Defects in meiotic chromosome segregation lead to unreduced male gametes in Arabidopsis SMC5/6 complex mutants

. 2021 Sep 24 ; 33 (9) : 3104-3119.

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid34240187

Structural maintenance of chromosome 5/6 (SMC5/6) complex is a crucial factor for preserving genome stability. Here, we show that mutants for several Arabidopsis (Arabidopsis thaliana) SMC5/6 complex subunits produce triploid offspring. This phenotype is caused by a meiotic defect leading to the production of unreduced male gametes. The SMC5/6 complex mutants show an absence of chromosome segregation during the first and/or the second meiotic division, as well as a partially disorganized microtubule network. Importantly, although the SMC5/6 complex is partly required for the repair of SPO11-induced DNA double-strand breaks, the nonreduction described here is SPO11-independent. The measured high rate of ovule abortion suggests that, if produced, such defects are maternally lethal. Upon fertilization with an unreduced pollen, the unbalanced maternal and paternal genome dosage in the endosperm most likely causes seed abortion observed in several SMC5/6 complex mutants. In conclusion, we describe the function of the SMC5/6 complex in the maintenance of gametophytic ploidy in Arabidopsis.

Zobrazit více v PubMed

Aragón L (2018) The Smc5/6 complex: new and old functions of the enigmatic long-distance relative. Annu Rev Genet 52 PubMed

Armstrong SJ, Caryl AP, Jones GH, Franklin FCH (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J Cell Sci 115 PubMed

Batista RA, Köhler C (2020) Genomic imprinting in plants—revisiting existing models. Genes Dev 34 PubMed PMC

Borges F, Gardner R, Lopes T, Calarco JP, Boavida LC, Slotkin RK (2012) FACS-based purification of Arabidopsis microspores, sperm cells and vegetative nuclei. Plant Methods 8 PubMed PMC

Bretagnolle F, Thompson JD (1995) Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol 129 PubMed

Brownfield L, Köhler C (2010) Unreduced gamete formation in plants: mechanisms and prospects. J Exp Bot 62 PubMed

Brownfield L, Yi J, Jiang H, Minina EA, Twell D, Köhler C (2015) Organelles maintain spindle position in plant meiosis. Nat. Commun 6 PubMed

Campell BR, Song Y, Posch TE, Cullis CA, Town CD (1992) Sequence and organization of 5S ribosomal RNA-encoding genes of Arabidopsis thaliana. Gene 112 PubMed

Copsey A, Tang S, Jordan PW, Blitzblau HG, Newcombe S, Chan AC-H, Newnham L, Li Z, Gray S, Herbert AD, et al. (2013). Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions. PLoS Genet 9 PubMed PMC

van der Crabben SN, Hennus MP, McGregor GA, Ritter DI, Nagamani SCS, Wells OS, Harakalova M, Chinn IK, Alt A, Vondrova L, et al. (2016) Destabilized SMC5/6 complex leads to chromosome breakage syndrome with severe lung disease. J Clin Invest 126 PubMed PMC

Cromer L, Heyman J, Touati S, Harashima H, Araou E, Girard C, Horlow C, Wassmann K, Schnittger A, De Veylder L, et al. (2012). OSD1 promotes meiotic progression via APC/C inhibition and forms a regulatory network with TDM and CYCA1;2/TAM. PLoS Genet 8 PubMed PMC

D’Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y, To JPC, Berchowitz LE, Copenhaver GP, Mercier R (2010) The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6 PubMed PMC

d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Simon M, Jenczewski E, Mercier R (2008) Mutations in AtPS1 (Arabidopsis thaliana parallel spindle 1) lead to the production of diploid pollen grains. PLoS Genet 4 PubMed PMC

Decorsière A, Mueller H, Van Breugel PC, Abdul F, Gerossier L, Beran RK, Livingston CM, Niu C, Fletcher SP, Hantz O, et al. (2016). Hepatitis B virus X protein identifies the Smc5/6 complex as a host restriction factor. Nature 531 PubMed

Díaz M, Pecinka A (2018) Scaffolding for repair: understanding molecular functions of the SMC5/6 complex. Genes (Basel) 9 PubMed PMC

Díaz M, Pečinková P, Nowicka A, Baroux C, Sakamoto T, Gandha PY, Jeřábková H, Matsunaga S, Grossniklaus U, Pecinka A (2019) The SMC5/6 complex subunit NSE4A is involved in DNA damage repair and seed development. Plant Cell 31 PubMed PMC

Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Scheid OM, Hennig L, Köhler C (2009) Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLOS Genet 5 PubMed PMC

Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A, Haering CH, Dekker C (2018) Real-time imaging of DNA loop extrusion by condensin. Science 360 PubMed PMC

Gerlach WL, Bedbrook JR (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7 PubMed PMC

Gómez R, Jordan PW, Viera A, Alsheimer M, Fukuda T, Jessberger R, Llano E, Pendás AM, Handel MA, Suja JA (2013) Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis suggests functions in distinct chromosome processes. J Cell Sci 126 PubMed PMC

Grelon M, Vezon D, Gendrot G, Pelletier G (2001) AtSPO11-1 is necessary for efficient meiotic recombination in plants. EMBO J 20 PubMed PMC

Heyman J, Van den Daele H, De Wit K, Boudolf V, Berckmans B, Verkest A, Alvim Kamei CL, De Jaeger G, Koncz C, De Veylder L (2011) Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell 23 PubMed PMC

Higgins JD, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Genes Dev 19 PubMed PMC

Hong Y, Sonneville R, Agostinho A, Meier B, Wang B, Blow JJ, Gartner A (2016) The SMC-5/6 complex and the HIM-6 (BLM) helicase synergistically promote meiotic recombination intermediate processing and chromosome maturation during Caenorhabditis elegans meiosis. PLoS Genet 12 PubMed PMC

Hwang G, Sun F, O’Brien M, Eppig JJ, Handel MA, Jordan PW (2017) SMC5/6 is required for the formation of segregation-competent bivalent chromosomes during meiosis I in mouse oocytes. Development 144 PubMed PMC

Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17 PubMed

Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21 PubMed PMC

Jeppsson K, Kanno T, Shirahige K, Sjögren C (2014) The maintenance of chromosome structure: positioning and functioning of SMC complexes. Nat Rev Mol Cell Biol 15 PubMed

Kawashima T, Berger F (2014). Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet 15 PubMed

Kegel A, Sjögren C (2010) The Smc5/6 complex: more than repair? Cold Spring Harb Symp Quant Biol 75 PubMed

Köhler C, Wolff P, Spillane C (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Annu Rev Plant Biol 63 PubMed

Kwak JS, Son GH, Kim SI, Song JT, Seo HS (2016) Arabidopsis HIGH PLOIDY2 Sumoylates and stabilizes flowering locus C through Its E3 ligase activity. Front Plant Sci 7 PubMed PMC

Leung GP, Lee L, Schmidt TI, Shirahige K, Kobor MS (2011) Rtt107 is required for recruitment of the SMC5/6 complex to DNA double strand breaks. J Biol Chem 286 PubMed PMC

Li X, Zhang Y, Clarke JD, Li Y, Dong X (1999) Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98 PubMed

Liu CM, Meinke DW (1998) The titan mutants of Arabidopsis are disrupted in mitosis and cell cycle control during seed development. Plant J 16 PubMed

Liu M, Shi S, Zhang S, Xu P, Lai J, Liu Y, Yuan D, Wang Y, Du J, Yang C (2014) SUMO E3 ligase AtMMS21 is required for normal meiosis and gametophyte development in Arabidopsis. BMC Plant Biol 14 PubMed PMC

Manzanero S, Arana P, Puertas MJ, Houben A (2000) The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109 PubMed

Martinez-Garcia M, Pradillo M (2017) Functional analysis of Arabidopsis ARGONAUTEs in meiosis and DNA repair. PubMed

Mengiste T, Revenkova E, Bechtold N, Paszkowski J (1999) An SMC-like protein is required for efficient homologous recombination in Arabidopsis. EMBO J 18 PubMed 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 PubMed PMC

Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43 PubMed

Payne F, Colnaghi R, Rocha N, Seth A, Harris J, Carpenter G, Bottomley WE, Wheeler E, Wong S, Saudek V, et al. (2014). Hypomorphism in human NSMCE2 linked to primordial dwarfism and insulin resistance. J Clin Invest 124 PubMed PMC

Pebernard S, Wohlschlegel J, McDonald WH, Yates JR, Boddy MN (2006) The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol Cell Biol 26 PubMed PMC

Preuss D, Rhee SY, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264 PubMed

Räschle M, PubMed PMC

Rowley MJ, Corces VG (2018) Organizational principles of 3D genome architecture. Nat Rev Genet 19 PubMed PMC

Sánchez Moran E, Armstrong SJ, Santos JL, Franklin FCH, Jones GH (2001) Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants. Chromosom Res 9 PubMed

Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9 PubMed PMC

Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125 PubMed

De Storme N, Geelen D (2011) The Arabidopsis mutant Jason produces unreduced first division restitution male gametes through a parallel/ fused spindle mechanism in meiosis II. Plant Physiol 155 PubMed PMC

Uhlmann F (2016) SMC complexes: from DNA to chromosomes. Nat Rev Mol Cell Biol 17 PubMed

Wang Y, Cheng Z, Huang J, Shi Q, Hong Y, Copenhaver GP, Gong Z, Ma H (2012) The DNA replication factor RFC1 is required for interference-sensitive meiotic crossovers in Arabidopsis thaliana. PLoS Genet 8 PubMed 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 PubMed PMC

Xaver M, Huang L, Chen D, Klein F (2013) Smc5/6-Mms21 prevents and eliminates inappropriate recombination intermediates in meiosis. PLoS Genet 9 PubMed PMC

Yan S, Wang W, Marqués J, Mohan R, Saleh A, Durrant WE, Song J, Dong X (2013) Salicylic acid activates DNA damage responses to potentiate plant immunity. Mol Cell 52 PubMed PMC

Zelkowski M, Zelkowska K, Conrad U, Hesse S, Lermontova I, Marzec M, Meister A, Houben A, Schubert V (2019) Arabidopsis NSE4 proteins act in somatic nuclei and meiosis to ensure plant viability and fertility. Front Plant Sci 10 PubMed PMC

Zhang H, Dawe RK (2011) Mechanisms of plant spindle formation. Chromosom Res 19 PubMed

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...