Abstract
Previously, the GRF-INTERACTING FACTOR1 (GIF1)/ANGUSTIFOLIA3 (AN3) transcription coactivator gene, a member of a small gene family comprising three genes, was characterized as a positive regulator of cell proliferation in lateral organs, such as leaves and flowers, of Arabidopsis (Arabidopsis thaliana). As yet, it remains unclear how GIF1/AN3 affects the cell proliferation process. In this study, we demonstrate that the other members of the GIF gene family, GIF2 and GIF3, are also required for cell proliferation and lateral organ growth, as gif1, gif2, and gif3 mutations cause a synergistic reduction in cell numbers, leading to small lateral organs. Furthermore, GIF1, GIF2, and GIF3 overexpression complemented a cell proliferation defect of the gif1 mutant and significantly increased lateral organ growth of wild-type plants as well, indicating that members of the GIF gene family are functionally redundant. Kinematic analysis on leaf growth revealed that the gif triple mutant as well as other strong gif mutants developed leaf primordia with fewer cells, which was due to the low rate of cell proliferation, eventually resulting in earlier exit from the proliferative phase of organ growth. The low proliferative activity of primordial leaves was accompanied by decreased expression of cell cycle-regulating genes, indicating that GIF genes may act upstream of cell cycle regulators. Analysis of gif double and triple mutants clarified a previously undescribed role of the GIF gene family: gif mutants had small vegetative shoot apical meristems, which was correlated with the development of small leaf primordia. gif triple mutants also displayed defective structures of floral organs. Taken together, our results suggest that the GIF gene family plays important roles in the control of cell proliferation via cell cycle regulation and in other developmental properties that are associated with shoot apical meristem function.
Highlights
The GROWTH-REGULATING FACTOR (GRF)-INTERACTING FACTOR1 (GIF1)/ANGUSTIFOLIA3 (AN3) transcription coactivator gene, a member of a small gene family comprising three genes, was characterized as a positive regulator of cell proliferation in lateral organs, such as leaves and flowers, of Arabidopsis (Arabidopsis thaliana)
Using RNA gel-blot analysis, we have previously shown that the GRF-INTERACTING FACTOR (GIF) family genes share an overlapping expression pattern and that GRF-INTERACTING FACTOR1 (GIF1)/AN3 mRNAs are most abundant compared with GIF2 and GIF3 (Kim and Kende, 2004)
We presented, to our knowledge, the first loss- and gain-of-function evidence that GIF2 and GIF3 acted as positive regulators for lateral organ growth, as did GIF1
Summary
The GRF-INTERACTING FACTOR1 (GIF1)/ANGUSTIFOLIA3 (AN3) transcription coactivator gene, a member of a small gene family comprising three genes, was characterized as a positive regulator of cell proliferation in lateral organs, such as leaves and flowers, of Arabidopsis (Arabidopsis thaliana). Like the grf triple mutant, the gif1 single mutant showed narrow and small leaves as well as flower petals, which were caused by a reduction in cell numbers, indicating that GRF and GIF1 proteins form a functional complex involved in regulating cell proliferation and, growth and shape of lateral organs (Kim and Kende, 2004).
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