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

2021 ◽  
Vol 12 ◽  
Author(s):  
Amanda K. Broz ◽  
Christopher M. Miller ◽  
You Soon Baek ◽  
Alejandro Tovar-Méndez ◽  
Pablo Geovanny Acosta-Quezada ◽  
...  

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.

Plants ◽  
2020 ◽  
Vol 9 (11) ◽  
pp. 1566
Author(s):  
Courtney M. Matzke ◽  
Joel S. Shore ◽  
Michael M. Neff ◽  
Andrew G. McCubbin

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.


2018 ◽  
Author(s):  
Thomas Brom ◽  
Vincent Castric ◽  
Sylvain Billiard

AbstractMany hermaphroditic flowering plants species possess a genetic self-incompatibility (SI) system that prevents self-fertilization and is typically controlled by a single multiallelic locus, the S-locus. The conditions under which SI can be stably maintained in single isolated populations are well known and depend chiefly on the level of inbreeding depression and the number of SI alleles segregating at the S-locus. However, while both the number of SI alleles and the level of inbreeding depression are potentially affected by population subdivision, the conditions for the maintenance of SI in subdivided populations remain to be studied. In this paper, we combine analytical predictions and two different individual-based simulation models to show that population subdivision can severely compromise the maintenance of SI. Under the conditions we explored, this effect is mainly driven by the decrease of the local diversity of SI alleles rather than by a change in the dynamics of inbreeding depression. We discuss the implications of our results for the interpretation of empirical data on the loss of SI in natural populations.Data accessibility statementNo data to be archived


1987 ◽  
Vol 65 (4) ◽  
pp. 660-665 ◽  
Author(s):  
S. P. Vander Kloet ◽  
P. M. Lyrene

The results of self-pollinations, sibling pollinations, and cross-pollinations were compared in terms of number of berries produced per 100 pollinated flowers, number of plump seeds per berry, percent seed germination, and time between pollination and fruit ripening. The population studied consisted of 344 Vaccinium corymbosum L. seedlings grown from seeds harvested from native populations at 26 sites extending from Florida to Nova Scotia. Diploid, tetraploid, and hexaploid plants were included in the study, but only homoploid crosses were made in order to avoid the confounding effect of the strong heteroploid crossing barriers in V. corymbosum. Self-pollinations resulted in great reductions in all fertility parameters. Sibling pollinations produced far fewer seedlings than cross-pollinations, mainly because the number of plump seeds per berry was reduced from an average of 21 for outcrosses to 13 for sibling crosses. Pollination with 1:1 mixtures of self and outcross pollen reduced plump seed number per berry to 5, compared with 14 for comparable outcrosses. The results were similar at all three ploidy levels. It is concluded that self-compatibility is low in natural populations of V. corymbosum.


2008 ◽  
Vol 90 (1) ◽  
pp. 27-35 ◽  
Author(s):  
BODIL K. EHLERS ◽  
MIKKEL H. SCHIERUP

SummaryThe occurrence of gynodioecy among angiosperms appears to be associated with self-compatibility. We use individual-based simulations to investigate the conditions for breakdown of a gametophytic self-incompatibility system in gynodioecious populations and make a comparison with hermaphroditic populations where the conditions are well known. We study three types of mutations causing self-compatibility. We track the fate of these mutations in both gynodioecious and hermaphroditic populations, where we vary the number of S-alleles, inbreeding depression and selfing rate. We find that the conditions for breakdown are less stringent if the population is gynodioecious and that the breakdown of self-incompatibility tends to promote stability of gynodioecious populations since it results in a higher frequency of females. We also find that fecundity selection has a large effect on the probability of breakdown of self-incompatibility, in particular if caused by a mutation destroying the female function of the S-locus.


2020 ◽  
Vol 7 (1) ◽  
Author(s):  
Donia Abdallah ◽  
Ghada Baraket ◽  
Veronica Perez ◽  
Amel Salhi Hannachi ◽  
Jose I. Hormaza

Abstract Self-incompatibility (SI) to self-compatibility (SC) transition is one of the most frequent and prevalent evolutionary shifts in flowering plants. Prunus L. (Rosaceae) is a genus of over 200 species most of which exhibit a Gametophytic SI system. Peach [Prunus persica (L.) Batsch; 2n = 16] is one of the few exceptions in the genus known to be a fully self-compatible species. However, the evolutionary process of the complete and irreversible loss of SI in peach is not well understood and, in order to fill that gap, in this study 24 peach accessions were analyzed. Pollen tube growth was controlled in self-pollinated flowers to verify their self-compatible phenotypes. The linkage disequilibrium association between alleles at the S-locus and linked markers at the end of the sixth linkage group was not significant (P > 0.05), except with the closest markers suggesting the absence of a signature of negative frequency dependent selection at the S-locus. Analysis of SFB1 and SFB2 protein sequences allowed identifying the absence of some variable and hypervariable domains and the presence of additional α-helices at the C-termini. Molecular and evolutionary analysis of SFB nucleotide sequences showed a signature of purifying selection in SFB2, while the SFB1 seemed to evolve neutrally. Thus, our results show that the SFB2 allele diversified after P. persica and P. dulcis (almond) divergence, a period which is characterized by an important bottleneck, while SFB1 diversified at a transition time between the bottleneck and population expansion.


Genetics ◽  
1999 ◽  
Vol 152 (3) ◽  
pp. 1123-1135 ◽  
Author(s):  
J F Golz ◽  
V Su ◽  
A E Clarke ◽  
E Newbigin

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.


Plants ◽  
2021 ◽  
Vol 10 (10) ◽  
pp. 2186
Author(s):  
Zhiquan Liu ◽  
Bing Li ◽  
Yong Yang ◽  
Changbin Gao ◽  
Bin Yi ◽  
...  

Self-incompatibility (SI) is a pollen-stigma recognition system controlled by a single and highly polymorphic genetic locus known as the S-locus. The S-locus exists in all Brassica napus (B. napus, AACC), but natural B. napus accessions are self-compatible. About 100 and 50 S haplotypes exist in Brassica rapa (AA) and Brassica oleracea (CC), respectively. However, S haplotypes have not been detected in B. napus populations. In this study, we detected the S haplotype distribution in B. napus and ascertained the function of a common S haplotype BnS-6 through genetic transformation. BnS-1/BnS-6 and BnS-7/BnS-6 were the main S haplotypes in 523 B. napus cultivars and inbred lines. The expression of SRK in different S haplotypes was normal (the expression of SCR in the A subgenome affected the SI phenotype) while the expression of BnSCR-6 in the C subgenome had no correlation with the SI phenotype in B. napus. The BnSCR-6 protein in BnSCR-6 overexpressed lines was functional, but the self-compatibility of overexpressed lines did not change. The low expression of BnSCR-6 could be a reason for the inactivation of BnS-6 in the SI response of B. napus. This study lays a foundation for research on the self-compatibility mechanism and the SI-related breeding in B. napus.


2007 ◽  
Vol 67 (1) ◽  
pp. 17-24
Author(s):  
Juan Mulato-Brito ◽  
Aureliano Peña-Lomelí ◽  
Jaime Sahagún-Castellanos ◽  
Clemente Villanueva-Verduzco ◽  
José de Jesús López-Reynoso

Self-Compatibility Inheritance in Tomatillo (Physalis IxocarpaBrot.)One of the main limiting factors to improve tomatillo is the presence of self-incompatibility which has been reported to be gametophytic. In an early research, a self-compatible plant was found in the Rendidora landrace and this allowed us to investigate the inheritance of self-compatibility gene (s) in tomatillo. The following crosses were performed: self-compatible x self-incompatible, self-compatible x self-compatible and self-incompatible x self-incompatible and their respective reciprocal crosses. Segregation ratios on self-compatibility versus self-incompatibility in their offspring indicate that self-compatibility is not inherited via cytoplasm, so the responsible gene is located in chromosomes. The inheritance of self-compatibility is due to a single dominant gene (Sc) which is a mutation at the S locus. Self-compatible individuals are strictly heterozygous (Sc,4) and finally, the self-compatibility allele (Sc), in the male side (Sc,4), seems to be non functional when self-pollinating the Sc,4stigma. A single gene controlling stem pubescence was also found.


2018 ◽  
Author(s):  
Jörg A. Bachmann ◽  
Andrew Tedder ◽  
Benjamin Laenen ◽  
Marco Fracassetti ◽  
Aurélie Désamoré ◽  
...  

AbstractShifts from outcrossing to self-fertilisation have occurred repeatedly in many different lineages of flowering plants, and often involve the breakdown of genetic outcrossing mechanisms. In the Brassicaceae, self-incompatibility (SI) allows plants to ensure outcrossing by recognition and rejection of self-pollen on the stigma. This occurs through the interaction of female and male specificity components, consisting of a pistil based receptor and a pollen-coat protein, both of which are encoded by tightly linked genes at the S-locus. When benefits of selfing are higher than costs of inbreeding, theory predicts that loss-of-function mutations in the male (pollen) SI component should be favoured, especially if they are dominant. However, it remains unclear whether mutations in the male component of SI are predominantly responsible for shifts to self-compatibility, and testing this prediction has been difficult due to the challenges of sequencing the highly polymorphic and repetitive ~100 kbp S-locus. The crucifer genus Capsella offers an excellent opportunity to study multiple transitions from outcrossing to self-fertilization, but so far, little is known about the genetic basis and timing of loss of SI in the self-fertilizing diploid Capsella orientalis. Here, we show that loss of SI in C. orientalis occurred within the past 2.6 Mya and maps as a dominant trait to the S-locus. Using targeted long-read sequencing of multiple complete S-haplotypes, we identify a frameshift deletion in the male specificity gene SCR that is fixed in C. orientalis, and we confirm loss of male SI specificity. We further analyze RNA sequencing data to identify a conserved, S-linked small RNA (sRNA) that is predicted to cause dominance of self-compatibility. Our results suggest that degeneration of pollen SI specificity in dominant S-alleles is important for shifts to self-fertilization in the Brassicaceae.Author SummaryAlready Darwin was fascinated by the widely varying modes of plant reproduction. The shift from outcrossing to self-fertilization is considered one of the most frequent evolutionary transitions in flowering plants, yet we still know little about the genetic basis of these shifts. In the Brassicaceae, outcrossing is enforced by a self-incompatibility (SI) system that enables the recognition and rejection of self pollen. This occurs through the action of two tightly linked genes at the S-locus, that encode a receptor protein located on the stigma (female component) and a pollen ligand protein (male component), respectively. Nevertheless, SI has frequently been lost, and theory predicts that mutations in the male component should have an advantage during the loss of SI, especially if they are dominant. To test this hypothesis, we mapped the loss of SI in a selfing species from the genus Capsella, a model system for evolutionary genomics. We found that loss of SI mapped to the S-locus, which harbored a dominant loss-of-function mutation in the male SI protein, and as expected, we found that male specificity was indeed lost in C. orientalis. Our results suggest that transitions to selfing often involve parallel genetic changes.


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