Proc Natl Acad Sci U S A 98(23): 13167-13171

Evolutionary relationships among self-incompatibility RNases

Section of Ecology, Behavior, and Evolution, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093

^{To whom reprint requests should be addressed. E-mail:}ude.dscu@cigib.

Edited by Barbara A. Schaal, Washington University, St. Louis, MO, and approved September 7, 2001

Received 2001 Jul 25

Abstract

T2-type RNases are responsible for self-pollen recognition and rejection in three distantly related families of flowering plants—the Solanaceae, Scrophulariaceae, and Rosaceae. We used phylogenetic analyses of 67 T2-type RNases together with information on intron number and position to determine whether the use of RNases for self-incompatibility in these families is homologous or convergent. All methods of phylogenetic reconstruction as well as patterns of variation in intron structure find that all self-incompatibility RNases along with non-S genes from only two taxa form a monophyletic clade. Several lines of evidence suggest that the best interpretation of this pattern is homology of self-incompatibility RNases from the Scrophulariaceae, Solanaceae, and Rosaceae. Because the most recent common ancestor of these three families is the ancestor of ≈75% of dicot families, our results indicate that RNase-based self-incompatibility was the ancestral state in the majority of dicots.

Abstract

Multiallelic self-incompatibility systems prevent self-fertilization in many flowering plants. The molecular bases of self-incompatibility in three angiosperm families—the Brassicaceae, Papaveraceae, and Solanaceae—are all different (1–3), contradicting early speculation (4) that all self-incompatibility systems have a single origin. Nevertheless, three distantly related families—the Solanaceae, Scrophulariaceae, and Rosaceae—use T2-type RNases as the mechanism of self-pollen recognition and rejection (5–7). In this study we use an extensive plant T2-RNase database to determine whether use of self-incompatibility RNases (S-RNases) in these families is homologous or convergent.

The Solanaceae and Scrophulariaceae belong to the subclass Asteridae whereas the Roasaceae are in the subclass Rosidae (Fig. (Fig.1).1). Homology of S-RNases would suggest that RNase-based gametophytic self-incompatibility (GSI) was present in the common ancestor of these subclasses, which together comprise roughly three-quarters of dicot families (8, 9). Moreover, a single origin would imply rampant losses of RNase-based GSI and several gains of other forms of incompatibility among higher dicots. Alternatively, polyphyletic relationships of extant S-RNases would represent a spectacular example of functional convergence.

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Figure 1

Relationships among selected dicots (modified from refs. 41 and 46). After each family the form of multiallelic self-incompatibility is indicated: G, gametophytic; S, sporophytic; +, use of S-RNases; −, use of alternative molecular mechanism. Lack of a sign indicates the mechanism of the incompatibility reaction is unknown.

Estimating the evolutionary relationships among S-RNases is difficult for several reasons. First, T2-type RNases are relatively short (≈650 bp of coding sequence), potentially providing limited information on relationships. Second, the time since divergence of the subclasses Asteridae and Rosidae is quite long, perhaps 110 million years (10). Finally, the strong negative frequency-dependent selection that operates on the S-locus is expected to cause extensive sequence divergence once the system originates (11). Thus, even if S-RNases arose separately in different groups, phylogenetic reconstructions might tend to unite them due to long-branch attraction (12), the tendency for methods of phylogenetic reconstruction to unite rapidly evolving taxa because of random homoplasies.

Previous analyses (7, 13, 14) found that S-RNases from the Scrophulariaceae and the Solanaceae likely share common ancestry, but the placement of S-RNases from the Rosaceae was uncertain. This finding is not surprising, as the Scrophulariaceae and Solanaceae share a more recent common ancestor (ref. 15; Fig. Fig.1).1). The current analysis relies on a much more extensive database of T2-type RNases, uses intron number and position to corroborate groupings based on phylogenetic reconstruction of DNA sequence information, and applies recent methods of phylogenetic hypothesis testing to determine whether the use of S-RNase-based GSI represents homology.

MP, MP using character transition weightings from the best-fit general time reversible model; NJ, NJ using the best-fit general time reversible model; MP-RASA, unweighted parsimony on RASA-reduced data; NJ-RASA, unweighted NJ (uncorrected “p”) on RASA-reduced data.

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Acknowledgments

We thank T. Wehner for providing seed of L. cylindrica and R. Doolittle, D. Tank, R. Glor, J. R. Macey, D. Weisrock, B. Emerson, J. Lyons-Weiler, and A. Rambaut for help with phylogenetic analyses. A. Angert, M. Streisfeld, and two anonymous reviewers offered suggestions that significantly improved the manuscript. This work was supported by National Science Foundation Awards DEB-9527834 and DEB-0108173 (to J.R.K).

Acknowledgments

Abbreviations

S-RNase	self-incompatibility RNase
GSI	gametophytic self-incompatibility
MP	maximum parsimony
NJ	neighbor joining
ML	maximum likelihood
RASA	relative apparent synapomorphy analysis

Abbreviations

Note Added in Proof.

A similar phylogenetic conclusion recently has been reached by J. Steinbachs and K. E. Holsinger by using a Bayesian approach (unpublished work).

Note Added in Proof.

Footnotes

This paper was submitted directly (Track II) to the PNAS office.

Footnotes

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