Expression of 10 S-Class <i>SLF-like</i> Genes in <i>Nicotiana alata</i> Pollen and Its Implications for Understanding the Pollen Factor of the S Locus

Wheeler, David; Newbigin, Ed

doi:10.1534/genetics.107.076885

Cited by 50 publications

(62 citation statements)

References 51 publications

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“…As with the Antirrhinum SLFs, variable amino acid positions are not clustered into distinct hypervariable regions but distributed over the sequence. Similar types of binding and transgenic experiments to those performed with Ah SLF-S 2 have also been done with the Petunia SLF alleles and have produced results that are consistent with expectations for pollen S (Sijacic et al, 2004;Hua and Kao, 2006;Hua et al, 2007).Attempts at identifying SLF orthologs in solanaceous species other than Petunia have highlighted one further evolutionary difference between this gene and the S-RNase gene (Wheeler and Newbigin, 2007). Phylogenetic clustering of S-RNases relative to nearly all other plant RNases points to a single common origin for S-RNase-based SI (Igic and Kohn, 2001;Steinbachs and Holsinger, 2002).…”

supporting

confidence: 60%

“…By comparison, the S-RNases associated with these four Antirrhinum S alleles appear just as expected, with pairwise amino acid identities ranging from 36 to 51%. Levels of nonsynonymous (amino acid-changing, Ka) and synonymous (silent, Ks) substitutions in the DNA sequence are both more than an order of magnitude lower at the Antirrhinum SLF locus than at the cognate S-RNase locus (Table 1; Xue et al, 1996;Zhou et al, 2003;Sassa et al, 2007;Wheeler and Newbigin, 2007). The high level of identity among the Antirrhinum…”

Section: What's Puzzling About the Slf And Sfbs?mentioning

confidence: 99%

“…For instance, Takebayashi et al (2003) rejected the S locus-linked, pollen-expressed gene 48a as a candidate for pollen S based on its low level of polymorphism and lack of evidence of positive selection. However, as the Antirrhinum example shows, abundant sequence polymorphism can no longer be considered a reliable diagnostic feature of pollen S. Compounding the problem is the fact that most taxa have many pollen-expressed F-box protein loci at or near the S locus (Sassa et al, 2007;Wheeler and Newbigin, 2007), all of which must be considered candidates until functional tests demonstrate otherwise.There are several possible ways to remove the requirement for coevolution of pollen and stylar determinants and allow pollen S lineages to be much younger than S-RNase lineages. Potentially, it is the existence of paralagous genes, as is the case for the SLF and SFB loci but not the S-RNase locus, that is responsible for eradicating evidence of frequency-dependent selection.…”

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confidence: 99%

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RNase-Based Self-Incompatibility: Puzzled byPollen S

2008

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Many plants have a genetically determined self-incompatibility system in which the rejection of self pollen grains is controlled by alleles of an S locus. A common feature of these S loci is that separate pollen-and style-expressed genes (pollen S and style S, respectively) determine S allele identity. The long-held view has been that pollen S and style S must be a coevolving gene pair in order for allelic recognition to be maintained as new S alleles arise. In at least three plant families, the Solanaceae, Rosaceae, and Plantaginaceae, the style S gene has long been known to encode an extracellular ribonuclease called the S-RNase. Pollen S in these families has more recently been identified and encodes an F-box protein known as either SLF or SFB. In this perspective, we describe the puzzling evolutionary relationship that exists between the SLF/SFB and S-RNase genes and show that in most cases cognate pairs of genes are not coevolving in the expected manner. Because some pollen S genes appear to have arisen much more recently than their style S cognates, we conclude that either some pollen S genes have been falsely identified or that there is a major problem with our understanding of how the S locus evolves.In three plant families, the Solanaceae, Rosaceae, and Plantaginaceae (formerly Scrophulariaceae; Albach et al. 2005), selfincompatibility (SI) is controlled by extracellular ribonucleases (S-RNases) in the style that are the products of an S locus characterized by large numbers of alleles (Takayama and Isogai, 2005). For many years the pollen counterpart of the S-RNases (pollen S) was unknown. However, a series of recent articles identified candidate genes in all three families (Lai et al., 2002;Entani et al., 2003;Ushijima et al., 2003;Ikeda et al., 2004;Sijacic et al., 2004) and provided evidence for involvement of these genes in the SI response Sijacic et al., 2004;Qiao et al., 2004aQiao et al., , 2004bUshijima et al., 2004;Sonneveld et al., 2005). The studies implicated genes encoding an F-box protein, involved in selecting targets for ubiquitination, as being pollen S in all three families. In the Solanaceae and Plantaginaceae, this F-box protein is called SLF and in the Rosaceae it is called SLF by some groups (Entani et al., 2003) and SFB by others (Ushijima et al., 2003;Ikeda et al., 2004). For simplicity, however, we will refer to the pollen S proteins from the Solanaceae and Plantaginaceae as SLF and from the Rosaceae as SFB. Commentaries heralding this exciting development appeared in many scientific journals, including this one (McClure, 2004), and it appeared that we were closer than ever to understanding RNase-based SI.However, many more questions than answers have been raised by our as yet limited understanding of pollen S. Rather than leading to elucidation of a single conserved SI mechanism among families that use S-RNases, subsequent studies have identified mechanistic differences between the Rosaceae and Solanaceae in the way incompatible pollen is rejected (Sonneveld et al., 2005;Hauck e...

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supporting

confidence: 60%

Section: What's Puzzling About the Slf And Sfbs?mentioning

confidence: 99%

mentioning

confidence: 99%

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RNase-Based Self-Incompatibility: Puzzled byPollen S

2008

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“…This question has recently become even more complicated (see section 8) as it appears that proteins originally identified as SLF-like (SLFL), and not involved in GSI, may in fact be true SLF proteins. Chromosome-walking, differential display or degenerate PCR-cloning approaches Wang et al, 2003Wang et al, ,2004Wheeler & Newbigin 2007;Zhou et al, 2003) in the Solanaceae and Plantaginaceae identified a number of SLF-like genes (SLFL) that were linked to the S-locus. These genes were thought not to be involved in self-incompatibility interactions specifically, since they did not show interaction with known S-RNases nor did they exhibit competitive interaction in transgenic assays (Hua et al, 2007;Meng et al, 2011).…”

Section: Protein Interactions Between Slf and S-rnase Proteinsmentioning

confidence: 99%

“…Additional sequence comparisons demonstrated that SLF proteins could be grouped into at least six subclasses. Because Wheeler & Newbigin (2007) identified at least 10 different SLF-like genes in Nicotiana, and because not all of the previously-identified SLFL genes from Petunia inflata were included in the comparative sequence analysis of Kubo et al (2010), it is possible that more than six SLF subclasses are present. As a result of this analysis, a new nomenclature for SLF proteins has been proposed.…”

Section: Collaborative Non-self Recognition By Slf Proteins In Gsimentioning

confidence: 99%

Protein Interactions in S-RNase-Based Gametophytic Self-Incompatibility

Sims¹

2012

Protein Interactions

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Self‐incompatibility in Petunia: a self/nonself‐recognition mechanism employing S‐locus F‐box proteins and S‐RNase to prevent inbreeding

Wang

Kao

2011

WIREs Developmental Biology

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Many flowering plants producing bisexual flowers have adopted self-incompatibility (SI), a reproductive strategy which allows pistils to distinguish between self and nonself pollen, and to only permit nonself pollen to effect fertilization. To date, three different SI mechanisms have been identified, and this article focuses on the S-RNase-based mechanism using Petunia (Solanaceae) as a model. The genetic basis of this type of SI was established nearly a century ago; the polymorphic S-locus specifies the genetic identity of pollen and the pistil. Molecular genetic studies carried out since the late 1980s have led to the identification of the polymorphic genes at the S-locus that control self/nonself-recognition between pollen and the pistil. The S-RNase gene, which controls pistil specificity, was identified first, and subsequent sequencing of the S-locus region containing S-RNase led to the identification of the S-locus F-box (SLF) gene (now named SLF1). A transgenic approach was used to show that S2-SLF1 (SLF1 of S2-halotype) of Petunia inflata controls pollen specificity. The S-locus contains additional pollen-expressed F-box genes that show sequence similarity with SLF1, and initially they were thought not to be involved in pollen specificity. However, further studies of SLF1 suggested that it is not the only pollen specificity gene. Indeed, it has recently been shown that two previously identified SLF-like genes in P. inflata (now named SLF2 and SLF3) and a yet unknown number of additional SLF-like genes (named SLF4, SLF5, etc.) collaboratively function to control pollen specificity. The significance and implications of this new finding are discussed.

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Expression of 10 S-Class SLF-like Genes in Nicotiana alata Pollen and Its Implications for Understanding the Pollen Factor of the S Locus

Cited by 50 publications

References 51 publications

RNase-Based Self-Incompatibility: Puzzled byPollen S

RNase-Based Self-Incompatibility: Puzzled byPollen S

Protein Interactions in S-RNase-Based Gametophytic Self-Incompatibility

Self‐incompatibility in Petunia: a self/nonself‐recognition mechanism employing S‐locus F‐box proteins and S‐RNase to prevent inbreeding

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