Highly Genotype- and Tissue-specific Single-Parent Expression Drives Dynamic Gene Expression Complementation in Maize Hybrids

Abstract

Maize exhibits tremendous gene expression variation between different lines.Complementation of diverse gene expression patterns in hybrids could play an important role in the manifestation of heterosis. In this study, we used transcriptome data of five different tissues from 33 maize inbreds and 89 hybrids (430 samples in total)to survey the global gene expression landscape of F 1 -hybrids relative to their inbred parents. Analysis of this data set revealed that single parent expression (SPE), which is defined as gene expression in only one of the two parents, while commonly observed, is highly genotype-and tissue-specific. Genes that have SPE in at least one pair of inbreds also tend to be tissue-specific. Genes with SPE caused by genomic presence/absence variation (PAV SPE) are much more frequently expressed in hybrids than genes that are present in the genome of both inbreds, but expressed in only a single-parent (non-PAV SPE) (74.7% vs. 59.7%). For non-PAV SPE genes, allele specific expression was used to investigate whether parental alleles not expressed in the inbred line ("silent allele") can be actively transcribed in the hybrid. We found that expression of the silent allele in the hybrid is relatively rare (~6.3% of non-PAV SPE genes), but is observed in almost all hybrids and tissues. Non-PAV SPE genes with expression of the silent allele in the hybrid are more likely to exhibit above high-parent expression level in the hybrid than those that do not express the silent allele. Finally, both PAV SPE and non-PAV SPE genes are highly enriched for being classified as non-syntenic, but depleted for curated genes with experimentally determined functions. This study provides a more comprehensive understanding of the potential role of non-PAV SPE and PAV SPE genes in heterosis.

Variation and inheritance of small RNAs in maize inbreds and F1 hybrids

“…Prior work has suggested that sRNA profiles may capture unique information missed by SNPs or gene (mRNA) expression data (Seifert et al, 2018a(Seifert et al, , 2018b. For each hybrid and inbred sample, gene expression levels were profiled by RNA-seq using the same RNA sample used for small RNA analysis (Li et al, 2019). To compare and contrast sRNA profiles with gene expression we summarised RNA-seq reads to counts per million (CPM) per B73v4 gene loci (APGv4 release 36).…”

“…To represent the maize heterotic groups, inbred lines were selected from the stiff stalk synthetic group (B73, B84, PHB47, PHJ40), the non-stiff stalk synthetic group (Mo17, Oh43) and the iodent group (PH207, PHG29). This investigation was also part of a larger germplasm sampled for mRNA analysis (Li et al, 2019). Hybrids were generated by crossing each of these selected inbred lines by three male genotypes that included B73 (stiff stalk synthetic), Mo17 (non-stiff stalk synthetic), and PH207 (iodent) in the scheme described in Supplemental Table 1.…”

“…Hybrids were generated by crossing each of these selected inbred lines by three male genotypes that included B73 (stiff stalk synthetic), Mo17 (non-stiff stalk synthetic), and PH207 (iodent) in the scheme described in Supplemental Table 1. Five tissues were sampled from the inbred and hybrid genotypes including seedling root at Vegetative 1 (V1) stage ("Seedling-root", "R"), seedling shoot at V1 ("Seedling-shoot", "S"), the middle of the eighth leaf at V7/8 ("Leaf", "L"), the upper most elongated internode at V7/V8 ("Internode", "I"), and endosperm at 15 days after pollination ("Endosperm", "E") (Li et al, 2019…”

“…RNA-seq samples are as described in (Li et al, 2019) and were downloaded from SRA. The samples analysed in this study, which were paired with the sRNA samples, are described in Supplemental Table S3.…”

“…The samples analysed in this study, which were paired with the sRNA samples, are described in Supplemental Table S3. Briefly, as detailed in (Li et al, 2019) total RNA was extracted using the miRNAeasy Mini Kit (Qiagen). Extracted RNA was DNase treated using the TURBO DNA-free kit (Life Technologies).…”