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.
Zobrazit více v PubMed
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. PubMed DOI
Aragón L. (2018). The Smc5/6 complex: new and old functions of the enigmatic long-distance relative. PubMed DOI
Blary A., Gonzalo A., Eber F., Bérard A., Bergès H., Bessoltane N., et al. (2018). FANCM limits meiotic crossovers in brassica crops. 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. PubMed DOI PMC
Comai L. (2005). The advantages and disadvantages of being polyploid. 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. PubMed DOI PMC
Crismani W., Girard C., Froger N., Pradillo M., Santos J. L., Chelysheva L., et al. (2012). FANCM limits meiotic crossovers. 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. PubMed DOI PMC
Henry I. M., Dilkes B. P., Comai L. (2006). Molecular karyotyping and aneuploidy detection in PubMed DOI
Hu Z., Cools T., De Veylder L. (2016). Mechanisms used by plants to cope with DNA damage. 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. 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. 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. PubMed DOI PMC
Jullien P. E., Berger F. (2010). Parental Genome Dosage Imbalance Deregulates Imprinting in Arabidopsis. PubMed DOI PMC
Kegel A., Sjögren C. (2010). The Smc5 / 6 Complex: more than repair? PubMed DOI
Köhler C., Wolff P., Spillane C. (2012). Epigenetic mechanisms underlying genomic imprinting in plants. 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. 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. 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. 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. PubMed DOI PMC
Mandáková T., Lysak M. A. (2018). Post-polyploid diploidization and diversification through dysploid changes. PubMed DOI
Mengiste T., Revenkova E., Bechtold N., Paszkowski J. (1999). An SMC-like protein is required for efficient homologous recombination in arabidopsis. 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. 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. PubMed DOI PMC
Palecek J. J., Gruber S. (2015). Kite Proteins: a superfamily of SMC/Kleisin partners conserved across bacteria, archaea, and eukaryotes. 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 PubMed DOI
Pecinka A., Fang W., Rehmsmeier M., Levy A. A., Mittelsten Scheid O. (2011). Polyploidization increases meiotic recombination frequency in Arabidopsis. PubMed DOI PMC
Preuss D., Rhee S. Y., Davis R. W. (1994). Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. 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. PubMed DOI PMC
Roy S. (2014). Maintenance of genome stability in plants: repairing DNA double strand breaks and chromatin structure stability. PubMed DOI PMC
Sánchez Moran E., Armstrong S. J., Santos J. L., Franklin F. C. H., Jones G. H. (2001). Chiasma formation in PubMed DOI
Santos J. L., Alfaro D., Armstrong S. J., Franklin F. C. H., Jones G. H. (2003). Partial diploidization of meiosis in autotetraploid 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. PubMed DOI PMC
Uhlmann F. (2016). SMC complexes: from DNA to chromosomes. PubMed DOI
Van De Peer Y., Fawcett J. A., Proost S., Sterck L., Vandepoele K. (2009). The flowering world: a tale of duplications. PubMed DOI
Voorrips R. E., Maliepaard C. A. (2012). The simulation of meiosis in diploid and tetraploid organisms using various genetic models. 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 PubMed DOI PMC
Xaver M., Huang L., Chen D., Klein F. (2013). Smc5/6-Mms21 prevents and eliminates inappropriate recombination intermediates in meiosis. 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. 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. 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. 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. 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. 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. PubMed DOI
SMC5/6 complex-mediated SUMOylation stimulates DNA-protein cross-link repair in Arabidopsis
Multiple Roles of SMC5/6 Complex during Plant Sexual Reproduction