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S locus-linked F-box genes expressed in anthers of Hordeum bulbosum

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Abstract

Diploid Hordeum bulbosum (a wild relative of cultivated barley) exhibits a two-locus self-incompatibility (SI) system gametophytically controlled by the unlinked multiallelic loci S and Z. This unique SI system is observed in the grasses (Poaceae) including the tribe Triticeae. This paper describes the identification and characterization of two F-box genes cosegregating with the S locus in H. bulbosum, named Hordeum S locus-linked F-box 1 (HSLF1) and HSLF2, which were derived from an S 3 haplotype-specific clone (HAS175) obtained by previous AMF (AFLP-based mRNA fingerprinting) analysis. Sequence analysis showed that both genes encode similar F-box proteins with a C-terminal leucine-rich repeat (LRR) domain, which are distinct from S locus (or S haplotype-specific) F-box protein (SLF/SFB), a class of F-box proteins identified as the pollen S determinant in S-RNase-based gametophytic SI systems. A number of homologous F-box genes with an LRR domain were found in the rice genome, although the functions of the gene family are unknown. One allele of the HSLF1 gene (HSLF1-S 3) was expressed specifically in mature anthers, whereas no expression was detected from the other two alleles examined. Although the degree of sequence polymorphism among the three HSLF1 alleles was low, a frameshift mutation was found in one of the unexpressed alleles. The HSLF2 gene showed a low level of expression with no tissue specificity as well as little sequence polymorphism among the three alleles. The multiplicity of S locus-linked F-box genes is discussed in comparison with those found in the S-RNase-based SI system.

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References

  • Baumann U, Juttner J, Bian XY, Langridge P (2000) Self-incompatibility in the grasses. Ann Bot 85(Suppl A):203–209

    Article  CAS  Google Scholar 

  • Bian XY, Friedrich A, Bai J-R, Baumann U, Hayman DL, Barker SJ, Langridge P (2004) High-resolution mapping of the S and Z loci of Phalaris coerulescens. Genome 47:918–930

    Article  PubMed  CAS  Google Scholar 

  • Cheng JH, Han ZH, Xu XF, Li TZ (2006) Isolation and identification of the pollen-expressed polymorphic F-box genes linked to the S-locus in apple (Malus × domestica). Sex Plant Reprod 19:175–183

    Article  CAS  Google Scholar 

  • de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin, Heidelberg, New York

    Google Scholar 

  • Entani T, Iwano M, Shiba H, Che FS, Isogai A, Takayama S (2003) Comparative analysis of the self-incompatibility (S) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213

    Article  PubMed  CAS  Google Scholar 

  • Gudu S, Laurie A, Kasha J, Xia J, Snape W (2002) RFLP mapping of a Hordeum bulbosum gene highly expressed in pistils and its relationship to homoeologous loci in other Gramineae species. Theor Appl Genet 105:271–276

    Article  PubMed  CAS  Google Scholar 

  • Hackauf B, Wehling P (2005) Approaching the self-incompatibility locus Z in rye (Secale cereale L.) via comparative genetics. Theor Appl Genet 110:832–845

    Article  PubMed  CAS  Google Scholar 

  • Hayman DL (1956) The genetic control of incompatibility in Phalaris coerulescens DESF. Aust J Biol Sci 9:321–331

    Google Scholar 

  • Kakeda K, Ibuki T, Kowyama Y (2000) Molecular genetic analysis of self-incompatibility in Hordeum bulbosum. Barley Genet 8(3):157–159

    Google Scholar 

  • Kakeda K, Hanai Y, Sato K (2004) Differential expression proteomics in barley and its wild relatives. Proceedings of the 9th international barley genetics symposium, pp 354–359

  • Kakeda K, Ibuki T, Suzuki J, Tadano H, Kurita Y, Hanai Y, Kowyama Y (2008) Molecular and genetic characterization of the S locus in Hordeum bulbosum L., a wild self-incompatible species related to cultivated barley. Mol Genet Genomics 280:509–519

    Article  PubMed  CAS  Google Scholar 

  • Lai Z, Ma WS, Han B, Liang LG, 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 50:289–296

    Article  Google Scholar 

  • Langridge P, Baumann U (2008) Self-Incompatibility in the grasses. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants—evolution, diversity, and mechanisms. Springer, Berlin, pp 275–287

    Chapter  Google Scholar 

  • Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638

    Article  PubMed  CAS  Google Scholar 

  • Li X, Nield J, Hayman D, Langridge P (1994) Cloning a putative self-incompatibility gene from the pollen of the grass Phalaris coerulescens. Plant Cell 6:1923–1932

    Article  PubMed  CAS  Google Scholar 

  • Li X, Paech N, Nield J, Hayman D, Langridge P (1997) Self-incompatibility in the grasses: evolutionary relationship of the S gene from Phalaris coerulescens to homologous sequences in other grasses. Plant Mol Biol 34:223–232

    Article  PubMed  CAS  Google Scholar 

  • Lundqvist A (1954) Studies on self-sterility in rye, Secale cereale L. Hereditas 40:278–294

    Article  Google Scholar 

  • Matsumoto D, Yamane H, Tao R (2008) Characterization of SLFL1, a pollen-expressed F-box gene located in the Prunus S locus. Sex Plant Reprod 21:113–121

    Article  CAS  Google Scholar 

  • McClure B (2008) Comparing models for S-RNase-based self-incompatibility. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants—evolution, diversity, and mechanisms. Springer, Berlin, pp 217–236

    Chapter  Google Scholar 

  • Qiao H, Wang F, Zhao L, Zhou JL, Lai Z, Zhang YS, Robbins TP, Xue YB (2004) The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self incompatibility. Plant Cell 16:2307–2322

    Article  PubMed  CAS  Google Scholar 

  • Rahman MH, Uchiyama M, Kuno M, Hirashima N, Suwabe K, Tsuchiya T, Kagaya Y, Kobayashi I, Kakeda K, Kowyama Y (2007) Expression of stigma- and anther-specific genes located in the S locus region of Ipomoea trifida. Sex Plant Reprod 20:73–85

    Article  Google Scholar 

  • Sassa H, Kakui H, Miyamoto M, Suzuki Y, Hanada T, Ushijima K, Kusaba M, Hirano H, Koba T (2007) S locus F-box brothers: multiple and pollen-specific F-box genes with S haplotype-specific polymorphisms in apple and Japanese pear. Genetics 175:1869–1881

    Article  PubMed  CAS  Google Scholar 

  • Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305

    Article  PubMed  CAS  Google Scholar 

  • Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15:771–781

    Article  PubMed  CAS  Google Scholar 

  • Van Daele I, Van Bockstaele E, Martens C, Roldán-Ruiz I (2008) Identification of transcribed derived fragments involved in self-incompatibility in perennial ryegrass (Lolium perenne L.) using cDNA-AFLP. Euphytica 163:67–80

    Article  CAS  Google Scholar 

  • Voylokov AV, Korzun V, Borner A (1997) Mapping of three self-fertility mutations in rye (Secale cereale L.) using RFLP, isozyme and morphological markers. Theor Appl Genet 97:147–153

    Article  Google Scholar 

  • Wehling P, Hackauf B, Wricke B (1994) Identification of S-locus linked PCR fragments in rye (Secale cereale L.) by denaturing gradient gel electrophoresis. Plant J 5:891–893

    Article  PubMed  CAS  Google Scholar 

  • Wheeler D, Newbigin E (2007) Expression of 10 S-class SLF-like genes in Nicotiana alata pollen and its implications for understanding the pollen factor of the S locus. Genetics 177:2171–2180

    Article  PubMed  CAS  Google Scholar 

  • Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: Different modes of sequence divergence and their relationships with functional diversification. PNAS 106:835–840

    Article  PubMed  CAS  Google Scholar 

  • Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003) A pollen-expressed gene for a novel protein with an F-box motif that is very tightly linked to a gene for S-RNase in two species of cherry, Prunus cerasus and P. avium. Plant Cell Physiol 44:764–769

    Article  PubMed  CAS  Google Scholar 

  • Yang B, Thorogood D, Armstead I, Barth S (2008) How far are we from unraveling self-incompatibility in grasses? New Phytol 179:740–753

    Article  CAS  Google Scholar 

  • Zhang Y, Xue Y (2008) Molecular biology of S-RNase-based self-incompatibility. In: Franklin-Tong VE (ed) Self-incompatibility in flowering plants—evolution, diversity, and mechanisms. Springer, Berlin, pp 193–215

    Chapter  Google Scholar 

  • Zhou J, Wang F, Ma W, Zhang Y, Han B, Xue Y (2003) Structural and transcriptional analysis of S-locus F-box genes in Antirrhinum. Sex Plant Reprod 16:165–177

    Article  CAS  Google Scholar 

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Acknowledgments

I thank M. Konoura, M. Kawai, K. Ohgishi and Y. Ishihama for technical assistance. This work was supported by Grant-in-Aids for Scientific Research C (Nos. 15580006 and 21580006) from the Ministry of Education, Culture, Sports, Science and Technology, Japan (MEXT).

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Correspondence to Katsuyuki Kakeda.

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Communicated by R. Schmidt.

Nucleotide sequence data reported are available in the DDBJ/EMBL/GenBank databases under the accession numbers AB511822–AB511825 and AB511859–AB511862.

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Kakeda, K. S locus-linked F-box genes expressed in anthers of Hordeum bulbosum. Plant Cell Rep 28, 1453–1460 (2009). https://doi.org/10.1007/s00299-009-0745-8

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