The long-term goal of this project is to elucidate how cell polarity and morphogenesis is coordinated locally (between adjacent cells) and globally (in a field of cells) along the organ surface, because this knowledge is sorely needed to understand mechanisms of development and pattern formation. This project focuses the mechanisms underlying cellular intercalation, a fundamental process critical for human and animal embryogenesis and plant morphogenesis. Mechanisms for the local and global coordination of cellular intercalation are poorly characterized, although some underlying signaling events (e.g., Rho GTPases and the cytoskeleton) are conserved across animal and plant kingdoms. In the model plant Arabidopsis, cell intercalation is important for the development of the leaf epidermis, in which pavement cells (PC) develop interdigitated lobes and indentations to form the puzzle-piece appearance. The PI's group has established PC as a model system for cell intercalation and has discovered an elaborate Rho GTPase signaling network underpinning the PC intercalation, which involves two interplaying but mutually exclusive Rho signaling pathways: The ROP2-RIC4-actin pathway activating lobe formation and the ROP6-RIC1-microtubule pathway promoting indentation. The two pathways are complementarily localized at the opposing sides of the cell wall, but are both activated by a small molecule hormone known as auxin via the cell-surface ABP1 receptor;and the ROP2 pathway forms a positive feedback loop by activating the polarization of PIN1, which exports auxin to the cell wall. This auxin-modulated network is proposed to locally coordinate PC intercalation and to be linked to the global coordination mediated by leaf tip- and margin-high auxin gradients, which are apparently generated by a different transcription-based auxin-signaling pathway dependent on the nuclear TIR1/AFB auxin receptor. The objective of this proposal is to test the hypothesis that PC intercalation is coordinated by hierarchical auxin signaling, which may be mirrored by WNT signaling that modulates developmental patterns in animals.
Aim 1 focuses detailed mechanisms by which auxin locally coordinates PC intercalation, including putative ABP1 co-receptors that are transmembrane receptor-like kinases, their differential activation of the two Rho pathways, PIN1-mediated local extracellular auxin, and its coordination of these pathways.
Aim 2 will elucidate the mechanisms by which ROP2 activates PIN1 polarization via endosomal PIN1 trafficking.
Aim 3 will determine roles of the TIR1/AFB pathway and its target genes in the global coordination. The work will provide a comprehensive view of the mechanisms coordinating cellular intercalation at multiple levels. Given the conserved Rho signaling underlying cell intercalation and planar cell polarity (PCP) across plants and humans, the proposed work may provide new insights into convergent extension (CE) and other PCP- mediated processes. Because failure in CE causes neural tube defects, a common developmental disorder (1 out of 1000 pregnancies), this research might ultimately be relevant to human health improvements.

Public Health Relevance

The signaling mechanisms under our investigation, including Rho GTPase coordination of cell polarity and cellular intercalation, their linkage to the cytoskeleton and endocytic trafficking, hierarchical signaling of morphogenetic or developmental triggers, are all conserved in plants and animals. Our knowledge gained in the PC system may synergize the advances in our understanding of similar mechanisms or processes in mammalian systems, which are clearly linked to human embryogenesis and genetic disorders. Hence our work could ultimately be relevant to the improvement of human health.

National Institute of Health (NIH)
National Institute of General Medical Sciences (NIGMS)
Research Project (R01)
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Cellular Signaling and Regulatory Systems Study Section (CSRS)
Program Officer
Flicker, Paula F
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University of California Riverside
Other Basic Sciences
Schools of Earth Sciences/Natur
United States
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Xu, Tongda; Dai, Ning; Chen, Jisheng et al. (2014) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025-8
Guan, Yuefeng; Guo, Jingzhe; Li, Hui et al. (2013) Signaling in pollen tube growth: crosstalk, feedback, and missing links. Mol Plant 6:1053-64
Li, Hongjiang; Xu, Tongda; Lin, Deshu et al. (2013) Cytokinin signaling regulates pavement cell morphogenesis in Arabidopsis. Cell Res 23:290-9
Nagawa, Shingo; Xu, Tongda; Lin, Deshu et al. (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol 10:e1001299
Li, Hongjiang; Lin, Deshu; Dhonukshe, Pankaj et al. (2011) Phosphorylation switch modulates the interdigitated pattern of PIN1 localization and cell expansion in Arabidopsis leaf epidermis. Cell Res 21:970-8
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Robert, Stephanie; Kleine-Vehn, Jurgen; Barbez, Elke et al. (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111-21
Yan, An; Xu, Guanshui; Yang, Zhen-Biao (2009) Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes. Proc Natl Acad Sci U S A 106:22002-7

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