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Hybrid decay: a transgenerational epigenetic decline in vigor and viability triggered in backcross populations of teosinte with maize

View ORCID ProfileWei Xue, View ORCID ProfileSarah N. Anderson, View ORCID ProfileXufeng Wang, View ORCID ProfileLiyan Yang, View ORCID ProfilePeter A. Crisp, View ORCID ProfileQing Li, View ORCID ProfileJaclyn Noshay, Patrice S. Albert, View ORCID ProfileJames A. Birchler, View ORCID ProfilePaul Bilinski, View ORCID ProfileMichelle C. Stitzer, View ORCID ProfileJeffrey Ross-Ibarra, View ORCID ProfileSherry Flint-Garcia, View ORCID ProfileXuemei Chen, View ORCID ProfileNathan M. Springer, View ORCID ProfileJohn F. Doebley
doi: https://doi.org/10.1101/588715
Wei Xue
*Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706
†College of Agronomy, Shenyang Agricultural University, 110866, Liaoning Province, China
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Sarah N. Anderson
‡Department of Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota 55108
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Xufeng Wang
§Guangdong Provincial Key Laboratory for Plant Epigenetics, Shenzhen University, 518060, Guangdong Province, China
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Liyan Yang
*Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706
**Life Science College, Shanxi Normal University, 041004, Shanxi Province, China
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Peter A. Crisp
‡Department of Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota 55108
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Qing Li
‡Department of Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota 55108
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Jaclyn Noshay
‡Department of Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota 55108
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Patrice S. Albert
††Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211
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James A. Birchler
††Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211
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Paul Bilinski
‡‡Department of Plant Sciences, University of California, Davis, California 95616
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Michelle C. Stitzer
‡‡Department of Plant Sciences, University of California, Davis, California 95616
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Jeffrey Ross-Ibarra
‡‡Department of Plant Sciences, University of California, Davis, California 95616
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Sherry Flint-Garcia
††Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211
§§Agricultural Research Service, United States Department of Agriculture, Columbia, Missouri, 65211
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Xuemei Chen
§Guangdong Provincial Key Laboratory for Plant Epigenetics, Shenzhen University, 518060, Guangdong Province, China
***Department of Botany and Plant Sciences, University of California, Riverside, California 92521
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Nathan M. Springer
‡Department of Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota 55108
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John F. Doebley
*Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706
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  • For correspondence: jdoebley@wisc.edu
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ABSTRACT

In the course of generating populations of maize with teosinte chromosomal introgressions, an unusual sickly plant phenotype was noted in individuals from crosses with two teosinte accessions collected near Valle de Bravo, Mexico. The plants of these Bravo teosinte accessions appear phenotypically normal themselves and the F1 plants appear similar to typical maize x teosinte F1s. However, upon backcrossing to maize, the BC1 and subsequent generations display a number of detrimental characteristics including shorter stature, reduced seed set and abnormal floral structures. This phenomenon is observed in all BC individuals and there is no chromosomal segment linked to the sickly plant phenotype in advanced backcross generations. Once the sickly phenotype appears in a lineage, normal plants are never again recovered by continued backcrossing to the normal maize parent. Whole-genome shotgun sequencing reveals a small number of genomic sequences, some with homology to transposable elements, that have increased in copy number in the backcross populations. Transcriptome analysis of seedlings, which do not have striking phenotypic abnormalities, identified segments of 18 maize genes that exhibit increased expression in sickly plants. A de novo assembly of transcripts present in plants exhibiting the sickly phenotype identified a set of 59 up-regulated novel transcripts. These transcripts include some examples with sequence similarity to transposable elements and other sequences present in the recurrent maize parent (W22) genome as well as novel sequences not present in the W22 genome. Genome-wide profiles of gene expression, DNA methylation and sRNAs are similar between sickly plants and normal controls, although a few up-regulated transcripts and transposable elements are associated with altered sRNA or methylation profiles. This study documents hybrid incompatibility and genome instability triggered by the backcrossing of Bravo teosinte with maize. We name this phenomenon “hybrid decay” and present ideas on the mechanism that may underlie it.

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Posted March 26, 2019.
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Hybrid decay: a transgenerational epigenetic decline in vigor and viability triggered in backcross populations of teosinte with maize
Wei Xue, Sarah N. Anderson, Xufeng Wang, Liyan Yang, Peter A. Crisp, Qing Li, Jaclyn Noshay, Patrice S. Albert, James A. Birchler, Paul Bilinski, Michelle C. Stitzer, Jeffrey Ross-Ibarra, Sherry Flint-Garcia, Xuemei Chen, Nathan M. Springer, John F. Doebley
bioRxiv 588715; doi: https://doi.org/10.1101/588715
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Hybrid decay: a transgenerational epigenetic decline in vigor and viability triggered in backcross populations of teosinte with maize
Wei Xue, Sarah N. Anderson, Xufeng Wang, Liyan Yang, Peter A. Crisp, Qing Li, Jaclyn Noshay, Patrice S. Albert, James A. Birchler, Paul Bilinski, Michelle C. Stitzer, Jeffrey Ross-Ibarra, Sherry Flint-Garcia, Xuemei Chen, Nathan M. Springer, John F. Doebley
bioRxiv 588715; doi: https://doi.org/10.1101/588715

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