Application of the gene dosage balance hypothesis to auxin-related ribosomal mutants in Arabidopsis

Abstract

Several proteomic studies in Arabidopsis have shown the presence of heterogeneous ribosomal populations in different tissues. However, the phenotypic consequences of the imbalance of those ribosomal populations, and the regulatory mechanisms activated to control specific ratios between them, have yet to be evaluated. In our previous report, the phenotypic characterization of the Arabidopsis ribosomal L4 (RPL4) family suggests that the maintenance of proper auxin-regulated developmental responses requires the simultaneous presence of RPL4A- and RPL4D-containing ribosomes. Based on the analysis of the compensatory mechanisms within the RPL4 family proteins in the rpl4a and rpl4d backgrounds, we propose the Gene Dosage Balance Hypothesis (GDBH) as a regulatory mechanism for ribosomal complexes in Arabidopsis. By using the concepts of dosage compensation and hierarchy, GDBH is able to explain the severity and specificity of different ribosomal mutant phenotypes associated with the same ribosomal complex.

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Acknowledgements

We thank Dr. Glenn Hicks (University of California, Riverside) for his critical reading of the manuscript. This work was funded by Department of Energy, Division of Energy Biosciences, Grant DE-FG03-02ER15295/A000.

Figures and Tables

Figure 1 Schematic representation of the Gene Dosage Balance Hypothesis applied to a hypothetic two member ribosomal protein family in Arabidopsis. (A) A wild type plant maintains the correct amount of protein and the balance among different family members. As a consequence, the equilibrium position is located in the middle of the graph (white) and no phenotypes are observed. (B) A silenced line maintains the balance among different ribosomal protein family members but fails to obtain optimal protein amounts. As a consequence, the equilibrium position is displaced to the upper area of the graph (grey) and aberrant phenotypes are observed. (C) A ribosomal overexpression line might maintain the balance among different family members, but the excess of ribosomal proteins displace the equilibrium position to the lower area of the graph (grey). As a consequence, aberrant phenotypes are observed. (D) An imbalanced line might have the sufficient protein amounts but fails to maintain the proportions among the different protein family members. As a consequence, the equilibrium position is displaced to both, the upper and lower areas of the graph (grey) and aberrant phenotypes are observed. The two arms of the scale represent different equilibrium positions, and the numbers of white a black circles represent the relative ribosomal protein amounts of two different ribosomal family members. Relative protein amounts are indicated as a continuum with increased (+) and decreased (−) shown on the Y-axis in this model. (E) The different regulatory boxes present in the promoter region of the RPL4 family members might act as a fine tuning mechanism to trigger specific compensatory mechanisms as a response to different ribosomal protein mutations. The regulatory boxes are indicated with different color patterns and were identified using ATHENA.21

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