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
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
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
de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin, Heidelberg, New York
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
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
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
Hayman DL (1956) The genetic control of incompatibility in Phalaris coerulescens DESF. Aust J Biol Sci 9:321–331
Kakeda K, Ibuki T, Kowyama Y (2000) Molecular genetic analysis of self-incompatibility in Hordeum bulbosum. Barley Genet 8(3):157–159
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
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
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
Lechner E, Achard P, Vansiri A, Potuschak T, Genschik P (2006) F-box proteins everywhere. Curr Opin Plant Biol 9:631–638
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
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
Lundqvist A (1954) Studies on self-sterility in rye, Secale cereale L. Hereditas 40:278–294
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
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
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
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
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
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
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
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
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
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
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
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
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
Yang B, Thorogood D, Armstead I, Barth S (2008) How far are we from unraveling self-incompatibility in grasses? New Phytol 179:740–753
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
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
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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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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DOI: https://doi.org/10.1007/s00299-009-0745-8