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A mutation near the active site of S-RNase causes self-compatibility in S-RNase-based self-incompatible plants

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The structurally simplest amino acid glycine could make contribution to nuclease activity of S-RNase and self-incompatibility in S-RNase-based plants.

Abstract

S-RNase is regarded as inhibitor of self-pollen tube in S-RNase-based self-incompatibility plants. Certain residues like histidine are necessary for RNase activity and self-incompatibility; however, it is unknown whether any other residues contribute to this. Previously, we identified an association between the self-compatible Chinese pear (Pyrus × bretschneideri) cultivar ‘Yanzhuang’ (YZ) and a mutation causing a residue shift (glycine-to-valine) in the 2nd conserved region (C2) of S21-RNase; however, it was unclear how this nonpolar aliphatic amino acid substitution caused self-compatibility. In this study, we observed that ‘YZ’ offspring were self-compatible when S21-RNases were all mutated. In vitro pollen tube (S21S21) growth was not completely arrested by the mutated S21-RNase. Residue frequency analysis showed that the glycine residue is highly conserved in diverse S-RNases across many plant species. We therefore generated a mutated petunia SV′-RNase (glycine to valine) and transformed it into S3LS3L petunia. The transformed pistil could not inhibit SV pollen tubes. Three-dimensional protein prediction suggested that the glycine-to-valine mutation alters the spatial structure near the active site, and RNase activity of mutated S-RNase was reducing. Thus, the glycine residue in the C2 is essential for RNase activity, substitution of this residue leads to a failure of self-incompatibility.

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References

  • Ai Y, Singh A, Coleman CE, Ioerger TR, Kheyr-Pour A, Kao T-H (1990) Self-incompatibility in Petunia inflata: isolation and characterization of cDNAs encoding three S-allele-associated proteins. Sex Plant Reprod 3:130–138

    Article  Google Scholar 

  • Ai Y, Tsai DS, Kao TH (1992) Cloning and sequencing of cDNAs encoding two S proteins of a self-compatible cultivar of Petunia hybrida. Plant Mol Biol 19:523–528

    Article  CAS  Google Scholar 

  • Anderson MA, Cornish EC, Mau SL, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of Cdna for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana-Alata. Nature 321:38–44

    Article  CAS  Google Scholar 

  • Certal AC, Sanchez AM, Kokko H, Broothaerts W, Oliveira MM, Feijó JA (1999) S-RNases in apple are expressed in the pistil along the pollen tube growth path. Sex Plant Reprod 12:94–98

    Article  CAS  Google Scholar 

  • De Nettancourt D, De Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants, 2nd edn. Springer, Berlin

    Book  Google Scholar 

  • Harbord RM, Napoli CA, Robbins TP (2000) Segregation distortion of T-DNA markers linked to the self-incompatibility (S) locus in Petunia hybrida. Genetics 154:1323–1333

    CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh N, Goto K, Asano J, Fukushima K, Yamada K, Kasai A, Li TZ, Takanoha M, Miyairi K, Okuno T (2002) S-RNases from self-incompatible and -compatible apple cultivars: purification, cloning, enzymic properties, and pollen tube growth inhibitory activity. Biosci Biotechnol Biochem 66:1185–1195

    Article  CAS  Google Scholar 

  • Kretsinger RH (1980) Structure and evolution of calcium-modulated proteins. CRC Crit Rev Biochem 8:119–174

    Article  CAS  Google Scholar 

  • Lai Z, Ma WS, Han B, Liang LZ, Zhang YS, Hong GF, Xue YB (2002) An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42

    Article  CAS  Google Scholar 

  • Lee HS, Huang S, Kao T (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563

    Article  CAS  Google Scholar 

  • Li TZ, Katoh N, Fujita T, Asada T, Shiozaki Y, Okuno T (2008) Observations on stylar transmitting tissue cells and cDNA cloning of S-RNase in a self-fruitful Apple 'Hirodai Ichigo'. Engei Gakkai Zasshi 71:553–560

    Article  Google Scholar 

  • Li MF, Li XF, Zh Han H, Shu HR, Li T (2009) Molecular analysis of two Chinese pear (Pyrus bretschneideri Rehd.) spontaneous self-compatible mutants, Yan Zhuang and Jin Zhui. Plant Biol 11:774–783

    Article  CAS  Google Scholar 

  • Li W, Yang Q, Gu Z, Wu C, Meng D, Yu J, Chen Q, Li Y, Yuan H, Wang D, Li T (2016) Molecular and genetic characterization of a self-compatible apple cultivar, 'CAU-1'. Plant Sci 252:162–175

    Article  CAS  Google Scholar 

  • Matsuura T, Sakai H, Unno M, Ida K, Sato M, Sakiyama F, Norioka S (2001) Crystal Structure at 1.5-Å Resolution of Pyrus pyrifolia Pistil Ribonuclease Responsible for Gametophytic Self-incompatibility. J Biol Chem 276, 45261.

  • McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotlana alata are ribonucleases. Nature 342:955–957

    Article  CAS  Google Scholar 

  • McCubbin AG, Chung Y-Y, Kao T-H (1997) A mutant S3 RNase of Petunia inflata lacking RNase activity has an allele-specific dominant negative effect on self-incompatibility interactions. Plant Cell 9:85–95

    Article  CAS  Google Scholar 

  • Meng X, Sun P, Kao TH (2011) S-RNase-based self-incompatibility in Petunia inflata. Ann Bot 108:637–646

    Article  CAS  Google Scholar 

  • Meng D, Gu Z, Li W, Wang A, Yuan H, Yang Q, Li T (2014) Apple MdABCF assists in the transportation of S-RNase into pollen tubes. Plant J 78:990–1002

    Article  CAS  Google Scholar 

  • Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367:563–566

    Article  CAS  Google Scholar 

  • Nelson DL, Cox MM, Lehninger AL (2017) Lehninger principles of biochemistry, 7th edn. Macmillan, New York

    Google Scholar 

  • Nerum IV, Incerti F, Keulemans J, Broothaerts W, Geibel M, Fischer M, Fischer C (2000) Analysis of self-fertility in transgenic apple lines transformed with an S-allele either in sense or antisense direction. Acta Hort 538:625–629

    Article  Google Scholar 

  • Sassa H (2016) Molecular mechanism of the S-RNase-based gametophytic self-incompatibility in fruit trees of Rosaceae. Breed Sci 66:116–121

    Article  CAS  Google Scholar 

  • Sassa H, Hirano H, Ikehashi H (1993) Identification and characterization of stylar glycoproteins associated with self-incompatibility genes of Japanese pear, Pyrus serotina Rehd. Mol Gen Genet 241:17–25

    Article  CAS  Google Scholar 

  • Sassa H, Mase N, Hirano H, Ikehashi H (1994) Identification of self-incompatibility-related glycoproteins in styles of apple (Malus x domestica). Theor Appl Genet 89:201–205

    Article  CAS  Google Scholar 

  • Sassa H, Hirano H, Nishio T, Koba T (1997) Style-specific self-compatible mutation caused by deletion of the S-RNase gene in Japanese pear (Pyrus serotina). Plant J 12:223–227

    Article  CAS  Google Scholar 

  • Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489

    Article  CAS  Google Scholar 

  • Tao R, Iezzoni AF (2010) The S-RNase-based gametophytic self-incompatibility system in Prunus exhibits distinct genetic and molecular features. Sci Hortic-Amsterdam 124:423–433

    Article  CAS  Google Scholar 

  • Tao R, Yamane H, Sugiura A, Murayama H, Sassa H, Mori H (1999) Molecular typing of S-alleles through identification, characterization and cDNA cloning for S-RNases in sweet cherry. J Am Soc Hortic Sci 124:224–233

    Article  CAS  Google Scholar 

  • Tao R, Watari A, Hanada T, Habu T, Yaegaki H, Yamaguchi M, Yamane H (2007) Self-compatible peach (Prunus persica) has mutant versions of the S haplotypes found in self-incompatible Prunus species. Plant Mol Biol 63:109–123

    Article  CAS  Google Scholar 

  • Wu J, Li M, Li T (2013) Genetic features of the spontaneous self-compatible mutant, ‘Jin Zhui’ (Pyrus bretschneideri Rehd). PLoS ONE 8:76509

    Article  Google Scholar 

  • Xue Y, Carpenter R, Dickinson HG, Coen ES (1996) Origin of allelic diversity in antirrhinum S locus RNases. Plant Cell 8:805–814

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan H, Meng D, Gu ZY, Li W, Wang AD, Yang Q, Zhu YD, Li TZ (2014) A novel gene, MdSSK1, as a component of the SCF complex rather than MdSBP1 can mediate the ubiquitination of S-RNase in apple. J Exp Bot 65:3121–3131

    Article  CAS  Google Scholar 

  • Zhang Q, Ma C, Zhang Y, Gu Z, Li W, Duan X, Wang S, Hao L, Wang Y, Wang S, Li T (2018) A single-nucleotide polymorphism in the promoter of a hairpin RNA contributes to Alternaria alternata leaf spot resistance in apple (Malus x domestica). Plant Cell 30:1924–1942

    Article  CAS  Google Scholar 

  • ZhiMing Y, Bo K, XiaoWei H, ShaoLei L, YouHuang B, WoNa D, Ming C, Hyung-Taeg C, Ping W (2011) Root hair-specific expansions modulate root hair elongation in rice. Plant J 66:725–734

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key Research and Development Program of China (2018YFD1000107), the National Natural Science Foundation of China (31630066), the Construction of Beijing Science and Technology Innovation and Service Capacity in Top Subjects (CEFF-PXM2019_014207_000032).

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Contributions

YL and TL conceived the research plans; YL performed most of the experiments; JW, WL, CW, JY, and CL performed the remaining experiments; YL and TL analyzed the data; and YL and TL, WL wrote the article.

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Correspondence to Tianzhong Li or Wei Li.

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Accession numbers

Sequence data from this article can be found in the GenBank/National Center for Biotechnology Information (NCBI) data libraries under the following accession numbers: KC529670.1 (Pyrus × bretschneideri S19-RNase19); AY250989.3 (Pyrus × bretschneideri S21-RNase); DQ494676.1 (Pyrus × bretschneideri S34-RNase); AJ271065.1 (Petunia S3L-RNase); AJ271062.1 (Petunia SV-RNase).

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Li, Y., Wu, J., Wu, C. et al. A mutation near the active site of S-RNase causes self-compatibility in S-RNase-based self-incompatible plants. Plant Mol Biol 103, 129–139 (2020). https://doi.org/10.1007/s11103-020-00979-z

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