The RING Domain of Rice HEI10 is Essential for Male, But Not Female Fertility
Tóm tắt
HEI10 is a conserved E3 ubiquitin ligase involved in crossover formation during meiosis, and is thus essential for both male and female gamete development. Here, we have discovered a novel allele of HEI10 in rice that produces a truncated HEI10 protein missing its N-terminal RING domain, namely sh1 (shorter hei10 1). Unlike previously reported hei10 null alleles that are completely sterile, sh1 exhibits complete male sterility but retains partial female fertility. The causative sh1 mutation is a 76 kb inversion between OsFYVE4 and HEI10, which breaks the integrity of both genes. Allelic tests and complementation assays revealed that the gamete developmental defects of sh1 were caused by disruption of HEI10. Further studies demonstrated that short HEI10 can correctly localise to the nucleus, where it could interact with other proteins that direct meiosis; expressing short HEI10 in hei10 null lines partially restores female fertility. Our data reveal an intriguing mutant allele of HEI10 with differential effects on male and female fertility, providing a new tool to explore similarities and differences between male and female meiosis.
Tài liệu tham khảo
Bhalla N, Wynne DJ, Jantsch V, Dernburg AF (2008) ZHP-3 acts at crossovers to couple meiotic recombination with synaptonemal complex disassembly and bivalent formation in C. elegans. PLoS Genet 4:e1000235. https://doi.org/10.1371/journal.pgen.1000235
Börner GV, Kleckner N, Hunter N (2004) Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis. Cell 117:29–45. https://doi.org/10.1016/S0092-8674(04)00292-2
Burt A, Bell G, Harvey PH (1991) Sex differences in recombination. J Evol Biol 4:259–277. https://doi.org/10.1046/j.1420-9101.1991.4020259.x
Capilla-Pérez L, Durand S, Hurel A et al (2021) The synaptonemal complex imposes crossover interference and heterochiasmy in Arabidopsis. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.2023613118/-/DCSupplemental
Chang Z, Xu C, Huang X et al (2020) The plant-specific ABERRANT GAMETOGENESIS 1 gene is essential for meiosis in rice. J Exp Bot 71:204–218. https://doi.org/10.1093/jxb/erz441
Chelysheva L, Vezon D, Chambon A et al (2012) The Arabidopsis HEI10 is a new ZMM protein related to Zip3. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002799
Chen L et al (2006) Isolation and genetic analysis for rice mutants treated with 60Co γ-Ray. J Xiamen Univ 45(1): 82–85
Cheng Z (2013) Analyzing meiotic chromosomes in rice. Plant Meiosis Methods Protoc 2013:125–134
de la Casa-Esperón E, Loredo-Osti JC, de Villena FP-M et al (2002) X chromosome effect on maternal recombination and meiotic drive in the mouse. Genetics 161:1651–1659. https://doi.org/10.1093/genetics/161.4.1651
De Muyt A, Zhang L, Piolot T et al (2014) E3 ligase Hei10: a multifaceted structure-based signaling molecule with roles within and beyond meiosis. Genes Dev 28:1111–1123. https://doi.org/10.1101/gad.240408.114
Deshaies RJ, Joazeiro CAP (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399–434. https://doi.org/10.1146/annurev.biochem.78.101807.093809
Drouaud J, Mercier R, Chelysheva L et al (2007) Sex-specific crossover distributions and variations in interference level along Arabidopsis thaliana chromosome 4. PLoS Genet 3:1096–1107. https://doi.org/10.1371/journal.pgen.0030106
Durand S, Lian Q, Jing J et al (2022) Joint control of meiotic crossover patterning by the synaptonemal complex and HEI10 dosage. Nat Commun. https://doi.org/10.1038/s41467-022-33472-w
Fung JC, Rockmill B, Odell M, Roeder GS (2004) Imposition of crossover interference through the nonrandom distribution of synapsis initiation complexes. Cell 116:795–802. https://doi.org/10.1016/S0092-8674(04)00249-1
Gerton JL, Hawley RS (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6:477–487
Giraut L, Falque M, Drouaud J et al (2011) Genome-wide crossover distribution in Arabidopsis thaliana meiosis reveals sex-specific patterns along chromosomes. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002354
Gray S, Cohen PE (2016) Control of Meiotic crossovers: from double-strand break formation to designation. Annu Rev Genet 50:175–210. https://doi.org/10.1146/annurev-genet-120215-035111
Gruhn JR, Al-Asmar N, Fasnacht R et al (2016) Correlations between synaptic initiation and meiotic recombination: a study of humans and mice. Am J Hum Genet 98:102–115. https://doi.org/10.1016/j.ajhg.2015.11.019
Hong L, Tang D, Zhu K et al (2012) Somatic and reproductive cell development in rice anther is regulated by a putative glutaredoxin. Plant Cell 24:577–588. https://doi.org/10.1105/tpc.111.093740
Johnston SE, Bérénos C, Slate J, Pemberton JM (2016) Conserved genetic architecture underlying individual recombination rate variation in a wild population of soay sheep (Ovis aries). Genetics 203:583–598. https://doi.org/10.1534/genetics.115.185553
Kleckner N, Storlazzi A, Zickler D (2003) Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19:623–628. https://doi.org/10.1016/j.tig.2003.09.004
Kong A, Thorleifsson G, Frigge ML et al (2014) Common and low-frequency variants associated with genome-wide recombination rate. Nat Genet 46:11–16. https://doi.org/10.1038/ng.2833
Lake CM, Nielsen RJ, Guo F et al (2015) Vilya, a component of the recombination nodule, is required for meiotic double-strand break formation in Drosophila. Elife. https://doi.org/10.7554/eLife.08287
Lenormand T (2003) The evolution of sex dimorphism in recombination. Genetics 163:811–822. https://doi.org/10.1093/genetics/163.2.811
Lenormand T, Dutheil J (2005) Recombination difference between sexes: a role for haploid selection. PLoS Biol 0396–0403
Lercher MJ, Hurst LD (2003) Imprinted chromosomal regions of the human genome have unusually high recombination rates. Genetics 165:1629–1632. https://doi.org/10.1093/genetics/165.3.1629
Li N, Zhang DS, Liu HS et al (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014. https://doi.org/10.1105/tpc.106.044107
Li Y, Qin B, Shen Y et al (2018) HEIP1 regulates crossover formation during meiosis in rice. Proc Natl Acad Sci USA 115:10810–10815. https://doi.org/10.1073/pnas.1807871115
Liu H, Chu H, Li H et al (2005) Genetic analysis and mapping of rice (Oryza sativa L.) male-sterile (OsMS-L) mutant. Chin Sci Bull 50:122–125. https://doi.org/10.1360/982004-423
Liu C, Cao Y, Hua Y et al (2021) Concurrent disruption of genetic interference and increase of genetic recombination frequency in hybrid rice using CRISPR/Cas9. Front Plant Sci. https://doi.org/10.3389/fpls.2021.757152
Lynn A, Soucek R, Börner GV (2007) ZMM proteins during meiosis: crossover artists at work. Chromosome Res 15:591–605. https://doi.org/10.1007/s10577-007-1150-1
Mercier R, Mézard C, Jenczewski E et al (2015) The molecular biology of meiosis in plants. Annu Rev Plant Biol 66:297–327. https://doi.org/10.1146/annurev-arplant-050213-035923
Morelli MA, Cohen PE (2005) Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction 130:761–781
Morgan C, Fozard JA, Hartley M et al (2021) Diffusion-mediated HEI10 coarsening can explain meiotic crossover positioning in Arabidopsis. Nat Commun. https://doi.org/10.1038/s41467-021-24827-w
Petkov PM, Broman KW, Szatkiewicz JP, Paigen K (2007) Crossover interference underlies sex differences in recombination rates. Trends Genet 23:539–542. https://doi.org/10.1016/j.tig.2007.08.015
Qiao H, Prasada Rao HBD, Yang Y et al (2014) Antagonistic roles of ubiquitin ligase HEI10 and SUMO ligase RNF212 regulate meiotic recombination. Nat Genet 46:194–199. https://doi.org/10.1038/ng.2858
Rao HBDP, Qiao H, Bhatt SK et al (2017) A SUMO-ubiquitin relay recruits proteasomes to chromosome axes to regulate meiotic recombination. Science 355:403–407. https://doi.org/10.1126/science.aaf6407
Reynolds A, Qiao H, Yang Y et al (2013) RNF212 is a dosage-sensitive regulator of crossing-over during mammalian meiosis. Nat Genet 45:269–278. https://doi.org/10.1038/ng.2541
Rockmill B, Fung JC, Branda SS, Roeder GS (2003) The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr Biol 13:1954–1962. https://doi.org/10.1016/j.cub.2003.10.059
Serrentino M-E, Chaplais E, Sommermeyer V, Borde V (2013) Differential association of the conserved SUMO ligase Zip3 with meiotic double-strand Break sites reveals regional variations in the outcome of meiotic recombination. PLoS Genet 9:e1003416. https://doi.org/10.1371/journal.pgen.1003416
Shang Y, Tan T, Fan C et al (2022) Meiotic chromosome organization and crossover patterns. Biol Reprod 107:275–288
Shao T, Tang D, Wang K et al (2011) OsREC8 is essential for chromatid cohesion and metaphase I monopolar orientation in rice meiosis. Plant Physiol 156:1386–1396. https://doi.org/10.1104/pp.111.177428
Singh MK, Nicolas E, Gherraby W et al (2007) HEI10 negatively regulates cell invasion by inhibiting cyclin B/Cdk1 and other promotility proteins. Oncogene 26:4825–4832. https://doi.org/10.1038/sj.onc.1210282
Toby GG, Gherraby W, Coleman TR, Golemis EA (2003) A novel RING finger protein, human enhancer of Invasion 10, alters mitotic progression through regulation of cyclin B levels. Mol Cell Biol 23:2109–2122. https://doi.org/10.1128/MCB.23.6.2109-2122.2003
Wang K, Wang M, Tang D et al (2012) The role of rice HEI10 in the formation of meiotic crossovers. PLoS Genet. https://doi.org/10.1371/journal.pgen.1002809
Wang C, Higgins JD, He Y et al (2017) Resolvase OsGEN1 mediates DNA repair by homologous recombination. Plant Physiol 173:1316–1329. https://doi.org/10.1104/pp.16.01726
Ward JO, Reinholdt LG, Motley WW et al (2007) Mutation in mouse Hei10, an E3 ubiquitin ligase, disrupts meiotic crossing over. PLoS Genet 3:e139. https://doi.org/10.1371/journal.pgen.0030139
Xiao S, Shao M, Wang D et al (2016) Identification and evolution of FYVE Domain-containing proteins and their expression patterns in response to Abiotic stresses in Rice. Plant Mol Biol Report 34:1064–1082. https://doi.org/10.1007/s11105-016-0988-9
Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genom 38:379–390. https://doi.org/10.1016/j.jgg.2011.08.001
Zhang J, Wang C, Higgins JD et al (2019) A multiprotein complex regulates interference-sensitive crossover formation in rice. Plant Physiol 181:221–235. https://doi.org/10.1104/pp.19.00082
Zhou S, Wang Y, Li W et al (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23:111–129. https://doi.org/10.1105/tpc.109.073692