Abstract
Background
MSH1 (MutS homolog1) is a nuclear-encoded protein that plays a crucial role in maintaining low mutation rates and stability of the organellar genome. While plastid MSH1 maintains nuclear epigenome plasticity and affects plant development patterns, mitochondrial MSH1 suppresses illegitimate recombination within the mitochondrial genome, affects mitochondrial genome substoichiometric shifting activity and induces cytoplasmic male sterility (CMS) in crops. However, a detailed functional investigation of onion MSH1 has yet to be achieved.
Materials and results
The homology analysis of onion genome database identified a single copy of the AcMSH1 gene in the onion cv. Bhima Super. In silico analysis of AcMSH1 protein sequence revealed the presence of 6 conserved functional domains including a unique MSH1-specific GIY-YIG endonuclease domain at the C-terminal end. At N-terminal end, it has signal peptide sequences targeting chloroplast and mitochondria. The concentration of AcMSH1 was found to be highest in isolated mitochondria, followed by chloroplasts, and negligible in the cytoplasmic fraction; which proved its localization to the mitochondria and chloroplasts. Quantitative expression analysis revealed that AcMSH1 protein levels were highest in leaves, followed by flower buds, root tips, flowers, and umbels, with the lowest amount found in callus tissue.
Conclusion
Onion genome has single copy of MSH1, with characteristic GIY-YIG endonuclease domain. AcMSH1 targeted towards both chloroplasts and mitochondria. The identification and characterisation of AcMSH1 may provide valuable insights into the development of CMS lines in onion.
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Data Availability
All data are included in the manuscript.
References
Larrea AA, Lujan SA, Nick McElhinny SA et al (2010) Genome-wide model for the normal eukaryotic DNA replication fork. Proc Natl Acad Sci U S A 107:17674–17679. https://doi.org/10.1073/pnas.1010178107
Lencina F, Landau A, Prina AR (2022) The Barley Chloroplast Mutator (cpm) mutant: all roads lead to the Msh1 gene. Int J Mol Sci 23:1814. https://doi.org/10.3390/IJMS23031814
Li GM (2007) Mechanisms and functions of DNA mismatch repair. Cell Res 2008 181 18:85–98. https://doi.org/10.1038/cr.2007.115
Lin Z, Nei M, Ma H (2007) The origins and early evolution of DNA mismatch repair genes - multiple horizontal gene transfers and co-evolution. Nucleic Acids Res 35:7591–7603. https://doi.org/10.1093/nar/gkm921
Fukui K, Harada A, Wakamatsu T et al (2018) The GIY-YIG endonuclease domain of Arabidopsis MutS homolog 1 specifically binds to branched DNA structures. FEBS Lett 592:4066–4077. https://doi.org/10.1002/1873-3468.13279
Wu SY, Culligan K, Lamers M, Hays J (2003) Dissimilar mispair-recognition spectra of Arabidopsis DNA-mismatch-repair proteins MSH2·MSH6 (MutSα) and MSH2·MSH7 (MutSγ). Nucleic Acids Res 31:6027–6034. https://doi.org/10.1093/nar/gkg780
Hoffman PD, Leonard JM, Lindberg GE et al (2004) Rapid accumulation of mutations during seed-to-seed propagation of mismatch-repair-defective Arabidopsis. Genes Dev 18:2676–2685. https://doi.org/10.1101/GAD.1217204
Jiang M, Wu X, Song Y et al (2020) Effects of OsMSH6 mutations on microsatellite Stability and Homeologous recombination in Rice. Front Plant Sci 11:220. https://doi.org/10.3389/FPLS.2020.00220
Abdelnoor RV, Yule R, Elo A et al (2003) Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proc Natl Acad Sci 100:5968–5973. https://doi.org/10.1073/PNAS.1037651100
Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA (2007) Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. Plant Cell 19:1251–1264. https://doi.org/10.1105/tpc.106.048355
Boesch P, Weber-Lotfi F, Ibrahim N et al (2011) DNA repair in organelles: pathways, organization, regulation, relevance in disease and aging. Biochim Biophys Acta - Mol Cell Res 1813(1):186–200. https://doi.org/10.1016/J.BBAMCR.2010.10.002
Odahara M, Kishita Y, Sekine Y (2017) MSH1 maintains organelle genome stability and genetically interacts with RECA and RECG in the moss Physcomitrella patens. Plant J 91:455–465. https://doi.org/10.1111/TPJ.13573
Davila JI, Arrieta-Montiel MP, Wamboldt Y et al (2011) Double-strand break repair processes drive evolution of the mitochondrial genome in Arabidopsis. BMC Biol 9:1–14. https://doi.org/10.1186/1741-7007-9-64
Wu Z, Waneka G, Broz AK et al (2020) MSH1 is required for maintenance of the low mutation rates in plant mitochondrial and plastid genomes. Proc Natl Acad Sci U S A 117:16448–16455. https://doi.org/10.1073/PNAS.2001998117/SUPPL_FILE/PNAS.2001998117.SD01.XLSX
Abdelnoor RV, Christensen AC, Mohammed S et al (2006) Mitochondrial genome dynamics in plants and animals: convergent gene fusions of a MutS homologue. J Mol Evol 63:165–173. https://doi.org/10.1007/s00239-005-0226-9
Ogata H, Ray J, Toyoda K et al (2011) Two new subfamilies of DNA mismatch repair proteins (MutS) specifically abundant in the marine environment. ISME J 5:1143–1151. https://doi.org/10.1038/ismej.2010.210
De La Rosa Santamaria R, Shao MR, Wang G et al (2014) MSH1-Induced non-genetic variation provides a source of phenotypic diversity in Sorghum bicolor. PLoS ONE 9:e108407. https://doi.org/10.1371/JOURNAL.PONE.0108407
Virdi KS, Laurie JD, Xu YZ et al (2015) Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth. Nat Commun 6:6386. https://doi.org/10.1038/NCOMMS7386
Virdi KS, Wamboldt Y, Kundariya H et al (2016) MSH1 is a plant Organellar DNA binding and thylakoid protein under precise spatial regulation to Alter Development. Mol Plant 9:245–260. https://doi.org/10.1016/j.molp.2015.10.011
Xu YZ, de la Rosa Santamaria R, Virdi KS et al (2012) The chloroplast triggers developmental reprogramming when MutS HOMOLOG1 is suppressed in plants. Plant Physiol 159:710–720. https://doi.org/10.1104/pp.112.196055
Xu YZ, Arrieta-Montiel MP, Virdi KS et al (2011) MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and Plastid Properties and Plant Response to High Light. Plant Cell 23:3428. https://doi.org/10.1105/TPC.111.089136
Zhao N, Xu X, Wamboldt Y et al (2016) MutS HOMOLOG1 silencing mediates ORF220 substoichiometric shifting and causes male sterility in Brassica juncea. J Exp Bot 67:435–444. https://doi.org/10.1093/JXB/ERV480
Sandhu APS, Abdelnoor RV, Mackenzie SA (2007) Transgenic induction of mitochondrial rearrangements for cytoplasmic male sterility in crop plants. Proc Natl Acad Sci U S A 104:1766–1770. https://doi.org/10.1073/PNAS.0609344104/ASSET/95679831-06DA-4751-930D-184958556EFF
Zhao N, Li Z, Zhang L et al (2021) MutS HOMOLOG1 mediates fertility reversion from cytoplasmic male sterile Brassica juncea in response to environment. Plant Cell Environ 44:234–246. https://doi.org/10.1111/pce.13895
Duangjit J, Bohanec B, Chan AP et al (2013) Transcriptome sequencing to produce SNP-based genetic maps of onion. Theor Appl Genet 126:2093–2101. https://doi.org/10.1007/s00122-013-2121-x
Finn RD, Coggill P, Eberhardt RY et al (2016) The pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120
Gualberto JM, Mileshina D, Wallet C et al (2014) The plant mitochondrial genome: Dynamics and maintenance. Biochimie 100:107–120. https://doi.org/10.1016/J.BIOCHI.2013.09.016
Terao Y, Imamura J (2013) Effects of suppression of Msh1 on mitochondrial genome in Brassica napus. Acta Hortic 1005:111–116. https://doi.org/10.17660/ACTAHORTIC.2013.1005.9
MacKenzie SA, Kundariya H (2020) Organellar protein multi-functionality and phenotypic plasticity in plants. Philos Trans R Soc B Biol Sci 375:20190182. https://doi.org/10.1098/RSTB.2019.0182
Beltrán J, Wamboldt Y, Sanchez R et al (2018) Specialized Plastids trigger tissue-specific signaling for systemic stress response in plants. Plant Physiol 178:672–683. https://doi.org/10.1104/PP.18.00804
Sun P, Arrieta-Montiel MP, Mackenzie SA (2012) Utility of in vitro culture to the study of plant mitochondrial genome configuration and its dynamic features. Theor Appl Genet 125:449–454. https://doi.org/10.1007/s00122-012-1844-4
Shiomi N, Benkeblia N, Onodera S, Kawazoe N (2006) Fructooligosaccharides changes during maturation in inflorescences and seeds of onion (Allium cepa L. ’W202’). Can J Plant Sci 86:269–278. https://doi.org/10.4141/P05-020
Mariani C, De Beuckeleer M, Truettner J et al (1990) Induction of male sterility in plants by a chimaeric ribonuclease gene. Nat 1990 3476295 347:737–741. https://doi.org/10.1038/347737a0
Lee Y-H, Chung K-H, Kim H-U et al (2003) Induction of male sterile cabbage using a tapetum-specific promoter from Brassica campestris L. ssp. pekinensis. Plant Cell Reports 2003 224 22:268–273. https://doi.org/10.1007/S00299-003-0688-4
Yue Y, Yin C, Guo R et al (2017) An anther-specific gene PhGRP is regulated by PhMYC2 and causes male sterility when overexpressed in petunia anthers. Plant Cell Rep 36:1401–1415. https://doi.org/10.1007/S00299-017-2163-7
Acknowledgements
Authors are thankful to Department of Science and Technology - Science and Engineering Research Board for financial support and fellowship provided to author SKK is gratefully acknowledged. Authors are highly thankful to Dr. Major Singh, ICAR-DOGR, Rajgurunagar for his suggestions during the entire work.
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This research work was supported by a grant from the Department of Science and Technology - Science and Engineering Research Board (DST-SERB) (Grant No. CRG/2019/000830).
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PM and SA conceived and designed the experiments. PM, TKM and SKK conducted all the experiments. PM, TKM and SKK drafted the manuscript. SA and VS carried out the data analysis and manuscript editing. SA supervised the entire work.
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The authors Pawan Mainkar, Tushar Kashinath Manape, and Snehal Krishna Kad have contributed equally to this work.
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Mainkar, P., Manape, T.K., Kad, S.K. et al. Identification, cloning and characterization of AcMSH1 from Onion (Allium cepa L.). Mol Biol Rep 50, 5147–5155 (2023). https://doi.org/10.1007/s11033-023-08414-4
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DOI: https://doi.org/10.1007/s11033-023-08414-4