Self‐incompatibility in
In self‐incompatible Solanaceae, the pistil protein S‐RNase contributes to
- NSF-PAR ID:
- 10161533
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- The Plant Journal
- Volume:
- 103
- Issue:
- 4
- ISSN:
- 0960-7412
- Page Range / eLocation ID:
- p. 1304-1317
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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SUMMARY Petunia is controlled by the polymorphicS ‐locus, which containsS‐RNase encoding the pistil determinant and 16–20S‐locus F‐box (SLF ) genes collectively encoding the pollen determinant. Here we sequenced and assembled approximately 3.1 Mb of theS2 ‐haplotype of theS ‐locus inPetunia inflata using bacterial artificial chromosome clones collectively containing all 17SLF genes,SLFLike1 , andS‐RNase . TwoSLF pseudogenes and 28 potential protein‐coding genes were identified, 20 of which were also found at theS ‐loci of both theS6a ‐haplotype ofP. inflata and theSN ‐haplotype of self‐compatiblePetunia axillaris , but not in theS ‐locus remnants of self‐compatible potato (Solanum tuberosum ) and tomato (Solanum lycopersicum ). Comparative analyses ofS ‐locus sequences of these threeS ‐haplotypes revealed potential genetic exchange in the flanking regions ofSLF genes, resulting in highly similar flanking regions between different types ofSLF and between alleles of the same type ofSLF of differentS ‐haplotypes. The high degree of sequence similarity in the flanking regions could often be explained by the presence of similar long terminal repeat retroelements, which were enriched at theS ‐loci of all threeS ‐haplotypes and in the flanking regions of allS ‐locus genes examined. We also found evidence of the association of transposable elements withSLF pseudogenes. Based on the hypothesis thatSLF genes were derived by retrotransposition, we identified 10F‐box genes as putativeSLF parent genes. Our results shed light on the importance of non‐coding sequences in the evolution of theS ‐locus, and on possible evolutionary mechanisms of generation, proliferation, and deletion ofSLF genes. -
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Summary Mating system transitions from self‐incompatibility (SI) to self‐compatibility (SC) are common in plants. In the absence of high levels of inbreeding depression, SC alleles are predicted to spread due to transmission advantage and reproductive assurance.
We characterized mating system and pistil‐expressed SI factors in 20 populations of the wild tomato species
Solanum habrochaites from the southern half of the species range.We found that a single SI to SC transition is fixed in populations south of the Rio Chillon valley in central Peru. In these populations, SC correlated with the presence of the
hab‐6 S ‐haplotype that encodes a low activity S‐RNase protein. We identified a single population segregating for SI/SC andhab‐6 . Intrapopulation crosses showed thathab‐6 typically acts in the expected codominant fashion to confer SC. However, we found one specificS ‐haplotype (hab‐10 ) that consistently rejects pollen of thehab‐6 haplotype, and results in SIhab‐6 /hab‐10 heterozygotes.We suggest that the
hab‐10 haplotype could act as a genetic mechanism to stabilize mixed mating in this population by presenting a disadvantage for thehab‐6 haplotype. This barrier may represent a mechanism allowing for the persistence of SI when an SC haplotype appears in or invades a population. -
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Summary Plants have mechanisms to recognize and reject pollen from other species. Although widespread, these mechanisms are less well understood than the self‐incompatibility (
SI ) mechanisms plants use to reject pollen from close relatives. Previous studies have shown that some interspecific reproductive barriers (IRB s) are related toSI in the Solanaceae. For example, the pistilSI proteins S‐RN ase andHT protein function in a pistil‐sideIRB that causes rejection of pollen from self‐compatible (SC ) red/orange‐fruited species in the tomato clade. However, S‐RN ase‐independentIRB s also clearly contribute to rejecting pollen from these species. We investigated S‐RN ase‐independent rejection ofSolanum lycopersicum pollen bySC Solanum pennellii LA 0716,SC .Solanum habrochaites LA 0407, andSC Solanum arcanum LA 2157, which lack functional S‐RN ase expression. We found that all three accessions expressHT proteins, which previously had been known to function only in conjunction with S‐RN ase, and then usedRNA i to test whether they also function in S‐RN ase‐independent pollen rejection. SuppressingHT SC S. pennellii LA 0716 allowsS. lycopersicum pollen tubes to penetrate farther into the pistil inHT HT SC .Solanum habrochaites LA 0407 and inSC S. arcanum LA 2157 allowsS. lycopersicum pollen tubes to penetrate to the ovary and produce hybrids that, otherwise, would be difficult to obtain. Thus,HT proteins are implicated in both S‐RN ase‐dependent and S‐RN ase‐independent pollen rejection. The results support the view that overall compatibility results from multiple pollen–pistil interactions with additive effects. -
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Summary We investigated the molecular basis and physiological implications of anion transport during pollen tube (
PT ) growth inArabidopsis thaliana (Col‐0).Patch‐clamp whole‐cell configuration analysis of pollen grain protoplasts revealed three subpopulations of anionic currents differentially regulated by cytoplasmic calcium ([Ca2+]cyt). We investigated the pollen‐expressed proteins
At SLAH 3,At ALMT 12,At TMEM 16 andAt CCC as the putative anion transporters responsible for these currents.At CCC ‐GFP was observed at the shank andAt SLAH 3‐GFP at the tip and shank of thePT plasma membrane. Both are likely to carry the majority of anion current at negative potentials, as extracellular anionic fluxes measured at the tip ofPT s with an anion vibrating probe were significantly lower inslah3 −/− andccc −/− mutants, but unaffected inalmt12 −/− andtmem16 −/− . We further characterised the effect ofpH andGABA by patch clamp. Strong regulation by extracellularpH was observed in the wild‐type, but not intmem16 −/− . Our results are compatible withAt TMEM 16 functioning as an anion/H+cotransporter and therefore, as a putativepH sensor.GABA presence: (1) inhibited the overall currents, an effect that is abrogated in thealmt12 −/− and (2) reduced the current inAt ALMT 12 transfectedCOS ‐7 cells, strongly suggesting the direct interaction ofGABA withAt ALMT12.Our data show that
At SLAH 3 andAt CCC activity is sufficient to explain the major component of extracellular anion fluxes, and unveils a possible regulatory system linkingPT growth modulation bypH ,GABA , and [Ca2+]cytthrough anionic transporters. -
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Summary The collaborative non‐self‐recognition model for S‐
RN ase‐based self‐incompatibility predicts that multiple S‐locus F‐box proteins (SLF s) produced by pollen of a givenS ‐haplotype collectively mediate ubiquitination and degradation of all non‐self S‐RN ases, but not self S‐RN ases, in the pollen tube, thereby resulting in cross‐compatible pollination but self‐incompatible pollination. We had previously used pollen extracts containingGFP ‐fused S2‐SLF 1 (SLF 1 with anS 2‐haplotype) ofPetunia inflata for co‐immunoprecipitation (Co‐IP ) and mass spectrometry (MS ), and identified PiCUL 1‐P (a pollen‐specific Cullin1), PiSSK 1 (a pollen‐specific Skp1‐like protein) and PiRBX 1 (a conventional Rbx1) as components of theSCFS 2–SLF 1complex. Using pollen extracts containing PiSSK 1:FLAG :GFP for Co‐IP /MS , we identified two additionalSLF s (SLF 4 andSLF 13) that were assembled intoSCFSLF complexes. As 17SLF SLF 1SLF 17S 2andS 3pollen, here we examined whether all 17SLF s are assembled into similar complexes and, if so, whether these complexes are unique toSLF s. We modified the previous Co‐IP /MS procedure, including the addition of style extracts from four differentS ‐genotypes to pollen extracts containing PiSSK 1:FLAG :GFP , to perform four separate experiments. The results taken together show that all 17SLF s and anSLF ‐like protein,SLFL ike1 (encoded by anS ‐locus‐linked gene), co‐immunoprecipitated with PiSSK 1:FLAG :GFP . Moreover, of the 179 other F‐box proteins predicted byS 2andS 3pollen transcriptomes, only a pair with 94.9% identity and another pair with 99.7% identity co‐immunoprecipitated with PiSSK 1:FLAG :GFP . These results suggest thatSCFSLF complexes have evolved specifically to function in self‐incompatibility.
