Detecting Site-Specific Physicochemical Selective Pressures: Applications to the Class I HLA of the Human Major Histocompatibility Complex and the SRK of the Plant Sporophytic Self-Incompatibility System

Sainudiin, Raazesh; Wong, Wendy S. W.; Yogeeswaran, Krithika; Nasrallah, June B.; Yang, Ziheng; Nielsen, Rasmus

doi:10.1007/s00239-004-0153-1

Cited by 72 publications

(81 citation statements)

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“…This approach calculates posterior probabilities of positive selection (as determined from the ratio of nonsynonymous substitution per nonsynonymous site to synonymous substitution per synonymous site) for individual codons, using an empirical Bayesian approach. The maximum-likelihood tree topology for the Lal2 sequences was first obtained using the branch-andbound algorithm as implemented in PAUP for the Kimura twoparameter model (Kimura 1980;Swofford 2002), and the selection analysis was conducted using the CODEML program of Yang (1997), as decribed by Sainudiin et al (2005). The number of Lal2 sequences available to us for analysis (10 sequences) was much smaller than those analyzed by Sainudiin et al (2005), who used the same method to detect specific classes of positive selection (e.g., polar-or volume-changing amino acid substitutions) in SRK sequences of Brassica and Arabidopsis.…”

Section: Methodsmentioning

confidence: 99%

“…The Lal2 sequences were examined for evidence of balancing selection and, in particular, evidence of ''hypervariable'' regions that have been proposed to harbor sites controlling S-allele recognition (Sainudiin et al 2005). Figure 5 shows a sliding-window analysis of nucleotide variability calculated for the alignment of long Lal2 sequences with alleles of SRK sampled in Arabidopsis and class I alleles in Brassica.…”

Section: Cross-incompatibility and Interactions Among Inferred S-allementioning

confidence: 99%

“…The maximum-likelihood tree topology for the Lal2 sequences was first obtained using the branch-andbound algorithm as implemented in PAUP for the Kimura twoparameter model (Kimura 1980;Swofford 2002), and the selection analysis was conducted using the CODEML program of Yang (1997), as decribed by Sainudiin et al (2005). The number of Lal2 sequences available to us for analysis (10 sequences) was much smaller than those analyzed by Sainudiin et al (2005), who used the same method to detect specific classes of positive selection (e.g., polar-or volume-changing amino acid substitutions) in SRK sequences of Brassica and Arabidopsis. Hence, our focus was on evidence of any type of positively selected amino acid substitution, regardless of the particular type of property-changing characteristic.…”

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confidence: 99%

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Molecular Characterization of Lal2, an SRK-Like Gene Linked to the S-Locus in the Wild Mustard Leavenworthia alabamica

2008

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Single-locus sporophytic self-incompatibility inhibits inbreeding in many members of the mustard family (Brassicaceae). To investigate the genetics of self-incompatibility in the wild mustard Leavenworthia alabamica, diallel crosses were conducted between full siblings. Patterns of incompatibility were consistent with the action of single-locus sporophytic self-incompatibility. DNA sequences related to S-locus receptor kinase (SRK), the gene involved in self-pollen recognition in mustards, were cloned and sequenced. A single sequence with high identity to SRK and several other groups of sequences (Lal1, Lal2, Lal3, Lal8, and Lal14) were isolated from L. alabamica. We propose that either Lal2 sequences are divergent alleles of SRK or Lal2 is in tight linkage with SRK because (1) Lal2 alleles cosegregate with S-alleles inferred from dialleles in all 97 cases tested in five families; (2) Lal2 sequences are highly diverse at both synonymous and nonsynonymous sites and exhibit patterns of selective constraint similar to those observed at SRK in Brassica and Arabidopsis; and (3) transcripts of one Lal2 allele were detected in leaves and the styles of open flowers, but were most abundant in the stigmas of maturing buds. We discuss the utility of the S-linked polymorphism at Lal2 for studying the evolutionary forces acting on self-incompatibility in Leavenworthia. I NBREEDING avoidance is thought to have contributed to the evolution and maintenance of genetically controlled self-incompatibility (SI) systems in flowering plants (Richards 1986). In SI systems, plants that share alleles at the self-incompatibility locus (i.e., S-locus) are incapable of producing seed. SI evolved early during the diversification of angiosperms, and it has been proposed that this system may have contributed to the success of flowering plants by contributing to the maintenance of population-genetic variation (Darlington and Mather 1949; Kohn 2001, 2006). SI systems are diverse in terms of the molecular mechanisms underlying self-recognition, as well as in associated floral traits that promote pollen transfer between compatible mates (Hiscock and Tabah 2003). A feature of most SI systems is the presence of a single linked complex of genes (or more rarely, several unlinked loci) that code for proteins involved in the recognition and rejection of self-pollen. Since individuals that possess rare S-alleles have a strong fertility advantage, negative frequency-dependent selection is expected to maintain a large amount of genetic diversity at S-loci in natural populations. Indeed, these loci are among the most polymorphic in eukaryotic organisms (Wright 1939;Lawrence 2000).Single-locus sporophytic SI has been studied in a number of genera in the mustard family (Brassicaceae) (Bateman 1954(Bateman , 1955Thompson 1957;Lloyd 1967;Sampson 1967;Schierup et al. 2001). Molecular genetic characterization of SI in Brassica and Arabidopsis species has shown that the S-locus consists of a tightly linked cluster of genes encoding proteins that function...

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Section: Methodsmentioning

confidence: 99%

Section: Cross-incompatibility and Interactions Among Inferred S-allementioning

confidence: 99%

mentioning

confidence: 99%

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Molecular Characterization of Lal2, an SRK-Like Gene Linked to the S-Locus in the Wild Mustard Leavenworthia alabamica

2008

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“…8). The variability in this ''linker'' region among SRK variants (19,20) suggests that the exact spacing of LLD1 and LLD2 is not critical for SRK function.…”

Section: Identification Of Structural Modules Within Esrk By Homologymentioning

confidence: 99%

“…The eSRK PAN APPLE domain is contained within the so-called C-terminal variable region (VR) (19,20), which is one of four regions that exhibit extensive variability among SRK alleles (SI Fig. 8).…”

Section: Identification Of Ligand-independent Dimerization Domains Inmentioning

confidence: 99%

Structural modules for receptor dimerization in the S -locus receptor kinase extracellular domain

Naithani¹,

Chookajorn²,

Ripoll

et al. 2007

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

Self Cite

109

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The highly polymorphic S-locus receptor kinase (SRK) is the stigma determinant of specificity in the self-incompatibility response of the Brassicaceae. SRK spans the plasma membrane of stigma epidermal cells, and it is activated in an allele-specific manner on binding of its extracellular region (eSRK) to its cognate pollen coat-localized S-locus cysteine-rich (SCR) ligand. SRK, like several other receptor kinases, forms dimers in the absence of ligand. To identify domains in SRK that mediate ligand-independent dimerization, we assayed eSRK for self-interaction in yeast. We show that SRK dimerization is mediated by two regions in eSRK, primarily by a C-terminal region inferred by homology modeling/fold recognition techniques to assume a PAN APPLE-like structure, and secondarily by a region containing a signature sequence of the S-domain gene family, which might assume an EGF-like structure. We also show that eSRK exhibits a marked preference for homodimerization over heterodimerization with other eSRK variants and that this preference is mediated by a small, highly variable region within the PAN APPLE domain. Thus, the extensive polymorphism exhibited by the eSRK not only determines differential affinity toward the SCR ligand, as has been assumed thus far, but also underlies a previously unrecognized allelic specificity in SRK dimerization. We propose that preference for SRK homodimerization explains the codominance exhibited by a majority of SRKs in the typically heterozygous stigmas of self-incompatible plants, whereas an increased propensity for heterodimerization combined with reduced affinity of heterodimers for cognate SCRs might underlie the dominant-recessive or mutual weakening relationships exhibited by some SRK allelic pairs.self-incompatibility ͉ ligand-independent receptor dimerization ͉ yeast two-hybrid T he S-locus receptor kinase (SRK) is a single-pass integral plasma membrane protein of the stigma epidermis that functions in the recognition and rejection of self-related pollen in self-incompatible members of the Brassicaceae (reviewed in refs. 1 and 2). The SRK receptor and its pollen-coat localized ligand, the S-locus cysteine-rich protein (SCR) (1), also designated SP-11 (2), are encoded by tightly linked and highly polymorphic genes within the S-locus haplotype. Specificity in the self-incompatibility response derives from allele-specific SRK-SCR interaction (3, 4). On self-pollination, the binding of SCR to the extracellular domain of its cognate SRK activates the receptor and triggers an intracellular signaling cascade that leads to arrest of ''self'' pollen tubes. In contrast, pollen tube growth in cross-pollinations proceeds unimpeded because ''nonself'' SCR cannot bind SRK. In view of this high degree of specificity in the affinity of SRK for its SCR ligand, the extensive polymorphisms exhibited by the SRK extracellular region (eSRK) have heretofore been considered in the context of specificity in the SRK-SCR interaction.The eSRK does more than interact with SCR, however. SRK forms oligo...

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Self-Incompatibility in the Brassicaceae

Nasrallah

2010

Genetics and Genomics of the Brassicaceae

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Detecting Site-Specific Physicochemical Selective Pressures: Applications to the Class I HLA of the Human Major Histocompatibility Complex and the SRK of the Plant Sporophytic Self-Incompatibility System

Cited by 72 publications

References 50 publications

Molecular Characterization of Lal2, an SRK-Like Gene Linked to the S-Locus in the Wild Mustard Leavenworthia alabamica

Molecular Characterization of Lal2, an SRK-Like Gene Linked to the S-Locus in the Wild Mustard Leavenworthia alabamica

Structural modules for receptor dimerization in the S -locus receptor kinase extracellular domain

Self-Incompatibility in the Brassicaceae

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