Abstract
Key message
CHR721 functions as a chromatin remodeler and interacts with a known single-stranded binding protein, OsRPA1a, to regulate both male and female reproductive development in rice.
Abstract
Reproductive development and fertility are important for seed production in rice. Here, we identified a sterile rice mutant, chr721, that exhibited defects in both male and female reproductive development. Approximately 5% of the observed defects in chr721, such as asynchronous dyad division, occurred during anaphase II of meiosis. During the mitotic stage, approximately 80% of uninucleate microspores failed to develop into tricellular pollen, leading to abnormal development. In addition, defects in megaspore development were detected after functional megaspore formation. CHR721, which encodes a nuclear protein belonging to the SNF2 subfamily SMARCAL1, was identified by map-based cloning. CHR721 was expressed in various tissues, especially in spikelets. CHR721 was found to interact with replication protein A (OsRPA1a), which is involved in DNA repair. The expressions of genes involved in DNA repair and cell-cycle checkpoints were consistently upregulated in chr721. Although numerous genes involved in male and female development have been identified, the mode of participation of chromatin-remodeling factors in reproductive development is still not well understood. Our results suggest that CHR721, a novel gene cloned from rice, plays a vital role in both male and female reproductive development.
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References
Boerkoel CF, Takashima H, John J, Yan J, Stankiewicz P, Rosenbarker L, Andre JL, Bogdanovic R, Burguet A, Cockfield S et al (2002) Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia. Nat Genet 30:215–220. https://doi.org/10.1038/ng821
Chang Y, Gong L, Yuan W, Li X, Chen G, Li X, Zhang Q, Wu C (2009) Replication protein A (RPA1a) is required for meiotic and somatic DNA repair but is dispensable for DNA replication and homologous recombination in rice. Plant Physiol 151(4):2162–2173. https://doi.org/10.1104/pp.109.142877
Chen SB, Tao LZ, Zeng LR, Vega-Sanchez ME, Umemura K, Wang GL (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol Plant Pathol 7(5):417–427. https://doi.org/10.1111/j.1364-3703.2006.00346.x
Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R, Tang X, Zhou JM (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146(2):368–376. https://doi.org/10.1104/pp.107.111740
Ciccia A, Bredemeyer AL, Sowa ME, Terret ME, Jallepalli PV, Harper JW, Elledge SJ (2009) The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes Dev 23(20):2415–2425. https://doi.org/10.1101/gad.1832309
Coleman MA, Eisen JA, Mohrenweiser HW (2000) Cloning and characterization of HARP/SMARCAL1: A prokaryotic HepA-related SNF2 helicase protein from human and mouse. Genomics 65:274–282. https://doi.org/10.1006/geno.2000.6174
Farrona S, Hurtado L, Bowman JL, Reyes JC (2004) The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering. Development 131:4965–4975. https://doi.org/10.1242/dev.01363
Flaus A, Martin DMA, Barton GJ, Owen-Hughes T (2006) Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res 34:2887–2905. https://doi.org/10.1093/nar/gkl295
Han JJ, Song ZT, Sun JL, Yang ZT, Xian MJ, Wang S, Sun L, Liu JX (2018) Chromatin remodeling factor CHR18 interacts with replication protein RPA1A to regulate the DNA replication stress response in Arabidopsis. New Phytol 220(2):476–487. https://doi.org/10.1111/nph.15311
Huanca-Mamani W, Garcia-Aguilar M, Leon-Martinez G, Grossniklaus U, Vielle-Calzada JP (2005) CHR11, a chromatin-remodeling factor essential for nuclear proliferation during female gametogenesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 102:17231–17236. https://doi.org/10.1073/pnas.0508186102
Iftode C, Daniely Y, Borowiec JA (1999) Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 34(3):141–180. https://doi.org/10.1080/10409239991209255
Ishibashi T, Kimura S, Sakaguchi K (2006) A higher plant has three different types of RPA heterotrimeric complex. J Biochem 139(1):99–104. https://doi.org/10.1093/jb/mvj014
Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46(1):23–47. https://doi.org/10.1093/pcp/pci501
Kleckner N (1996) Meiosis: how could it work? Proc Natl Acad Sci USA 93(16):8167–8174. https://doi.org/10.1073/pnas.93.16.8167
Lenormand T, Engelstädter J, Johnston SE, Wijnker E, Haag CR (2016) Evolutionary mysteries in meiosis. Philos Trans R Soc Lond B. https://doi.org/10.1098/rstb.2016.0001
Luo Q, Li Y, Shen Y, Cheng Z (2014) Ten years of gene discovery for meiotic event control in rice. J Genet Genomics 41(3):125–137. https://doi.org/10.1016/j.jgg.2014.02.002
Maréchal A, Zou L (2015) RPA-coated single-stranded DNA as a platform for post-translational modifications in the DNA damage response. Cell Res 25(1):9–23. https://doi.org/10.1038/cr.2014.147
McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275. https://doi.org/10.1105/tpc.5.10.1265
McCormick S (2004) Control of male gametophyte development. Plant Cell 16:S142–S153. https://doi.org/10.1105/tpc.016659
Muthuswami R, Truman PA, Mesner LD, Hockensmith JW (2000) A eukaryotic SWI2/SNF2 domain, an exquisite detector of double-stranded to single-stranded DNA transition elements. J Bio Chem 275:7648–7655. https://doi.org/10.1074/jbc.275.11.7648
Shultz RW, Tatineni VM, Hanley-Bowdoin L, Thompson WF (2007) Genome-wide analysis of the core DNA replication machinery in the higher plants Arabidopsis and rice. Plant Physiol 144(4):1697–1714. https://doi.org/10.1104/pp.107.101105
Tanaka I (1997) Differentiation of generative and vegetative cells in angiosperm pollen. Sex Plant Reprod 10:1–7
Wold MS (1997) (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66:61–92. https://doi.org/10.1146/annurev.biochem.66.1.61
Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell 16(Suppl):S133–141
Yusufzai T, Kadonaga JT (2008) HARP is an ATP-driven annealing helicase. Science 322:748–750. https://doi.org/10.1126/science.1161233
Yusufzai T, Kong X, Yokomori K, Kadonaga JT (2009) The annealing helicase HARP is recruited to DNA repair sites via an interaction with RPA. Genes Dev 23(20):2400–2404. https://doi.org/10.1101/gad.1831509
Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54:2342–2353. https://doi.org/10.1016/bs.ctdb.2018.11.00
Acknowledgements
This work was supported by grants from the National Natural Science Foundation of China (31991204) and Chinese Academy of Sciences (XDA24010101).
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Material preparation, data collection and analysis were performed mainly by YZ. QC and GZ participated in a part of experiments. The first draft of the manuscript was written by YZ. FC, XF and FZ commented on previous versions of the manuscript. All authors read and approved the final manuscript. Conceptualization: YZ, FC, XF; Methodology: YZ, FC, QC, JJ, GZ; Formal analysis and investigation: YZ; Writing—original draft preparation: YZ; Writing—review and editing: YZ, FC, HR; Funding acquisition: FC; Material resources: DZ, FY; Supervision: FC.
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Zhang, Y., Chen, Q., Zhu, G. et al. CHR721, interacting with OsRPA1a, is essential for both male and female reproductive development in rice. Plant Mol Biol 103, 473–487 (2020). https://doi.org/10.1007/s11103-020-01004-z
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DOI: https://doi.org/10.1007/s11103-020-01004-z