SCR-22 of pollen-dominant S haplotype class is recessive to SCR-44 of pollen-recessive S haplotype class in Brassica rapa

Chun-Lei Wang , Zhi-Ping Zhang , Eriko Oikawa , Hiroyasu Kitashiba , Takeshi Nishio

Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) : 25

PDF (1230KB)
Horticulture Research ›› 2019, Vol. 6 ›› Issue (1) :25 DOI: 10.1038/s41438-018-0103-5
Article
research-article
SCR-22 of pollen-dominant S haplotype class is recessive to SCR-44 of pollen-recessive S haplotype class in Brassica rapa
Author information +
History +
PDF (1230KB)

Abstract

SCR/SP11 encodes the male determinant of recognition specificity of self-incompatibility (SI) in Brassica species and is sporophytically expressed in the anther tapetum. Based on dominance relationships in pollen and nucleotide sequence similarity, the S haplotypes in Brassica have been classified as class I or class II, with class-I S haplotypes being dominant over class-II S haplotypes. Here, we revealed that S-22 in B. rapa belonging to class I is recessive to class-II S-44 and class-I S-36 in pollen, whereas it is dominant over S-60, S-40, and S-29 based on pollination tests. SCR/SP11 of S-22 (SCR-22) was sequenced, revealing that the deduced amino-acid sequence of SCR-22 has the longest C-terminal domain among the SCR/SP11 sequences. The expression of SCR-22 was found to be suppressed in S-22/S-44 and S-22/S-36 heterozygotes. Normal transcription of SCR-44 was considered to be due to the transcription suppression of Smi sRNA of the S-22 haplotype and a very low methylation state of the SCR-44 promoter region in the tapetum of S-22/S-44 heterozygotes. In SCR-22, only the cytosine residue located at the –37 bp position of the promoter region was hypermethylated in the tapetum of S-22/S-44 heterozygotes, and few methylated cytosines were detected in the promoter and coding regions of SCR-22 in S-22/S-36 heterozygotes. SCR-22 was also expressed in microspores in S-22 homozygotes but not in S-22/S-44 and S-22/S-36 heterozygotes. These results suggest that a mechanism different from class-II SCR/SP11 suppression may operate for the suppression of recessive class-I SCR-22 in S heterozygotes.

Cite this article

Download citation ▾
Chun-Lei Wang, Zhi-Ping Zhang, Eriko Oikawa, Hiroyasu Kitashiba, Takeshi Nishio. SCR-22 of pollen-dominant S haplotype class is recessive to SCR-44 of pollen-recessive S haplotype class in Brassica rapa. Horticulture Research, 2019, 6 (1) : 25 DOI:10.1038/s41438-018-0103-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Stein, J. C., Howlett, B., Boyes, D. C., Nasrallah, M. E. & Nasrallah, J. B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl Acad. Sci. USA 88, 8816-8820 (1991).

[2]

Takasaki, T. et al. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913-916 (2000).

[3]

Schopfer, C. R., Nasrallah, M. E. & Nasrallah, J. B. The male determinant of self-incompatibility in Brassica. Science 286, 1697-1700 (1999).

[4]

Suzuki, G. et al. Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S-9 haplotype of Brassica campestris (syn. rapa). Genetics 153, 391-400 (1999).

[5]

Nasrallah, J. B., Yu, S. M. & Nasrallah, M. E. Self-incompatibility genes of Brassica oleracea: expression, isolation, and structure. Proc. Natl Acad. Sci. USA 85, 5551-5555 (1988).

[6]

Watanabe, M. et al. Highly divergent sequences of the pollen self-incompatibility (S) gene in class-I S haplotypes of Brassica campestris (syn. rapa) L.. FEBS Lett. 473, 139-144 (2000).

[7]

Schopfer, C. R. & Nasrallah, J. B. Self-incompatibility: prospects for a novel putative peptide-signaling molecule. Plant Physiol. 124, 935-939 (2000).

[8]

Sato, K. et al. Coevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B-rapa. Genetics 162, 931-940 (2002).

[9]

Okamoto, S., Sato, Y., Sakamoto, K. & Nishio, T. Distribution of similar self-incompatibility (S) haplotypes in different genera, Raphanus and Brassica. Sex. Plant. Reprod. 17, 33-39 (2004).

[10]

Takayama, S. et al. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl Acad. Sci. USA 97, 1920-1925 (2000).

[11]

Iwano, M. et al. Immunohistochemical studies on translocation of pollen S-haplotype determinant in self-incompatibility of Brassica rapa. Plant Cell Physiol. 44, 428-436 (2003).

[12]

Shiba, H. et al. A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125, 2095-2103 (2001).

[13]

Nasrallah, J. B., Nishio, T. & Nasrallah, M. E. The self-incompatibility genes of Brassica: expression and use in genetic ablation of floral tissues. Annu. Rev. Plant. Physiol. Plant. Mol. Biol. 42, 393-422 (1991).

[14]

Kakizaki, T. et al. Linear dominance relationship among four class-II S haplotypes in pollen is determined by the expression of SP11 in Brassica self-incompatibility. Plant Cell Physiol. 44, 70-75 (2003).

[15]

Shiba, H. et al. The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14, 491-504 (2002).

[16]

Kusaba, M., Tung, C. W., Nasrallah, M. E. & Nasrallah, J. B. Monoallelic expression and dominance interactions in anthers of self-incompatible Arabidopsis lyrata. Plant Physiol. 128, 17-20 (2002).

[17]

Fujimoto, R., Sugimura, T., Fukai, E. & Nishio, T. Suppression of gene expression of a recessive SP11/SCR allele by an untranscribed SP11/SCR allele in Brassica self-incompatibility. Plant Mol. Biol. 61, 577-587 (2006).

[18]

Shiba, H. et al. Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat. Genet. 38, 297-299 (2006).

[19]

Tarutani, Y. et al. Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466, 983-U110 (2010).

[20]

Yasuda, S. et al. A complex dominance hierarchy is controlled by polymorphism of small RNAs and their targets. Nat. Plants 3, 16206 (2016).

[21]

Hatakeyama, K. et al. The S receptor kinase gene determines dominance relationships in stigma expression of self-incompatibility in Brassica. Plant J. 26, 69-76 (2001).

[22]

Saze, H., Tsugane, K., Kanno, T. & Nishimura, T. DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol. 53, 766-784 (2012).

[23]

Zhang, B. H., Wang, Q. L. & Pan, X. P. MicroRNAs and their regulatory roles in animals and plants. J. Cell Physiol. 210, 279-289 (2007).

[24]

Usadel, B. et al. Multilevel genomic analysis of the response of transcripts, enzyme activities and metabolites in Arabidopsis rosettes to a progressive decrease of temperature in the non-freezing range. Plant Cell Environ. 31, 518-547 (2008).

[25]

Halford, N. G. in Plant Developmental Biology - Biotechnological Perspectives (eds Pua, E.C & Davey, M. R.) Ch. 4, 67-82 (Springer, Berlin Heidelberg, 2010).

[26]

Kakizaki, T. et al. Comparative analysis of the S-intergenic region in class-II S haplotypes of self-incompatible Brassica rapa (syn. campestris). Genes Genet. Syst. 81, 63-67 (2006).

[27]

Zhu, W. G. et al. Methylation of adjacent CpG sites affects Sp1/Sp3 binding and activity in the p21(Cip1) promoter. Mol. Cell Biol. 23, 4056-4065 (2003).

[28]

Boyes, J. & Bird, A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 64, 1123-1134 (1991).

[29]

Puranik, S., Sahu, P. P., Srivastava, P. S. & Prasad, M. NAC proteins: regulation and role in stress tolerance. Trends Plant. Sci. 17, 369-381 (2012).

[30]

Nou, S., Watanabe, M., Isogai, A. & Hinata, K. Comparison of S-alleles and S-glycoproteins between two wild populations of Brassica campestris in Turkey and Japan. Sex. Plant Reprod. 6, 79-86 (1993).

[31]

Kimura, R., Sato, K., Fujimoto, R. & Nishio, T. Recognition specificity of self-incompatibility maintained after the divergence of Brassica oleracea and Brassica rapa. Plant J. 29, 215-223 (2002).

[32]

Pavlopoulos, A. in Molecular Methods for Evolutionary Genetics (eds Orgogozo, V. & Rockman, M. V.) 267-275 (Humana Press, New York, USA 2011).

[33]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25, 402-408 (2001).

[34]

Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E. F. & Hellens, R. P. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3, 12 (2007).

PDF (1230KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/