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

doi:10.1111/tpj.15042

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 journal › Article › peer-review

10 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 language	English (US)
Pages (from-to)	93-107
Number of pages	15
Journal	Plant Journal
Volume	105
Issue number	1
DOIs	https://doi.org/10.1111/tpj.15042
State	Published - 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. CNH, NS, SMK, CRB, CDH and NDL conceived the experiment. BV, AL, CD and KB performed the experiments. ZL, PZ, RDC, TZ, ABB, COC and CDH analyzed the data. ZL and CNH wrote the article, with contributions from all authors. All the authors have read and approved the final version for publication. The authors declare no conflicts of interest.

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.

Publisher Copyright:
© 2020 Society for Experimental Biology and John Wiley & Sons Ltd

Keywords

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

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10.1111/tpj.15042

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Li, Z., Zhou, P., Della Coletta, R., Zhang, T., Brohammer, A. B., H. O’Connor, C., Vaillancourt, B., Lipzen, A., Daum, C., Barry, K., de Leon, N., Hirsch, C. D., Buell, C. R., Kaeppler, S. M., Springer, N. M., & Hirsch, C. N. (2021). Single-parent expression drives dynamic gene expression complementation in maize hybrids. Plant Journal, 105(1), 93-107. https://doi.org/10.1111/tpj.15042

Li, Z, Zhou, P, Della Coletta, R, Zhang, T, Brohammer, AB, H. O’Connor, C, Vaillancourt, B, Lipzen, A, Daum, C, Barry, K, de Leon, N, Hirsch, CD, Buell, CR, Kaeppler, SM, Springer, NM & Hirsch, CN 2021, 'Single-parent expression drives dynamic gene expression complementation in maize hybrids', Plant Journal, vol. 105, no. 1, pp. 93-107. https://doi.org/10.1111/tpj.15042

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title = "Single-parent expression drives dynamic gene expression complementation in maize hybrids",

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.",

keywords = "complementation, gene expression regulation, maize, presence/absence variation, single-parent expression, transposable element",

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

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. CNH, NS, SMK, CRB, CDH and NDL conceived the experiment. BV, AL, CD and KB performed the experiments. ZL, PZ, RDC, TZ, ABB, COC and CDH analyzed the data. ZL and CNH wrote the article, with contributions from all authors. All the authors have read and approved the final version for publication. The authors declare no conflicts of interest. 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. Publisher Copyright: {\textcopyright} 2020 Society for Experimental Biology and John Wiley & Sons Ltd",

year = "2021",

month = jan,

doi = "10.1111/tpj.15042",

language = "English (US)",

volume = "105",

pages = "93--107",

journal = "Plant Journal",

issn = "0960-7412",

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T1 - Single-parent expression drives dynamic gene expression complementation in maize hybrids

AU - Li, Zhi

AU - Zhou, Peng

AU - Della Coletta, Rafael

AU - Zhang, Tifu

AU - Brohammer, Alex B.

AU - H. O’Connor, Christine

AU - Vaillancourt, Brieanne

AU - Lipzen, Anna

AU - Daum, Chris

AU - Barry, Kerrie

AU - de Leon, Natalia

AU - Hirsch, Cory D.

AU - Buell, C. Robin

AU - Kaeppler, Shawn M.

AU - Springer, Nathan M.

AU - Hirsch, Candice N.

N1 - 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. CNH, NS, SMK, CRB, CDH and NDL conceived the experiment. BV, AL, CD and KB performed the experiments. ZL, PZ, RDC, TZ, ABB, COC and CDH analyzed the data. ZL and CNH wrote the article, with contributions from all authors. All the authors have read and approved the final version for publication. The authors declare no conflicts of interest. 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. Publisher Copyright: © 2020 Society for Experimental Biology and John Wiley & Sons Ltd

PY - 2021/1

Y1 - 2021/1

N2 - 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.

AB - 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.

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KW - gene expression regulation

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KW - transposable element

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

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