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. 2023 Jul 19:12:RP86324.
doi: 10.7554/eLife.86324.

Transposons are important contributors to gene expression variability under selection in rice populations

Raúl Castanera  1 , Noemia Morales-Díaz  1 , Sonal Gupta  2 , Michael Purugganan  2   3 , Josep M Casacuberta  1
Affiliations

Transposons are important contributors to gene expression variability under selection in rice populations

Raúl Castanera et al. Elife. .

Abstract

Transposable elements (TEs) are an important source of genome variability. Here, we analyze their contribution to gene expression variability in rice by performing a TE insertion polymorphism expression quantitative trait locus mapping using expression data from 208 varieties from the Oryza sativa ssp. indica and O. sativa ssp. japonica subspecies. Our data show that TE insertions are associated with changes of expression of many genes known to be targets of rice domestication and breeding. An important fraction of these insertions were already present in the rice wild ancestors, and have been differentially selected in indica and japonica rice populations. Taken together, our results show that small changes of expression in signal transduction genes induced by TE insertions accompany the domestication and adaptation of rice populations.

Keywords: Oriza rufipogon; Oriza sativa; eQTL; evolutionary biology; genetics; genomics; positive selection; transposable elements.

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Conflict of interest statement

RC, NM, SG, MP, JC No competing interests declared

Figures

Figure 1.
Figure 1.. Characterization of rice transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs).
(A, B) Association between TIPs and gene expression levels in cis (TIP-eQTLs) found in indica and japonica population along the 12 rice chromosomes. Horizontal lines represent 5% significance thresholds corrected for multiple testing using false discovery rate (FDR) method. (C) Number of TIP-eQTLs found in each condition classified at the order transposable element (TE) level. White bars represent the number of total TIPs (secondary axis). (D) Expression variance explained by leading TIP-eQTL and SNP-eQTL. Each point represents a gene. Indica and japonica TIP-eQTLs are combined into a single plot. Number of TIP-eQTLs (E) or SNP-eQTL (F) per Mb of gene feature. Upstream and downstream regions are 1 kb long. Gene region includes 5′ and 3′ UTRs. All the TIPs and SNPs with a significant association (FDR <5%) were used in this analysis.
Figure 1—figure supplement 1.
Figure 1—figure supplement 1.. Expression variance explained by leading transposon insertion polymorphism (TIP)-expression quantitative trait locus (eQTL) and SNP-eQTL in the associations detected for each gene (dot).
Panels in (A) represent the analysis performed using a combined genotype matrix including all SNPs and TIPs. Panels in (B) represent the analysis performed using a combined genotype matrix including TIPs and a subsampled number of SNPs matching the exact number of TIPs.
Figure 2.
Figure 2.. Effect size and population frequencies of wet and drought-stress transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs).
Representation of the effect size (beta) of the TIP-eQTLs with respect to their population frequency in indica (A, C) and japonica (B, D) for positive (A, B) and negative (C, D) effects. Venn diagram illustrating the intersection between TIP-eQTLs detected in each condition of the two subspecies analyzed, indica (ind) and japonica (jap) (E). Percentage of condition-specific (F) and species-specific (G) TIP-eQTLs. Shared TIPs are those falling in the intersection between the false discovery rate (FDR)-corrected TIP-eQTLs found in a given population/condition and all the associations of the other population/condition using a relaxed cutoff (p < 0.05, no FDR correction). Relationship between the frequencies in indica and japonica populations of the and 829 TIP-eQTLs (H) and the 33,389 non-eQTL-TIPs (I).
Figure 2—figure supplement 1.
Figure 2—figure supplement 1.. Effect size of transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs) based on their population frequency on the drought condition.
Figure 2—figure supplement 2.
Figure 2—figure supplement 2.. Population frequencies of transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs) and TIP-no-eQTLs present at 1 kb upstream genes.
Figure 3.
Figure 3.. Signatures of positive selection on transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs).
(A) Absolute Population Branch Statistic (PBS) of 354 TIP-eQTLs (left) and 11,344 TIPs (no-eQTL, right) present in indica, japonica, and rufipogon populations. Dotted vertical lines represent the 95th and 99th percentiles of the PBS values of the whole dataset (11,698 TIPs). Red dots represent two examples of TIP-eQTLs with extreme PBS values. (B) Population frequency of the two TIPs with extreme PBS values, marked as red dots in the left panel (A), as well as of the whole TIP dataset. (C) Fst-based tree of the two TIPs with extreme PBS values, as well as of the whole TIP dataset (average Fst).
Figure 4.
Figure 4.. Selection on transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs) associated with EG2 expression.
(A) Representation of the two main EG2 haplotypes present in rice and rufipogon/nivara populations identified in the rice super-pangenome. Conserved nucleotide regions are connected by gray marks. Structural variants longer than 50 bp are shown as white spaces. TIP-eQTLs are shown as red boxes. Additional TIPs are shown as white boxes. (B) Boxplot representation of the expression of the two EG2 haplotypes in the indica population. Numbers inside boxplots represent the number of accessions in each group. Analysis of nucleotide diversity (π) and diversity in haplotypes homozygosity tracts (H12) for Hap A (C, E) and Hap B (D, F) in japonica (C, D) and indica (E, F) populations. The vertical dotted black line shows the position of the TIP insertion. The EG2 gene is schematically shown in blue. The horizontal dashed black line represents the mean of 1000 random permutation pulls (for p-value see Supplementary file 6).
Figure 4—figure supplement 1.
Figure 4—figure supplement 1.. Boxplots representing the expression differences between haplotypes in OsJAZ1.
Three independent experimental replicates are shown separately.
Figure 5.
Figure 5.. Selection on transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs) associated with OsGAP expression.
(A) Representation of the two main OsGAP haplotypes present in rice and rufipogon/nivara populations identified in the rice super-pangenome. Conserved nucleotide regions are connected by gray marks. Structural variants longer than 50 bp are shown as white spaces. TIP-eQTLs are shown as red boxes. Additional TIPs are shown as white boxes. (B) Boxplot representation of the expression of the two OsGAP haplotypes in the japonica population. Numbers inside boxplots represent the number of accessions in each group. Analysis of nucleotide diversity (π) and diversity in haplotypes homozygosity tracts (H12) for Hap A (C) and Hap B (D) in japonica population. The vertical dotted black line shows the position of the TIP insertion. The OsGAP gene is schematically shown in blue. The horizontal dashed black line represents the mean of 1000 random permutation pulls (for p-value see Supplementary file 6).
Figure 5—figure supplement 1.
Figure 5—figure supplement 1.. Boxplots representing the expression differences between haplotypes in OsGAP.
Three independent experimental replicates are shown separately.
Figure 6.
Figure 6.. Selection on transposon insertion polymorphism (TIP)-expression quantitative trait loci (eQTLs) associated with OsMPH1 expression.
Representation of the two main OsMPH1 haplotypes present in rice and rufipogon/nivara populations identified in the rice super-pangenome. Conserved nucleotide regions are connected by gray marks. Structural variants longer than 50 bp are shown as white spaces. TIP-eQTLs are shown as red boxes. (B) Boxplot representation of the expression of the two OsMPH1 haplotypes in the japonica population. Numbers inside boxplots represent the number of accessions in each group. Analysis of nucleotide diversity (π) and diversity in haplotypes homozygosity tracts (H12) for Hap A in indica population (C) and in japonica population (D). The vertical dotted black line shows the position of the TIP insertion. The OsMPH1 gene, which is schematically shown in blue. The horizontal dashed black line represents the mean of 1000 random permutation pulls (for p-value see Supplementary file 6).
Figure 6—figure supplement 1.
Figure 6—figure supplement 1.. Boxplots representing the expression differences between haplotypes in OsMPH1.
Three independent experimental replicates are shown separately.
See this image and copyright information in PMC

Update of

  • doi: 10.21203/rs.3.rs-2197876/v1
  • doi: 10.7554/eLife.86324.1
  • doi: 10.7554/eLife.86324.2

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