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DEVELOPMENT AND HORMONE ACTION

Analysis of Leaf Development in fugu Mutants of Arabidopsis Reveals Three Compensation Modes That Modulate Cell Expansion in Determinate Organs^1,[W]

Graduate School of Science, University of Tokyo, Tokyo 113–0033, Japan (A.F., G.H., H.T.); and National Institute for Basic Biology/Okazaki Institute for Integrated Bioscience, Okazaki, Aichi 444–8585, Japan (S.Y., H.T.)

In multicellular organisms, the coordination of cell proliferation and expansion is fundamental for proper organogenesis, yet the molecular mechanisms involved in this coordination are largely unexplored. In plant leaves, the existence of this coordination is suggested by compensation, in which a decrease in cell number triggers an increase in mature cell size. To elucidate the mechanisms of compensation, we isolated five new Arabidopsis (Arabidopsis thaliana) mutants (fugu1–fugu5) that exhibit compensation. These mutants were characterized together with angustifolia3 (an3), erecta (er), and a KIP-RELATED PROTEIN2 (KRP2) overexpressor, which were previously reported to exhibit compensation. Time-course analyses of leaf development revealed that enhanced cell expansion in fugu2-1, fugu5-1, an3-4, and er-102 mutants is induced postmitotically, indicating that cell enlargement is not caused by the uncoupling of cell division from cell growth. In each of the mutants, either the rate or duration of cell expansion was selectively enhanced. In contrast, we found that enhanced cell expansion in KRP2 overexpressor occurs during cell proliferation. We further demonstrated that enhanced cell expansion occurs in cotyledons with dynamics similar to that in leaves. In contrast, cell expansion was not enhanced in roots even though they exhibit decreased cell numbers. Thus, compensation was confirmed to occur preferentially in determinate organs. Flow cytometric analyses revealed that increases in ploidy level are not always required to trigger compensation, suggesting that compensation is only partially mediated by ploidy-dependent processes. Our results suggest that compensation reflects an organ-wide coordination of cell proliferation and expansion in determinate organs, and involves at least three different expansion pathways.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Gorou Horiguchi (ghori{at}biol.s.u-tokyo.ac.jp).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.107.099325

^* Corresponding author; e-mail ghori{at}biol.s.u-tokyo.ac.jp; fax 81–3–5841–1889.

Received March 10, 2007; accepted April 4, 2007; published April 27, 2007.

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