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A role for heritable transcriptomic variation in maize adaptation to temperate environments

Guangchao Sun, Huihui Yu, Peng Wang, Martha Lopez Guerrero, Ravi V. Mural, Olivier N. Mizero, Marcin Grzybowski, Baoxing Song, Karin van Dijk, Daniel P. Schachtman, Chi Zhang, James C. Schnable
doi: https://doi.org/10.1101/2022.01.28.478212
Guangchao Sun
1Quantitative Life Sciences Initiative, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Huihui Yu
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
4School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Peng Wang
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Martha Lopez Guerrero
5Department of Biochemistry, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Ravi V. Mural
1Quantitative Life Sciences Initiative, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Olivier N. Mizero
1Quantitative Life Sciences Initiative, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Marcin Grzybowski
1Quantitative Life Sciences Initiative, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Baoxing Song
6Institute for Genomic Diversity, Cornell University, Ithaca, New York 14853, USA
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Karin van Dijk
5Department of Biochemistry, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Daniel P. Schachtman
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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Chi Zhang
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
4School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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James C. Schnable
1Quantitative Life Sciences Initiative, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
2Center for Plant Science Innovation, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
3Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, NE, 68588 USA
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ABSTRACT

Transcription bridges genetic information and phenotypes. Here, we evaluated how changes in transcriptional regulation enable maize (Zea mays), a crop originally domesticated in the tropics, to adapt to temperate environments. We generated 572 unique RNA-seq datasets from the roots of 340 maize genotypes. Genes involved in core processes such as cell division, chromosome organization and cytoskeleton organization showed lower heritability of gene expression. While genes involved in anti-oxidation activity exhibited higher expression heritability. An expression genome-wide association study (eGWAS) identified 19,602 expression quantitative trait loci (eQTLs) associated with the expression of 11,444 genes. A GWAS for alternative splicing identified 49,897 splicing QTLs (sQTLs) for 7,614 genes. Rare allele burden within genomic intervals with trans-eQTLs correlated with extremes of expression in target genes as previously reported for cis-eQTLs. Genes harboring both cis-eQTLs and cis-sQTLs in linkage disequilibrium were disproportionately likely to encode transcription factors or were annotated as responding to one or more stresses. Independent component analysis of gene expression data identified loci regulating co-expression modules involved in phytohormone pathways, cell wall biosynthesis, lipid metabolism and stress response. Several genes involved in cell proliferation, flower development, DNA replication and gene silencing showed lower gene expression variation explained by genetic factors between temperate and tropical maize lines. A GWAS of 27 previously published phenotypes identified several candidate genes overlapping with genomic intervals showing signatures of selection during adaptation to temperate environments. Our results illustrate how maize transcriptional regulatory networks enable changes in transcriptional regulation to adapt to temperate regions.

Competing Interest Statement

James C. Schnable has equity interests in Data2Bio, LLC; Dryland Genetics LLC; and EnGeniousAg LLC. He is a member of the scientific advisory board of GeneSeek and currently serves as a guest editor for The Plant Cell. The authors declare no other competing interests.

Footnotes

  • ↵* schnable{at}unl.edu

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted January 28, 2022.
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A role for heritable transcriptomic variation in maize adaptation to temperate environments
Guangchao Sun, Huihui Yu, Peng Wang, Martha Lopez Guerrero, Ravi V. Mural, Olivier N. Mizero, Marcin Grzybowski, Baoxing Song, Karin van Dijk, Daniel P. Schachtman, Chi Zhang, James C. Schnable
bioRxiv 2022.01.28.478212; doi: https://doi.org/10.1101/2022.01.28.478212
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A role for heritable transcriptomic variation in maize adaptation to temperate environments
Guangchao Sun, Huihui Yu, Peng Wang, Martha Lopez Guerrero, Ravi V. Mural, Olivier N. Mizero, Marcin Grzybowski, Baoxing Song, Karin van Dijk, Daniel P. Schachtman, Chi Zhang, James C. Schnable
bioRxiv 2022.01.28.478212; doi: https://doi.org/10.1101/2022.01.28.478212

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