The long-term goal of this project is to elucidate design principles and paradigms that govern rapid tip growth to produce cells with extraordinary lengths. Rapid tip growth is essential for many cells to efficiently explore their environment or to reach their long-distance destination, e.g., fungal mycelia invades host cells or forage the environment, pollen tubes (PT) travel through female tissues to deliver sperms, and neuronal cells are targeted to their destination for unilateral signal propagation. Rapid tip growth requires efficient and targeted fusion of vesicles (containing cell membrane and wall materials) to the cell apex. This targeted exocytosis is highly coordinated in space and time and is orchestrated by a Rho GTPase-based signaling machinery localized to the cell tip. Little is known about how the signaling machinery is spatially and temporally coordinated at the rapidly expanding tip and how the tip-targeted exocytosis contributes to rapid tip growth. To address these questions, the principal investigator's group has established the Arabidopsis PT as a model system. Using this system, the principal investigator's group was the first to demonstrate the tip localization of a Rho GTPase and its essential role in a rapidly tip-growing cell. They uncover a tip-localized ROP1 signaling network and demonstrate that this network modulates tip-targeted exocytosis and self-regulates ROP1 in a manner dependent upon tip-localized actin microfilaments. Their genetic studies reveal a global mechanism for restricting ROP1 signaling to the tip, which involves exocytosis-based tip targeting of the REN1 RhoGAP that inactivates ROP1. The objective of this project is to test the hypothesis that ROP1-dependent exocytosis orchestrates the self-organizing rapid tip growth via multiple regulatory roles including the positive and negative feedback-based spatiotemporal coordination of the growth-signaling machinery and the modulation of the cell wall mechanics required for turgor-driven growth in PT.
Aim 1 focuses on investigating the role of ROP1-dependent exocytosis in the feedback activation of ROP1 through its targeting of a cell surface receptor and its extracellular ligand that activate ROP1.
Aim 2 will elucidate the mechanism behind the feedback inhibition of ROP1 by analyzing how exocytosis-mediated REN1 targeting coordinates with exocytosis-independent REN1 activation at the tip.
Aim 3 will determine how ROP1-dependent exocytosis coordinates with clathrin-dependent endocytosis to modulate the cell wall mechanics necessary for sustained tip expansion. This work will provide a comprehensive view of the molecular and cellular mechanisms that control rapid tip growth in PT and will establish new paradigms and design principles for this fundamental process. Given the conserved Rho signaling underlying this process in diverse systems, these paradigms and principles will most likely enlighten mechanistic studies of similar processes in other medically relevant systems such as the invasive hyphal growth by pathogenic fungi. Therefore, the proposed research might ultimately be relevant to human health improvements.
Rapid tip growth, in which cells elongate at a speed up to 1 cm/hr by restricting growth to the apical end, is a fundamental developmental strategy that cells use to efficiently reach their destination or explore the environment, e.g., invasion of human host cells by fungal hyphae and delivery of sperms for fertilization by pollen tubes. It is not clear how cells orchestrate such speedy local growth. By using Arabidopsis pollen tube as a model system, this project will elucidate the molecular and cellular principles that coordinate rapid tip growth, which may provide a basis for designing drugs that target fungal pathogens.
|Li, Hui; Luo, Nan; Wang, Weidong et al. (2018) The REN4 rheostat dynamically coordinates the apical and lateral domains of Arabidopsis pollen tubes. Nat Commun 9:2573|
|Luo, Nan; Yan, An; Yang, Zhenbiao (2016) Measuring Exocytosis Rate Using Corrected Fluorescence Recovery After Photoconversion. Traffic 17:554-64|
|Yamamuro, Chizuko; Zhu, Jian-Kang; Yang, Zhenbiao (2016) Epigenetic Modifications and Plant Hormone Action. Mol Plant 9:57-70|
|Rong, Duoyan; Luo, Nan; Mollet, Jean Claude et al. (2016) Salicylic Acid Regulates Pollen Tip Growth through an NPR3/NPR4-Independent Pathway. Mol Plant 9:1478-1491|
|Pan, Xue; Chen, Jisheng; Yang, Zhenbiao (2015) Auxin regulation of cell polarity in plants. Curr Opin Plant Biol 28:144-53|
|Zhao, Lihua; He, Jiangman; Cai, Hanyang et al. (2014) Comparative expression profiling reveals gene functions in female meiosis and gametophyte development in Arabidopsis. Plant J 80:615-28|
|Xu, Tongda; Dai, Ning; Chen, Jisheng et al. (2014) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025-8|
|Chang, Fang; Gu, Ying; Ma, Hong et al. (2013) AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth. Mol Plant 6:1187-201|
|Yang, Zhenbiao; Lavagi, Irene (2012) Spatial control of plasma membrane domains: ROP GTPase-based symmetry breaking. Curr Opin Plant Biol 15:601-7|
|Craddock, Christian; Lavagi, Irene; Yang, Zhenbiao (2012) New insights into Rho signaling from plant ROP/Rac GTPases. Trends Cell Biol 22:492-501|
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