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Mechanical regulation of organ asymmetry in leaves

How appendages, such as plant leaves or animal limbs, develop asymmetric shapes remains a fundamental question in biology. Although ongoing research has revealed the genetic regulation of organ pattern formation, how gene activity ultimately directs organ shape remains unclear. Here, we show that leaf dorsoventral (adaxial-abaxial) polarity signals lead to mechanical heterogeneity of the cell wall, related to the methyl-esterification of cell-wall pectins in tomato and Arabidopsis. Numerical simulations predicate that mechanical heterogeneity is sufficient to produce the asymmetry seen in planar leaves. Experimental tests that alter pectin methyl-esterification, and therefore cell wall mechanical properties, support this model and lead to polar changes in gene expression, suggesting the existence of a feedback mechanism for mechanical signals in morphogenesis. Thus, mechanical heterogeneity within tissue may underlie organ shape asymmetry.

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Fig. 1: Dynamic changes of the asymmetry of the elastic modulus of epidermal cell walls.
Fig. 2: Methyl-esterification of cell wall pectin in leaf primordia.
Fig. 3: A conceptual mechanical model is sufficient to predict organ asymmetry formation.
Fig. 4: Dynamics of cell wall pectin methyl-esterification are critical for leaf polarity patterning in tomato.
Fig. 5: Dynamics of cell wall pectin methyl-esterification are critical for leaf polarity patterning in Arabidopsis.
Fig. 6: Epidermal restriction is necessary for polarity patterning.

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Acknowledgements

We thank K.-I. Hayashi (Okayama University of Science) for providing auxinole, N. Li (Institute of Mechanics, Chinese Academy of Sciences) and Z. Huang (Bruker Nano Surfaces Business, Beijing) for assistance with AFM measurement, the Core Facilities of Life Sciences of Peking University for use of the TEM and S.-N. Bai (Peking University) and S. Poethig (University of Pennsylvania) for discussions. This work was supported by National Natural Science Foundation of China grants 31430010 and 31627804, National Basic Research Program of China (973 Program) grants 2014CB943500 and 2011CB710900, National Key Research and Development Program of China grant 2016YFA0501601, the National Program for Support of Top-Notch Young Professionals, China Postdoctoral Science Foundation grant 2015M570171 and the State Key Laboratory of Plant Genomics.

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Contributions

Y.J. conceived and designed experiments. J.Q. and B.W. carried out most of the experiments. S.F., S.L. and M.L. carried out numerical simulations. C.G. contributed to phenotypic analysis. X.Z. and D.Q. contributed to AFM experiments. Y.H. performed TEM experiments. Y.Z. and C.L. provided materials/reagents. Y.J. and M.L. wrote the manuscript, with contributions from all the authors.

Corresponding authors

Correspondence to Mian Long or Yuling Jiao.

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Supplementary Information

Supplementary Figures 1–11, Supplementary Table 1, Supplementary Table 3, Supplementary Table 4, Supplementary Video Legends, Supplementary Methods, Supplementary References.

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Supplementary Table 2

Raw AFM measurements for Figure 1 and Supplementary Figures 4–6.

Supplementary Source Code

Supplementary source code.

Supplementary Video 1

Normal leaf growth, related to Figure 2i–l.

Supplementary Video 2

Hastened adaxial cell wall loosening leads to reduced asymmetry, related to Figure 3c.

Supplementary Video 3

Two-domain partition leads to reduced asymmetry, related to Figure 3d.

Supplementary Video 4

Reduced epidermal restriction leads to reduced asymmetry, related to Figure 6a.

Supplementary Video 5

Enhanced epidermal restriction leads to reduced asymmetry, related to Figure 6b.

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Qi, J., Wu, B., Feng, S. et al. Mechanical regulation of organ asymmetry in leaves. Nature Plants 3, 724–733 (2017). https://doi.org/10.1038/s41477-017-0008-6

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