Breakdown of Self-Incompatibility in a Natural Population of Petunia axillaris Caused by Loss of Pollen Function (original) (raw)
Related papers
Sexual Plant Reproduction, 1999
Although Petunia axillaris subsp. axillaris is described as a self-incompatible taxon, some of the natural populations we have identified in Uruguay are composed of both self-incompatible and self-compatible plants. Here, we studied the selfincompatibility (SI) behavior of 50 plants derived from such a mixed population, designated U83, and examined the cause of the breakdown of SI. Thirteen plants were found to be self-incompatible, and the other 37 were found to be selfcompatible. A total of 14 S-haplotypes were represented in these 50 plants, including two that we had previously identified from another mixed population, designated U1. All the 37 self-compatible plants carried either an S C1 -or an S C2 -haplotype. S C1 S C1 and S C2 S C2 homozygotes were generated by self-pollination of two of the self-compatible plants, and they were reciprocally crossed with 40 self-incompatible S-homozygotes (S 1 S 1 through S 40 S 40 ) generated from plants identified from three mixed populations, including U83. The S C1 S C1 homozygote was reciprocally compatible with all the genotypes examined. The S C2 S C2 homozygote accepted pollen from all but the S 17 S 17 homozygote (identified from the U1 population), but the S 17 S 17 homozygote accepted pollen from the S C2 S C2 homozygote. cDNAs encoding S C2 -and S 17 -RNases were cloned and sequenced, and their nucleotide sequences were completely identical. Analysis of bud-selfed progeny of heterozygotes carrying S C1 or S C2 showed that the SI behavior of S C1 and S C2 was identical to that of S C1 and S C2 homozygotes, respectively. All these results taken together suggested that the S C2 -haplotype was a mutant form of the S 17 -haplotype, with the defect lying in the pollen function. The possible nature of the mutation is discussed. ; fax 814 -863-9416.
THE PLANT CELL ONLINE, 1996
In self-incompatible (SI) plants, the S locus acts to prevent growth of self-pollen and thus promotes outcrossing within the species. lnterspecific crosses between SI and self-compatible (SC) species often show unilateral lncompatibility that follows the S I x SC rule: S I specles reject pollen from SC specles, but the reciproca1 crosses are usually compatible. The general validity of the S I x SC rule suggests a link between S I and interspeclflc pollen rejectlon; however, this link has been questioned because of a number of exceptlons to the rule. To clarlfy the role of the S locus in interspecific pollen rejection, we transformed severa1 Nicotlana species and hybrids with genes encodlng S A~ or SC,O RNase from S I N. alata. Compatibillty phenotypes in the transgenlc plants were tested using pollen from three SC specles showing unilateral incompatibility with N. alata. S RNase was lmpllcated ln rejecting pollen from all three specles. Rejection of N. plumbaginifolia pollen was similar to S allele-speclfic pollen rejection, showing a requirement for both S RNase and other genetic factors from N. alata. In contrast, S RNase-dependent rejectlon of N. glutinosa and N. tabacum pollen proceeded without these additional factors. N. alata also rejects pollen fmm the latter two specles through an S RNaseindependent mechanism. Our results lmplicate the S locus in all three systems, but lt 1s clear that multlple mechanisms contribute to interspecific pollen rejectlon.
THE PLANT CELL ONLINE, 1990
We investigated the structure and expression of three S-alleles of Petunia hybrida in self-incompatible varieties and in a pseudo-self-compatible line in which the self-incompatibility response is defective. Comparison of derived amino acid sequences from different gametophytic S-alleles revealed a pattern of sequence conservation and variability that was highly nonrandom. In self-incompatible varieties, petunia S-locus mRNA accumulates preferentially in styles during the transition from bud self-compatibility to self-incompatibility. S-Allele sequences homologous to the cloned S, allele were present in a pseudo-self-compatible variety, and were expressed at levels indistinguishable from those observed in a self-incompatible line homozygous for the SI allele. Taken together, our data indicate that (1) limited sequence differences may confer allelic specificity, (2) S-locus mRNAs accumulate in a precise organ-specific pattern during floral development, and (3) the ability to inhibit the growth of incompatible pollen tubes appears to require a threshold accumulation of the stylar gene product, along with the participation of as yet undefined pollen gene products.
In self-incompatible (SI) plants, the S locus acts to prevent growth of self-pollen and thus promotes outcrossing within the species. lnterspecific crosses between SI and self-compatible (SC) species often show unilateral lncompatibility that follows the S I x SC rule: S I specles reject pollen from SC specles, but the reciproca1 crosses are usually compatible. The general validity of the S I x SC rule suggests a link between S I and interspeclflc pollen rejectlon; however, this link has been questioned because of a number of exceptlons to the rule. To clarlfy the role of the S locus in interspecific pollen rejection, we transformed severa1 Nicotlana species and hybrids with genes encodlng S A~ or SC,O RNase from S I N. alata. Compatibillty phenotypes in the transgenlc plants were tested using pollen from three SC specles showing unilateral incompatibility with N. alata. S RNase was lmpllcated ln rejecting pollen from all three specles. Rejection of N. plumbaginifolia pollen was similar to S allele-speclfic pollen rejection, showing a requirement for both S RNase and other genetic factors from N. alata. In contrast, S RNase-dependent rejectlon of N. glutinosa and N. tabacum pollen proceeded without these additional factors. N. alata also rejects pollen fmm the latter two specles through an S RNaseindependent mechanism. Our results lmplicate the S locus in all three systems, but lt 1s clear that multlple mechanisms contribute to interspecific pollen rejectlon.
Plant Self-Incompatibility: Or, Self-Induction of Population Genetic Diversity
The Molecular Basis of Plant Genetic Diversity, 2012
The Molecular Basis of Plant Genetic Diversity 74 system protects plants from pollination with pollen carrying the same S-haplotype (McClure & Franklin, 2006). Two main systems of homomorphic SI comprise: gametophytic self-incompatibility (GSI) and sporophytic self-incompatibility (SSI). In GSI, the incompatibility phenotype is determined by the pollen haploid genome. The S-locus determines S-specificity of pollen recognition and rejection, so the pollen is rejected by the GSI system when the S-haplotype is the same as one of two S-alleles of the diploid pistil. This indicates that the S-locus products readily expressed in the pistil and pollen interact with each other and determine the compatibility or incompatibility of the emerging pollen tube. In sporophytic SI, the pollen S-phenotype is determined by the diploid genome of the parental plant. Therefore, in GSI systems half-compatibility is shown between individuals that share one S-allele, while in SSI systems crosses are always fully compatible or fully incompatible (Allen & Hiscock, 2008). The SSI system has been reported in six families: Asteraceae, Berulaceae, Brassicaceae, Caryopgyllaceae, Convolvulaceae and Polemoniaceae. The molecular mechanism of the SSI has only been well characterized in Brassicaceae (see below) (Hiscock & McInnis, 2003). Studies of GSI species at the molecular level have identified two completely different SI mechanisms. One GSI mechanism, which is found in the Solanaceae, Rosaceae and Scrophulariaceae, has S-RNase as the pistil S-component and an F-box protein as the pollen S-component (see below). The second mechanism has been identified only in Papaver (poppy), where the interaction between male and female determinants transmits a cellular signal into the pollen tube, resulting in an influx of calcium cations. This influx interferes with the intracellular concentration gradient of calcium ions which exists inside the pollen tube, essential for its elongation (McClure & Franklin-Tong, 2006; Zhang & Xue, 2008).
New Phytologist, 2006
• Current models for the generation of new gametophytic self-incompatibility specificities require that neutral variability segregates within specificity classes. Furthermore, one of the models predicts greater ratios of nonsynonymous to synonymous substitutions in pollen than in pistil specificity genes. All models assume that new specificities arise by mutation only.• To test these models, 21 SFB (the pollen S-locus) alleles from a wild Prunus spinosa (Rosaceae) population were obtained. For seven of these, the corresponding S-haplotype was also characterized. The SFB data set was also used to identify positively selected sites. Those sites are likely to be the ones responsible for defining pollen specificities.• Of the 23 sites identified as being positively selected, 21 are located in the variable (including a new region described here) and hypervariable regions. Little variability is found within specificity classes. There is no evidence for selective sweeps being more frequent in pollen than in pistil specificity genes. The S-RNase and the SFB genes have only partially correlated evolutionary histories.• None of the models is compatible with the variability patterns found in the SFB and the S-haplotype data.Current models for the generation of new gametophytic self-incompatibility specificities require that neutral variability segregates within specificity classes. Furthermore, one of the models predicts greater ratios of nonsynonymous to synonymous substitutions in pollen than in pistil specificity genes. All models assume that new specificities arise by mutation only.To test these models, 21 SFB (the pollen S-locus) alleles from a wild Prunus spinosa (Rosaceae) population were obtained. For seven of these, the corresponding S-haplotype was also characterized. The SFB data set was also used to identify positively selected sites. Those sites are likely to be the ones responsible for defining pollen specificities.Of the 23 sites identified as being positively selected, 21 are located in the variable (including a new region described here) and hypervariable regions. Little variability is found within specificity classes. There is no evidence for selective sweeps being more frequent in pollen than in pistil specificity genes. The S-RNase and the SFB genes have only partially correlated evolutionary histories.None of the models is compatible with the variability patterns found in the SFB and the S-haplotype data.
2013
The breakdown of self-incompatibility, which could result from the accumulation of non-functional S-haplotypes or competitive interaction between two different functional S-haplotypes, has been studied extensively at the molecular level in tetraploid Rosaceae species. In this study, two tetraploid Chinese cherry (Prunus pseudocerasus) cultivars and one diploid sweet cherry (Prunus avium) cultivar were used to investigate the ploidy of pollen grains and inheritance of pollen-S alleles. Genetic analysis of the S-genotypes of two intercross-pollinated progenies showed that the pollen grains derived from Chinese cherry cultivars were hetero-diploid, and that the two S-haplotypes were made up of every combination of two of the four possible S-haplotypes. Moreover, the distributions of single S-haplotypes expressed in self- and intercross-pollinated progenies were in disequilibrium. The number of individuals of the two different S-haplotypes was unequal in two self-pollinated and two intercross-pollinated progenies. Notably, the number of individuals containing two different S-haplotypes (S1- and S5-, S5- and S8-, S1- and S4-haplotype) was larger than that of other individuals in the two self-pollinated progenies, indicating that some of these hetero-diploid pollen grains may have the capability to inactivate stylar S-RNase inside the pollen tube and grow better into the ovaries.
The Plant Cell, 2002
Self-incompatibility (SI) in Brassica is controlled sporophytically by the multiallelic S-locus. The SI phenotype of pollen in an S-heterozygote is determined by the relationship between the two S-haplotypes it carries, and dominant/recessive relationships often are observed between the two S-haplotypes. The S-locus protein 11 (SP11 , also known as the S-locus cysteine-rich protein) gene has been cloned from many pollen-dominant S-haplotypes (class I) and shown to encode the pollen S-determinant. However, SP11 from pollen-recessive S-haplotypes (class II) has never been identified by homology-based cloning strategies, and how the dominant/recessive interactions between the two classes occur was not known. We report here the identification and molecular characterization of SP11 s from six class II S-haplotypes of B. rapa and B. oleracea. Phylogenetic analysis revealed that the class II SP11s form a distinct group separated from class I SP11s. The promoter sequences and expression patterns of SP11 s also were different between the two classes. The mRNA of class II SP11 , which was detected predominantly in the anther tapetum in homozygotes, was not detected in the heterozygotes of class I and class II S-haplotypes, suggesting that the dominant/recessive relationships of pollen are regulated at the mRNA level of SP11 s.