exhibits reproductive defects and reveals a dual role for this gene in mitotic recombination. Plant J. 51, 431-440.
    Feng, Z., Zhang, B., Ding, W., Liu, X., Yang, D.-L., Wei, P., Cao, F., Zhu, S., Zhang, F., Mao, Y., et al., 2013. Efficient genome editing in plants using a CRISPR/Cas system. Cell Res. 23, 1229-1232.
    Gray, S., Cohen, P.E., 2016. Control of meiotic crossovers: from double-strand break formation to designation. Annu. Rev. Genet. 50, 175-210.
    Harper, L., Golubovskaya, I., Cande, W.Z., 2004. A bouquet of chromosomes. J. Cell Sci. 117, 4025-4032.
    Higgins, J.D., Armstrong, S.J., Franklin, F.C., Jones, G.H., 2004. The Arabidopsis MutS homolog AtMSH4 functions at an early step in recombination: evidence for two classes of recombination in Arabidopsis. Genes Dev. 18, 2557-2570.
    Higgins, J.D., Buckling, E.F., Franklin, F.C., Jones, G.H., 2008. Expression and functional analysis of AtMUS81 in Arabidopsis meiosis reveals a role in the second pathway of crossing-over. Plant J. 54, 152-162.
    Hollingsworth, N.M., Brill, S.J., 2004. The Mus81 solution to resolution: generating meiotic crossovers without Holliday junctions. Genes Dev. 18, 117-125.
    Hunter, N., Kleckner, N., 2001. The single-end invasion: an asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106, 59-70.
    Jackson, N., Sanchez-Moran, E., Buckling, E., Armstrong, S.J., Jones, G.H., Franklin, F.C., 2006. Reduced meiotic crossovers and delayed prophase I progression in AtMLH3-deficient Arabidopsis. EMBO J. 25, 1315-1323.
    Keeney, S., 2008. Spo11 and the formation of DNA double-strand breaks in meiosis. Genome Dyn. Stab. 2, 81-123.
    Kolodner, R.D., 2016. A personal historical view of DNA mismatch repair with an emphasis on eukaryotic DNA mismatch repair. DNA Repair 38, 3-13.
    Kunkel, T.A., Erie, D.A., 2015. Eukaryotic mismatch repair in relation to DNA replication. Annu. Rev. Genet. 49, 291-313.
    Lambing, C., Franklin, F.C.H., Wang, C.J.R., 2017. Understanding and manipulating meiotic recombination in plants. Plant Physiol. 173, 1530-1542.
    Lhuissier, F.G., Offenberg, H.H., Wittich, P.E., Vischer, N.O., Heyting, C., 2007. The mismatch repair protein MLH1 marks a subset of strongly interfering crossovers in tomato. Plant Cell 19, 862-876.
    Li, X., Chang, Y., Xin, X., Zhu, C., Li, X., Higgins, J.D., Wu, C., 2013. Replication protein A2c coupled with replication protein A1c regulates crossover formation during meiosis in rice. Plant Cell 25, 3885-3899.
    Li, Y., Cheng, Z., 2016. Fluorescence in situ hybridization on rice chromosomes. Methods Mol. Biol. 1370, 105-112.
    Luo, Q., Tang, D., Wang, M., Luo, W., Zhang, L., Qin, B., Shen, Y., Wang, K., Li, Y., Cheng, Z., 2013. The role of OsMSH5 in crossover formation during rice meiosis. Mol. Plant 6, 729-742.
    Lynn, A., Soucek, R., Borner, G.V., 2007. ZMM proteins during meiosis: crossover artists at work. Chromosome Res. 15, 591-605.
    Ma, X., Liu, Y.G., 2016. CRISPR/Cas9-based multiplex genome editing in monocot and dicot plants. Curr. Protoc. Mol. Biol. 115, 31.6.1-31.6.21.
    Manhart, C.M., Alani, E., 2016. Roles for mismatch repair family proteins in promoting meiotic crossing over. DNA Repair 38, 84-93.
    Mao, B., Zheng, W., Huang, Z., Peng, Y., Shao, Y., Liu, C., Tang, L., Hu, Y., Li, Y., Hu, L., et al., 2021. Rice MutLγ, the MLH1-MLH3 heterodimer, participates in the formation of type I crossovers and regulation of embryo sac fertility. Plant Biotechnol. J 19, 1443-1455.
    Martinez-Garcia, M., Schubert, V., Osman, K., Darbyshire, A., Sanchez-Moran, E., Franklin, F.C.H., 2018. TOP Ⅱ and chromosome movement help remove interlocks between entangled chromosomes during meiosis. J. Cell Biol. 217, 4070-4079.
    Nonomura, K., Nakano, M., Eiguchi, M., Suzuki, T., Kurata, N., 2006. PAIR2 is essential for homologous chromosome synapsis in rice meiosis I. J. Cell Sci. 119, 217-225.
    Osman, K., Higgins, J.D., Sanchez-Moran, E., Armstrong, S.J., Franklin, F.C.H., 2011. Pathways to meiotic recombination in Arabidopsis thaliana. New Phytol. 190, 523-544.
    Qiao, H., Prasada Rao, H.B.D., Yang, Y., Fong, J.H., Cloutier, J.M., Deacon, D.C., Nagel, K.E., Swartz, R.K., Strong, E., Holloway, J.K., et al., 2014. Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat. Genet. 46, 194-199.
    Ranjha, L., Anand, R., Cejka, P., 2014. The Saccharomyces cerevisiae Mlh1-Mlh3 heterodimer is an endonuclease that preferentially binds to Holliday junctions. J. Biol. Chem. 289, 5674-5686.
    Rao, H.B., Qiao, H., Bhatt, S.K., Bailey, L.R., Tran, H.D., Bourne, S.L., Qiu, W., Deshpande, A., Sharma, A.N., Beebout, C.J., et al., 2017. A SUMO-ubiquitin relay recruits proteasomes to chromosome axes to regulate meiotic recombination. Science 355, 403-407.
    Ren, Y., Chen, D., Li, W., Zhou, D., Luo, T., Yuan, G., Zeng, J., Cao, Y., He, Z., Zou, T., et al., 2019. OsSHOC1 and OsPTD1 are essential for crossover formation during rice meiosis. Plant J. 98, 315-328.
    Reynolds, A., Qiao, H., Yang, Y., Chen, J.K., Jackson, N., Biswas, K., Holloway, J.K., Baudat, F., de Massy, B., Wang, J., et al., 2013. RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat. Genet. 45, 269-278.
    Sanchez Moran, E., Armstrong, S.J., Santos, J.L., Franklin, F.C., Jones, G.H., 2001. Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 9, 121-128.
    Shao, T., Tang, D., Wang, K., Wang, M., Che, L., Qin, B., Yu, H., Li, M., Gu, M., Cheng, Z., 2011. OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol. 156, 1386-1396.
    Shen, Y., Tang, D., Wang, K., Wang, M., Huang, J., Luo, W., Luo, Q., Hong, L., Li, M., Cheng, Z., 2012. ZIP4 in homologous chromosome synapsis and crossover formation in rice meiosis. J. Cell Sci. 125, 2581-2591.
    Storlazzi, A., Gargano, S., Ruprich-Robert, G., Falque, M., David, M., Kleckner, N., Zickler, D., 2010. Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141, 94-106.
    Svetlanov, A., Baudat, F., Cohen, P.E., de Massy, B., 2008. Distinct functions of MLH3 at recombination hot spots in the mouse. Genetics 178, 1937-1945.
    Wang, C., Wang, Y., Cheng, Z., Zhao, Z., Chen, J., Sheng, P., Yu, Y., Ma, W., Duan, E., Wu, F., et al., 2016. The role of OsMSH4 in male and female gamete development in rice meiosis. J. Exp. Bot. 67, 1447-1459.
    Wang, C.J., Carlton, P.M., Golubovskaya, I.N., Cande, W.Z., 2009a. Interlock formation and coiling of meiotic chromosome axes during synapsis. Genetics 183, 905-915.
    Wang, K., Tang, D., Wang, M., Lu, J., Yu, H., Liu, J., Qian, B., Gong, Z., Wang, X., Chen, J., et al., 2009b. MER3 is required for normal meiotic crossover formation, but not for presynaptic alignment in rice. J. Cell Sci. 122, 2055-2063.
    Wang, K., Wang, M., Tang, D., Shen, Y., Miao, C., Hu, Q., Lu, T., Cheng, Z., 2012. The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genet. 8, e1002809.
    Wang, M., Wang, K., Tang, D., Wei, C., Li, M., Shen, Y., Chi, Z., Gu, M., Cheng, Z., 2010. The central element protein ZEP1 of the synaptonemal complex regulates the number of crossovers during meiosis in rice. Plant Cell 22, 417-430.
    Wang, T.F., Kleckner, N., Hunter, N., 1999. Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc. Natl. Acad. Sci. U. S. A. 96, 13914-13919.
    Wang, Y., Copenhaver, G.P., 2018. Meiotic recombination: mixing it up in plants. Annu. Rev. Plant Biol. 69, 577-609.
    Wu, C., Li, X., Yuan, W., Chen, G., Kilian, A., Li, J., Xu, C., Li, X., Zhou, D.X., Wang, S., et al., 2003. Development of enhancer trap lines for functional analysis of the rice genome. Plant J. 35, 418-427.
    Wu, C., You, C., Li, C., Long, T., Chen, G., Byrne, M.E., Zhang, Q., 2008. RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc. Natl. Acad. Sci. U. S. A. 105, 12915-12920.
    Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C., Li, X., et al., 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40, 761-767.
    Yang, Y., Fu, D., Zhu, C., He, Y., Zhang, H., Liu, T., Li, X., Wu, C., 2015. The RINGfinger ubiquitin ligase HAF1 mediates heading date 1 degradation during photoperiodic flowering in rice. Plant Cell 27, 2455-2468.
    Yuan, W., Li, X., Chang, Y., Wen, R., Chen, G., Zhang, Q., Wu, C., 2009. Mutation of the rice gene PAIR3 results in lack of bivalent formation in meiosis. Plant J. 59, 303-315.
    Zakharyevich, K., Tang, S., Ma, Y., Hunter, N., 2012. Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149, 334-347.
    Zhang, J., Wang, C., Higgins, J.D., Kim, Y.J., Moon, S., Jung, K.H., Qu, S., Liang, W., 2019. A multiprotein complex regulates interference-sensitive crossover formation in rice. Plant Physiol. 181, 221-235.
    Zeng, Y.X., Hu, C.Y., Lu, Y.G., Li, J.Q., Liu, X.D., 2009. Abnormalities occurring during female gametophyte development result in the diversity of abnormal embryo sacs and leads to abnormal fertilization in indica/japonica hybrids in rice. J. Integr. Plant Biol. 51, 3-12.
    Zhang, L., Tang, D., Luo, Q., Chen, X., Wang, H., Li, Y., Cheng, Z., 2014. Crossover formation during rice meiosis relies on interaction of OsMSH4 and OsMSH5. Genetics 198, 1447-1456.
    Ziolkowski, P.A., Underwood, C.J., Lambing, C., Martinez-Garcia, M., Lawrence, E.J., Ziolkowska, L., Griffin, C., Choi, K., Franklin, F.C., Martienssen, R.A., et al., 2017. Natural variation and dosage of the HEI10 meiotic E3 ligase control Arabidopsis crossover recombination. Genes Dev. 31, 306-317.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (227) PDF downloads (40) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return