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Evolutionary consequences of dominance at the Brassicaceae self-incompatibility locus
Stockholm University, Faculty of Science, Department of Ecology, Environment and Plant Sciences.
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Self-incompatibility (SI) is a genetic mechanism that allows plants to enforce outcrossing by rejecting self-pollen and pollen from close relatives. In the Brassicaceae, SI is sporophytic and controlled by the self-incompatibility locus (S-locus). The S-locus harbors two tightly linked genes SRK and SCR, which encode the female and male SI specificity determinants, respectively. S-locus heterozygotes often only express the S-specificity of the more dominant allele, and at the pollen level such dominance relationships are mediated by small RNAs (sRNAs). The S-locus is thus an example of a locus under strong balancing selection, where dominance modifiers have evolved.

In this thesis, I investigate the consequences of S-locus dominance for plant mating system evolution and allopolyploid speciation. I further investigate evolutionary conservation and sequence-level effects of dominance relationships among S-alleles. For this purpose, I used the crucifer genus Capsella as a model system.

First, I demonstrated that targeted long-read sequencing results in structurally accurate assemblies of full-length S-haplotype sequences, and that indel errors in such assemblies can be corrected using short reads. Second, I investigated the genetic basis of loss of SI, the first step in the evolution of self-fertilisation, in the self-compatible (SC) Capsella orientalis. I found that loss of SI was dominant and mapped to the S-locus, where C. orientalis harbored a fixed coding frameshift deletion in SCR that is likely to lead to loss of male specificity. I further identified a sRNA-based dominance modifier that is associated with dominant suppression of recessive SCR alleles. Taken together, these results suggest that loss of SI in C. orientalis involved a dominant S-haplotype, suggesting that dominant haplotypes may be favored under conditions that select for loss of SI. Third, I show that a dominant S-haplotype may also have contributed to the shift to SC in the widespread allotetraploid Capsella bursa-pastoris. Fourth, I showed that dominance relationships at the S-locus are largely conserved between the SI outcrossing species C. grandiflora and Arabidopsis halleri which diverged ~8 Mya. I also found that dominant S-haplotypes accumulate more transposable elements than recessive S-haplotypes, in line with expected sequence-level consequences of S-locus dominance. In sum, this thesis provides new insights into the broad conservation of dominance hierarchies at the Brassicaceae S-locus, and the role of dominant S-alleles in allopolyploid speciation and plant mating system shifts.

Place, publisher, year, edition, pages
Stockholm: Department of Ecology, Environment and Plant Sciences, Stockholm University , 2020. , p. 50
Keywords [en]
Capsella, mating system shift, self-fertilization, self-incompatibility, small RNA, dominance, Arabidopsis, population genetics, genomics, gene expression
National Category
Evolutionary Biology Genetics
Research subject
Ecology and Evolution
Identifiers
URN: urn:nbn:se:su:diva-179377ISBN: 978-91-7911-078-9 (print)ISBN: 978-91-7911-079-6 (electronic)OAI: oai:DiVA.org:su-179377DiVA, id: diva2:1415821
Public defence
2020-05-15, digitally via video conference (Zoom), public link shared at www.su.se/deep in connection with nailing of the thesis, Stockholm, 13:00 (English)
Opponent
Supervisors
Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 3: Manuscript. Paper 4: Manuscript.

Available from: 2020-04-22 Created: 2020-03-19 Last updated: 2020-05-25Bibliographically approved
List of papers
1. Targeted Long-Read Sequencing of a Locus Under Long-Term Balancing Selection in Capsella
Open this publication in new window or tab >>Targeted Long-Read Sequencing of a Locus Under Long-Term Balancing Selection in Capsella
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2018 (English)In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 8, no 4, p. 1327-1333Article in journal (Refereed) Published
Abstract [en]

Rapid advances in short-read DNA sequencing technologies have revolutionized population genomic studies, but there are genomic regions where this technology reaches its limits. Limitations mostly arise due to the difficulties in assembly or alignment to genomic regions of high sequence divergence and high repeat content, which are typical characteristics for loci under strong long-term balancing selection. Studying genetic diversity at such loci therefore remains challenging. Here, we investigate the feasibility and error rates associated with targeted long-read sequencing of a locus under balancing selection. For this purpose, we generated bacterial artificial chromosomes (BACs) containing the Brassicaceae S-locus, a region under strong negative frequency-dependent selection which has previously proven difficult to assemble in its entirety using short reads. We sequence S-locus BACs with single-molecule long-read sequencing technology and conduct de novo assembly of these S-locus haplotypes. By comparing repeated assemblies resulting from independent long-read sequencing runs on the same BAC clone we do not detect any structural errors, suggesting that reliable assemblies are generated, but we estimate an indel error rate of 5.7x10(-5). A similar error rate was estimated based on comparison of Illumina short-read sequences and BAC assemblies. Our results show that, until de novo assembly of multiple individuals using long-read sequencing becomes feasible, targeted long-read sequencing of loci under balancing selection is a viable option with low error rates for single nucleotide polymorphisms or structural variation. We further find that short-read sequencing is a valuable complement, allowing correction of the relatively high rate of indel errors that result from this approach.

Keywords
single-molecule real-time sequencing, bacterial artificial chromosomes, sequencing errors, assembly, self-incompatibility locus, Capsella, Brassicaceae
National Category
Biological Sciences
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-156060 (URN)10.1534/g3.117.300467 (DOI)000428693600022 ()29476024 (PubMedID)
Available from: 2018-05-24 Created: 2018-05-24 Last updated: 2020-04-03Bibliographically approved
2. Genetic basis and timing of a major mating system shift in Capsella
Open this publication in new window or tab >>Genetic basis and timing of a major mating system shift in Capsella
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2019 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 224, no 1, p. 505-517Article in journal (Refereed) Published
Abstract [en]

A crucial step in the transition from outcrossing to self-fertilization is the loss of genetic self-incompatibility (SI). In the Brassicaceae, SI involves the interaction of female and male specificity components, encoded by the genes SRK and SCR at the self-incompatibility locus (S-locus). Theory predicts that S-linked mutations, and especially dominant mutations in SCR, are likely to contribute to loss of SI. However, few studies have investigated the contribution of dominant mutations to loss of SI in wild plant species. Here, we investigate the genetic basis of loss of SI in the self-fertilizing crucifer species Capsella orientalis, by combining genetic mapping, long-read sequencing of complete S-haplotypes, gene expression analyses and controlled crosses. We show that loss of SI in C. orientalis occurred S-locus. We identify a fixed frameshift deletion in the male specificity gene SCR and confirm loss of male SI specificity. We further identify an S-linked small RNA that is predicted to cause dominance of self-compatibility. Our results agree with predictions on the contribution of dominant S-linked mutations to loss of SI, and thus provide new insights into the molecular basis of mating system transitions.

Keywords
Capsella, dominance modifier, long-read sequencing, parallel evolution, plant mating system shift, self-compatibility, S-locus, small RNA
National Category
Biological Sciences
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-173013 (URN)10.1111/nph.16035 (DOI)000479176400001 ()31254395 (PubMedID)
Available from: 2019-10-07 Created: 2019-10-07 Last updated: 2020-04-03Bibliographically approved
3. Evolutionary stability of genetic dominance in the Brassicaceae self-incompatibility system
Open this publication in new window or tab >>Evolutionary stability of genetic dominance in the Brassicaceae self-incompatibility system
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

The question of whether dominance-recessivity relationships between associated alleles in a diploid genotype can evolve independently from the activity of the gene products encoded has been a hot topic in evolutionary genetics throughout the 20th century. In hermaphroditic plants of the Brassicaceae family, the self-incompatibility locus (S-locus) confers the ability to recognize and reject self-pollen. Dominance relationships between self-incompatibility alleles (S-alleles) in pollen are governed by small RNA (sRNA) transcriptional regulators produced by dominant S-alleles and their target sites on recessive S-alleles. These regulators and their target sites segregate together with but are distinct from the genes encoding self-recognition specificities themselves, providing the opportunity for dominance to evolve independently from the recognition specificities. Dominance interactions between the many segregating S-alleles have been described in the distantly related Arabidopsis and Brassica, but little is known about the evolutionary stability of the dominance networks given that divergent sets of S-alleles are segregating in these two genera. In this study, we take advantage of the extensive trans-specific sharing of S-haplotypes between the self-incompatible species Capsella grandiflora and Arabidopsis halleri to investigate the conservation of S-locus dominance relationships across their approximately 8 million years of divergence. For this purpose, we use a combination of controlled crosses and full-length long-read sequencing of S-haplotypes. We find that the dominance network among six C. grandiflora S-alleles has a largely parallel structure to that among their orthologous S-alleles in A. halleri. We test the theoretical prediction that dominant S-alleles should be found at lower population frequencies using a large sample of a natural C. grandiflora population. Finally, we test whether dominant C. grandiflora S-alleles show increased accumulation of repeats (TEs) than recessive S-alleles, as expected due to their lower chance of recombination and lower effective population sizes. Our results contribute to an improved understanding of the maintenance of dominance relationships at loci under balancing selection.

Keywords
Self-incompatibility, dominance, Capsella, Arabidopsis, SCR, sRNA
National Category
Evolutionary Biology Genetics
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-179374 (URN)
Funder
Science for Life Laboratory - a national resource center for high-throughput molecular bioscienceSwedish Research Council, 621-2013-4320EU, European Research Council, 648321
Available from: 2020-03-18 Created: 2020-03-18 Last updated: 2020-04-20Bibliographically approved
4. On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae)
Open this publication in new window or tab >>On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae)
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Polyploidy, or whole genome duplication, is common in plants and can contribute to rapid evolution of reproductive barriers and thus speciation. An important barrier to polyploid establishment and persistence is a lack of compatible mates. Because self-compatibility alleviates this problem, it has long been hypothesized that there should be an association between polyploidy and self-compatibility (SC), but empirical support for this prediction has been mixed. Here, we investigate whether the molecular makeup of the Brassicaceae self-incompatibility (SI) system, and specifically dominance relationships among S-haplotypes mediated by small RNAs, could facilitate the loss of SI in allopolyploid crucifers. We focus on the allotetraploid species Capsella bursa-pastoris, which formed ~300 kya by hybridization and whole genome duplication involving progenitors from the lineages of Capsella orientalis and Capsella grandiflora. We conduct targeted long-read sequencing to assemble and analyze eight full-length S-locus haplotypes, representing both homeologous subgenomes of C. bursa-pastoris. We further analyze small RNA (sRNA) sequencing data from flower buds to identify candidate dominance modifiers. We find that the C. orientalis-derived S-haplotypes of C. bursa-pastoris harbor truncated versions of the male SI specificity gene SCR and express a conserved sRNA-based candidatedominance modifier with a target in the C. grandiflora-derivedS-haplotype. These results suggest that pollen-level dominance may have facilitated loss of SI in C. bursa-pastoris. Finally, we report on the spontaneous somatic tetraploidization and production of tetraploid offspring after a wide cross between C. orientalis and C. grandiflora, and discuss the implications of this finding on the mode of formation of this widespread weed. 

Keywords
allopolyploid, artificial hybrid, dominance modifier, long-read sequencing, mating system, polyploidy, self-fertilization, S-locus
National Category
Evolutionary Biology Genetics
Research subject
Ecology and Evolution
Identifiers
urn:nbn:se:su:diva-179375 (URN)
Funder
Swedish Research Council, 621-2013-4320Science for Life Laboratory - a national resource center for high-throughput molecular bioscience
Available from: 2020-03-18 Created: 2020-03-18 Last updated: 2020-04-20Bibliographically approved

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