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Tomato (Solanum lycopersicum L.) domestication and later introduction into Europe resulted in a genetic bottleneck that reduced genetic variation. Crosses with other wild tomato species from the Lycopersicon clade can be used to increase genetic diversity and improve important agronomic traits such as stress tolerance. However, many species in the Lycopersicon clade have intraspecific and interspecific incompatibility, such as gametophytic self-incompatibility and unilateral incompatibility. In this review, we provide an overview of the known incompatibility barriers in Lycopersicon. We begin by addressing the general mechanisms self-incompatibility, as well as more specific mechanisms in the Rosaceae, Papaveraceae, and Solanaceae. Incompatibility in the Lycopersicon clade is discussed, including loss of self-incompatibility, species exhibiting only self-incompatibility and species presenting both self-compatibility and selfincompatibility. We summarize unilateral incompatibility in general and specifically in Lycopersicon, with details on the ’self-compatible x selfincompatible’ rule, implications of self-incompatibility in unilateral incompatibility and self-incompatibility-independent pathways of unilateral incompatibility. Finally, we discuss advances in the understanding of compatibility barriers and their implications for tomato breeding. [ABSTRACT FROM AUTHOR]

Tomato (Solanum lycopersicum L.) domestication and later introduction into Europe resulted in a genetic bottleneck that reduced genetic variation. Crosses with other wild tomato species from the Lycopersicon clade can be used to increase genetic diversity and improve important agronomic traits such as stress tolerance. However, many species in the Lycopersicon clade have intraspecific and interspecific incompatibility, such as gametophytic self-incompatibility and unilateral incompatibility. In this review, we provide an overview of the known incompatibility barriers in Lycopersicon. We begin by addressing the general mechanisms self-incompatibility, as well as more specific mechanisms in the Rosaceae, Papaveraceae, and Solanaceae. Incompatibility in the Lycopersicon clade is discussed, including loss of self-incompatibility, species exhibiting only self-incompatibility and species presenting both self-compatibility and self-incompatibility. We summarize unilateral incompatibility in general and specifically in Lycopersicon, with details on the ’self-compatible x self-incompatible’ rule, implications of self-incompatibility in unilateral incompatibility and self-incompatibility-independent pathways of unilateral incompatibility. Finally, we discuss advances in the understanding of compatibility barriers and their implications for tomato breeding.

Hybridisation between individuals of different species can lead to maladapted or inviable progeny due to genetic incompatibilities between diverging species. On the other hand, mating with close relatives, or self-fertilisation may lead to inbreeding depression. Thus, both too much or too little divergence may lead to problems and the organisms have to carefully choose mating partners to avoid both of these pitfalls. In plants this choice occurs at many stages during reproduction, but pollen-pistil interactions play a particularly important role in avoiding inbreeding and hybridisation with other species. Interestingly, the mechanisms involved in avoidance of selfing and interspecific hybridisation may work via shared molecular pathways, as self-incompatible species tend to be more ‘choosy’ with heterospecific pollen compared to self-compatible ones. This review discusses various prezygotic post-pollination barriers to interspecific hybridisation, with a focus on the mechanisms of pollen-pistil interactions and their role in the maintenance of species integrity.

Abstract: The evolutionary concurrence of intraspecies self‐incompatibility (SI) and explosive angiosperm radiation in the Cretaceous have led to the hypothesis that SI was one of the predominant drivers of rapid speciation in angiosperms. Interspecies unilateral incompatibility (UI) usually occurs when pollen from a self‐compatible (SC) species is rejected by the pistils of a SI species, while the reciprocal pollination is compatible (UC). Although this SI × SC type UI is most prevalent and viewed as a prezygotic isolation barrier to promote incipient speciation of angiosperms, comparative evidence to support such a role is lacking. We show that SI × SI type UI in SI species pairs is also common in the well‐characterized accessions representing the four major lineages of the Arabidopsis genus and is developmentally regulated. This allowed us to reveal a strong correlation between UI strength and species divergence in these representative accessions. In addition, analyses of a SC accession and the pseudo‐self‐compatible (psc) spontaneous mutant of Arabidopsis lyrata indicate that UI shares, at least, common pollen rejection pathway with SI. Furthermore, genetic and genomic analyses of SI × SI type UI in A. lyrata × A. arenosa species pair showed that two major‐effect quantitative trait loci are the stigma and pollen‐side determinant of UI, respectively, which could be involved in heterospecies pollen discrimination. By revealing a close link between UI and SI pathway, particularly between UI and species divergence in these representative accessions, our findings establish a connection between SI and speciation. Thus, the pre‐existence of SI system would have facilitated the evolution of UI and accordingly promote speciation. [ABSTRACT FROM AUTHOR]

Background: Unilateral incompatibility (UI) is an asymmetric reproductive barrier that unidirectionally prevents gene flow between species and/or populations. UI is characterized by a compatible interaction between partners in one direction, but in the reciprocal cross fertilization fails, generally due to pollen tube rejection by the pistil. Although UI has long been observed in crosses between different species, the underlying molecular mechanisms are only beginning to be characterized. The wild tomato relative Solanum habrochaites provides a unique study system to investigate the molecular basis of this reproductive barrier, as populations within the species exhibit both interspecific and interpopulation UI. Here we utilized a transcriptomic approach to identify genes in both pollen and pistil tissues that may be key players in UI. Results: We confirmed UI at the pollen-pistil level between a self-incompatible population and a self-compatible population of S. habrochaites. A comparison of gene expression between pollinated styles exhibiting the incompatibility response and unpollinated controls revealed only a small number of differentially expressed transcripts. Many more differences in transcript profiles were identified between UI-competent versus UI-compromised reproductive tissues. A number of intriguing candidate genes were highly differentially expressed, including a putative pollen arabinogalactan protein, a stylar Kunitz family protease inhibitor, and a stylar peptide hormone Rapid ALkalinization Factor. Our data also provide transcriptomic evidence that fundamental processes including reactive oxygen species (ROS) signaling are likely key in UI pollen-pistil interactions between both populations and species. Conclusions: Gene expression analysis of reproductive tissues allowed us to better understand the molecular basis of interpopulation incompatibility at the level of pollen-pistil interactions. Our transcriptomic analysis highlighted specific genes, including those in ROS signaling pathways that warrant further study in investigations of UI. To our knowledge, this is the first report to identify candidate genes involved in unilateral barriers between populations within a species. [ABSTRACT FROM AUTHOR]

In plants, transitions in mating system from outcrossing to self-fertilization are common; however, the impact of these transitions on interspecific and interpopulation reproductive barriers is not fully understood. We examined the consequences of mating system transition for reproductive barriers in 19 populations of the wild tomato species Solanum habrochaites., We identified S. habrochaites populations with self-incompatible (SI), self-compatible (SC) and mixed population (MP) mating systems, and characterized pollen-pistil interactions among S. habrochaites populations and between S. habrochaites and other tomato species. We examined the relationship between mating system, floral morphology, interspecific and interpopulation compatibility and pistil SI factors., We documented five distinct phenotypic groups by combining reproductive behavior with molecular data. Transitions from SI to MP were not associated with weakened interspecific reproductive barriers or loss of known pistil SI factors. However, transitions to SC at the northern range margin were accompanied by loss of S-RNase, smaller flowers, and weakened (or absent) interspecific pollen−pistil barriers. Finally, we identified a subset of SC populations that exhibited a partial interpopulation reproductive barrier with central SI populations., Our results support the hypothesis that shifts in mating system, followed by additional loss-of-function mutations, impact reproductive barriers within and between species. [ABSTRACT FROM AUTHOR]

PREMISE OF THE STUDY: Interspecific reproductive barriers (IRBs) often prevent hybridization between closely related species in sympatry. In the tomato clade ( Solanum section Lycopersicon ), interspecific interactions between natural sympatric populations have not been evaluated previously. In this study, we assessed IRBs between members of the tomato clade from nine sympatric sites in Peru. METHODS: Coflowering was assessed at sympatric sites in Peru. Using previously collected seeds from sympatric sites in Peru, we evaluated premating prezygotic (floral morphology), postmating prezygotic (pollen-tube growth), and postzygotic barriers (fruit and seed development) between sympatric species in common gardens. Pollen-tube growth and seed development were examined in reciprocal crosses between sympatric species. KEY RESULTS: We confirmed coflowering of sympatric species at five sites in Peru. We found three types of postmating prezygotic IRBs during pollen-pistil interactions: (1) unilateral pollen-tube rejection between pistils of self-incompatible species and pollen of self-compatible species; (2) potential conspecific pollen precedence in a cross between two self-incompatible species; and (3) failure of pollen tubes to target ovules. In addition, we found strong postzygotic IRBs that prevented normal seed development in 11 interspecific crosses, resulting in seed-like structures containing globular embryos and aborted endosperm and, in some cases, overgrown endothelium. Viable seed and F1 hybrid plants were recovered from three of 19 interspecific crosses. CONCLUSIONS: We have identified diverse prezygotic and postzygotic IRBs that would prevent hybridization between sympatric wild tomato species, but interspecific hybridization is possible in a few cases. [ABSTRACT FROM AUTHOR]

The wild tomato relative Solanum sitiens is a rare endemic plant of the Atacama Desert of Chile. This species exhibits unique traits-tolerance to drought, salinity and low temperatures, resistances to certain pathogens, and modified fruit ripening-that could be of interest to tomato breeders. However, strong reproductive barriers, including hybrid inviability, sterility, and unilateral incompatibility (UI), prevent or impede introgression with cultivated tomato. Using embryo culture, we obtained a large number of F S. lycopersicum × S. sitiens hybrids, and evaluated their fertility and compatibility as male or female parents. Diploid hybrids were functionally male-sterile and strongly rejected pollen of S. lycopersicum by UI. Chromosome doubling produced fertile allotetraploids, from which allotriploids (two genomes of S. lycopersicum, one of S. sitiens) were derived by crossing to diploid tomato. Rejection of tomato pollen occurred lower in styles of allotriploid than diploid hybrids. The pollen compatibility factors ui1.1 and ui6.1 were not sufficient for compatibility on S. sitiens allotriploid hybrids, unlike comparable hybrids with S. lycopersicoides. Pollen from F S. lycopersicum × S. pennellii was used to overcome UI on pistils of diploid S. lycopersicum × S. sitiens hybrids. This cross yielded progeny that were fertile and compatible in direct backcrosses to S. lycopersicum. These results establish a feasible method for transferring the S. sitiens genome into cultivated tomato. [ABSTRACT FROM AUTHOR]

* Premise of the study: Interspecific reproductive barriers (IRBs) act to ensure species integrity by preventing hybridization. Previous studies on interspecific crosses in the tomato clade have focused on the success of fruit and seed set. The SI x SC rule (SI species x SC species crosses are incompatible, but the reciprocal crosses are compatible) often applies to interspecific crosses. Because SI systems in the Solanaceae affect pollen tube growth, we focused on this process in a comprehensive study of interspecific crosses in the tomato clade to test whether the SI x SC rule was always followed. * Methods: Pollen tube growth was assessed in reciprocal crosses between all 13 species of the tomato clade using fluorescence microscopy. * Key results: In crosses between SC and SI species, pollen tube growth follows the SI x SC rule: interspecific pollen tube rejection occurs when SI species are pollinated by SC species, but in the reciprocal crosses (SC x SI), pollen tubes reach ovaries. However, pollen tube rejection occurred in some crosses between pairs of SC species, demonstrating that a fully functional SI system is not necessary for pollen tube rejection in interspecific crosses. Further, gradations in the strength of both pistil and pollen IRBs were revealed in interspecific crosses using SC populations of generally SI species. * Conclusion: The SI x SC rule explains many of the compatibility relations in the tomato clade, but exceptions occur with more recently evolved SC species and accessions, revealing differences in strength of both pistil and pollen IRBs. [ABSTRACT FROM AUTHOR]

The self-incompatibility mechanism that reduces inbreeding in many plants of the Rosaceae is attributed to a multi-allelic S locus which, in the Prunoideae and Maloideae subfamilies, comprises two complementary genes, a stylar-expressed S-RNase and a pollen-expressed SFB. To elucidate incompatibility in the subfamily Rosoideae, stylar-specific RNases and self-(in)compatibility status were analysed in various diploid strawberries, especially Fragaria nubicola and F. viridis, both self-incompatible, and F. vesca, self-compatible, and in various progenies derived from them. Unexpectedly, two unlinked RNase loci, S and T, were found, encoding peptides distinct from Prunoideae and Maloideae S-RNases; the presence of a single active allele at either is sufficient to confer self-incompatibility. By contrast, in diploid Maloideae and Prunoideae a single locus encodes S-RNases that share several conserved regions and two active alleles are required for self-incompatibility. Our evidence implicates the S locus in unilateral inter-specific incompatibility and shows that S and T RNases can, remarkably, confer not only allele-specific rejection of cognate pollen but also unspecific rejection of Sn Tn pollen, where n indicates a null allele, consistent with the the presence of the pollen component, SFB, activating the cognitive function of these RNases. Comparison of relevant linkage groups between Fragaria and Prunus suggests that Prunus S-RNases, unique in having two introns, may have resulted from gene conversion in an ancestor of Prunus. In addition, it is shown that there is a non-S locus that is essential for self-incompatibility in diploid Fragaria. [ABSTRACT FROM PUBLISHER]

Plants have evolved many systems to prevent inappropriate fertilization. Among them, incompatibility is a well-organized system in which pollen germination or pollen-tube growth is inhibited in pistils. Self-incompatibility (SI), rejecting self-pollen, promotes outbreeding in flowering plants. On the other hand, inter-species incompatibility, preventing gene flow among species to restrict outbreeding, usually occurs unilaterally, and is known as unilateral incompatibility (UI). In Brassicaceae, little is known about the molecular mechanism of UI, althoughS-locus genes involved in recognition of self-pollen have been characterized in the SI system. In the present study, we characterized novel UI observed between members of the same species,Brassica rapa; pollen of Turkish SI lines was specifically rejected by pistils of the Japanese commercial SI variety ‘Osome’. The incompatible phenotype of this intra-species UI closely resembled that of SI. Segregation analysis revealed that the pollen factor of this UI was not linked to theS-locus. [ABSTRACT FROM AUTHOR]

In recent years, unilateral incompatibility (UI), which is an incompatibility system for recognizing and rejecting foreign pollen that operates in one direction, has been shown to be closely related to self-incompatibility (SI) in Brassica rapa. The stigma- and pollen-side recognition factors (SUI1 and PUI1, respectively) of this UI are similar to those of SI (stigma-side SRK and pollen-side SP11), indicating that SUI1 and PUI1 interact with each other and cause pollen-pistil incompatibility only when a specific genotype is pollinated. To clarify the genetic diversity of SUI1 and PUI1 in Japanese B. rapa, here we investigated the UI phenotype and the SUI1/PUI1 sequences in Japanese commercial varieties of Chinese cabbage. The present study showed that multiple copies of nonfunctional PUI1 were located within and in the vicinity of the UI locus region, and that the functional SUI1 was highly conserved in Chinese cabbage. In addition, we found a novel nonfunctional SUI1 allele with a dominant negative effect on the functional SUI1 allele in the heterozygote. [ABSTRACT FROM AUTHOR]

Unilateral pollen-pistil incompatibility within the Brassicaceae has been re-examined in a series of interspecific and intergeneric crosses using 13 self-compatible (SC, Sc) species and 12 self-incompatible (SI) species from ten tribes. SC x SC crosses were usually compatible, SI x SC crosses showed unilateral incompatibility, while SI x SI crosses were often incompatible or unilaterally incompatible. Unilateral incompatibility (UI) is shown to be overcome by bud pollination or treating stigmas with cycloheximide - features in common with self-incompatibility. Treating stigmas with pronase prevents pollen tubes from penetrating the stigma in normally compatible intra-and interspecific pollinations. The results presented show that the presence of an incompatibility system is important in predicting the outcome of interspecific and intergeneric crosses and, combined with the physiological similarities between UI and SI, would suggest an involvement of the S-locus in UI. [ABSTRACT FROM AUTHOR]

The S-locus-related gene SLR1 is highly conserved and highly expressed in several species of the Brassicaceae family. Its function has not been determined, although several features would suggest a fundamental role in pollination. A second related gene ( SLR2) is conserved and expressed in a subset of Brassica genotypes. We analysed the stigmatic expression of SLR1 and SLR2 genes among 11 different plants from various species or genera of the Brassicaceae and examined the extent of the pollen-stigma interaction during intraspecific, interspecific and intergeneric pollinations between them. Appropriate statistical tests on these variables (pollen adhesion, germination, penetration into the stigma, style and ovary, and SLR gene expression) showed that expression of SLR1 (but not SLR2) may be a factor in pollen-stigma adhesion. This hypothesis was supported by the observation of reduced pollen-stigma adhesion in transgenic B. napus plants modified for SLR1 expression. [ABSTRACT FROM AUTHOR]

Unilateral incompatibility often occurs between self-incompatible (SI) species and their self-compatible (SC) relatives. For example, SI Nicotiana alata rejects pollen from SC N. plumbaginifolia, but the reciprocal pollination is compatible. This interspecific pollen rejection system closely resembles intraspecific S-allele-specific pollen rejection. However, the two systems differ in degree of specificity. In SI, rejection is S-allele-specific, meaning that only a single S-RNase causes rejection of pollen with a specific S genotype. Rejection of N. plumbaginifolia pollen is less specific, occurring in response to almost any S-RNase. Here, we have tested whether a non-S-RNase can cause rejection of N. plumbaginifolia pollen. The Escherichia coli rna gene encoding RNaseI was engineered for expression in transgenic (N. plumbaginifolia × SC N. alata) hybrids. Expression levels and pollination behavior of hybrids expressing E. coli RNaseI were compared to controls expressing SA2-RNase from N. alata. Immunoblot analysis and RNase activity assays showed that RNaseI and SA2-RNase were expressed at comparable levels. However, expression of SA2-RNase caused rejection of N. plumbaginifolia pollen, whereas expression of RNaseI did not. Thus, in this system, RNase activity alone is not sufficient for rejection of N. plumbaginifolia pollen. The results suggest that S-RNases may be specially adapted to function in pollen rejection. [ABSTRACT FROM AUTHOR]

Unilateral incompatibility was discovered when crossing was attempted between different self-compatible types and subspecies of V. faba. Crossing in the direction female less self-fertile x male more self-fertile failed, whereas the reciprocal-crossing succeeded. Unilateral incompatibility developed with the evolution of less fertile and large seeded field bean types. How a cross fertilized (and self-incompatible) system may develop from a self fertilized one is discussed. The unilateral incompatibility in V. faba and other plant species is compared. The two-power competition hypothesis can explain all kinds of unilateral incompatibility reported so far in the literature. Breeding field beans for improved self-fertility is discussed. [ABSTRACT FROM AUTHOR]