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Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana

Nature volume 439, pages 805–810 (2006)Cite this article

Abstract

Pollen–pistil interactions are crucial for controlling plant mating. For example, S-RNase-based self-incompatibility prevents inbreeding in diverse angiosperm species. S-RNases are thought to function as specific cytotoxins that inhibit pollen that has an S-haplotype that matches one of those in the pistil. Thus, pollen and pistil factors interact to prevent mating between closely related individuals. Other pistil factors, such as HT-B, 4936-factor and the 120 kDa glycoprotein, are also required for pollen rejection but do not contribute to S-haplotype-specificity per se. Here we show that S-RNase is taken up and sorted to a vacuolar compartment in the pollen tubes. Antibodies to the 120 kDa glycoprotein label the compartment membrane. When the pistil does not express HT-B or 4936-factor, S-RNase remains sequestered, unable to cause rejection. Similarly, in wild-type pistils, compatible pollen tubes degrade HT-B and sequester S-RNase. We suggest that S-RNase trafficking and the stability of HT-B are central to S-specific pollen rejection.

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Figure 1: S-RNase uptake in style-side defective backgrounds.
Figure 2: S-RNase compartmentalization.
Figure 3: Differential protein stability after compatible versus incompatible pollination.
Figure 4: HT-B in pollen tubes.
Figure 5: A model for S-RNase-based SI. S-RNases, 120K and HT-B are taken up from the ECM by endocytosis.

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Acknowledgements

We thank M. Kroll for manuscript assistance; H. Sassa for helpful discussions; J. Rogers for antibodies; and C. S. Gasser, S. J. Hiscock and C. Staiger for pre-review. The MU-Monsanto Plant Biology Program and grants from the US National Science Foundation supported this work. F.C.-G. was also supported by a grant from the Universidad Nacional Autonoma de Mexico.

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Author notes

  1. Ariel Goldraij and Katsuhiko Kondo: *These authors contributed equally to this work

Authors and Affiliations

  1. CIQUIBIC, Departamento de Quimica Biologica, Facultad de Ciencias Quimicas, Universidad Nacional de Cordoba, Ciudad Universitaria, 5000, Cordoba, Argentina

    Ariel Goldraij

  2. Division of Biochemistry, 105 Life Sciences Center, 1201 E. Rollins Street, Missouri, 65211, Columbia, USA

    Katsuhiko Kondo, Christopher B. Lee, Sunran Kim & Bruce McClure

  3. Division of Biological Sciences, 2 Tucker Hall, Missouri, 65211, Columbia, USA

    Christopher B. Lee, Mayandi Sivaguru & Thomas E. Phillips

  4. Department of Plant Biology, 4505 Miller Plant Sciences Building, Georgia, 30602, Athens, USA

    C. Nathan Hancock

  5. Departamento de Biologia, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico, Ave Universidad y Copilco, D.F. 04510, Mexico, Mexico

    Sonia Vazquez-Santana

  6. Departamento de Bioquimica, Facultad de Quimica, Universidad Nacional Autonoma de Mexico, Ave Universidad y Copilco, D.F. 04510, Mexico, Mexico

    Felipe Cruz-Garcia

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Correspondence to Bruce McClure.

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Supplementary information

Supplementary Notes

This PDF file contains Supplementary Figs 1-4, 7 and 8 along with the legends for these figures. The file also contains a Supplementary Methods section and the legends for Supplementary Video Figs. 5 and 6. (PDF 413 kb)

Supplementary Movie S5

Compartmentalization in a compatible pollination. Animation of the image stack in Figure 2a (compatible, 16 h). The animation pans up and down through the image stack from two different views. (MOV 5637 kb)

Supplementary Movie S6

Compartment breakdown in an incompatible pollination. Animation of the image stack in Figure 2e (incompatible, 36 h). The animation pans up and down through the image stack from two different views. (MOV 7126 kb)

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Goldraij, A., Kondo, K., Lee, C. et al. Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439, 805–810 (2006). https://doi.org/10.1038/nature04491

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