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Genetics. 2019 Sep;213(1):143-160. doi: 10.1534/genetics.119.302378. Epub 2019 Jul 18.

Hybrid Decay: A Transgenerational Epigenetic Decline in Vigor and Viability Triggered in Backcross Populations of Teosinte with Maize.

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College of Agronomy, Shenyang Agricultural University, 110866 Liaoning Province, China.
Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706.
Department of Plant and Microbial Biology, University of Minnesota, St. Paul, Minnesota 55108.
Guangdong Provincial Key Laboratory for Plant Epigenetics, Shenzhen University, 518060 Guangdong Province, China.
Life Science College, Shanxi Normal University, 041004 Shanxi Province, China.
Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211.
Department of Plant Sciences, University of California, Davis, California 95616.
Agricultural Research Service, United States Department of Agriculture, Columbia, Missouri 65211.
Department of Botany and Plant Sciences, University of California, Riverside, California 92521.
Department of Genetics, University of Wisconsin, Madison, Wisconsin 53706


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 × 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 upregulated 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 small RNAs are similar between sickly plants and normal controls, although a few upregulated transcripts and transposable elements are associated with altered small RNA 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.


CNVs; Zea mays; epigenetic; maize; sRNAs; teosinte; transposable element (TE)

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