Skip to main content
Log in

An S-RNase-Based Gametophytic Self-Incompatibility System Evolved Only Once in Eudicots

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

It has been argued that the common ancestor of about 75% of all dicots possessed an S-RNase-based gametophytic self-incompatibility (GSI) system. S-RNase genes should thus be found in most plant families showing GSI. The S-RNase gene (or a duplicate) may also acquire a new function and thus genes belonging to the S-RNase lineage may also persist in plant families without GSI. Nevertheless, sequences that belong to the S-RNase lineage have been found in the Solanaceae, Scrophulariaceae, Rosaceae, Cucurbitaceae, and Fabaceae plant families only. Here we search for new sequences that may belong to the S-RNase lineage, using both a phylogenetic and a much faster and simpler amino acid pattern-based approach. We show that the two methods have an apparently similar false-negative rate of discovery (~10%). The amino acid pattern-based approach produces about 15% false positives. Genes belonging to the S-RNase lineage are found in three new plant families, namely, the Rubiaceae, Euphorbiaceae, and Malvaceae. Acquisition of a new function by genes belonging to the S-RNase lineage is shown to be a frequent event. A putative S-RNase sequence is identified in Lotus, a plant genus for which molecular studies on GSI are lacking. The hypothesis of a single origin for S-RNase-based GSI (before the split of the Asteridae and Rosidae) is further supported by the finding of genes belonging to the S-RNase lineage in some of the oldest lineages of the Asteridae and Rosidae, and by Baysean constrained tree analyses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson MA, Cornish EC, Mau SL et al (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 

  • Barrett SCH, Harder LD, Worley AC (1996) The comparative biology of pollination and mating in flowering plants. Philos Trans Roy Soc B 351:1271–1280

    Article  Google Scholar 

  • de Nettancourt D (1997) Incompatibility in angiosperms. Springer-Verlag, Berlin

    Google Scholar 

  • Dodds PN, Clarke AE, Newbigin E (1996) Molecular characterisation of an S-like RNase of Nicotiana alata that is induced by phosphate starvation. Plant Mol Biol 31:227–238

    Article  PubMed  CAS  Google Scholar 

  • Ferrer MM, Good-Avila SV (2007) Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. New Phytol 173:401–414

    Article  PubMed  Google Scholar 

  • Gaikwad A, Tewari KK, Kumar D, Chen W, Mukherjee SK (1999) Isolation and characterisation of the cDNA encoding a glycosylated accessory protein of pea chloroplast DNA polymerase. Nucleic Acids Res 27:3120–3129

    Article  PubMed  CAS  Google Scholar 

  • Golz JF, Clarke AE, Newbigin E, Anderson M (1998) A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. Plant J 16:591–599

    Article  PubMed  CAS  Google Scholar 

  • Green PJ (1994) The ribonucleases of higher plants. Annu Rev Plant Physiol Plant Molec Biol 45:421–445

    Article  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 

  • Hauck NR, Yamane H, Tao R, Iezzoni AF (2006) Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172:1191–1198

    Article  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98:13167–13171

    Article  PubMed  CAS  Google Scholar 

  • Itagaki T, Koyama H, Daigo S, Kobayashi H, Koyama T, Iwama M, Ohgi K, Irie M, Inokuchi N (2006) Primary structure and properties of ribonuclease Bm2 (RNase Bm2) from Bryopsis maxima. Biol Pharm Bull 29:875–883

    Article  PubMed  CAS  Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Lee HS, Singh A, Kao T-H (1992) RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol Biol 20:1131–1141

    Article  PubMed  CAS  Google Scholar 

  • Liang L, Huang J, Xue Y (2003) Identification and evolutionary analysis of a relic S-RNase in Antirrhinum. Sex Plant Reprod 16:17–22

    CAS  Google Scholar 

  • Marchler-Bauer A, Anderson JB, Derbyshire MK et al (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35:D237–D240

    Article  PubMed  CAS  Google Scholar 

  • McClure BA, Franklin-Tong V (2006) Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224:233–245

    Article  PubMed  CAS  Google Scholar 

  • Nunes MDS, Santos RAM, Ferreira SM, Vieira J, Vieira CP (2006) Variability patterns and positively selected sites at the gametophytic self-incompatibility pollen SFB gene in a wild self-incompatible Prunus spinosa (Rosaceae) population. New Phytol 172:577–587

    Article  PubMed  CAS  Google Scholar 

  • Pereira P, Fonseca NA, Silva F (2006a) Fast discovery of statistically interesting words. Technical Report DCC-2007-01. DCC-FC & LIACC, Universidade do Porto, Porto, Portugal

  • Pereira P, Fonseca NA, Silva F (2006b) A high performance distributed tool for mining patterns in biological sequences. Technical Report DCC-2006-08. DCC-FC & LIACC. Universidade do Porto, Porto, Portugal

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Ross MD, Jones WT (1985) The origin of Lotus corniculatus. Theor Appl Genet 71:284–288

    Google Scholar 

  • Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T, Ikehashi H (1996) Self-incompatibility (S) alleles of the Rosaceae encode members of a distinct class of the T2/S ribonuclease superfamily. Mol Gen Genet 250:547–557

    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 

  • Sims TL (1993) Genetic regulation of self-incompatibility. Crit Rev Plant Sci 12:129–167

    Article  Google Scholar 

  • Steinbachs JE, Holsinger KE (2002) S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol 19:825–829

    PubMed  CAS  Google Scholar 

  • Stephenson AG, Winsor JA, Richardson TE, Singh A, Kao TH (1992) Effects of style age on the performance of self and cross pollen in Campanula rapunculoides. In: Ottaviano E, Mulcahy DL, Ms Gorla, Mulcahy GB (eds) Angiosperm pollen and ovules. Springer-Verlag, New York, pp 117–121

    Google Scholar 

  • Tao R, Yamane H, Sassa H, Mori H, Gradziel TM, Dandekar AM, Sugiura A (1997) Identification of stylar RNases associated with gametophytic self-incompatibility in almond (Prunus dulcis). Plant Cell Physiol 38:304–311

    PubMed  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  PubMed  CAS  Google Scholar 

  • Taylor CB, Bariola PA, delCardayre SB, Raines RT, Green PJ (1993) RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. Proc Natl Acad Sci USA 90:5118–5122

    Article  PubMed  CAS  Google Scholar 

  • Thompson J, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX window interface: flexible stategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto T, Ando T, Watanabe H, Marchesi E, Kao TH (2005) Duplication of the S-locus F-box gene is associated with breakdown of pollen function in an S-haplotype identified in a natural population of self-incompatible Petunia axillaris. Plant Mol Biol 57:141–153

    Article  PubMed  CAS  Google Scholar 

  • Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (1998) Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet 260:261–268

    Article  PubMed  CAS  Google Scholar 

  • Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni AF, Tao R (2004) The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J 39:573–586

    Article  CAS  Google Scholar 

  • Vieira J, Morales-Hojas R, Santos RA, Vieira CP (2007) Different positively selected sites at the gametophytic self-incompatibility pistil S-RNase gene in the Solanaceae and Rosaceae (Prunus, Pyrus, and Malus). J Mol Evol 65:175–185

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Dong L, Zhang Y, Zhang Y, Wu W, Deng X, Xue Y (2004) Genome-wide analysis of S-Locus F-box-like genes in Arabidopsis thaliana. Plant Mol Biol 56:929–945

    Article  PubMed  CAS  Google Scholar 

  • Weller SG, Donoghue MJ, Charlesworth D (1995) The evolution of self-incompatibility in flowering plants: a phylogenetic approach. In: Hoch PC, Stephenson AG (eds) Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St Louis, MO, pp 355–382

    Google Scholar 

  • Wikstrom N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc Biol Sci 268:2211–2220

    Article  PubMed  CAS  Google Scholar 

  • Yamane H, Tao R, Mori H, Sugiura A (2003a) Identification of a non-S RNase, a possible ancestral form of S-RNases, in Prunus. Mol Genet Genomics 269:90–100

    PubMed  CAS  Google Scholar 

  • Yamane H, Ikeda K, Hauck NR, Iezzoni AF, Tao R (2003b) Self-incompatibility (S) locus region of the mutated S6-haplotype of sour cherry (Prunus cerasus) contains a functional pollen S allele and a non-functional pistil S allele. J Exp Bot 54:2431–2437

    Article  PubMed  CAS  Google Scholar 

  • Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation. The University of Texas at Austin, Austin

Download references

Acknowledgments

This work was partially funded by Fundação para a Ciência e Tecnologia (FCT), research projects POCTI/AGG/44800/2002 and POCI/BIA-BDE/59887/2004 (funded by POCI 2010, cofunded by FEDER funds). Nuno A. Fonseca is the recipient of postdoctoral grant SFRH/BPD/26737/2006 from the FCT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cristina P. Vieira.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vieira, J., Fonseca, N.A. & Vieira, C.P. An S-RNase-Based Gametophytic Self-Incompatibility System Evolved Only Once in Eudicots. J Mol Evol 67, 179–190 (2008). https://doi.org/10.1007/s00239-008-9137-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-008-9137-x

Keywords

Navigation