Base-pairing requirements for small RNA-mediated gene silencing of recessive self-incompatibility alleles in<i>Arabidopsis halleri</i>

Burghgraeve, Nicolas; Simon, Samson; Barral, Simon; Fobis-Loisy, Isabelle; Holl, Anne-Catherine; Ponitzki, Chloé; Schmitt, Éric; Vekemans, Xavier; Castric, Vincent

doi:10.1101/370239

Cited by 5 publications

(8 citation statements)

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“…CC-BY-NC-ND 4.0 International license a certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under The copyright holder for this preprint (which was not this version posted March 3, 2020. ; https://doi.org/10.1101/370239 doi: bioRxiv preprint and is quickly degraded as the development of pollen grains inside the anther progresses (Murphy & Ross, 1998;Takayama et al, 2000). We confirmed that differences exist in the temporal dynamics of expression among alleles, as suggested by Kusaba et al (2002) in A. lyrata, possibly as the result of strong sequence divergence of the promotor sequences of the different SCR alleles.…”

Section: Expression Profilesupporting

confidence: 72%

“…It is made available under The copyright holder for this preprint (which was not this version posted March 3, 2020. ; https://doi.org/10.1101/370239 doi: bioRxiv preprint et al, 2006). Furthermore, the position of mismatches along the microRNA:target duplex also seems to be crucial, with a greater tolerance in the 3' than the 5' region of the microRNA (up to four mismatches generally have limited functional consequences in the 3' region, while only two mismatches in the 5' region seem sufficient to abolish the target recognition capability; Liu et al, 2014, Mallory et al, 2004Parizotto et al, 2004;Schwab et al, 2005). These observations have led to the formulation of general "rules" for microRNA targeting (Axtell & Meyers, 2018), but at the same time they also revealed a large number of exceptions.…”

Section: Introductionmentioning

confidence: 99%

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Base-Pairing Requirements for Small RNA-Mediated Gene Silencing of Recessive Self-Incompatibility Alleles inArabidopsis halleri

et al. 2020

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Small noncoding RNAs are central regulators of genome activity and stability. Their regulatory function typically involves sequence similarity with their target sites, but understanding the criteria by which they specifically recognize and regulate their targets across the genome remains a major challenge in the field, especially in the face of the diversity of silencing pathways involved. The dominance hierarchy among self-incompatibility alleles in Brassicaceae is controlled by interactions between a highly diversified set of small noncoding RNAs produced by dominant S-alleles and their corresponding target sites on recessive S-alleles. By controlled crosses, we created numerous heterozygous combinations of S-alleles in Arabidopsis halleri and developed an real-time quantitative PCR assay to compare allele-specific transcript levels for the pollen determinant of self-incompatibility (SCR). This provides the unique opportunity to evaluate the precise base-pairing requirements for effective transcriptional regulation of this target gene. We found strong transcriptional silencing of recessive SCR alleles in all heterozygote combinations examined. A simple threshold model of base pairing for the small RNA–target interaction captures most of the variation in SCR transcript levels. For a subset of S-alleles, we also measured allele-specific transcript levels of the determinant of pistil specificity (SRK), and found sharply distinct expression dynamics throughout flower development between SCR and SRK. In contrast to SCR, both SRK alleles were expressed at similar levels in the heterozygote genotypes examined, suggesting no transcriptional control of dominance for this gene. We discuss the implications for the evolutionary processes associated with the origin and maintenance of the dominance hierarchy among self-incompatibility alleles.

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Section: Expression Profilesupporting

confidence: 72%

Section: Introductionmentioning

confidence: 99%

Base-Pairing Requirements for Small RNA-Mediated Gene Silencing of Recessive Self-Incompatibility Alleles inArabidopsis halleri

et al. 2020

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“…4b ). We found one potential target region of CbpBmirS3 sRNA in the C. grandiflora derived subgenome A S -locus of C. bursa-pastoris with an affinity >18 (Durand et al 2014 ; Burghgraeve et al 2018 ), within 2 kb of the closest BLAST hit of SCR (Fig. 4d , e).…”

Section: Resultsmentioning

confidence: 83%

“…We used Trimmomatic v0.36 for removing sequencing adapters and for quality filtering of reads, before mapping small RNA of 18–27 nt length with STAR v2.5.3a (Dobin et al 2013 ) to an adjusted genome of C. rubella (Slotte et al 2013 ), where the C. rubella S -locus was replaced with a C. bursa-pastoris subgenome A or B S- locus, as in Bachmann et al ( 2019 ), and the annotation of identified sRNA precursors predicted above. To identify targets of expressed candidate sRNA dominance modifiers, we used a modified Smith and Waterman algorithm (Smith and Waterman 1981 ) as in Durand et al ( 2014 ) with the following scoring matrix: matches = +1; mismatches = −1; gaps = −2; G:U wobbles = −0.5 and a cutoff score for identifying targets of 18 (Burghgraeve et al 2018 ).…”

Section: Methodsmentioning

confidence: 99%

On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae)

et al. 2021

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Polyploidy, or whole-genome duplication, is a common speciation mechanism in plants. An important barrier to polyploid establishment 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 is 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 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 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 candidate dominance modifier with a target in the C. grandiflora-derived S-haplotype. These results suggest that pollen-level dominance may have facilitated loss of SI in C. bursa-pastoris. Finally, we demonstrate that spontaneous somatic tetraploidization after a wide cross between C. orientalis and C. grandiflora can result in production of self-compatible tetraploid offspring. We discuss the implications of this finding on the mode of formation of this widespread weed.

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“…c). The sRNA target affinity was similar to that of functional Arabidopsis dominance modifiers (Durand et al ., ; Burghgraeve et al ., ). As expected if ComirS3 sRNAs silence C. grandiflora SCR , C. grandiflora SCR was specifically downregulated in S‐ locus heterozygotes (Fig.…”

Section: Resultsmentioning

confidence: 97%

Genetic basis and timing of a major mating system shift inCapsella

et al. 2019

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Summary 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 < 2.6 Mya and maps as a dominant trait to the 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.

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Base-pairing requirements for small RNA-mediated gene silencing of recessive self-incompatibility alleles inArabidopsis halleri

Cited by 5 publications

References 52 publications

Base-Pairing Requirements for Small RNA-Mediated Gene Silencing of Recessive Self-Incompatibility Alleles inArabidopsis halleri

Base-Pairing Requirements for Small RNA-Mediated Gene Silencing of Recessive Self-Incompatibility Alleles inArabidopsis halleri

On the origin of the widespread self-compatible allotetraploid Capsella bursa-pastoris (Brassicaceae)

Genetic basis and timing of a major mating system shift inCapsella

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