Sporophytic self-incompatibility genes and mating system variation in Arabis alpina

Tedder, Andrew; Ansell, Stephen W.; Lao, Xintian; Vogel, Johannes; Mable, Barbara K.

doi:10.1093/aob/mcr157

Cited by 55 publications

(93 citation statements)

References 110 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The 200 bp sequences produced similar resolution in phylogenetic clustering as previous studies using 600 bp (Tedder et al, 2011) and resulted in consistent patterns of polymorphism expected for dominant and recessive alleles at SRK. Examination of relative frequency distributions also generally met theoretical expectations but indicated no obvious differences in diversity between ploidy levels.…”

Section: Objectives 1 and 2: Diversity And Allele Sharing Of Srk In Dsupporting

confidence: 63%

“…Other alleles predicted to be unlinked to the SI phenotype were also resolved by the clustering analysis but none of these would have been assigned as SRK-like based on BLAST (Table 6; Supplementary Table 10). One published allele (AlySRK32) whose phylogenetic position and dominance have not been resolved in previous studies was pulled out from six accessions; based on the length of its branch to other SRK sequences, it has been predicted to be unlinked to the SI phenotype (Tedder et al, 2011). AlySRK47 (found in four of the accessions) is also predicted to be unlinked, based on its phylogenetic position relative to linked sequences.…”

Section: Objective 4: Copy Number Variation In the Srk-related Gene Fmentioning

confidence: 99%

“…For example, genes controlling sporophytically controlled self-incompatibility (SI) in plants have been found to be missing from resequencing assemblies because they are too divergent from the reference genome and so trawling in the unassembled reads is necessary to characterize these highly polymorphic genes (Mable et al, 2017). Both male and female components are members of large gene families that show extensive trans-specific polymorphism, with highly similar alleles shared across species and even genera but high divergence between functional specificities (Schierup et al, 1998;Paetsch et al, 2006;Castric and Vekemans, 2007;Busch et al, 2008;Guo et al, 2011;Tedder et al, 2011;Leducq et al, 2014). The gene controlling female specificity (S-receptor kinase, SRK) is part of a large family of receptor kinases, which evolved through a complex history of gene duplication and loss, followed by gene fission and fusion (Xing et al, 2013).…”

Section: Introduction Background and Aimsmentioning

confidence: 99%

See 2 more Smart Citations

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

et al. 2018

View full text Add to dashboard Cite

Comparative genomics of non-model organisms has resurrected whole genome duplication (WGD) from being viewed as a somewhat obscure process that happens in plants to a primary driver of eukaryotic diversification. The shadow of past ploidy increases has left a strong signature of duplicated genes organized into gene families, even in small genomes that have undergone effectively complete rediploidization. Nevertheless, despite continually advancing technologies and bioinformatics pipelines, resolving the fate of duplicate genes remains a substantial challenge. For example, many important recognition processes are driven not only by allelic expansion through retention of duplicates but also by diversification and copy number variation. This creates technical difficulties with assembly to reference genomes and accurate interpretation of homology. Thus, relatively little is known about the impacts of recent polyploidization and hybridization on the evolution of gene families under selective forces that maintain diversity, such as balancing selection. Here we use a complex of species and ploidy levels in the genus Arabidopsis (A. lyrata and A. arenosa) as a model to investigate the evolutionary dynamics of a large and complicated gene family known to be under strong balancing selection: the receptor-like kinases, which include the female component of genetically controlled self-incompatibility. Specifically, we question: (1) How does diversity of S-receptor kinase (SRK) alleles in tetraploids compare to that in their close diploid relatives? (2) Is there increased trans-specific polymorphism (i.e., sharing of alleles that transcend speciation, characteristic of balancing selection) in tetraploids compared to diploids due to the higher number of copies they carry? (3) Do these highly variable loci show evidence of introgression among extant species/ploidy levels within or outside known zones of hybridization? (4) Is there evidence for copy number variation among paralogs? We use this example to highlight specific issues to consider when interpreting gene family evolution, particularly in relation to polyploids but also more generally in diploids. We conclude with recommendations for strategies to address the challenges of resolving such complex loci in the future, using advances in deep sequencing approaches.

show abstract

Section: Objectives 1 and 2: Diversity And Allele Sharing Of Srk In Dsupporting

confidence: 63%

Section: Objective 4: Copy Number Variation In the Srk-related Gene Fmentioning

confidence: 99%

Section: Introduction Background and Aimsmentioning

confidence: 99%

See 1 more Smart Citation

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

et al. 2018

View full text Add to dashboard Cite

show abstract

“…Bars ¼ 10 mm. siliques containing seed (Mable et al, 2005;Bechsgaard et al, 2006;Tedder et al, 2011). In Brassica oleracea, instead of 20 to 25 seeds per pod produced in compatible pollinations, manual self-pollination of selfincompatible stigmas produces, on average, 0.15 to 0.25 seeds per pod (Nasrallah and Wallace, 1968;Nakanishi and Hinata, 1975) or as much as one to two seeds per pod (Thompson and Taylor, 1971 We previously reported that SRKb-SCRb transformants of the Col-0 accession produce amounts of seed equivalent to those produced by untransformed plants (Nasrallah et al, 2002(Nasrallah et al, , 2004Tantikanjana et al, 2009;Tantikanjana and Nasrallah, 2012), and this phenotype was observed in the Indriolo et al (2014) study.…”

Section: Robust Si In Srkb-scrb Transformants Of the Sha Accession Inmentioning

confidence: 99%

Robust Self-Incompatibility in the Absence of a Functional ARC1 Gene in Arabidopsis thaliana

Nasrallah

2014

Plant Cell

View full text Add to dashboard Cite

Self-incompatibility (SI) is the primary determinant of the outbreeding mode of sexual reproduction in the Brassicaceae. All Arabidopsis thaliana accessions analyzed to date carry mutations that disrupt SI functions by inactivating the SI specificitydetermining S locus or SI modifier loci. S-locus genes isolated from self-incompatible close relatives of A. thaliana restore robust SI in several accessions that harbor only S-locus mutations and confer transient SI in accessions that additionally harbor mutations at modifier loci. Self-incompatible transgenic A. thaliana plants have proved to be valuable for analysis of the recognition and signaling events that underlie SI in the Brassicaceae. Here, we review results demonstrating that S-locus genes are necessary and sufficient for SI signaling and for restoration of a strong and developmentally stable SI phenotype in several accessions of A. thaliana. The data indicate that introduction of a functional E3 ligase-encoding ARC1 gene, which is deleted in all accessions that have been analyzed to date, is not required for SI signaling leading to inhibition of self pollen or for reversion of A. thaliana to its fully self-incompatible ancestral state.It is well established that specific pollen recognition in the self-incompatibility (SI) response of the Brassicaceae is determined by allele-specific interactions that occur at the stigma surface between two highly polymorphic proteins encoded in the S locus: the S-locus receptor kinase SRK and its ligand, the S-locus cysteine-rich protein SCR. Arabidopsis thaliana lacks a functional SI system and harbors nonfunctional S-locus variants that contain defective alleles of the SRK and/or SCR genes (Kusaba et al., 2001; ShermanBroyles et al., 2007;Tang et al., 2007;Shimizu et al., 2008;Boggs et al., 2009a;Tsuchimatsu et al., 2010;Dwyer et al., 2013). Despite being highly self-fertile, A. thaliana can be made to express SI upon transformation with functional SRK-SCR gene pairs isolated from its self-incompatible close relatives (Nasrallah et al., 2002(Nasrallah et al., , 2004Boggs et al., 2009aBoggs et al., , 2009b. The first transfer of the SI trait into A. thaliana was achieved using the SRKbSCRb gene pair isolated from the Sb locus of Arabidopsis lyrata (Kusaba et al., 2001;Nasrallah et al., 2002Nasrallah et al., , 2004 (Gu et al., 1998), and it was subsequently inferred to be required for SI because downregulation of the ARC1 gene in B. napus (Stone et al., 1999) and A. lyrata (Indriolo et al., 2012), as well as overexpression of ARC1's target, Exo70A1, in B. napus (Samuel et al., 2009), caused partial breakdown of the SI response. However, the involvement of the proposed SRK-ARC1-Exo70A1 pathway in SI has been questioned because the ARC1 gene was found to be deleted in all A. thaliana accessions analyzed to date (Kitashiba et al., 2011;Indriolo et al., 2012), including those in which the SRKb-SCRb transgenes confer a strong SI phenotype (Kitashiba et al., 2011). Additionally, overexpression of Exo70A1 did not cause weakenin...

show abstract

“…Some (inconclusive) empirical evidence for this was found in S. carolinense, where three out of five alleles without a strong genetic load were part of a clade that exhibits strong diversification, and one out of two alleles with a strong load was positioned on a long terminal branch (Stone, 2004). In sporophytic systems, relationships among S-alleles normally have low bootstrap support (Prigoda et al, 2005;Tedder et al, 2011). Moreover, comprehensive sampling of alleles is difficult (for example, Mable et al, 2003) which may compromise robust interpretation of diversification patterns (for example if close relatives of some alleles have not been sampled).…”

Section: Genetic Load Attributable To the S-locusmentioning

confidence: 99%

Inbreeding depression in self-incompatible North-American Arabidopsis lyrata: disentangling genomic and S-locus-specific genetic load

et al. 2012

View full text Add to dashboard Cite

Newly formed selfing lineages may express recessive genetic load and suffer inbreeding depression. This can have a genome-wide genetic basis, or be due to loci linked to genes under balancing selection. Understanding the genetic architecture of inbreeding depression is important in the context of the maintenance of self-incompatibility and understanding the evolutionary dynamics of S-alleles. We addressed this using North-American subspecies of Arabidopsis lyrata. This species is normally self-incompatible and outcrossing, but some populations have undergone a transition to selfing. The goals of this study were to: (1) quantify the strength of inbreeding depression in North-American populations of A. lyrata; and (2) disentangle the relative contribution of S-linked genetic load compared with overall inbreeding depression. We enforced selfing in self-incompatible plants with known S-locus genotype by treatment with CO 2 , and compared the performance of selfed vs outcrossed progeny. We found significant inbreeding depression for germination rate (d ¼ 0.33), survival rate to 4 weeks (d ¼ 0.45) and early growth (d ¼ 0.07), but not for flowering rate. For two out of four S-alleles in our design, we detected significant S-linked load reflected by an under-representation of S-locus homozygotes in selfed progeny. The presence or absence of S-linked load could not be explained by the dominance level of S-alleles. Instead, the random nature of the mutation process may explain differences in the recessive deleterious load among lineages.

show abstract

Sporophytic self-incompatibility genes and mating system variation in Arabis alpina

Abstract: The results strongly suggest that, as with other species in the Brassicaceae, A. alpina has a sporophytic SI system but shows variation in the strength of SI within and between populations.

Cited by 55 publications

References 110 publications

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

Robust Self-Incompatibility in the Absence of a Functional ARC1 Gene in Arabidopsis thaliana

Inbreeding depression in self-incompatible North-American Arabidopsis lyrata: disentangling genomic and S-locus-specific genetic load

Contact Info

Product

Resources

About