The Turnera Style S-Locus Gene TsBAHD Possesses Brassinosteroid-Inactivating Activity When Expressed in Arabidopsis thaliana

Heterostyly distinct hermaphroditic floral morphs enforce outbreeding. Morphs differ structurally, promote cross-pollination, and physiologically block self-fertilization. In Turnera the self-incompatibility (S)-locus controlling heterostyly possesses three genes specific to short-styled morph genomes. Only one gene, TsBAHD, is expressed in pistils and this has been hypothesized to possess brassinosteroid (BR)-inactivating activity. We tested this hypothesis using heterologous expression in Arabidopsis thaliana as a bioassay, thereby assessing growth phenotype, and the impacts on the expression of endogenous genes involved in BR homeostasis and seedling photomorphogenesis. Transgenic A. thaliana expressing TsBAHD displayed phenotypes typical of BR-deficient mutants, with phenotype severity dependent on TsBAHD expression level. BAS1, which encodes an enzyme involved in BR inactivation, was downregulated in TsBAHD-expressing lines. CPD and DWF, which encode enzymes involved in BR biosynthesis, were upregulated. Hypocotyl growth of TsBAHD dwarfs responded to application of brassinolide in light and dark in a manner typical of plants over-expressing genes encoding BR-inactivating activity. These results provide empirical support for the hypothesis that TsBAHD possesses BR-inactivating activity. Further this suggests that style length in Turnera is controlled by the same mechanism (BR inactivation) as that reported for Primula, but using a different class of enzyme. This reveals interesting convergent evolution in a biochemical mechanism to regulate floral form in heterostyly.

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Sequence and Structural Diversity of the S Locus Genes From Different Lines With the Same Self-Recognition Specificities in Brassica oleracea

Genetics ◽

10.1093/genetics/154.1.413 ◽

2000 ◽

Vol 154 (1) ◽

pp. 413-420 ◽

Cited By ~ 2

Author(s):

Makoto Kusaba ◽

Masanori Matsushita ◽

Keiichi Okazaki ◽

Yoko Satta ◽

Takeshi Nishio

Keyword(s):

Structural Diversity ◽

Receptor Protein ◽

Self Incompatibility ◽

S Locus ◽

High Similarity ◽

Putative Receptor ◽

Recognition Specificity ◽

Polymorphic Genes ◽

Self Recognition ◽

Self Fertilization

Abstract Self-incompatibility (SI) is a mechanism for preventing self-fertilization in flowering plants. In Brassica, it is controlled by a single multi-allelic locus, S, and it is believed that two highly polymorphic genes in the S locus, SLG and SRK, play central roles in self-recognition in stigmas. SRK is a putative receptor protein kinase, whose extracellular domain exhibits high similarity to SLG. We analyzed two pairs of lines showing cross-incompatibility (S2 and S2-b; S13 and S13-b). In S2 and S2-b, SRKs were more highly conserved than SLGs. This was also the case with S13 and S13-b. This suggests that the SRKs of different lines must be conserved for the lines to have the same self-recognition specificity. In particular, SLG2-b showed only 88.5% identity to SLG2, which is comparable to that between the SLGs of different S haplotypes, while SRK2-b showed 97.3% identity to SRK2 in the S domain. These findings suggest that the SLGs in these S haplotypes are not important for self-recognition in SI.

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Transcriptome and Network Analyses of Heterostyly in Turnera subulata Provide Mechanistic Insights: Are S-Loci a Red-Light for Pistil Elongation?

Plants ◽

10.3390/plants9060713 ◽

2020 ◽

Vol 9 (6) ◽

pp. 713 ◽

Cited By ~ 1

Author(s):

Paige M. Henning ◽

Joel S. Shore ◽

Andrew G. McCubbin

Keyword(s):

Red Light ◽

Genetic Networks ◽

Light Signaling ◽

Self Incompatibility ◽

S Locus ◽

Network Analyses ◽

S Gene ◽

Self Fertilization ◽

Pistil Length ◽

S Genes

Heterostyly employs distinct hermaphroditic floral morphs to enforce outbreeding. Morphs differ structurally in stigma/anther positioning, promoting cross-pollination, and physiologically blocking self-fertilization. Heterostyly is controlled by a self-incompatibility (S)-locus of a small number of linked S-genes specific to short-styled morph genomes. Turnera possesses three S-genes, namely TsBAHD (controlling pistil characters), TsYUC6, and TsSPH1 (controlling stamen characters). Here, we compare pistil and stamen transcriptomes of floral morphs of T. subulata to investigate hypothesized S-gene function(s) and whether hormonal differences might contribute to physiological incompatibility. We then use network analyses to identify genetic networks underpinning heterostyly. We found a depletion of brassinosteroid-regulated genes in short styled (S)-morph pistils, consistent with hypothesized brassinosteroid-inactivating activity of TsBAHD. In S-morph anthers, auxin-regulated genes were enriched, consistent with hypothesized auxin biosynthesis activity of TsYUC6. Evidence was found for auxin elevation and brassinosteroid reduction in both pistils and stamens of S- relative to long styled (L)-morph flowers, consistent with reciprocal hormonal differences contributing to physiological incompatibility. Additional hormone pathways were also affected, however, suggesting S-gene activities intersect with a signaling hub. Interestingly, distinct S-genes controlling pistil length, from three species with independently evolved heterostyly, potentially intersect with phytochrome interacting factor (PIF) network hubs which mediate red/far-red light signaling. We propose that modification of the activities of PIF hubs by the S-locus could be a common theme in the evolution of heterostyly.

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Patterns of polymorphism at the self-incompatibility locus in 1,083 Arabidopsis thaliana genomes

10.1101/098228 ◽

2017 ◽

Author(s):

Takashi Tsuchimatsu ◽

Pauline M. Goubet ◽

Sophie Gallina ◽

Anne-Catherine Holl ◽

Isabelle Fobis-Loisy ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Glacial Refugia ◽

The Self ◽

Ice Age ◽

Self Incompatibility ◽

S Locus ◽

Sequencing Data ◽

Functional Studies ◽

Large Deletions ◽

Last Ice Age

AbstractAlthough the transition to selfing in the model plant Arabidopsis thaliana involved the loss of the self-incompatibility (SI) system, it clearly did not occur due to the fixation of a single inactivating mutation at the locus determining the specificities of SI (the S-locus). At least three groups of divergent haplotypes (haplogroups), corresponding to ancient functional S-alleles, have been maintained at this locus, and extensive functional studies have shown that all three carry distinct inactivating mutations. However, the historical process of loss of SI is not well understood, in particular its relation with the last glaciation. Here, we took advantage of recently published genomic re-sequencing data in 1,083 Arabidopsis thaliana accessions that we combined with BAC sequencing to obtain polymorphism information for the whole S-locus region at a species-wide scale. The accessions differed by several major rearrangements including large deletions and inter-haplogroup recombinations, forming a set of haplogroups that are widely distributed throughout the native range and largely overlap geographically. ‘Relict’ A. thaliana accessions that directly derive from glacial refugia are polymorphic at the S-locus, suggesting that the three haplogroups were already present when glacial refugia from the last Ice Age became isolated. Inter-haplogroup recombinant haplotypes were highly frequent, and detailed analysis of recombination breakpoints suggested multiple independent origins. These findings suggest that the complete loss of SI in A. thaliana involved independent self-compatible mutants that arose prior to the last Ice Age, and experienced further rearrangements during post-glacial colonization.

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Single Gene Control of Postzygotic Self-Incompatibility in Poke Milkweed, Asclepias exaltata L.

Genetics ◽

10.1093/genetics/154.2.893 ◽

2000 ◽

Vol 154 (2) ◽

pp. 893-907

Author(s):

Sara R Lipow ◽

Robert Wyatt

Keyword(s):

Inbreeding Depression ◽

Single Gene ◽

Diallel Cross ◽

Gene Control ◽

Self Incompatibility ◽

S Locus ◽

Fertile Plant ◽

Diallel Crosses ◽

Prezygotic Barriers ◽

Self Fertilization

Abstract Most individuals of Asclepias exaltata are self-sterile, but all plants lack prezygotic barriers to self-fertilization. To determine whether postzygotic rejection of self-fertilized ovules is due to late-acting self-incompatibility or to extreme, early acting inbreeding depression, we performed three diallel crosses among self-sterile plants related as full-sibs. The full-sibs segregated into four compatibility classes, suggesting that late acting self-incompatibility is controlled by a single gene (S-locus). Crosses between plants sharing one or both alleles at the S-locus are incompatible. An additional diallel cross was done among full-sib progeny from a cross of a self-sterile and a self-fertile plant. These progeny grouped into two compatibility classes, and plants within classes displayed varying levels of self-fertility. This suggests that the occasional self-fertility documented in natural pollinations is caused by pseudo-self-fertility alleles that alter the functioning of the S-locus.

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In vivo imaging of the S-locus receptor kinase, the female specificity determinant of self-incompatibility, in transgenic self-incompatible Arabidopsis thaliana

Annals of Botany ◽

10.1093/aob/mcv008 ◽

2015 ◽

Vol 115 (5) ◽

pp. 789-805 ◽

Cited By ~ 4

Author(s):

Anne C. Rea ◽

June B. Nasrallah

Keyword(s):

Arabidopsis Thaliana ◽

In Vivo Imaging ◽

Self Incompatibility ◽

Receptor Kinase ◽

S Locus

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A Molecular Description of Mutations Affecting the Pollen Component of the Nicotiana alata S locus

Genetics ◽

10.1093/genetics/152.3.1123 ◽

1999 ◽

Vol 152 (3) ◽

pp. 1123-1135 ◽

Cited By ~ 2

Author(s):

J F Golz ◽

V Su ◽

A E Clarke ◽

E Newbigin

Keyword(s):

Extra Chromosome ◽

Nicotiana Alata ◽

Self Incompatibility ◽

S Locus ◽

Cytological Examination ◽

Mutagenesis Screen ◽

Genes Encoding ◽

Additional Chromosome ◽

S Allele ◽

Molecular Description

Abstract Mutations affecting the self-incompatibility response of Nicotiana alata were generated by irradiation. Mutants in the M1 generation were selected on the basis of pollen tube growth through an otherwise incompatible pistil. Twelve of the 18 M1 plants obtained from the mutagenesis screen were self-compatible. Eleven self-compatible plants had mutations affecting only the pollen function of the S locus (pollen-part mutants). The remaining self-compatible plant had a mutation affecting only the style function of the S locus (style-part mutant). Cytological examination of the pollen-part mutant plants revealed that 8 had an extra chromosome (2n + 1) and 3 did not. The pollen-part mutation in 7 M1 plants was followed in a series of crosses. DNA blot analysis using probes for S-RNase genes (encoding the style function of the S locus) indicated that the pollen-part mutation was associated with an extra S allele in 4 M1 plants. In 3 of these plants, the extra S allele was located on the additional chromosome. There was no evidence of an extra S allele in the 3 remaining M1 plants. The breakdown of self-incompatibility in plants with an extra S allele is discussed with reference to current models of the molecular basis of self-incompatibility.

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S-RNase Alleles Associated With Self-Compatibility in the Tomato Clade: Structure, Origins, and Expression Plasticity

Frontiers in Genetics ◽

10.3389/fgene.2021.780793 ◽

2021 ◽

Vol 12 ◽

Author(s):

Amanda K. Broz ◽

Christopher M. Miller ◽

You Soon Baek ◽

Alejandro Tovar-Méndez ◽

Pablo Geovanny Acosta-Quezada ◽

...

Keyword(s):

Natural Populations ◽

Reproductive Barriers ◽

Self Incompatibility ◽

S Locus ◽

Loss Of Function ◽

Resistance Factors ◽

Tomato Species ◽

Genes Encoding ◽

Self Compatibility ◽

Barrier Resistance

The self-incompatibility (SI) system in the Solanaceae is comprised of cytotoxic pistil S-RNases which are countered by S-locus F-box (SLF) resistance factors found in pollen. Under this barrier-resistance architecture, mating system transitions from SI to self-compatibility (SC) typically result from loss-of-function mutations in genes encoding pistil SI factors such as S-RNase. However, the nature of these mutations is often not well characterized. Here we use a combination of S-RNase sequence analysis, transcript profiling, protein expression and reproductive phenotyping to better understand different mechanisms that result in loss of S-RNase function. Our analysis focuses on 12 S-RNase alleles identified in SC species and populations across the tomato clade. In six cases, the reason for gene dysfunction due to mutations is evident. The six other alleles potentially encode functional S-RNase proteins but are typically transcriptionally silenced. We identified three S-RNase alleles which are transcriptionally silenced under some conditions but actively expressed in others. In one case, expression of the S-RNase is associated with SI. In another case, S-RNase expression does not lead to SI, but instead confers a reproductive barrier against pollen tubes from other tomato species. In the third case, expression of S-RNase does not affect self, interspecific or inter-population reproductive barriers. Our results indicate that S-RNase expression is more dynamic than previously thought, and that changes in expression can impact different reproductive barriers within or between natural populations.

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