Compatibility and incompatibility in S-RNase-based systems

Abstract

Background: S-RNase-based self-incompatibility (SI) occurs in the Solanaceae, Rosaceae and Plantaginaceae. In all three families, compatibility is controlled by a polymorphic S-locus encoding at least two genes. S-RNases determine the specificity of pollen rejection in the pistil, and S-locus F-box proteins fulfill this function in pollen. S-RNases are thought to function as S-specific cytotoxins as well as recognition proteins. Thus, incompatibility results from the cytotoxic activity of S-RNase, while compatible pollen tubes evade S-RNase cytotoxicity.

Scope: The S-specificity determinants are known, but many questions remain. In this review, the genetics of SI are introduced and the characteristics of S-RNases and pollen F-box proteins are briefly described. A variety of modifier genes also required for SI are also reviewed. Mutations affecting compatibility in pollen are especially important for defining models of compatibility and incompatibility. In Solanaceae, pollen-side mutations causing breakdown in SI have been attributed to the heteroallelic pollen effect, but a mutation in Solanum chacoense may be an exception. This has been interpreted to mean that pollen incompatibility is the default condition unless the S-locus F-box protein confers resistance to S-RNase. In Prunus, however, S-locus F-box protein gene mutations clearly cause compatibility.

Conclusions: Two alternative mechanisms have been proposed to explain compatibility and incompatibility: compatibility is explained either as a result of either degradation of non-self S-RNase or by its compartmentalization so that it does not have access to the pollen tube cytoplasm. These models are not necessarily mutually exclusive, but each makes different predictions about whether pollen compatibility or incompatibility is the default. As more factors required for SI are identified and characterized, it will be possible to determine the role each process plays in S-RNase-based SI.

Fig. 1.

Genetic behaviour of S-locus inhibitor (Sli) from Solanum chacoense. Cross #1, a cross between the inbred S. chacoense S₁S₁ Sli source plant and an SI S. phureja plant designated S₂S₃. The S. chacoense parent is heterozygous for Sli and behaves as a dominant factor that inhibits SI in half the progeny. SC is unlikely to be due to a defective S-locus since half the progeny are SI. Crosses #2 and #3, selfing the S. chacoense parent or one of the SC progeny of cross #1 also results in SI progeny. Thus, functional S-haplotypes are transmitted through the pollen even when Sli is not.

Fig. 2.

Possible functions of Sli. In S-RNase-based SI, S-RNase is secreted into the pistil extracellular matrix (SRN_o). It is taken up into the pollen tube (SRN_i), where it interacts with SLF (SRN + SLF) to determine whether a pollination is compatible or incompatible. Sli may prevent S-RNase uptake, its interaction with SLF, or a downstream step needed for incompatibility. It may also prevent the action of non-S-RNase factors needed for pollen rejection. It is not, however, required for pollen tube growth per se and does not appear to interfere with the compatible pathway.

Fig. 3.

Expression of NaTrxh. (A) RNA level expression: pistil RNA (10 µg) from N. alata ‘Breakthrough’ (BT) or N. plumbaginifolia hybridized with ³²P-labelled probes for NaTrxh, HT-B or a non-differential clone AFLP-15. (B) Protein blot analysis: left, total pistil protein (15 µg) probed with anti-NaTrxh; right, a similar gel stained with Coomassie Blue.

Fig. 4.

Models for S-specific pollen rejection. Pollen tubes are shown in the pistil ECM containing a single S-RNase (SRN_x, purple); although, in a typical S-heterozygote two S-RNases would be present. Compatible (top, S_y-pollen tube in a pistil expressing S_x-RNase) and incompatible (bottom, S_x-pollen tube) pollinations are shown. Left: an S-RNase degradation model that implicates multiple SLF proteins (SLF1, red; SLF2, yellow; SLF3, black regardless of whether they are derived from the S_x- or S_y-haplotype) collaborating to cause S-RNase degradation. These models do not specify a route from the ECM to the pollen cytoplasm where the S-RNase-SLF interaction occurs. Right: the compartmentalization model shows most S-RNase taken up by endocytosis and trafficking by default to progressively larger vacuoles in more mature regions of the pollen tube. S-RNase must exit the endomembrane system to interact with SLF; a single SLF (red, SLF_x; blue SLF_y) is shown. Both models show degradation of pollen RNA (cross) in incompatible pollen tubes, a process that do not occur in compatible pollen tubes (no cross). In S-RNase degradation models, compatibility is attributed to wholesale degradation of S-RNase. The compartmentalization model, in contrast, emphasizes S-RNase isolation from the cytoplasm.