Genome-wide disruption of gene expression in allopolyploids but not hybrids of rice subspecies

Abstract

Hybridization and polyploidization are prominent processes in plant evolution. Hybrids and allopolyploids typically exhibit radically altered gene expression patterns relative to their parents, a phenomenon termed "transcriptomic shock." To distinguish the effects of hybridization from polyploidization on coregulation of divergent alleles, we analyzed expression of parental copies (homoeologs) of 11,608 genes using RNA-seq-based transcriptome profiling in reciprocal hybrids and tetraploids constructed from subspecies japonica and indica of Asian rice (Oryza sativa L.). The diploid hybrids and their derived allopolyploids differ dramatically in morphology, despite having the same suite of genes and genic proportions. Allelic and homoeolog-specific transcripts were unequivocally diagnosed in the hybrids and tetraploids based on parent-specific SNPs. Compared with the in silico hybrid (parental mix), the range of progenitor expression divergence was significantly reduced in both reciprocally generated F1 hybrids, presumably due to the ameliorating effects of a common trans environment on divergent cis-factors. In contrast, parental expression differences were greatly elaborated at the polyploid level, which we propose is a consequence of stoichiometric disruptions associated with the numerous chromosomal packaging and volumetric changes accompanying nascent polyploidy. We speculate that the emergent property of "whole genome doubling" has repercussions that reverberate throughout the transcriptome and downstream, ultimately generating altered phenotypes. This perspective may yield insight into the nature of adaptation and the origin of evolutionary novelty accompanying polyploidy.

Keywords: Oryza sativa L; evolution of gene regulation; homoeologous expression; hybridization; polyploidization.

Fig. 1.

Cytological and phenotypic characteristics of the two diploid parental genotypes, Nipponbare and 93-11, representing the two subspecies, japonica and indica, respectively, of Asian rice (Oryza sativa L.), their reciprocal F1 hybrids and S1 tetraploids. Somatic chromosome numbers of the two parental genotypes, Nipponbare (A) and 93-11 (B), and the reciprocal tetraploids (C and D) are shown, which are 2n = 24 and 48, respectively. (E–G) Overall morphology of mature plants of the parental genotypes, Nipponbare (E, left) and 93-11 (E, right), their reciprocal F1 hybrids, N9 (F, left) and 9N (F, right), and the reciprocal tetraploids, NN99 (G, left) and 99NN (G, right). (H) Typical grain morphology of parents, hybrids, and tetraploids. Scale bars in (A–D) are 5 μm and in H is 0.5 cm.

Fig. 2.

RNA-seq-based whole-genome expression spectra of parental (allelic, at the diploid level) and homoeologous (at the polyploid level) expression divergence for a total of 11,608 genes in the in silico hybrid, reciprocal F1 hybrids, and reciprocal tetraploids, revealed by a log2-transformed boxplot (A), and the numbers of genes showing differential expression of parental homoeologs in each pairwise comparison (B).

Fig. 3.

Plot summarizes the relative, homoeolog-specific expression levels in parental (in silico hybrid) and both F1 hybrids. Each point represents a single gene and is color-coded according to the mechanism of regulatory evolution inferred from statistical tests. The bar graph depicts the number of genes in each category.

Fig. 4.

Summary of the numbers of genes belonging to each of the regulatory groups and their relative proportions (A), as well as overlaps of the numbers of genes of each of the three regulatory groups between or among all possible comparisons of the four plants, reciprocal hybrids, and reciprocal tetraploids, presented by Venn diagrams (B–D).