The Skp1-like protein SSK1 is required for cross-pollen compatibility in<i>S</i>-RNase-based self-incompatibility

Zhao, Lan; Huang, Jian; Zhao, Zhonghua; Li, Qun; Sims, Thomas L.; Xue, Yongbiao

doi:10.1111/j.1365-313x.2010.04123.x

Cited by 83 publications

(91 citation statements)

References 54 publications

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“…A total of 176 recombinants were recovered, representing a recombination frequency of 10 used to further genotype the recombinants (Fig. 1B and SI Appendix, Table S1).…”

Section: Ui11mentioning

confidence: 99%

“…In a compatible pollination, the SLF/S-RNase interaction leads to protection of pollen tubes against cytotoxic S-RNase, whereas in incompatible pollinations, a failure to recognize self-S-RNase results in pollen tube arrest. In addition, modifier genes, such as those encoding HT-B, NaStEP, and 120-kDa proteins in the pistil, and CUL1 and SSK1 proteins in pollen, are required for SI function but do not confer S-specificity (7)(8)(9)(10)(11).…”

mentioning

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.

109

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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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“…A total of 176 recombinants were recovered, representing a recombination frequency of 10 used to further genotype the recombinants (Fig. 1B and SI Appendix, Table S1).…”

Section: Ui11mentioning

confidence: 99%

mentioning

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.

109

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“…Additional protein-protein interaction assays suggest that SLF/SFB may be a component of an SCF (for Skp1-Cullin1-F-box) or SCF-like complex (Qiao et al, 2004;Hua and Kao, 2006). Notably, data from Zhao et al (2010) in Petunia hybrida show that reduction of PhSSK1 (for P. hybrida SLF-interacting Skp-like1) and its Antirrhinum hispanicum ortholog, AhSSK1, is also required for cross-pollen compatibility.…”

mentioning

confidence: 99%

NaStEP: A Proteinase Inhibitor Essential to Self-Incompatibility and a Positive Regulator of HT-B Stability inNicotiana alataPollen Tubes

et al. 2012

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In Solanaceae, the self-incompatibility S-RNase and S-locus F-box interactions define self-pollen recognition and rejection in an S-specific manner. This interaction triggers a cascade of events involving other gene products unlinked to the S-locus that are crucial to the self-incompatibility response. To date, two essential pistil-modifier genes, 120K and High Top-Band (HT-B), have been identified in Nicotiana species. However, biochemistry and genetics indicate that additional modifier genes are required. We recently reported a Kunitz-type proteinase inhibitor, named NaStEP (for Nicotiana alata Stigma-Expressed Protein), that is highly expressed in the stigmas of self-incompatible Nicotiana species. Here, we report the proteinase inhibitor activity of NaStEP. NaStEP is taken up by both compatible and incompatible pollen tubes, but its suppression in Nicotiana spp. transgenic plants disrupts S-specific pollen rejection; therefore, NaStEP is a novel pistil-modifier gene. Furthermore, HT-B levels within the pollen tubes are reduced when NaStEP-suppressed pistils are pollinated with either compatible or incompatible pollen. In wild-type self-incompatible N. alata, in contrast, HT-B degradation occurs preferentially in compatible pollinations. Taken together, these data show that the presence of NaStEP is required for the stability of HT-B inside pollen tubes during the rejection response, but the underlying mechanism is currently unknown.

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“…Figure 1A shows the strategy for testing the effects of suppressing ui6.1 CUL1 expression in intraspecific crosses. A similar approach was used to test the function of PhSSK1, another putative pollen SI factor that, like CUL1, is proposed to form part of an SCF complex (Zhao et al 2010). We used the S. arcanum accessions LA2163 (SI) and LA2157 (SC), which are similar in most respects, apart from mating system (Rick 1986).…”

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confidence: 99%

The Role of a Pollen-Expressed Cullin1 Protein in Gametophytic Self-Incompatibility in Solanum

Chetelat

2014

Genetics

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We previously isolated a pollen factor, ui6.1, which encodes a Cullin1 protein (CUL1) that functions in unilateral interspecific incompatibility (UI) in Solanum. Here we show that CUL1 is also required for pollen function in self-incompatibility (SI). We used RNA interference (RNAi) to reduce CUL1 expression in pollen of Solanum arcanum, a wild SI tomato relative. Hemizygous T 0 plants showed little or no transmission of the transfer DNA (T-DNA) through pollen when crossed onto nontransgenic SI plants, indicating that CUL1-deficient pollen are selectively eliminated. When crossed onto a related self-compatible (SC) accession lacking active S-RNase, pollen transmission of the T-DNA followed Mendelian ratios. These results provide further evidence for functional overlap between SI and UI on the pollen side and suggest that CUL1 mutations will reinforce SI-to-SC transitions in natural populations only if preceded by loss of pistil S-RNase expression.S ELF-INCOMPATIBILITY (SI) is a widespread genetic mechanism in hermaphroditic plants that allows for the recognition and rejection of closely related pollen to prevent inbreeding. The breakdown of SI to self-compatibility (SC) through mutation occurs frequently (Igic et al. 2008), presumably driven by reproductive assurance under conditions where pollen from compatible mates is limiting. Pollen from SC species or populations is typically rejected on pistils of related SI species or populations, while, in the reciprocal crosses (SC pollinated by SI), no pollen rejection occurs. This pattern of unilateral incompatibility (UI) is known as the "SI 3 SC rule" (Lewis and Crowe 1958). While the mechanisms underlying SI have been the subject of much investigation, pollen rejection by UI is less well understood.The cultivated tomato (Solanum lycopersicum) and related wild Solanum species provide a powerful system with which to study these reproductive barriers. They exhibit a wide range of mating systems, including SI-enforced obligate outcrossing, SC with facultative outcrossing, and SC with high levels of inbreeding (Rick 1988). Self-compatible biotypes or accessions of mostly SI species provide a source of natural variation for studying SI-related factors.Self-incompatibility in Solanum and other Solanaceae is the S-RNase based, gametophytic type, in which S-specificity is determined by S-RNases in the pistil (McClure et al. 1989) and S-locus F-box proteins (SLFs) in pollen (Sijacic et al. 2004). F-box proteins, together with Skp1 and Cullin1 proteins, are components of Skp, Cullin, Fbox type (SCF) ubiquitin E3 ligases that mark proteins for degradation by the 26S proteasome (Zheng et al. 2002;Moon et al. 2004). The ubiquitinproteasome pathway is thought to regulate pollen-side SI responses in the Solanaceae (Zhang et al. 2009). In the "collaborative non-self-recognition" model (Kubo et al. 2010), the S-locus encodes multiple SLF proteins that together recognize different suites of S-RNases. In compatible pollinations, SLF/SRNase interactions lead to protection of p...

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The Skp1-like protein SSK1 is required for cross-pollen compatibility inS-RNase-based self-incompatibility

Cited by 83 publications

References 54 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

NaStEP: A Proteinase Inhibitor Essential to Self-Incompatibility and a Positive Regulator of HT-B Stability inNicotiana alataPollen Tubes

The Role of a Pollen-Expressed Cullin1 Protein in Gametophytic Self-Incompatibility in Solanum

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