The long-term goal of this project is to understand the underlying signaling mechanisms of cell intercalation, in which neighboring cells change their shapes to become intercalated with each other. Cell intercalation is critical for the proper development and morphogenesis of multi-cellular organisms. Cell intercalation is required for the process of convergent extension during gastrulation, neurulation, axis elongation, and organogenesis of animal and human embryos. However, signals and pathways governing this fundamental process are poorly characterized, though some underlying signaling events (e.g., Rho GTPases and the cytoskeleton) are known to be 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 develop intercalary lobes and indentations to form the jigsaw-puzzle appearance. The Pi's group has developed the pavement cell as a model system for cell intercalation, and has established the first framework of a Rho GTPase-dependent intracellualr signaling network that controls this process. It is composed of two counteracting pathways: a ROP2-RIC4-actin pathway activating lobe formation and a ROP6-RIC1- microtubule pathway promoting indentation. In this project, signals, receptors and new components will be determined and linked to this framework.
In aim 1, signaling events activating the ROP2 GTPase, e.g., signaling by the SPK1 ROP guanine nucleotide exchange factor, will be investigated using biochemical, genetic, and cell biological methods.
In aim 2, molecules upstream of the ROP6 GTPase will be determined using similar approaches, and the intercellular signaling between the ROP6 and the ROP2 pathways will be investigated to understand how lobing and indenting are coordinated between the neighboring cells.
Aim 3 is to investigate how auxin gradients, acting as a developmental signal, induce intercalary growth. A combination of rop mutants and biochemical and cell biological assays will be used to determine whether auxin activates the ROP2 or ROP6 pathway. The TMK receptor-like kinases that are required for intercalary growth will be tested for their participation in auxin perception. From these aims, a comprehensive picture of the molecular and cellular mechanisms for intercalary growth will be revealed. Given the conservation of the signaling mechanisms underlying cell intercalation across plants and humans, the knowledge gained from this research may provide new insights into our understanding of convergent extension. Because failure in convergent extension causes neural tube defects (NTDs), a common developmental disorder (1 out of 1000 pregnancies), this research is relevant to human health improvements. ^_^^

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
3R01GM081451-03S2
Application #
7927968
Study Section
Intercellular Interactions (ICI)
Program Officer
Flicker, Paula F
Project Start
2009-09-30
Project End
2011-08-31
Budget Start
2009-09-30
Budget End
2011-08-31
Support Year
3
Fiscal Year
2009
Total Cost
$243,200
Indirect Cost
Name
University of California Riverside
Department
Other Basic Sciences
Type
Schools of Earth Sciences/Natur
DUNS #
627797426
City
Riverside
State
CA
Country
United States
Zip Code
92521
Yamamuro, Chizuko; Zhu, Jian-Kang; Yang, Zhenbiao (2016) Epigenetic Modifications and Plant Hormone Action. Mol Plant 9:57-70
Pan, Xue; Chen, Jisheng; Yang, Zhenbiao (2015) Auxin regulation of cell polarity in plants. Curr Opin Plant Biol 28:144-53
Chen, Jisheng; Wang, Fei; Zheng, Shiqin et al. (2015) Pavement cells: a model system for non-transcriptional auxin signalling and crosstalks. J Exp Bot 66:4957-70
Xu, Tongda; Dai, Ning; Chen, Jisheng et al. (2014) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025-8
Lin, Deshu; Cao, Lingyan; Zhou, Zhenzhen et al. (2013) Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr Biol 23:290-7
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
Craddock, Christian; Lavagi, Irene; Yang, Zhenbiao (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol 22:492-501
Yang, Zhenbiao; Lavagi, Irene (2012) Spatial control of plasma membrane domains: ROP GTPase-based symmetry breaking. Curr Opin Plant Biol 15:601-7
Lin, Deshu; Nagawa, Shingo; Chen, Jisheng et al. (2012) A ROP GTPase-dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr Biol 22:1319-25

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