Domestication of rice has reduced the occurrence of transposable elements within gene coding regions

Abstract

Background: Transposable elements (TEs) are prominent features in many plant genomes, and patterns of TEs in closely related rice species are thus proposed as an ideal model to study TEs roles in the context of plant genome evolution. As TEs may contribute to improved rice growth and grain quality, it is of pivotal significance for worldwide food security and biomass production.

Results: We analyzed three cultivated rice species and their closest five wild relatives for distribution and content of TEs in their genomes. Despite that the three cultivar rice species contained similar copies and more total TEs, their genomes contained much longer TEs as compared to their wild relatives. Notably, TEs were largely depleted from genomic regions that corresponded to genes in the cultivated species, while this was not the case for their wild relatives. Gene ontology and gene homology analyses revealed that while certain genes contained TEs in all the wild species, the closest homologs in the cultivated species were devoid of them. This distribution of TEs is surprising as the cultivated species are more distantly related to each other as compared to their closest wild relative. Hence, cultivated rice species have more similar TE distributions among their genes as compared to their closest wild relatives. We, furthermore, exemplify how genes that are conferring important rice traits can be regulated by TE associations.

Conclusions: This study demonstrate that the cultivation of rice has led to distinct genomic distribution of TEs, and that certain rice traits are closely associated with TE distribution patterns. Hence, the results provide means to better understand TE-dependent rice traits and the potential to genetically engineer rice for better performance.

Keywords: Cultivated rice; Evolution; Oryza; Transposable elements; Wild rice.

Fig. 1

Comparative genomics of the eight AA-genome Oryza species. a Phylogenetic relationship of the eight AA-genome Oryza species inferred from orthologous gene sequences. Estimates of divergence time (million years) are given at each node (6.5 × 10⁻⁹ substitutions per site per year), all supported with 100% bootstrap values. b Comparative genome analysis. Each line in the circle represents one of the 12 chromosomes of Oryza genomes, along with the number of all TEs (blue) and TEs in genes (red). And the slide window size is 100,000 bp. c Blown-up image of Chr1 for six of the rice species

Fig. 2

TEs occupy more space in cultivated rice genomes as compared to their wild relatives. a The proportion and copy number of Gypsy and Total TEs in the different rice genomes. The left bars represent relative amounts of Gypsy and Total TE sizes compared to the genome sizes, and the right bars represent the number of Gypsy and Total transposons in the respective genomes. b-c Violin graphs of the length of LTR transposons (b), and DNA transposons (c), in the different rice genomes. The violin bars followed by the same letter are not significantly different (P < 0.05) as determined by Student’s t test

Fig. 3

Gene regions contain lower amounts of TEs as compared to their wild relatives. a Pie charts showing the relative distributions of TEs associated with genes, and upstream and downstream gene regions. Note that the gene regions in the domesticated species contain relatively less TEs as compared to their wild relatives. Such differences are not evident in the upstream and downstream regions of the genes. b k-means clustering with heatmap based on the distribution of TEs in genes of the 12 chromosomes of the Oryza genomes. The color scale represents the number per 100,000 bases of TEs in genes (green, black and red refer to low, medium and high TEs numbers, respectively)

Fig. 4

TEs are preferentially located to intronic gene regions. a Expressed genes with or without TEs. b Numbers of TEs in expressed or not expressed genes based on RNA-seq transcriptomic data

Fig. 5

Pair-wise comparisons of gene structure and TE locations of two examples within GO:0016301. a LOC_Os07g48290 gene. b LOC_Os02g45750 gene

Fig. 6

Comparisons of gene structure and TE locations of GIF1 gene critical for grain filling in the eight rice species. Organization of exons, introns and TEs of GIF1 (GRAIN INCOMPLETE FILLING 1; LOC_Os04g33740) gene in gene body and 2-kbp flanking sequences of the gene. Seed images of ancestral wild rice and cultivated rice are shown to the right

Fig. 7

Comparison of gene structure and TE locations of BH4 gene critical for grain filling in the eight rice species. Organization of exons, introns and TEs of BH4 (BLACK HULL4; LOC_Os04g38660) gene in gene body and 2-kbp flanking sequences of the gene. A blown-up image of BH4 gene structure of O. sativa Japonica is shown above the main image. This mutation changed the black-colored seed hull of the ancestral wild rice to the straw-white seed hull of cultivated rice