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Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species.
Genetics 2019; 212(3):801-813G

Abstract

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. briggsae X 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.

Authors+Show Affiliations

Department of Biology, Hong Kong Baptist University, Hong Kong, China.Department of Biology, Hong Kong Baptist University, Hong Kong, China.Department of Biology, Hong Kong Baptist University, Hong Kong, China.Department of Biology, Hong Kong Baptist University, Hong Kong, China.Department of Biology, Hong Kong Baptist University, Hong Kong, China.Department of Biology, Hong Kong Baptist University, Hong Kong, China zyzhao@hkbu.edu.hk. State Key Laboratory of Environmental and Biological Analysis, Hong Kong Baptist University, Hong Kong, China.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

Language

eng

PubMed ID

31064822

Citation

Bi, Yu, et al. "Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species." Genetics, vol. 212, no. 3, 2019, pp. 801-813.
Bi Y, Ren X, Li R, et al. Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species. Genetics. 2019;212(3):801-813.
Bi, Y., Ren, X., Li, R., Ding, Q., Xie, D., & Zhao, Z. (2019). Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species. Genetics, 212(3), pp. 801-813. doi:10.1534/genetics.119.302202.
Bi Y, et al. Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species. Genetics. 2019;212(3):801-813. PubMed PMID: 31064822.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Specific Interactions Between Autosome and X Chromosomes Cause Hybrid Male Sterility in Caenorhabditis Species. AU - Bi,Yu, AU - Ren,Xiaoliang, AU - Li,Runsheng, AU - Ding,Qiutao, AU - Xie,Dongying, AU - Zhao,Zhongying, Y1 - 2019/05/07/ PY - 2019/01/28/received PY - 2019/05/03/accepted PY - 2020/07/01/pmc-release PY - 2019/5/9/pubmed PY - 2019/5/9/medline PY - 2019/5/9/entrez KW - C. nigoni KW - Caenorhabditis briggsae KW - X–autosome interaction KW - hybrid male sterility KW - introgression SP - 801 EP - 813 JF - Genetics JO - Genetics VL - 212 IS - 3 N2 - 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. briggsae X 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. SN - 1943-2631 UR - https://www.unboundmedicine.com/medline/citation/31064822/Specific_Interactions_Between_Autosome_and_X_Chromosomes_Cause_Hybrid_Male_Sterility_in_Caenorhabditis_Species L2 - http://www.genetics.org/cgi/pmidlookup?view=long&pmid=31064822 DB - PRIME DP - Unbound Medicine ER -