Single-parent expression drives dynamic gene expression complementation in maize hybrids

Zhi Li, Peng Zhou, Rafael Della Coletta, Tifu Zhang, Alex B. Brohammer, Christine H. O’Connor, Brieanne Vaillancourt, Anna Lipzen, Chris Daum, Kerrie Barry, Natalia de Leon, Cory D. Hirsch, C. Robin Buell, Shawn M. Kaeppler, Nathan M. Springer, Candice N. Hirsch

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Single-parent expression (SPE) is defined as gene expression in only one of the two parents. SPE can arise from differential expression between parental alleles, termed non-presence/absence (non-PAV) SPE, or from the physical absence of a gene in one parent, termed PAV SPE. We used transcriptome data of diverse Zea mays (maize) inbreds and hybrids, including 401 samples from five different tissues, to test for differences between these types of SPE genes. Although commonly observed, SPE is highly genotype and tissue specific. A positive correlation was observed between the genetic distance of the two inbred parents and the number of SPE genes identified. Regulatory analysis showed that PAV SPE and non-PAV SPE genes are mainly regulated by cis effects, with a small fraction under trans regulation. Polymorphic transposable element insertions in promoter sequences contributed to the high level of cis regulation for PAV SPE and non-PAV SPE genes. PAV SPE genes were more frequently expressed in hybrids than non-PAV SPE genes. The expression of parentally silent alleles in hybrids of non-PAV SPE genes was relatively rare but occurred in most hybrids. Non-PAV SPE genes with expression of the silent allele in hybrids are more likely to exhibit above high parent expression level than hybrids that do not express the silent allele, leading to non-additive expression. This study provides a comprehensive understanding of the nature of non-PAV SPE and PAV SPE genes and their roles in gene expression complementation in maize hybrids.

Original languageEnglish (US)
Pages (from-to)93-107
Number of pages15
JournalPlant Journal
Volume105
Issue number1
DOIs
StatePublished - Jan 2021

Bibliographical note

Funding Information:
We are grateful to Katie Heslip for performing RNA extractions of samples included in this study. This work was funded in part by NSF grants IOS‐1546727 to CNH and IOS‐1934384 to CNH and NMS, and USDA grant 2018‐67013‐27571 to CNH. This work was also supported in part by the DOE/GLBRC (DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science DE‐FC02‐07ER64494). The work conducted by the US Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, is supported by the Office of Science of the US Department of Energy under contract no. DE‐AC02‐05CH11231. ABB was supported by the DuPont Pioneer Bill Kuhn Honorary Fellowship and the University of Minnesota MnDRIVE Global Food Ventures Graduate Fellowship. TZ was supported by the National Natural Science Foundation of China (31671760). The authors acknowledge the Minnesota Supercomputing Institute (MSI) at the University of Minnesota for providing resources that contributed to the research results reported within this article.

Keywords

  • complementation
  • gene expression regulation
  • maize
  • presence/absence variation
  • single-parent expression
  • transposable element

PubMed: MeSH publication types

  • Journal Article

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