Structural Maintenance of Chromosomes 5/6 Complex Is Necessary for Tetraploid Genome Stability in Arabidopsis thaliana
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
34675953
PubMed Central
PMC8525318
DOI
10.3389/fpls.2021.748252
Knihovny.cz E-zdroje
- Klíčová slova
- NSE2, SMC5/6 complex, genome stability, meiosis, polyploidy, seed development,
- Publikační typ
- časopisecké články MeSH
Polyploidization is a common phenomenon in the evolution of flowering plants. However, only a few genes controlling polyploid genome stability, fitness, and reproductive success are known. Here, we studied the effects of loss-of-function mutations in NSE2 and NSE4A subunits of the Structural Maintenance of Chromosomes 5/6 (SMC5/6) complex in autotetraploid Arabidopsis thaliana plants. The diploid nse2 and nse4a plants show partially reduced fertility and produce about 10% triploid offspring with two paternal and one maternal genome copies. In contrast, the autotetraploid nse2 and nse4a plants were almost sterile and produced hexaploid and aneuploid progeny with the extra genome copies or chromosomes coming from both parents. In addition, tetraploid mutants had more severe meiotic defects, possibly due to the presence of four homologous chromosomes instead of two. Overall, our study suggests that the SMC5/6 complex is an important player in the maintenance of tetraploid genome stability and that autotetraploid Arabidopsis plants have a generally higher frequency of but also higher tolerance for aneuploidy compared to diploids.
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Alonso J. M., Stepanova A. N., Leisse T. J., Kim C. J., Chen H., Shinn P., et al. (2003). Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 301 653–657. 10.1126/science.1086391 PubMed DOI
Aragón L. (2018). The Smc5/6 complex: new and old functions of the enigmatic long-distance relative. Annu. Rev. Genet. 52 89–107. 10.1146/annurev-genet-120417-031353 PubMed DOI
Blary A., Gonzalo A., Eber F., Bérard A., Bergès H., Bessoltane N., et al. (2018). FANCM limits meiotic crossovers in brassica crops. Front. Plant Sci. 9:368. 10.3389/fpls.2018.00368 PubMed DOI PMC
Chen H., He C., Wang C., Wang X., Ruan F., Yan J., et al. (2021). RAD51 supports DMC1 by inhibiting the SMC5/6 complex during meiosis. Plant Cell 33 2869–2882. 10.1093/plcell/koab136 PubMed DOI PMC
Comai L. (2005). The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6 836–846. 10.1038/nrg1711 PubMed DOI
Copsey A., Tang S., Jordan P. W., Blitzblau H. G., Newcombe S., Chan A. C., et al. (2013). Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions. PLoS Genet. 9:e1004071. 10.1371/journal.pgen.1004071 PubMed DOI PMC
Crismani W., Girard C., Froger N., Pradillo M., Santos J. L., Chelysheva L., et al. (2012). FANCM limits meiotic crossovers. Science 336 1588–1590. 10.1126/science.1220381 PubMed DOI
Díaz M., Pečinková P., Nowicka A., Baroux C., Sakamoto T., Gandha P. Y., et al. (2019). The SMC5/6 complex subunit NSE4A is involved in DNA damage repair and seed development. Plant Cell 31 1579–1597. 10.1105/tpc.18.00043 PubMed DOI PMC
Henry I. M., Dilkes B. P., Comai L. (2006). Molecular karyotyping and aneuploidy detection in Arabidopsis thaliana using quantitative fluorescent polymerase chain reaction. Plant J. 48 307–319. 10.1111/j.1365-313X.2006.02871.x PubMed DOI
Hu Z., Cools T., De Veylder L. (2016). Mechanisms used by plants to cope with DNA damage. Annu. Rev. Plant Biol. 67 439–462. 10.1146/annurev-arplant-043015-111902 PubMed DOI
Huang L., Yang S., Zhang S., Liu M., Lai J., Qi Y., et al. (2009). The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. Plant J. 60 666–678. 10.1111/j.1365-313X.2009.03992.x PubMed DOI
Ishida T., Fujiwara S., Miura K., Stacey N., Yoshimura M., Schneider K., et al. (2009). SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21 2284–2297. 10.1105/tpc.109.068072 PubMed DOI PMC
Ishida T., Yoshimura M., Miura K., Sugimoto K. (2012). MMS21/HPY2 and SIZ1, Two Arabidopsis SUMO E3 Ligases, Have Distinct Functions in Development. PLoS One 7:e46897. 10.1371/journal.pone.0046897 PubMed DOI PMC
Jullien P. E., Berger F. (2010). Parental Genome Dosage Imbalance Deregulates Imprinting in Arabidopsis. PLoS Genet. 6:e1000885. 10.1371/journal.pgen.1000885 PubMed DOI PMC
Kegel A., Sjögren C. (2010). The Smc5 / 6 Complex: more than repair? Cold Spring Harb. Symp. Quant. Biol. 75 179–187. 10.1101/sqb.2010.75.047 PubMed DOI
Köhler C., Wolff P., Spillane C. (2012). Epigenetic mechanisms underlying genomic imprinting in plants. Annu. Rev. Plant Biol. 63 331–352. 10.1146/annurev-arplant-042811-105514 PubMed DOI
Kwak J. S., Son G. H., Kim S. I., Song J. T., Seo H. S. (2016). Arabidopsis HIGH PLOIDY2 Sumoylates and stabilizes flowering locus C through Its E3 ligase activity. Front. Plant Sci. 7:530. 10.3389/fpls.2016.00530 PubMed DOI PMC
Li X., Yu M., Bolaños-Villegas P., Zhang J., Ni D., Ma H., et al. (2021). Fanconi anemia ortholog FANCM regulates meiotic crossover distribution in plants. Plant Physiol. 186 344–360. 10.1093/plphys/kiab061 PubMed DOI PMC
Liu C. M., Meinke D. W. (1998). The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. Plant J. 16 21–31. 10.1046/j.1365-313x.1998.00268.x PubMed DOI
Liu M., Shi S., Zhang S., Xu P., Lai J., Liu Y., et al. (2014). SUMO E3 ligase AtMMS21 is required for normal meiosis and gametophyte development in Arabidopsis. BMC Plant Biol. 14:153. 10.1186/1471-2229-14-153 PubMed DOI PMC
Mandáková T., Lysak M. A. (2018). Post-polyploid diploidization and diversification through dysploid changes. Curr. Opin. Plant Biol. 42 55–65. 10.1016/j.pbi.2018.03.001 PubMed DOI
Mengiste T., Revenkova E., Bechtold N., Paszkowski J. (1999). An SMC-like protein is required for efficient homologous recombination in arabidopsis. EMBO J. 18 4505–4512. 10.1093/emboj/18.16.4505 PubMed DOI PMC
Menolfi D., Delamarre A., Lengronne A., Pasero P., Branzei D. (2015). Essential Roles of the Smc5/6 Complex in replication through natural pausing sites and endogenous DNA damage tolerance. Mol. Cell 60 835–846. 10.1016/j.molcel.2015.10.023 PubMed DOI PMC
Morgan C., Zhang H., Henry C. E., Franklin F. C. H., Bomblies K. (2020). Derived alleles of two axis proteins affect meiotic traits in autotetraploid Arabidopsis arenosa. Proc. Natl. Acad. Sci. U. S. A. 117 8980–8988. 10.1073/pnas.1919459117 PubMed DOI PMC
Palecek J. J., Gruber S. (2015). Kite Proteins: a superfamily of SMC/Kleisin partners conserved across bacteria, archaea, and eukaryotes. Structure 23 2183–2190. 10.1016/j.str.2015.10.004 PubMed DOI
Parra-Nunez P., Pradillo M., Santos J. L. (2020). “How to Perform an Accurate Analysis of Metaphase I Chromosome Configurations in Autopolyploids of Arabidopsis thaliana,” in Plant Meiosis: Methods and Protocols, eds Pradillo M., Heckmann S. (New York: Springer; ), 25–36. 10.1007/978-1-4939-9818-0_3 PubMed DOI
Pecinka A., Fang W., Rehmsmeier M., Levy A. A., Mittelsten Scheid O. (2011). Polyploidization increases meiotic recombination frequency in Arabidopsis. BMC Biol. 9:24. 10.1186/1741-7007-9-24 PubMed DOI PMC
Preuss D., Rhee S. Y., Davis R. W. (1994). Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264 1458–1460. 10.1126/science.8197459 PubMed DOI
Raz A., Dahan-Meir T., Melamed-Bessudo C., Leshkowitz D., Levy A. A. (2021). Redistribution of meiotic crossovers along wheat chromosomes by virus-induced gene silencing. Front. Plant Sci. 11:635139. 10.3389/fpls.2020.635139 PubMed DOI PMC
Roy S. (2014). Maintenance of genome stability in plants: repairing DNA double strand breaks and chromatin structure stability. Front. Plant Sci. 5:487. 10.3389/fpls.2014.00487 PubMed DOI PMC
Sánchez Moran E., Armstrong S. J., Santos J. L., Franklin F. C. H., Jones G. H. (2001). Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosome Res. 9 121–128. 10.1023/A:1009278902994 PubMed DOI
Santos J. L., Alfaro D., Armstrong S. J., Franklin F. C. H., Jones G. H. (2003). Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165 1533–1540. 10.1093/genetics/165.3.1533 PubMed DOI PMC
Seear P. J., France M. G., Gregory C. L., Heavens D., Schmickl R., Yant L., et al. (2020). A novel allele of ASY3 is associated with greater meiotic stability in autotetraploid Arabidopsis lyrata. PLoS Genet. 16:e1008900. 10.1371/journal.pgen.1008900 PubMed DOI PMC
Uhlmann F. (2016). SMC complexes: from DNA to chromosomes. Nat. Rev. Mol. Cell Biol. 17 399–412. 10.1038/nrm.2016.30 PubMed DOI
Van De Peer Y., Fawcett J. A., Proost S., Sterck L., Vandepoele K. (2009). The flowering world: a tale of duplications. Trends Plant Sci. 14 680–688. 10.1016/j.tplants.2009.09.001 PubMed DOI
Voorrips R. E., Maliepaard C. A. (2012). The simulation of meiosis in diploid and tetraploid organisms using various genetic models. BMC Bioinformatics 13:248. 10.1186/1471-2105-13-248 PubMed DOI PMC
Watanabe K., Pacher M., Dukowic S., Schubert V., Puchta H., Schubert I. (2009). The Structural maintenance of chromosomes 5/6 complex promotes sister chromatid alignment and homologous recombination after DNA damage in Arabidopsis thaliana. Plant Cell 21 2688–2699. 10.1105/tpc.108.060525 PubMed DOI PMC
Xaver M., Huang L., Chen D., Klein F. (2013). Smc5/6-Mms21 prevents and eliminates inappropriate recombination intermediates in meiosis. PLoS Genet. 9:e1004067. 10.1371/journal.pgen.1004067 PubMed DOI PMC
Xu P., Yuan D., Liu M., Li C., Liu Y., Zhang S., et al. (2013). AtMMS21, an SMC5/6 complex subunit, is involved in stem cell niche maintenance and DNA damage responses in Arabidopsis roots. Plant Physiol. 161 1755–1768. 10.1104/pp.112.208942 PubMed DOI PMC
Yan S., Wang W., Marqués J., Mohan R., Saleh A., Durrant W. E., et al. (2013). Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol. Cell 52 602–610. 10.1016/j.molcel.2013.09.019 PubMed DOI PMC
Yang F., Fernández-Jiménez N., Tučková M., Vrána J., Cápal P., Díaz M., et al. (2021). Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants. Plant Cell 33 3104–3119. 10.1093/plcell/koab178 PubMed DOI PMC
Yuan D., Lai J., Xu P., Zhang S., Zhang J., Li C., et al. (2014). AtMMS21 regulates DNA damage response and homologous recombination repair in Arabidopsis. DNA Repair (Amst). 21 140–147. 10.1016/j.dnarep.2014.04.006 PubMed DOI
Zelkowski M., Zelkowska K., Conrad U., Hesse S., Lermontova I., Marzec M., et al. (2019). Arabidopsis NSE4 proteins act in somatic nuclei and meiosis to ensure plant viability and fertility. Front. Plant Sci. 10:774. 10.3389/fpls.2019.00774 PubMed DOI PMC
Zou W., Li G., Jian L., Qian J., Liu Y., Zhao J. (2021). Arabidopsis SMC6A and SMC6B have redundant function in seed and gametophyte development. J. Exp. Bot. 72 4871–4887. 10.1093/jxb/erab181 PubMed DOI
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