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. 2001 Sep;159(1):329–335. doi: 10.1093/genetics/159.1.329

Rejection of S-heteroallelic pollen by a dual-specific s-RNase in Solanum chacoense predicts a multimeric SI pollen component.

D T Luu 1, X Qin 1, G Laublin 1, Q Yang 1, D Morse 1, M Cappadocia 1
PMCID: PMC1461794  PMID: 11560908

Abstract

S-heteroallelic pollen (HAP) grains are usually diploid and contain two different S-alleles. Curiously, HAP produced by tetraploids derived from self-incompatible diploids are typically self-compatible. The two different hypotheses previously advanced to explain the compatibility of HAP are the lack of pollen-S expression and the "competition effect" between two pollen-S gene products expressed in a single pollen grain. To distinguish between these two possibilities, we used a previously described dual-specific S(11/13)-RNase, termed HVapb-RNase, which can reject two phenotypically distinct pollen (P(11) and P(13)). Since the HVapb-RNase does not distinguish between the two pollen types (it recognizes both), P(11)P(13) HAP should be incompatible with the HVapb-RNase in spite of the competition effect. We show here that P(11)P(13) HAP is accepted by S(11)S(13) styles, but is rejected by the S(11/13)-RNase, which demonstrates that the pollen-S genes must be expressed in HAP. A model involving tetrameric pollen-S is proposed to explain both the compatibility of P(11)P(13) HAP on S(11)S(13)-containing styles and the incompatibility of P(11)P(13) HAP on styles containing the HVapb-RNase.

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Selected References

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  1. Birchler J. A., Newton K. J. Modulation of protein levels in chromosomal dosage series of maize: the biochemical basis of aneuploid syndromes. Genetics. 1981 Oct;99(2):247–266. doi: 10.1093/genetics/99.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brewbaker J L. Incompatibility in Autotetraploid Trifolium Repens L. I. Competition and Self-Compatibility. Genetics. 1954 May;39(3):307–316. doi: 10.1093/genetics/39.3.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Golz J. F., Su V., Clarke A. E., Newbigin E. A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. Genetics. 1999 Jul;152(3):1123–1135. doi: 10.1093/genetics/152.3.1123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Huang S., Lee H. S., Karunanandaa B., Kao T. H. Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell. 1994 Jul;6(7):1021–1028. doi: 10.1105/tpc.6.7.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Kao T. H., McCubbin A. G. How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12059–12065. doi: 10.1073/pnas.93.22.12059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. LEWIS D. Chromosome fragments and mutation of the incompatibility gene. Nature. 1961 Jun 10;190:990–991. doi: 10.1038/190990a0. [DOI] [PubMed] [Google Scholar]
  7. Lee H. S., Huang S., Kao T. S proteins control rejection of incompatible pollen in Petunia inflata. Nature. 1994 Feb 10;367(6463):560–563. doi: 10.1038/367560a0. [DOI] [PubMed] [Google Scholar]
  8. Lee H. S., Singh A., Kao T. RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol Biol. 1992 Dec;20(6):1131–1141. doi: 10.1007/BF00028899. [DOI] [PubMed] [Google Scholar]
  9. Luu D. T., Qin X., Morse D., Cappadocia M. S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature. 2000 Oct 5;407(6804):649–651. doi: 10.1038/35036623. [DOI] [PubMed] [Google Scholar]
  10. Markert C. L. Lactate Dehydrogenase Isozymes: Dissociation and Recombination of Subunits. Science. 1963 Jun 21;140(3573):1329–1330. doi: 10.1126/science.140.3573.1329. [DOI] [PubMed] [Google Scholar]
  11. Matton D. P., Luu D. T., Xike Q., Laublin G., O'Brien M., Maes O., Morse D., Cappadocia M. Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell. 1999 Nov;11(11):2087–2097. doi: 10.1105/tpc.11.11.2087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Matton D. P., Maes O., Laublin G., Xike Q., Bertrand C., Morse D., Cappadocia M. Hypervariable Domains of Self-Incompatibility RNases Mediate Allele-Specific Pollen Recognition. Plant Cell. 1997 Oct;9(10):1757–1766. doi: 10.1105/tpc.9.10.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Matton DP, Luu DT, Morse D, Cappadocia M. Reply. Establishing A paradigm for the generation of new s alleles. Plant Cell. 2000 Mar;12(3):313–316. doi: 10.1105/tpc.12.3.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McClure B. A., Haring V., Ebert P. R., Anderson M. A., Simpson R. J., Sakiyama F., Clarke A. E. Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature. 1989 Dec 21;342(6252):955–957. doi: 10.1038/342955a0. [DOI] [PubMed] [Google Scholar]
  15. Mittelsten Scheid O., Jakovleva L., Afsar K., Maluszynska J., Paszkowski J. A change of ploidy can modify epigenetic silencing. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7114–7119. doi: 10.1073/pnas.93.14.7114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Murfett J., Atherton T. L., Mou B., Gasser C. S., McClure B. A. S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature. 1994 Feb 10;367(6463):563–566. doi: 10.1038/367563a0. [DOI] [PubMed] [Google Scholar]
  17. Qi X., Luu D. T., Yang Q., Maës O., Matton D. P., Morse D., Cappadocia M. Genotype-dependent differences in S12-RNase expression lead to sporadic self-compatibility. Plant Mol Biol. 2001 Feb;45(3):295–305. doi: 10.1023/a:1006445120648. [DOI] [PubMed] [Google Scholar]
  18. Rivard S. R., Saba-El-Leil M. K., Landry B. S., Cappadocia M. RFLP analyses and segregation of molecular markers in plants produced by in vitro anther culture, selfing, and reciprocal crosses of two lines of self-incompatible Solanum chacoense. Genome. 1994 Oct;37(5):775–783. doi: 10.1139/g94-111. [DOI] [PubMed] [Google Scholar]
  19. Saba-el-Leil M. K., Rivard S., Morse D., Cappadocia M. The S11 and S13 self incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol Biol. 1994 Feb;24(4):571–583. doi: 10.1007/BF00023555. [DOI] [PubMed] [Google Scholar]
  20. Thompson R. D., Kirch H. H. The S locus of flowering plants: when self-rejection is self-interest. Trends Genet. 1992 Nov;8(11):381–387. doi: 10.1016/0168-9525(92)90299-j. [DOI] [PubMed] [Google Scholar]
  21. Uyenoyama M. K. On the evolution of genetic incompatibility systems. III. Introduction of weak gametophytic self-incompatibility under partial inbreeding. Theor Popul Biol. 1988 Aug;34(1):47–91. doi: 10.1016/0040-5809(88)90035-4. [DOI] [PubMed] [Google Scholar]

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