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

Authors: XUE, WEI - University Of Wisconsin; ANDERSON, SARAH - University Of Minnesota; WANG, XUFENG - Shenzhen University; YANG, LIYAN - University Of Wisconsin; CRISP, PETER - University Of Minnesota; LI, QING - University Of Minnesota; NOSHAY, JACLYN - University Of Minnesota; ALBERT, PATRICE - University Of Missouri; BIRCHLER, JAMES - University Of Missouri; BILINSKI, PAUL - University Of California; STITZER, MICHELLE - University Of California; ROSS-IBARRA, JEFFREY - University Of California; Flint-Garcia, Sherry; CHEN, XUEMEI - Shenzhen University; SPRINGER, NATHAN - University Of Minnesota; DOEBLEY, JOHN - University Of Wisconsin

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/2/2019
Publication Date: 9/1/2019
Citation: Xue, W., Anderson, S.N., Wang, X., Yang, L., Crisp, P.A., Li, Q., Noshay, J., Albert, P.S., Birchler, J.A., Bilinski, P., Stitzer, M.C., Ross-Ibarra, J., Flint-Garcia, S.A., Chen, X., Springer, N.M., Doebley, J.F. 2019. Hybrid decay: A transgenerational epigenetic decline in vigor and viability triggered in backcross populations of teosinte with maize. Genetics. 213(1):143-160. https://doi.org/10.1534/genetics.119.302378.
DOI: https://doi.org/10.1534/genetics.119.302378

Interpretive Summary: Plant breeders and geneticists make crosses among varieties and/or with wild relatives of crop species in order to generate variation that can be used to improve traits or study the genes underlying traits. In the course of our previous research with corn and its wild ancestor, teosinte, two labs independently discovered a specific teosinte that caused the derived corn-teosinte back-crossed population to become sickly, despite the fact that the teosinte itself appears to be completely normal. Advanced progeny of the corn-teosinte population exhibit a sickly whole-plant phenotype involving changes in plant, ear, and kernel morphology, plant vigor and viability in both male and female floral structures. This sickly syndrome is quite abnormal as it appears to be permanent and cannot be remedied by crossing back to normal corn. We characterized sickly plants and normal plants by multiple assays, including both traditional genetic and non-genetic (epigenetic) methods. Our results suggest that non-genetic factors are responsible for this irreversible condition, and likely involve transposable elements originating in the teosinte and several mechanisms that usually suppress transposable elements. While this sickly phenomenon appears to be rare, it is important to understand how this phenomenon occurred and how prevalent it is in crop species. Our study provides several hypotheses for breeders and geneticists on how non-genetic factors can control important characteristics in crop plants.

Technical 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 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.