Commonalities and differences between Brassica and Arabidopsis self-incompatibility

Masaya Yamamoto , Takeshi Nishio

Horticulture Research ›› 2014, Vol. 1 ›› Issue (1) : 14054

PDF (274KB)
Horticulture Research ›› 2014, Vol. 1 ›› Issue (1) :14054 DOI: 10.1038/hortres.2014.54
MINI REVIEW
research-article
Commonalities and differences between Brassica and Arabidopsis self-incompatibility
Author information +
History +
PDF (274KB)

Abstract

In higher plants, the self-incompatibility mechanism is important for inhibition of self-fertilization and facilitation of out-crossing. In Brassicaceae, the self-incompatibility response is mediated by allele-specific interaction of the stigma-localized S-locus receptor kinase (SRK) with the pollen coat-localized ligand (SCR/SP11). All self-incompatible Brassicaceae plants analyzed have been found to have the SRK and SCR/SP11 genes in the S-locus region. Although Arabidopsis thaliana is self-compatible, transformation with functional SRK-SCR genes from self-incompatible Arabidopsis species confers the self-incompatibility phenotype to A. thaliana. The allele-specific interaction between SRK and SCR activates the downstream signaling cascade of self-incompatibility. Yeast two-hybrid analysis with a kinase domain of SRK as bait and genetic analysis suggested several candidate components of self-incompatibility signaling in Brassica. Recently, A. thaliana genes orthologous to the identified genes for Brassica self-incompatibility signaling were evaluated by using a self-incompatible transgenic A. thaliana plant and these orthologous genes were found not to be involved in self-incompatibility signaling in the transgenic A. thaliana. In this review, we describe common and different aspects of S-locus genomic regions and self-incompatibility signaling between Brassica and Arabidopsis.

Cite this article

Download citation ▾
Masaya Yamamoto, Takeshi Nishio. Commonalities and differences between Brassica and Arabidopsis self-incompatibility. Horticulture Research, 2014, 1 (1) : 14054 DOI:10.1038/hortres.2014.54

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB . Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci USA 1991; 88: 8816-8820.

[2]

Schopfer CR, Nasrallah ME, Nasrallah JB . The male determinant of self-incompatibility in Brassica. Science 1999; 286: 1697-1700.

[3]

Suzuki G, Kai N, Hirose T et al. Genomic organization of the S locus: Identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa) . Genetics 1999; 153: 391-400.

[4]

Nasrallah JB, Nasrallah ME . Pollen-stigma signaling in the sporophytic self-incompatibility response. Plant Cell 1993; 5: 1325-1335.

[5]

Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K . The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 2000; 403: 913-916.

[6]

Chen CH, Nasrallah JB . A new class of S sequences defined by a pollen recessive self-incompatibility allele of Brassica oleracea. Mol Gen Genet 1990; 222: 241-248.

[7]

Sato K, Nishio T, Kimura R et al. Coevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa. Genetics 2002; 162: 931-940.

[8]

Iwano M, Shiba H, Funato M, Shimosato H, Takayama S, Isogai A . Immunohistochemical studies on translocation of pollen S-haplotype determinant in self-incompatibility of Brassica rapa. Plant Cell Physiol 2003; 44: 428-436.

[9]

Kachroo A, Schopfer CR, Nasrallah ME, Nasrallah JB . Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 2001; 293: 1824-1826.

[10]

Takayama S, Shimosato H, Shiba H et al. Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 2001; 413: 534-538.

[11]

Schopfer CR, Nasrallah JB . Self-incompatibility. Prospects for a novel putative peptide-signaling molecule. Plant Physiol 2000; 124: 935-940.

[12]

Watanabe M, Ito A, Takada Y 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 2000; 473: 139-144.

[13]

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

[14]

Mishima M, Takayama S, Sasaki KI et al. Structure of the male determinant factor for Brassica self-incompatibility. J Biol Chem 2003; 278: 36389-36395.

[15]

Chookajorn T, Kachroo A, Ripoll DR, Clark AG, Nasrallah JB . Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc Natl Acad Sci USA 2004; 101: 911-917.

[16]

Kusaba M, Dwyer K, Hendershot J, Vrebalov J, Nasrallah JB, Nasrallah ME . Self-incompatibility in the genus Arabidopsis: characterization of the S locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 2001; 13: 627-643.

[17]

Sherman-Broyles S, Boggs NA, Farkas A et al. S locus genes and the evolution of self-fertility in Arabidopsis thaliana. Plant Cell 2007; 19: 94-106.

[18]

Tang C, Toomajian C, Sherman-Broyles S et al. The evolution of selfing in Arabidopsis thaliana. Science 2007; 317: 1070-1072.

[19]

Shimizu KK, Shimizu-Inatsugi R, Tsuchimatsu T, Purugganan MD . Independent origins of self-compatibility in Arabidopsis thaliana. Mol Ecol 2008; 17: 704-714.

[20]

Boggs NA, Nasrallah JB, Nasrallah ME . Independent S-locus mutations caused self-fertility in Arabidopsis thaliana. PLoS Genet 2009; 5: e1000426.

[21]

Dwyer KG, Berger MT, Ahmed R et al. Molecular characterization and evolution of self-incompatibility genes in Arabidopsis thaliana: the case of the Sc haplotype. Genetics 2013; 193: 985-994.

[22]

Nasrallah ME, Liu P, Nasrallah JB . Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A. lyrata. Science 2002; 297: 247-249.

[23]

Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB . Natural variation in expression of self-incompatibility in Arabidopsis thaliana: Implications for the evolution of selfing. Proc Natl Acad Sci USA 2004; 101: 16070-16074.

[24]

Liu P, Sherman-Broyles S, Nasrallah ME, Nasrallah JB . A cryptic modifier causing transient self-incompatibility in Arabidopsis thaliana. Curr Biol 2007; 17: 734-740.

[25]

Boggs NA, Dwyer KG, Shah P et al. Expression of distinct self-incompatibility specificities in Arabidopsis thaliana. Genetics 2009; 182: 1313-1321.

[26]

Tsuchimatsu T, Suwabe K, Shimizu-Inatsugi R et al. Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 2010; 464: 1342-1346.

[27]

Warwick SI, Francis A, Al-Shehbaz IA . Brassicaceae: species checklist and database on CD-Rom. Plant Syst Evol 2006; 259: 249-258.

[28]

Warwick SI, Mummenhoff K, Sauder CA, Koch MA, Al-Shehbaz IA . Closing the gaps: phylogenetic relationships in the Brassicaceae based on DNA sequence data of nuclear ribosomal ITS region. Plant Syst Evol 2010; 285: 209-232.

[29]

Al-Shehbaz IA, Beilstein MA, Kellogg EA . Systematics and phylogeny of the Brassicaceae (Cruciferae): an overview. Plant Syst Evol 2006; 259: 89-120.

[30]

Bailey CD, Koch MA, Mayer M et al. Toward a global phylogeny of the Brassicaceae. Mol Biol Evol 2006; 23: 2142-2160.

[31]

Beilstein MA, Al-Shehbaz IA, Kellogg EA . Brassicaceae phylogeney and trichome evolution. Am J Bot 2006; 93: 607-619.

[32]

Beilstein MA, Al-Shehbaz IA, Mathews S, Kellogg EA . Brassicaceae phylogeny inferred from phytochrome A and NDHF sequence data: tribes and trichomes revisited. Am J Bot 2008; 95: 1307-1327.

[33]

Franzke A, Lysak MA, Al-Shehbaz IA, Koch MA, Mummenhoff K . Cabbage family affairs: the evolutionary history of Brassicaceae. Trends Plant Sci 2011; 16: 108-116.

[34]

Bi YM, Brugière N, Cui Y, Goring DR, Rothstein SJ . Transformation of Arabidopsis with a Brassica SLG/SRK region and ARC1 gene is not sufficient to transfer the self-incompatibility phenotype. Mol Gen Genet 2000; 263: 648-654.

[35]

Suzuki T, Kusaba M, Matsushita M, Okazaki K, Nishio T . Characterization of Brassica S-haplotypes lacking S-locus glycoprotein. FEBS Lett 2000; 482: 102-108.

[36]

Fujimoto R, Sugimura T, Nishio T . Gene conversion from SLG to SRK resulting in self-compatibility in Brassica rapa. FEBS Lett 2006; 580: 425-430.

[37]

Guo YL, Zhao X, Lanz C, Weigel D . Evolution of the S-locus region in Arabidopsis relatives. Plant Physiol 2011; 157: 937-946.

[38]

Murase K, Shiba H, Iwano M et al. A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 2004; 303: 1516-1519.

[39]

Kakita M, Murase K, Iwano M et al. Two distinct forms of M-locus protein kinase localize to the plasma membrane and interact directly with S-locus receptor kinase to transduce self-incompatibility signaling in Brassica rapa. Plant Cell 2007; 19: 3961-3973.

[40]

Kakita M, Shimosato H, Murase K, Isogai A, Takayama S . Direct interaction between S-locus receptor kinase and M-locus protein kinase involved in Brassica self-incompatibility signaling. Plant Biotechnology 2007; 24: 185-190.

[41]

Gu T, Mazzurco M, Sulaman W, Matias DD, Goring DR . Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci USA 1998; 95: 382-387.

[42]

Samuel MA, Mudgil Y, Salt JN et al. Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol 2008; 147: 2084-2095.

[43]

Stone SL, Anderson EM, Mullen RT, Goring DR . ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 2003; 15: 885-898.

[44]

Stone SL, Arnoldo M, Goring DR . A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 1999; 286: 1729-1731.

[45]

Samuel MA, Chong YT, Haasen KE, Aldea-Brydges MG, Stone SL, Goring DR . Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 2009; 21: 2655-2671.

[46]

Li S, Chen M, Yu D et al. EXO70A1-mediated vesicle trafficking is critical for tracheary element development in Arabidopsis. Plant Cell 2013; 25: 1774-1786.

[47]

Franklin TM, Centre JI . SLR1 function is dispensable for both self-incompatible rejection and self-compatible pollination processes in Brassica. Sex Plant Reprod 1996; 9: 203-208.

[48]

Bower MS, Matias DD, Fernandes-Carvalho E et al. Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. Plant Cell 1996; 8: 1641-1650.

[49]

Mazzurco M, Sulaman W, Elina H, Cock JM, Goring DR . Further analysis of the interactions between the Brassica S receptor kinase and three interacting proteins (ARC1, THL1 and THL2) in the yeast two-hybrid system. Plant Mol Biol 2001; 45: 365-376.

[50]

Cabrillac D, Cock JM, Dumas C, Gaude T . The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 2001; 410: 220-223.

[51]

Haffani YZ, Gaude T, Cock JM, Goring DR . Antisense suppression of thioredoxin h mRNA in Brassica napus cv. Westar pistils causes a low level constitutive pollen rejection response. Plant Mol Biol 2004; 55: 619-630.

[52]

Vanoosthuyse V, Tichtinsky G, Dumas C et al. Interaction of calmodulin, a sorting nexin and kinase-associated protein phosphatase with the Brassica oleracea S locus receptor kinase. Plant Physiol 2003; 133: 919-929.

[53]

Kitashiba H, Liu P, Nishio T, Nasrallah JB, Nasrallah ME . Functional test of Brassica self-incompatibility modifiers in Arabidopsis thaliana. Proc Natl Acad Sci USA 2011; 108: 18173-18178.

[54]

Rea AC, Liu P, Nasrallah JB . A transgenic self-incompatible Arabidopsis thaliana model for evolutionary and mechanistic studies of crucifer self-incompatibility. J Exp Bot 2010; 61: 1897-1906.

[55]

Elhaddad NS, Hunt L, Sloan J, Gray JE . Light-induced stomatal opening is affected by the guard cell protein kinase APK1b. PLoS One 2014; 9: e97161.

[56]

Indriolo E, Tharmapalan P, Wright SI, Goring DR . The ARC1 E3 ligase gene is frequently deleted in self-compatible Brassicaceae species and has a conserved role in Arabidopsis lyrata self-pollen rejection. Plant Cell 2012; 24: 4607-4620.

[57]

Indriolo E, Safavian D, Goring DR . The ARC1 E3 ligase promotes two different self-pollen avoidance traits in Arabidopsis. Plant Cell 2014; 26: 1525-1543.

[58]

Safavian D, Jamshed M, Sankaranarayanan S, Indriolo E, Samuel MA, Goring DR . High humidity partially rescues the Arabidopsis thaliana exo70A1 stigmatic defect for accepting compatible pollen. Plant Reprod 2014; 27: 121-127.

[59]

Yamamoto M, Nasrallah JB . In planta assessment of the role of thioredoxin h proteins in the regulation of S-locus receptor kinase signaling in transgenic Arabidopsis thaliana. Plant Physiol 2013; 163: 1387-1395.

[60]

Kim H, Kim JS . A guide to genome engineering with programmable nucleases. Nat Rev Genet 2014; 15: 321-334.

PDF (274KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/