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

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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 3 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.

Original languageEnglish (US)
Pages (from-to)143-160
Number of pages18
JournalGenetics
Volume213
Issue number1
DOIs
StatePublished - 2019

Bibliographical note

Funding Information:
We thank Xuehua Zhong and Chin Jian Yang for helpful discussions regarding this work, and Eric Rentmeester, Adam Mittermaier, Elizabeth Buschert, and Jonathan Giesler for technical assistance. We thank the University of Wisconsin Biotechnology Center DNA Sequencing Facility for providing next-generation sequencing consultation and services. This research was supported by the National Science Foundation grants IOS-1238014 (J.F.D. and S.F.-G.), IOS-1237931 (to N.M.S.), and IOS-1444514 (J.A.B.), and by USDA-NIFA (United States Department of Agriculture National Institute for Food and Agriculture) grant 2016-67013-24747 (to N.M.S.) and USDA-ARS base funds (to S.F.-G.).

Keywords

  • CNVs
  • Epigenetic
  • Maize
  • SRNAs
  • Teosinte
  • Transposable element (TE)
  • Zea mays

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