Evolutionary relationships among self-incompatibility RNases

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 approximately 75% of dicot families, our results indicate that RNase-based self-incompatibility was the ancestral state in the majority of dicots.

Figure 1

Relationships among selected dicots (modified from refs. 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.

Figure 2

(a) ML phylogeny of plant T2-type RNases. Nonparametric bootstrap support for nodes 1–3 is in Table 1. Ant., Antirrhinum; Ara., Arabidopsis; Cal., Calystegia; Cic., Cicer; Hor., Hordeum; Luf., Luffa; Lyc., Lycopersicon; Mal., Malus; Med., Medicago; Nel., Nelumbo; Nic., Nicotiana; Ory., Oryza; Pin., Pinus; Pis., Pisum; Pru., Prunus; Pyr., Pyrus; Sol., Solanum; Tri., Triticum; Vol., Volvox; Zea., Zea; Zin., Zinnia. * indicate genes for which intron structure information was obtained. (b) Patterns of intron presence/absence. Boxes indicate the presence (shaded) or absence (unshaded) of introns as numbered in Fig. 3.

Figure 3

Intron structure of plant T2-type RNases. Boxes represent exons, lines are introns (not to scale). Dashed lines connect homologous regions. Introns are numbered from 5′ to 3′.

Figure 4

Parametric bootstrap (–31) results for the hypothesis that nonmonophyly of class III RNases is consistent with the observed data. One hundred sets of DNA sequence data were generated by using seq-gen (47) to match the ML topology found under the constraint that class III RNases were nonmonophyletic. For each replicate, we subtracted the length of the shortest constrained MP tree from the length of the shortest unconstrained MP tree. The distribution of differences was compared with the difference between shortest unconstrained and constrained trees by using the empirical data. A difference as great or greater than that observed was found in only 4% of simulated datasets.