Testing the SI × SC rule: Pollen–pistil interactions in interspecific crosses between members of the tomato clade (<i>Solanum</i> section <i>Lycopersicon</i>, Solanaceae)

Baek, You Soon; Covey, Paul A.; Petersen, Jennifer J.; Chetelat, Roger T.; McClure, Bruce; Bedinger, Patricia A.

doi:10.3732/ajb.1400484

Cited by 71 publications

(173 citation statements)

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“…Two wild relatives of cultivated tomato, S. cheesmaniae and S. galapagense, both SC, also lack an SLF-23 ortholog, and their pollen is also rejected on pistils of SI species (16,18). These taxa also lack functional ui6.1 (21).…”

Section: Discussionmentioning

confidence: 99%

“…Three other red-or orange-fruited species, S. cheesmaniae, S. galapagense, and S. pimpinellifolium, are bilaterally cross-compatible with each other and with S. lycopersicum. There are notable exceptions to SI × SC rule in the tomato clade (18). One is that pollen of all of the red/ orange-fruited species (SC) are rejected on pistils of the SC greenfruited species.…”

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confidence: 99%

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Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species

Chetelat

2015

Proc. Natl. Acad. Sci. U.S.A.

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Unilateral interspecific incompatibility (UI) is a postpollination, prezygotic reproductive barrier that prevents hybridization between related species when the female parent is self-incompatible (SI) and the male parent is self-compatible (SC). In tomato and related Solanum species, two genes, ui1.1 and ui6.1, are required for pollen compatibility on pistils of SI species or hybrids. We previously showed that ui6.1 encodes a Cullin1 (CUL1) protein. Here we report that ui1.1 encodes an S-locus F-box (SLF) protein. The ui1.1 gene was mapped to a 0.43-cM, 43.2-Mbp interval at the S-locus on chromosome 1, but positional cloning was hampered by low recombination frequency. We hypothesized that ui1.1 encodes an SLF protein(s) that interacts with CUL1 and Skp1 proteins to form an SCF-type (Skp1, Cullin1, F-box) ubiquitin E3 ligase complex. We identified 23 SLF genes in the S. pennellii genome, of which 19 were also represented in cultivated tomato (S. lycopersicum). Data from recombination events, expression analysis, and sequence annotation highlighted 11 S. pennellii genes as candidates. Genetic transformations demonstrated that one of these, SpSLF-23, is sufficient for ui1.1 function. A survey of cultivated and wild tomato species identified SLF-23 orthologs in each of the SI species, but not in the SC species S. lycopersicum, S. cheesmaniae, and S. galapagense, pollen of which lacks ui1.1 function. These results demonstrate that pollen compatibility in UI is mediated by protein degradation through the ubiquitinproteasome pathway, a mechanism related to that which controls pollen recognition in SI.interspecific incompatibility | self-incompatibility | Solanum lycopersicum | Solanum pennellii | S-locus F-box protein

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species

Chetelat

2015

Proc. Natl. Acad. Sci. U.S.A.

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109

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“…They noted that this so-called SI 3 SC rule applies to many crosses in the Solanaceae and Scrophulariaceae (McGuire and Rick, 1954) and suggested that it was regulated by the S-locus (Lewis and Crowe, 1958). A recent comprehensive study of interspecific compatibility in the tomato clade demonstrated that the SI 3 SC rule is closely followed at the species level (Baek et al, 2015). In addition to the Solanaceae, UI consistent with the SI 3 SC rule has been recorded in Lilliaceae (Ascher and Peloquin, 1968), Poaceae (Heslop-Harrison, 1982), Brassicaceae (Sampson, 1962;Hiscock and Dickinson, 1993), and Orchidaceae (Pinheiro et al, 2015).…”

Section: Si and Interspecific Incompatibility: A Common Toolkitmentioning

confidence: 99%

“…Right, SI S. chilense LA2884 pollinated by S. lycopersicum 'VF36'. The UI rejection response in this example occurs closer to the stigma and is typical of crosses between SI green-fruited species and SC red-fruited species (Baek et al, 2015). Arrows indicate the position in the style where fewer than three pollen tubes pass at 48 h after pollination (compatible pollen tubes reach the ovary after 24 h).…”

Section: S-rnase-based Simentioning

confidence: 99%

“…For instance, there are many exceptions to the SI 3 SC rule (e.g. SC 3 SC incompatibilities; Baek et al, 2015), and there are physiological and morphological differences between SI and UI. For example, pollen tube staining of pollinated pistils often shows that interspecific pollen tube rejection occurs closer to the stigma than SI pollen rejection ( Fig.…”

Section: Differences Between Si and Ui: Additional Ui Mechanismsmentioning

confidence: 99%

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Pollen-Pistil Interactions and Their Role in Mate Selection

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The role of hybrid seed inviability in angiosperm speciation

Coughlan

2023

American J of Botany

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Understanding which reproductive barriers contribute to speciation is essential to understanding the diversity of life on earth. Several contemporary examples of strong hybrid seed inviability (HSI) between recently diverged species suggest that HSI may play a fundamental role in plant speciation. Yet, a broader synthesis of HSI is needed to clarify its role in diversification. Here, I review the incidence and evolution of HSI. Hybrid seed inviability is common and evolves rapidly, suggesting that it may play an important role early in speciation. The developmental mechanisms that underlie HSI involve similar developmental trajectories in endosperm, even between evolutionarily deeply diverged incidents of HSI. In hybrid endosperm, HSI is often accompanied by whole‐scale gene misexpression, including misexpression of imprinted genes which have a key role in endosperm development. I explore how an evolutionary perspective can clarify the repeated and rapid evolution of HSI. In particular, I evaluate the evidence for conflict between maternal and paternal interests in resource allocation to offspring (i.e., parental conflict). I highlight that parental conflict theory generates explicit predictions regarding the expected hybrid phenotypes and genes responsible for HSI. While much phenotypic evidence supports a role of parental conflict in the evolution of HSI, an understanding of the underlying molecular mechanisms of this barrier is essential to test parental conflict theory. Lastly, I explore what factors may influence the strength of parental conflict in natural plant populations as an explanation for why rates of HSI may differ between plant groups and the consequences of strong HSI in secondary contact.

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Testing the SI × SC rule: Pollen–pistil interactions in interspecific crosses between members of the tomato clade (Solanum section Lycopersicon, Solanaceae)

Abstract: The SI × 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.

Cited by 71 publications

References 55 publications

Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species

Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species

Pollen-Pistil Interactions and Their Role in Mate Selection

The role of hybrid seed inviability in angiosperm speciation

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