Genetic complexity underlying hybrid male sterility in Drosophila

Recent genetic analyses of closely related species of Drosophila have indicated that hybrid male sterility is the consequence of highly complex synergistic effects among multiple genes, both conspecific and heterospecific. On the contrary, much evidence suggests the presence of major genes causing hybrid female sterility and inviability in the less-related species, D. melanogaster and D. simulans. Does this contrast reflect the genetic distance between species? Or, generally, is the genetic basis of hybrid male sterility more complex than that of hybrid female sterility and inviability? To clarify this point, the D. simulans introgression of the cytological region 34D-36A to the D. melanogaster genome, which causes recessive male sterility, was dissected by recombination, deficiency, and complementation mapping. The 450-kb region between two genes, Suppressor of Hairless and snail, exhibited a strong effect on the sterility. Males are (semi-)sterile if this region of the introgression is made homozygous or hemizygous. But no genes in the region singly cause the sterility; this region has at least two genes, which in combination result in male sterility. Further, the males are less fertile when heterozygous with a larger introgression, which suggests that dominant modifiers enhance the effects of recessive genes of male sterility. Such an epistatic view, even in the less-related species, suggests that the genetic complexity is special to hybrid male sterility.     

Cytoplasmic male sterility in relation to hybrid wheat breeding

Summary The method of substitution and restoration of nucleus is briefly described.Three species, Aegilops caudata, Ae. ovata and Triticum timopheevi, were used as donors of male sterility cytoplasms.The characteristics of these three cytoplasms are summarized as follows: Caudata-cytoplasm: This cytoplasm has in many respects deleterious effects on the manifestation of alien genomes. Substitution lines having hexaploid wheat genome constitution are mostly male sterile while the female organ is normal. Some lines set frequently germless seeds. Haploid and twin seedlings are of common occurrence in other lines. Pistillody is common in the substitution lines with tetraploid wheat genomes. Ovata-cytoplasm: No pistillody was found in the substitution lines, both with hexaploid and tetraploid wheats. Male sterility is always complete in the substitution lines of hexaploid wheats with the exception of P 168, a variety of common wheat having a pair of satchromosomes of Ae. caudata. This variety restores male fertility completely. No effective restorers were found for the substitution lines of emmer wheat. Delayed heading is common in the 4x substitution lines. Timopheevi-cytoplasm: Substitution lines of 6x wheats are mostly male sterile, while those of 4x wheats are more or less male fertile. Only the genome of T. spelta duhamelianum restores completely pollen fertility.Among the indispensable factors for the success of hybrid wheat, five were discussed. They were (1) hetero sis, (2) selection of male sterile cytoplasms, (3) discovery of restoring genes, (4) production of hybrid seeds and (5) quality.

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Zusammenfassung Die Methode der Substitution und Restoration des Nucleus wird kurz beschrieben.Drei Arten, Aegilops caudata, Ae. ovata und Triticum timopheevi, wurden als Donor cytoplasmatisch bedingter männlicher Sterilität verwendet. Die Charakteristika der jeweiligen Cytoplasmen lassen sich wie folgt zusammenfassen: Caudata-Cytoplasma: Dieses Cytoplasma hat in vieler Hinsicht einen schädlichen Einfluß auf die Manifestation fremder Genome. Substitutionslinien mit einem hexaploiden Weizengenom sind meist männlich steril, das weibliche Organ ist normal. Einige Linien bringen häufig keimlose Samen; in anderen Linien treten haploide und Zwillingssamen auf. Bei Substitutionslinien mit tetraploiden Weizengenomen werden häufig andere Blütenorgane in Karpelle umgewandelt. Ovata-Cytoplasma: In den Substitutionslinien sowohl der hexaploiden wie tetraploiden Weizen wurden keine anderen Blütenorgane in Karpelle umgewandelt. Die Substitutionslinien der hexaploiden Weizen sind stets vollkommen männlich steril mit Ausnahme von P 168, einer Weizenvarietät, die ein Paar Sat-Chromosomen von Ae. caudata besitzt. Diese Varietät stellt die männliche Fertilität vollkommen wieder her. In den Emmer-Substitutionslinien wurden keine wirksamen Restorer gefunden. Bei den 4x-Substitutionslinien zeigt sich häufig verzögertes Ährenschieben. Timopheevi-Cytoplasma: Die Substitutionslinien der 6x-Weizen sind meist männlich steril, die von 4x-Weizen dagegen mehr oder weniger männlich fertil. Nur das Genom von T. spelta duhamelianum stellt die Pollenfertilität völlig wieder her.Von den für den Erfolg der Hybridweizenzüchtung unabdingbaren Faktoren wurden die folgenden 5 besprochen: 1. Heterosis, 2. Selektion männliche Sterilität bedingender Cytoplasmen, 3. Auffinden von Restorergenen, 4. Produktion von Hybridsaatgut und 5. Qualität.

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Dedicated to Professor Hans Stubbe on the occasion of his 65^th birthday.

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Contribution from the National Institute of Genetics, Japan, No. 636. This paper has been prepared for a lecture delivered July 18, 1966, at the Lenin All-Union Academy of Agricultural Science. This work has been supported by the Rockefeller Foundation, Grant GA AGR 65111.     

Evolution of male tail development in rhabditid nematodes related to Caenorhabditis elegans

The evolutionary pathway that has led to male tails of diverse morphology among species of the nematode family Rhabditidae was reconstructed. This family includes the well-studied model species Caenorhabditis elegans. By relating the steps of male tail morphological evolution to the phenotypic changes brought about by developmental mutations induced experimentally in C. elegans, the goal is to identify genes responsible for morphological evolution. The varying morphological characters of the male tails of several rhabiditid species have been described previously (Fitch and Emmons, 1995, Dev. Biol. 170:564-582). The developmental events preceding differentiation of the adult structures have also been analyzed; in many cases the origins of varying adult morphological characters were traced to differences during ontogeny. In the present work, the evolutionary changes producing these differences were reconstructed in the context of the four possible phylogenies supported independently by sequences of 18S ribosomal RNA genes (rDNA). Two or more alternative states were defined for 36 developmental and adult morphological characters. These characters alone do not provide sufficient data to resolve most species relationships; however, when combined with the rDNA characters, they provide stronger support for one of the four rDNA phylogenies. Assuming a model of ordered transformations for multistate developmental characters generally results in greater resolution. Transformations between character states can be assigned unequivocally by parsimony to unambiguous branches for most of the characters. Correlations are thereby revealed for some of the developmental characters, indicating a probability of a shared developmental or genetic regulatory pathway. Four of the unequivocal character state changes on unambiguously supported branches closely resemble the phenotypic changes brought about by known mutations in C. elegans. These mutations define genes that are known to act in genetic regulatory hierarchies controlling pattern formation, differentiation, and morphogenesis. Although these studies are still at an early stage, these results strongly suggest that parallel studies of developmental mutants in C. elegans and of morphological and developmental evolution among related nematodes will help define genetic changes underlying the evolution of form.     

Genetics and evolution of hybrid male sterility in house mice

Comparative genetic mapping provides insights into the evolution of the reproductive barriers that separate closely related species. This approach has been used to document the accumulation of reproductive incompatibilities over time, but has only been applied to a few taxa. House mice offer a powerful system to reconstruct the evolution of reproductive isolation between multiple subspecies pairs. However, studies of the primary reproductive barrier in house mice-hybrid male sterility-have been restricted to a single subspecies pair: Mus musculus musculus and Mus musculus domesticus. To provide a more complete characterization of reproductive isolation in house mice, we conducted an F(2) intercross between wild-derived inbred strains from Mus musculus castaneus and M. m. domesticus. We identified autosomal and X-linked QTL associated with a range of hybrid male sterility phenotypes, including testis weight, sperm density, and sperm morphology. The pseudoautosomal region (PAR) was strongly associated with hybrid sterility phenotypes when heterozygous. We compared QTL found in this cross with QTL identified in a previous F(2) intercross between M. m. musculus and M. m. domesticus and found three shared autosomal QTL. Most QTL were not shared, demonstrating that the genetic basis of hybrid male sterility largely differs between these closely related subspecies pairs. These results lay the groundwork for identifying genes responsible for the early stages of speciation in house mice.     

A simple genetic incompatibility causes hybrid male sterility in mimulus

Much evidence has shown that postzygotic reproductive isolation (hybrid inviability or sterility) evolves by the accumulation of interlocus incompatibilities between diverging populations. Although in theory only a single pair of incompatible loci is needed to isolate species, empirical work in Drosophila has revealed that hybrid fertility problems often are highly polygenic and complex. In this article we investigate the genetic basis of hybrid sterility between two closely related species of monkeyflower, Mimulus guttatus and M. nasutus. In striking contrast to Drosophila systems, we demonstrate that nearly complete hybrid male sterility in Mimulus results from a simple genetic incompatibility between a single pair of heterospecific loci. We have genetically mapped this sterility effect: the M. guttatus allele at the hybrid male sterility 1 (hms1) locus acts dominantly in combination with recessive M. nasutus alleles at the hybrid male sterility 2 (hms2) locus to cause nearly complete hybrid male sterility. In a preliminary screen to find additional small-effect male sterility factors, we identified one additional locus that also contributes to some of the variation in hybrid male fertility. Interestingly, hms1 and hms2 also cause a significant reduction in hybrid female fertility, suggesting that sex-specific hybrid defects might share a common genetic basis. This possibility is supported by our discovery that recombination is reduced dramatically in a cross involving a parent with the hms1-hms2 incompatibility.     

转基因雄性不育系及其在杂种种子生产上的应用

雄性不育为农作物杂种优势的利用开辟了一条经济有效的途径。本综述了利用生物技术培育转基因雄性不育的多种策略,以及繁育用作大田配制杂交种的母本雄性不育系的新方法;探讨了其应用于商业化杂种生产的重要性及前景。     

The effects of cytoplasmic male sterility on cytonuclear disequilibria in hybrid zones

Male sterility is studied in hybrid zones by different measures of cytonuclear disequilibria, D, D₁, D₂, and D₃. Of particular interest are the dynamics of disequilibria as the system evolves to equilibrium. Our first model, the hybrid swarm model, yields equilibrium results identical to those observed in a model with random mating. In our second model of a hybrid zone, predictions of the sign pattern of disequilibrium values can be made based on migration values. A characteristic sign pattern may help to distinguish cytoplasmic male sterility (CMS) from other mechanisms of selection. Our simple CMS model with migration is successfully fit to cytonuclear data on a hybrid population of cottonwoods.     

Cytoplasmic male sterility (CMS) in hybrid breeding in field crops

Key message

A comprehensive understanding of CMS/Rf system enabled by modern omics tools and technologies considerably improves our ability to harness hybrid technology for enhancing the productivity of field crops.

Abstract

Harnessing hybrid vigor or heterosis is a promising approach to tackle the current challenge of sustaining enhanced yield gains of field crops. In the context, cytoplasmic male sterility (CMS) owing to its heritable nature to manifest non-functional male gametophyte remains a cost-effective system to promote efficient hybrid seed production. The phenomenon of CMS stems from a complex interplay between maternally-inherited (mitochondrion) and bi-parental (nucleus) genomic elements. In recent years, attempts aimed to comprehend the sterility-inducing factors (orfs) and corresponding fertility determinants (Rf) in plants have greatly increased our access to candidate genomic segments and the cloned genes. To this end, novel insights obtained by applying state-of-the-art omics platforms have substantially enriched our understanding of cytoplasmic-nuclear communication. Concomitantly, molecular tools including DNA markers have been implicated in crop hybrid breeding in order to greatly expedite the progress. Here, we review the status of diverse sterility-inducing cytoplasms and associated Rf factors reported across different field crops along with exploring opportunities for integrating modern omics tools with CMS-based hybrid breeding.

     

Patterns of male sterility in a grasshopper hybrid zone imply accumulation of hybrid incompatibilities without selection

It is now widely accepted that post-zygotic reproductive isolation is the result of negative epistatic interactions between derived alleles fixed independently at different loci in diverging populations (the Dobzhansky-Muller model). What is less clear is the nature of the loci involved and whether the derived alleles increase in frequency through genetic drift, or as a result of natural or sexual selection. If incompatible alleles are fixed by selection, transient polymorphisms will be rare and clines for these alleles will be steep where divergent populations meet. If they evolve by drift, populations are expected to harbour substantial genetic variation in compatibility and alleles will introgress across hybrid zones once they recombine onto a genetic background with which they are compatible. Here we show that variation in male sterility in a naturally occurring Chorthippus parallelus grasshopper hybrid zone conforms to the neutral expectations. Asymmetrical clines for male sterility have long tails of introgression and populations distant from the zone centre show significant genetic variation for compatibility. Our data contrast with recent observations on 'speciation genes' that have diverged as a result of strong natural selection.     

Genetic interactions underlying hybrid male sterility in the Drosophila bipectinata species complex

Understanding genetic mechanisms underlying hybrid male sterility is one of the most challenging problems in evolutionary biology especially speciation. By using the interspecific hybridization method roles of Y chromosome, Major Hybrid Sterility (MHS) genes and cytoplasm in sterility of hybrid males have been investigated in a promising group, the Drosophila bipectinata species complex that consists of four closely related species: D. pseudoananassae, D. bipectinata, D. parabipectinata and D. malerkotliana. The interspecific introgression analyses show that neither cytoplasm nor MHS genes are involved but X-Y interactions may be playing major role in hybrid male sterility between D. pseudoananassae and the other three species. The results of interspecific introgression analyses also show considerable decrease in the number of males in the backcross offspring and all males have atrophied testes. There is a significant positive correlation between sex - ratio distortion and severity of sterility in backcross males. These findings provide evidence that D. pseudoananassae is remotely related with other three species of the D. bipectinata species complex.     

The contribution of the y chromosome to hybrid male sterility in house mice

Hybrid sterility in the heterogametic sex is a common feature of speciation in animals. In house mice, the contribution of the Mus musculus musculus X chromosome to hybrid male sterility is large. It is not known, however, whether F(1) male sterility is caused by X-Y or X-autosome incompatibilities or a combination of both. We investigated the contribution of the M. musculus domesticus Y chromosome to hybrid male sterility in a cross between wild-derived strains in which males with a M. m. musculus X chromosome and M. m. domesticus Y chromosome are partially sterile, while males from the reciprocal cross are reproductively normal. We used eight X introgression lines to combine different X chromosome genotypes with different Y chromosomes on an F(1) autosomal background, and we measured a suite of male reproductive traits. Reproductive deficits were observed in most F(1) males, regardless of Y chromosome genotype. Nonetheless, we found evidence for a negative interaction between the M. m. domesticus Y and an interval on the M. m. musculus X that resulted in abnormal sperm morphology. Therefore, although F(1) male sterility appears to be caused mainly by X-autosome incompatibilities, X-Y incompatibilities contribute to some aspects of sterility.     

Inbreeding and outbreeding depression in Caenorhabditis nematodes

The nematode Caenorhabditis elegans reproduces primarily by self-fertilization of hermaphrodites, yet males are present at low frequencies in natural populations (androdioecy). The ancestral state of C. elegans was probably gonochorism (separate males and females), as in its relative C. remanei. Males may be maintained in C. elegans because outcrossed individuals escape inbreeding depression. The level of inbreeding depression is, however, expected to be low in such a highly selfing species, compared with an outcrosser like C. remanei. To investigate these issues, we measured life-history traits in the progeny of inbred versus outcrossed C. elegans and C. remanei individuals derived from recently isolated natural populations. In addition, we maintained inbred lines of C. remanei through 13 generations of full-sibling mating. Highly inbred C. remanei showed dramatic reductions in brood size and relative fitness compared to outcrossed individuals, with evidence of both direct genetic and maternal-effect inbreeding depression. This decline in fitness accumulated over time, causing extinction of nearly 90% of inbred lines, with no evidence of purging of deleterious mutations from the remaining lines. In contrast, pure strains of C. elegans performed better than crosses between strains, indicating outbreeding depression. The results are discussed in relation to the evolution of androdioecy and the effect of mating system on the level of inbreeding depression.     

Genetic basis of hybrid male sterility among three closely related species of Drosophila

The genetic basis of hybrid male sterility among three closely related species, Drosophila bipectinata, D. parabipectinata and D. malerkotliana has been investigated by using backcross analysis methods. The role of Y chromosome, major hybrid sterility (MHS) genes (genetic factors) and cytoplasm (non-genetic factor) have been studied in the hybrids of these three species. In the species pair, bipectinata--parabipectinata, Y chromosome introgression of parabipectinata in the genomic background of bipectinata and the reciprocal Y chromosome introgression were unsuccessful as all males in second backcross generation were sterile. Neither MHS genes nor cytoplasm was found important for sterility. This suggests the involvement of X-Y, X-autosomes or polygenic interactions in hybrid male sterility. In bipectinata--malerkotliana and parabipectinata--malerkotliana species pairs, Y chromosome substitution in reciprocal crosses did not affect male fertility. Backcross analyses also show no involvement of MHS genes or cytoplasm in hybrid male sterility in these two species pairs. Therefore, X- autosome interaction or polygenic interaction is supposed to be involved in hybrid male sterility in these two species pairs. These findings also provide evidence that even in closely related species, genetic interactions underlying hybrid male sterility may vary.     

Cytoplasmic male sterility in barley

The maternal male sterile barley msm1 with or without a dominant gene, Rfmla, which restores male fertility, was studied. Determined with SDS-PAGE, the polypeptide pattern in the anthers of unrestored msm1 plants remains juvenile in the middle of anther development, two major zones being absent or weak. At the stage when anther development stops in msm1 plants, the anther proteins appear to be hydrolyzed to short-chain peptides. Restored plants, heterozygous for the restorer gene, Rfmla, behaved like the near-isogenic normal barley, cv. Adorra. The total leaf protein pattern of young leaf tissue and the chloroplastidic membrane protein pattern are normal in msm1 cytoplasm when studied with this technique. Chlorophyll b is unnecessary for restoration by Rfmla, though the restored plants have a lower chlorophyll a/b ratio than an unrestored plant in the mature stem leaf. Mature stem leaf pieces of unrestored msm1 plants were induced to senesce with 20 mM NaCl solution. This senescence was inhibited by exogenous kinetin. Leaf pieces of restored msm1 plants or those of near-isogenic normal barley behaved in the same way in the NaCl solution as in distilled water. Many features of the physiology of restored plants can be explained as the functions of cytokinins. Kernels of male sterile plants have a more rapid root elongation at germination than near-isogenic normal barley.     

Cytoplasmic male sterility in barley

Summary Restoration in the msm1 cytoplasm of barley (Hordeum vulgare L. s.l.) was studied from the standpoint of population biology and physiological effects on kernel protein. Restorer genes of 82 accessions of wild barley (ssp. spontaneum) from Israel were determined. 38% of the accessions were maintainers of sterility, 48% were partial restorers, and 14% were restorers. Fourteen dominant restorer genes are described, and evidence for three cases of allelism to Rfm1a is presented. The restorer accessions and their designated gene symbols are: PI 282636 (Rfm,,e), PI 282637 (Rfm,f), PI 282646 (Rfm,,g), PI 284742 (Rfm,h), PI 284743 (Rfm,,i), PI 284753 (Rfm,,j), PI 284755 (Rfm1d), PI 296838 (Rfm,,k), PI 296850 isolate 16/7 (Rfm,,l), PI 296853 (Rfm,,m), PI 296856 (Rfm1b), PI 296899 (Rfm,,n), PI 296919 (Rfm1c), PI 296944 (Rfm,,o). PI 296850 was found to contain both a restorer and a non-restorer genotype. None of the PI accessions with a restorer gene is a carrier of an msm1-type male sterilizing cytoplasm. In the present sample, plants with restoration ability occurred with a higher frequency in the material from the Judean Foothills than that from the other regions of Israel. The greater adaptive value of plants with restoration ability on certain soil associations in semiarid and subhumic climate is suggested. The considerable frequency of restorers and partial restorers in male fertile cytoplasm suggests that the restoration system evolved before the msm1-type cytoplasm. In the nuclear genotype near-isogenic with either Adorra or Risø 1508, msm1 plants heterozygous for Rfm1a produced 98.6 or 98.5% of the protein content in the respective recurrent pollen parent varieties. The amino acid compositions of the derivatives differed little from those of the varieties. In the derivatives, a consistent decrease was found in tryptophan, and consistent increases in isoleucine, phenyalanine, lysine, histidine, and arginine. In relation to glucose consumption, the bioenergetic cost calculated for the amino acid patterns found in the restored msm1 derivatives was slightly higher than that for the near-isogenic pollen parent varieties. The results suggest that the restorer gene in the heterozygous state normalizes the physiology of msm1 cytoplasm to a great extent.