scholarly journals Genome wide screen reveals a specific interaction between autosome and X that is essential for hybrid male sterility

2018 ◽  
Author(s):  
Zhongying Zhao ◽  
Yu Bi ◽  
Xiaoliang Ren ◽  
Runsheng Li ◽  
Qiutao Ding ◽  
...  
Keyword(s):  
Male Sterility ◽  
Male Fertility ◽  
Hybrid Male ◽  
Female Progeny ◽  
Hybrid Male Sterility ◽  
Male And Female ◽  
Genome Wide ◽  
F1 Progeny ◽  
Asymmetric Hybrid ◽  
Parent Of Origin

Hybrid male progeny from interspecies cross are more prone to sterility or inviability than hybrid female progeny, and the male sterility and inviability often demonstrate a parent-of-origin asymmetry. However, the underlying mechanism of asymmetric sterility or inviability remains elusive. We previously established a genome-wide hybrid incompatibility (HI) landscape between Caenorhabditis briggsae and C. nigoni by phenotyping a large collection of C. nigoni strains each carrying a C. briggsae introgression. In this study, we investigate the genetic mechanism of asymmetric sterility and inviability in both hybrid male and female progeny between the two species. Specifically, we performed reciprocal crosses between C. briggsae and different C. nigoni strains that each carries a GFP-labeled C. briggsae genomic fragment referred to as introgression, and scored the HI phenotypes in the F1 progeny. The aggregated introgressions cover 94.6% of the C. briggsae genome, including 100% of the X chromosome. Surprisingly, we observed that two C. briggsae X fragments that produce C. nigoni male sterility as an introgression rescued hybrid F1 sterility in males fathered by C. briggsae, indicating that at least two separate X-autosome interactions are involved in the hybrid male sterility. In addition, we identified another two C. briggsae genomic intervals on the Chromosome II or IV, respectively, which can rescue the inviability, but not the sterility, of hybrid F1 males fathered by C. nigoni, suggesting the involvement of differential epistatic interactions in the asymmetric hybrid male fertility and inviability. Importantly, backcrossing of the rescued sterile males with C. nigoni led to isolation of a 1.1-Mb genomic interval that specifically interacts with an X-linked introgression, which is essential for hybrid male fertility. We further identified three C. briggsae genomic intervals on the Chromosome I, II and III, respectively that produce inviability in all F1 progeny dependent or independent of the parent-of-origin. Taken together, we identified multiple independent interacting loci that are responsible for asymmetric hybrid male and female sterility and inviability, which provides important insights into the asymmetric HI and lays a foundation for their molecular characterization.

scholarly journals Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species

Genetics ◽  
2019 ◽  
Vol 212 (3) ◽  
pp. 801-813 ◽  
Author(s):  
Yu Bi ◽  
Xiaoliang Ren ◽  
Runsheng Li ◽  
Qiutao Ding ◽  
Dongying Xie ◽  
...  
Keyword(s):  
Male Sterility ◽  
Male Fertility ◽  
Genetic Mechanism ◽  
Hybrid Male ◽  
Female Progeny ◽  
Hybrid Male Sterility ◽  
Male And Female ◽  
F1 Progeny ◽  
Asymmetric Hybrid ◽  
Parent Of Origin

Hybrid male progeny from interspecies crosses are more prone to sterility or inviability than hybrid female progeny, and the male sterility and inviability often demonstrate parent-of-origin asymmetry. However, the underlying genetic mechanism of asymmetric sterility or inviability remains elusive. We previously established a genome-wide hybrid incompatibility (HI) landscape between Caenorhabditis briggsae and C. nigoni by phenotyping a large collection of C. nigoni strains each carrying a C. briggsae introgression. In this study, we systematically dissect the genetic mechanism of asymmetric sterility and inviability in both hybrid male and female progeny between the two species. Specifically, we performed reciprocal crosses between C. briggsae and different C. nigoni strains that each carry a GFP-labeled C. briggsae genomic fragment referred to as introgression, and scored the HI phenotypes in the F1 progeny. The aggregated introgressions cover 94.6% of the C. briggsae genome, including 100% of the X chromosome. Surprisingly, we observed that two C. briggsaeX fragments that produce C. nigoni male sterility as an introgression rescued hybrid F1 sterility in males fathered by C. briggsae. Subsequent backcrossing analyses indicated that a specific interaction between the X-linked interaction and one autosome introgression is required to rescue the hybrid male sterility. In addition, we identified another two C. briggsae genomic intervals on chromosomes II and IV that can rescue the inviability, but not the sterility, of hybrid F1 males fathered by C. nigoni, suggesting the involvement of differential epistatic interactions in the asymmetric hybrid male fertility and inviability. Importantly, backcrossing of the rescued sterile males with C. nigoni led to the isolation of a 1.1-Mb genomic interval that specifically interacts with an X-linked introgression, which is essential for hybrid male fertility. We further identified three C. briggsae genomic intervals on chromosome I, II, and III that produced inviability in all F1 progeny, dependent on or independent of the parent-of-origin. Taken together, we identified multiple independent interacting loci that are responsible for asymmetric hybrid male and female sterility, and inviability, which lays a foundation for their molecular characterization.

scholarly journals Genome-wide misexpression of X-linked versus autosomal genes associated with hybrid male sterility

2010 ◽  
Vol 20 (8) ◽  
pp. 1097-1102 ◽  
Author(s):  
X. Lu ◽  
J. A. Shapiro ◽  
C.-T. Ting ◽  
Y. Li ◽  
C. Li ◽  
...  
Keyword(s):  
Male Sterility ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Genome Wide

scholarly journals Rampant Misexpression in a Mimulus (Monkeyflower) Introgression Line Caused by Hybrid Sterility, Not Regulatory Divergence

2020 ◽  
Vol 37 (7) ◽  
pp. 2084-2098 ◽  
Author(s):  
Rachel E Kerwin ◽  
Andrea L Sweigart
Keyword(s):  
Male Sterility ◽  
Gene Expression Regulation ◽  
Hybrid Sterility ◽  
Introgression Line ◽  
Transcript Abundance ◽  
Stabilizing Selection ◽  
Hybrid Male ◽  
Specific Expression ◽  
Hybrid Male Sterility ◽  
Genome Wide

Abstract Divergence in gene expression regulation is common between closely related species and may give rise to incompatibilities in their hybrid progeny. In this study, we investigated the relationship between regulatory evolution within species and reproductive isolation between species. We focused on a well-studied case of hybrid sterility between two closely related yellow monkeyflower species, Mimulus guttatus and Mimulus nasutus, that is caused by two epistatic loci, hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2). We compared genome-wide transcript abundance across male and female reproductive tissues (i.e., stamens and carpels) from four genotypes: M. guttatus, M. nasutus, and sterile and fertile progeny from an advanced M. nasutus–M. guttatus introgression line carrying the hms1–hms2 incompatibility. We observed substantial variation in transcript abundance between M. guttatus and M. nasutus, including distinct but overlapping patterns of tissue-biased expression, providing evidence for regulatory divergence between these species. We also found rampant genome-wide misexpression, but only in the affected tissues (i.e., stamens) of sterile introgression hybrids carrying incompatible alleles at hms1 and hms2. Examining patterns of allele-specific expression in sterile and fertile introgression hybrids, we found evidence for interspecific divergence in cis- and trans-regulation, including compensatory cis–trans mutations likely to be driven by stabilizing selection. Nevertheless, species divergence in gene regulatory networks cannot explain the vast majority of the gene misexpression we observe in Mimulus introgression hybrids, which instead likely manifests as a downstream consequence of sterility itself.

scholarly journals Genome-wide misexpression associated with hybrid sterility in Mimulus (monkeyflower)

2019 ◽  
Author(s):  
Rachel E. Kerwin ◽  
Andrea L. Sweigart
Keyword(s):  
Male Sterility ◽  
Gene Expression Regulation ◽  
Hybrid Sterility ◽  
Introgression Line ◽  
Transcript Abundance ◽  
Stabilizing Selection ◽  
Hybrid Male ◽  
Specific Expression ◽  
Hybrid Male Sterility ◽  
Genome Wide

ABSTRACTDivergence in gene expression regulation is common between closely related species and may give rise to incompatibilities in their hybrid progeny. In this study, we investigated the relationship between regulatory evolution within species and reproductive isolation between species. We focused on a well-studied case of hybrid sterility between Mimulus guttatus and M. nasutus, two closely related yellow monkeyflower species, that is caused by two epistatic loci, hybrid male sterility 1 (hms1) and hybrid male sterility 2 (hms2). We quantified and compared global transcript abundance across male and female reproductive tissues (i.e. stamens and carpels) of M. guttatus and M. nasutus, as well as sterile and fertile progeny from an advanced M. nasutus-M. guttatus introgression line that carries the hms1-hms2 incompatibility. We observed substantial variation in transcript abundance between M. guttatus and M. nasutus, including distinct but overlapping patterns of tissue-biased expression, providing evidence for regulatory divergence between these species. Furthermore, we found pervasive genome-wide misexpression exclusively associated with hybrid sterility – only observed in the affected tissues (i.e. stamens) of sterile introgression hybrids. Examining patterns of allele-specific expression in sterile and fertile hybrids, we found evidence of cis- and trans- regulatory divergence, as well as cis-trans compensatory evolution (likely to be driven by stabilizing selection). However, regulatory divergence does not appear to cause misexpression in sterile hybrids, which instead likely manifests as a downstream consequence of sterility itself.

scholarly journals Genetics of Male and Female Sterility in Hybrids of Drosophila pseudoobscura and D. persimilis

Genetics ◽  
1987 ◽  
Vol 116 (4) ◽  
pp. 555-563
Author(s):  
H Allen Orr
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Male Fertility ◽  
Genetic Basis ◽  
Female Sterility ◽  
Drosophila Pseudoobscura ◽  
Testis Size ◽  
Hybrid Male ◽  
Male And Female ◽  
Male And Female Sterility

ABSTRACT The genetic basis of male and female sterility in hybrids of Drosophila pseudoobscura-Drosophila persimilis was studied using backcross analysis. Previous studies indirectly assessed male fertility by measuring testis size; these studies concluded that male sterility results from an X chromosome-autosome imbalance. By directly scoring for the production of motile sperm, male sterility is shown to be largely due to an incompatibility between genes on the X and Y chromosomes of these two species. These species have diverged at a minimum of nine loci affecting hybrid male fertility. Semisterility of hybrid females appears to result from an X chromosome-cytoplasm interaction; the X chromosome thus has the largest effect on sterility in both male and female hybrids. This is apparently the first analysis of the genetic basis of female sterility, or of sterility/inviability affecting both sexes, in an animal hybridization.

scholarly journals Hidden Effects of X Chromosome Introgressions on Spermatogenesis in Drosophila simulans × D. mauritiana Hybrids Unveiled by Interactions Among Minor Genetic Factors

Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 745-754 ◽  
Author(s):  
Xulio R Maside ◽  
José P Barral ◽  
Horacio F Naveira
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Seminal Vesicles ◽  
Genetic Dissection ◽  
Research Strategies ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Epistatic Interactions ◽  
Drosophila Mauritiana ◽  
Chromosome Segments

Abstract One of the most frequent outcomes of interspecific hybridizations in Drosophila is hybrid male sterility. Genetic dissection of this reproductive barrier has revealed that the number of responsible factors is very high and that these factors are frequently engaged in complex epistatic interactions. Traditionally, research strategies have been based on contrasting introgressions of chromosome segments that produce male sterility with those that allow fertility. Few studies have investigated the phenotypes associated with the boundary between fertility and sterility. In this study, we cointrogressed three different X chromosome segments from Drosophila mauritiana into D. simulans. Hybrid males with these three segments are usually fertile, by conventional fertility assays. However, their spermatogenesis shows a significant slowdown, most manifest at lower temperatures. Each of the three introgressed segments retards the arrival of sperm to the seminal vesicles. Other small disturbances in spermatogenesis are evident, which altogether lead to an overall reduction in the amount of motile sperm in their seminal vesicles. These results suggest that a delay in the timing of spermatogenesis, which might be brought about by the cumulative action of many different factors of minor segment, may be the primary cause of hybrid male sterility.

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