Evolutionary pathways for the generation of new self-incompatibility haplotypes in a non-self recognition system

AbstractSelf-incompatibility (SI) is a genetically based recognition system that functions to prevent self-fertilization and mating among related plants. An enduring puzzle in SI is how the high diversity observed in nature arises and is maintained. Based on the underlying recognition mechanism, SI can be classified into two main groups: self- and non-self recognition. Most work has focused on diversification within self-recognition systems despite expected differences between the two groups in the evolutionary pathways and outcomes of diversification. Here, we use a deterministic population genetic model and stochastic simulations to investigate how novel S-haplotypes evolve in a gametophytic non-self recognition (SRNase/S Locus F-box (SLF)) SI system. For this model the pathways for diversification involve either the maintenance or breakdown of SI and can vary in the order of mutations of the female (SRNase) and male (SLF) components. We show analytically that diversification can occur with high inbreeding depression and self-pollination, but this varies with evolutionary pathway and level of completeness (which determines the number of potential mating partners in the population), and in general is more likely for lower haplotype number. The conditions for diversification are broader in stochastic simulations of finite population size. However, the number of haplotypes observed under high inbreeding and moderate to high self-pollination is less than that commonly observed in nature. Diversification was observed through pathways that maintain SI as well as through self-compatible intermediates. Yet the lifespan of diversified haplotypes was sensitive to their level of completeness. By examining diversification in a non-self recognition SI system, this model extends our understanding of the evolution and maintenance of haplotype diversity observed in a recognition system common in flowering plants.

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Evolutionary Pathways for the Generation of New Self-Incompatibility Haplotypes in a Non-self Recognition System

Genetics ◽

10.1534/genetics.118.300748 ◽

2018 ◽

pp. genetics.300748.2018 ◽

Cited By ~ 6

Author(s):

Katarína Boďová ◽

Tadeas Priklopil ◽

David L. Field ◽

Nicholas H. Barton ◽

Melinda Pickup

Keyword(s):

Recognition System ◽

Self Incompatibility ◽

Self Recognition ◽

Evolutionary Pathways

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Small peptide–mediated self-recognition prevents cannibalism in predatory nematodes

Science ◽

10.1126/science.aav9856 ◽

2019 ◽

Vol 364 (6435) ◽

pp. 86-89 ◽

Cited By ~ 22

Author(s):

James W. Lightfoot ◽

Martin Wilecki ◽

Christian Rödelsperger ◽

Eduardo Moreno ◽

Vladislav Susoy ◽

...

Keyword(s):

Hypervariable Region ◽

Recognition System ◽

Natural World ◽

Single Amino Acid ◽

Biological Processes ◽

Small Peptide ◽

Recognition Mechanism ◽

Self Recognition ◽

C Terminus ◽

Molecular Machinery

Self-recognition is observed abundantly throughout the natural world, regulating diverse biological processes. Although ubiquitous, often little is known of the associated molecular machinery, and so far, organismal self-recognition has never been described in nematodes. We investigated the predatory nematode Pristionchus pacificus and, through interactions with its prey, revealed a self-recognition mechanism acting on the nematode surface, capable of distinguishing self-progeny from closely related strains. We identified the small peptide SELF-1, which is composed of an invariant domain and a hypervariable C terminus, as a key component of self-recognition. Modifications to the hypervariable region, including single–amino acid substitutions, are sufficient to eliminate self-recognition. Thus, the P. pacificus self-recognition system enables this nematode to avoid cannibalism while promoting the killing of competing nematodes.

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Cullin1-P is an Essential Component of Non-Self Recognition System in Self-Incompatibility inPetunia

Plant and Cell Physiology ◽

10.1093/pcp/pcw152 ◽

2016 ◽

Vol 57 (11) ◽

pp. 2403-2416 ◽

Cited By ~ 8

Author(s):

Ken-ichi Kubo ◽

Mai Tsukahara ◽

Sota Fujii ◽

Kohji Murase ◽

Yuko Wada ◽

...

Keyword(s):

Recognition System ◽

Self Incompatibility ◽

Essential Component ◽

Self Recognition

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On the Origin of Self-Incompatibility Haplotypes: Transition Through Self-Compatible Intermediates

Genetics ◽

10.1093/genetics/157.4.1805 ◽

2001 ◽

Vol 157 (4) ◽

pp. 1805-1817

Author(s):

Marcy K Uyenoyama ◽

Yu Zhang ◽

Ed Newbigin

Keyword(s):

Evolutionary Analysis ◽

Self Incompatibility ◽

S Locus ◽

Pollen Type ◽

Evolutionary Pathway ◽

Loss Of Self ◽

Inhibiting Factor ◽

Self Recognition ◽

Relative Viability ◽

Unknown Gene

AbstractSelf-incompatibility (SI) in flowering plants entails the inhibition of fertilization by pollen that express specificities in common with the pistil. In species of the Solanaceae, Rosaceae, and Scrophulariaceae, the inhibiting factor is an extracellular ribonuclease (S-RNase) secreted by stylar tissue. A distinct but as yet unknown gene (provisionally called pollen-S) appears to determine the specific S-RNase from which a pollen tube accepts inhibition. The S-RNase gene and pollen-S segregate with the classically defined S-locus. The origin of a new specificity appears to require, at minimum, mutations in both genes. We explore the conditions under which new specificities may arise from an intermediate state of loss of self-recognition. Our evolutionary analysis of mutations that affect either pistil or pollen specificity indicates that natural selection favors mutations in pollen-S that reduce the set of pistils from which the pollen accepts inhibition and disfavors mutations in the S-RNase gene that cause the nonreciprocal acceptance of pollen specificities. We describe the range of parameters (rate of receipt of self-pollen and relative viability of inbred offspring) that permits the generation of a succession of new specificities. This evolutionary pathway begins with the partial breakdown of SI upon the appearance of a mutation in pollen-S that frees pollen from inhibition by any S-RNase presently in the population and ends with the restoration of SI by a mutation in the S-RNase gene that enables pistils to reject the new pollen type.

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The identification of the Rosa S-locus and implications on the evolution of the Rosaceae gametophytic self-incompatibility systems

Scientific Reports ◽

10.1038/s41598-021-83243-8 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

J. Vieira ◽

J. Pimenta ◽

A. Gomes ◽

J. Laia ◽

S. Rocha ◽

...

Keyword(s):

Single Gene ◽

Expression Patterns ◽

Recognition System ◽

Acid Sites ◽

Self Incompatibility ◽

Self Recognition ◽

Phylogenetic Lineages ◽

Low Coverage ◽

Ornamental Traits ◽

Practical Implications

AbstractIn Rosaceae species, two gametophytic self-incompatibility (GSI) mechanisms are described, the Prunus self-recognition system and the Maleae (Malus/Pyrus/Sorbus) non-self- recognition system. In both systems the pistil component is a S-RNase gene, but from two distinct phylogenetic lineages. The pollen component, always a F-box gene(s), in the case of Prunus is a single gene, and in Maleae there are multiple genes. Previously, the Rosa S-locus was mapped on chromosome 3, and three putative S-RNase genes were identified in the R. chinensis ‘Old Blush’ genome. Here, we show that these genes do not belong to the S-locus region. Using R. chinensis and R. multiflora genomes and a phylogenetic approach, we identified the S-RNase gene, that belongs to the Prunus S-lineage. Expression patterns support this gene as being the S-pistil. This gene is here also identified in R. moschata, R. arvensis, and R. minutifolia low coverage genomes, allowing the identification of positively selected amino acid sites, and thus, further supporting this gene as the S-RNase. Furthermore, genotype–phenotype association experiments also support this gene as the S-RNase. For the S-pollen GSI component we find evidence for multiple F-box genes, that show the expected expression pattern, and evidence for diversifying selection at the F-box genes within an S-haplotype. Thus, Rosa has a non-self-recognition system, like in Maleae species, despite the S-pistil gene belonging to the Prunus S-RNase lineage. These findings are discussed in the context of the Rosaceae GSI evolution. Knowledge on the Rosa S-locus has practical implications since genes controlling floral and other ornamental traits are in linkage disequilibrium with the S-locus.

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S-RNase-Based Self-Incompatibility in Petunia: A Complex Non-Self Recognition System Between Pollen and Pistil

Sexual Reproduction in Animals and Plants ◽

10.1007/978-4-431-54589-7_24 ◽

2014 ◽

pp. 289-303

Author(s):

Penglin Sun ◽

Justin Stephen Williams ◽

Shu Li ◽

Teh-hui Kao

Keyword(s):

Recognition System ◽

Self Incompatibility ◽

Self Recognition

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Diversification or collapse of self-incompatibility haplotypes as a rescue process

10.1101/2020.03.30.017376 ◽

2020 ◽

Author(s):

Alexander Harkness ◽

Emma E. Goldberg ◽

Yaniv Brandvain

Keyword(s):

Gene Conversion ◽

Conversion Rate ◽

Markov Chain Model ◽

The Self ◽

Allelic Polymorphism ◽

Chain Model ◽

Self Incompatibility ◽

Recognition Mechanism ◽

Self Recognition ◽

Incompatibility Locus

AbstractIn angiosperm self-incompatibility systems, pollen with an allele matching the pollen recipient at the self-incompatibility locus is rejected. Extreme allelic polymorphism is maintained by frequency-dependent selection favoring rare alleles. However, two challenges limit the spread of a new allele (a tightly linked haplotype in this case) under the widespread “collaborative non-self recognition” mechanism. First, there is no obvious selective benefit for pollen compatible with non-existent stylar incompatibilities, which themselves cannot spread if no pollen can fertilize them. However, a pistil-function mutation complementary to a previously neutral pollen mutation may spread if it restores self-incompatibility to a self-compatible intermediate. Second, we show that novel haplotypes can drive elimination of existing ones with fewer siring opportunities. We calculate relative probabilities of increase and collapse in haplotype number given the initial collection of incompatibility haplotypes and the population gene conversion rate. Expansion in haplotype number is possible when population gene conversion rate is large, but large contractions are likely otherwise. A Markov chain model derived from these expansion and collapse probabilities generates a stable haplotype number distribution in the realistic range of 10–40 under plausible parameters. However, smaller populations might lose many haplotypes beyond those lost by chance during bottlenecks.

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