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, 110 (6), 2395-400

Small Open Reading Frames Associated With Morphogenesis Are Hidden in Plant Genomes

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Small Open Reading Frames Associated With Morphogenesis Are Hidden in Plant Genomes

Kousuke Hanada et al. Proc Natl Acad Sci U S A.

Abstract

It is likely that many small ORFs (sORFs; 30-100 amino acids) are missed when genomes are annotated. To overcome this limitation, we identified ∼8,000 sORFs with high coding potential in intergenic regions of the Arabidopsis thaliana genome. However, the question remains as to whether these coding sORFs play functional roles. Using a designed array, we generated an expression atlas for 16 organs and 17 environmental conditions among 7,901 identified coding sORFs. A total of 2,099 coding sORFs were highly expressed under at least one experimental condition, and 571 were significantly conserved in other land plants. A total of 473 coding sORFs were overexpressed; ∼10% (49/473) induced visible phenotypic effects, a proportion that is approximately seven times higher than that of randomly chosen known genes. These results indicate that many coding sORFs hidden in plant genomes are associated with morphogenesis. We believe that the expression atlas will contribute to further study of the roles of sORFs in plants.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Expression atlas of sORFs and annotated genes. (A) Heat map of all coding sORFs and annotated genes. Color key shows relationship between color and z-score of expression intensities in each tissue or condition. Red and green indicate low and high expression, respectively. These data can be viewed at our website (HANADB-AT: http://evolver.psc.riken.jp/seiken). (B) Correlation of expression intensities between technical replicates in our designed array and in seedling, as an example. x and y axes represent log10 values of expression intensities in technical replicate 1 and technical replicate 2 in seedlings (control in A), respectively. (C) Correlation of expression intensities between our designed array and the ATH1 array for annotated genes. x and y axes represent log10 values of expression intensities in our designed array and ATH1 array in seedlings (control in A), respectively.
Fig. 2.
Fig. 2.
Expression intensities in annotated genes, negative controls, pseudogenes, and coding sORFs. x axis represents log10 values of (A) annotated genes, (B) negative controls, (C) pseudogenes, and (D) coding sORFs in the same sample (control in A). x axis indicates log10 values of expression intensities. y axis indicates frequency of probes in each bin size. In A, expression intensities of annotated genes were fitted to lower (blue solid line) and higher (red solid line) Gaussian distribution. The 5% false-positive rate, which is the top 5% in the lower distribution of expression intensities, was defined as the threshold for high expression. In B, the 5% false-positive rate, which is the top 5% in expression intensities of negative controls, was defined as the threshold for high expression. In C, the 5% false-positive rate, which is the top 5% in expression intensities of pseudogenes, was defined as the threshold for high expression.
Fig. 3.
Fig. 3.
Phenotypes of transgenic plants overexpressing sORFs. (A) WT plant. (B) Mutant overexpressing sORF5491 showing a large adult plant phenotype. (C) Mutant overexpressing sORF5634 showing a small adult plant phenotype. (D) Overexpression of sORF3416 resulted in a pale green leaf phenotype. (E) Overexpression of sORF2813 resulted in a bent stem phenotype. (F) Overexpression of sORF5697 resulted in a penta-petal phenotype, whereas most WTs have tetra-petals. GO categories of biological process (G) and molecular function (H) with overrepresented numbers of coexpressed genes for 49 coding sORFs with phenotypic effects. Arrowheads point to subcategories. Red circles indicate categories with significantly (χ2 test, FDR < 0.05) more genes among the coexpressed genes.

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