UCR

Department of Botany & Plant Sciences



Faculty


YangZhenbiao Yang

Professor in Plant Cell Biology (Ph.D., 1990, Virginia Tech)
Office: 4234B Genomics Building
Phone: (951) 827-7351
Fax: (951) 827-5155
Email: zhenbiao.yang@ucr.edu

 

 

 

Background
A Global Study of Rop Signaling Networks in Arabidopsis
Cell Polarity Development and Cell Shape Formation
Selected Publications (Bibliography page)
The Yang Group

Background

My laboratory has focused on two inter-linked areas in plant cell biology: molecular basis for cell polarity development/cell shape formation and signaling networks controlled by a plant-specific GTPase switch called Rop.

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A Global Study of Rop Signaling Networks in Arabidopsis

Although our knowledge of plant signal tranduction has leaped over the last few years owing to genetic studies in Arabidopsis, intracellular signaling pathways linking cell surface receptors to nuclear components remain poorly understood. In animals and yeast, G proteins or GTPases are pivotal switches that turn on and off intracellular signaling pathways by cycling between GTP-bound active and GDP-bound inactive forms. The Arabidopsis genome sequence reveals that plants lack many of the signaling G proteins used by animals and yeast; instead, plants contain a unique family of small GTPases, termed Rop. Evidence has emerged from my laboratory and several other laboratories that Rop acts as a versatile switch in signal transduction in plants. We have been interested in elucidating the function of 11 ROP genes and identifying various Rop-dependent pathways in Arabidopsis. Towards this goal, we have used an integrated approach by investigating Rop gene expression and protein localization, by characterizing phenotypes of rop knockout mutants and transgenic plants expressing dominant rop mutants, and by identifying Rop-interacting proteins. From these studies, we have concluded that Rop participates in various signaling pathways that control a wide variety of processes during plant growth, development, and responses to the environment (see Figure 1). This functional diversity of the Rop GTPasse family is further supported by our identification of receptor Ser/Thr kinases as putative Rop interactors and by our demonstration that the Arabidopsis genome contains 11 genes encoding putative Rop targets called RICs (Rop-interacting CRIB motif-containing proteins). RICs are divergent novel proteins containing a CRIB (Cdc42/Rac-interactive binding) motif required for the interaction with the GTP-bound active form of Rop. Subcellular localization and overexpression in pollen tubes suggest distinct functions for different RICs. With the aid of knockout mutants and analysis of Rop-RIC differential interaction, we are aiming to determine whether each Rop and RIC are functionally distinct or redundant and whether specific Rop-RIC pairs act in distinct Rop signaling pathways.

Figure 1. A generalized scheme illustrating the functional diversity of Rop GTPasesCell Polarity Development and Cell Shape Formation. GEF, guanine nucleotide exchange factor; GDI, guanine nucleotide dissociation inhibitor; RopGAP, Rop GTPase activating protein. RIC, Rop-interacting CRIB-containing proteins.

 

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Cell Polarity Development and Cell Shape Formation

Cell polarity is fundamentally important to plant growth and development. Some well-known examples of polarity in plant cells include asymmetric distribution of auxin carriers in the plasma membrane (PM) that is essential for polar auxin transport, asymmetric cell division (generally preceded by polar cytoplasmic distribution) that is critical for cell differentiation (e.g., zygote division of zygotes and division of precursors for guard cells), and polar cell expansion that is important for cell shape formation. Unlike single-celled yeast or cultured mammalian cell lines, cell polarity in higher plants is generally expressed in multi-cellular context and is not expressed normally in cultured cells. This contributes to the difficulties in studying the molecular basis of cell polarity control in higher plants, which remained mysterious until recent studies of Rop GTPases. We have used the "single-celled" tip-growing pollen tube as a model to generate hypotheses about the Rop-dependent pathways leading to polar cell expansion and extended these hypotheses to other cell types including non-tip-growing cells in intact tissues.

A spatially-regulated Rop signaling network controls polar growth in pollen tubes.

Pollen tubes provide an ideal model system for the study of cell polarity. As a male gametophyte, pollen tube growth is controlled by the haploid genome. In culture, pollen tubes develop a uniform cylindrical shape through an extreme form of polar growth--tip growth, a process involving continuous targeting and fusion of Golgi vesicles to a defined region of the plasma membrane, termed tip growth domain (Figure 2). What are the mechanisms that define the tip growth domain and control localized vesicle targeting and fusion is of significant interests. Our studies have demonstrated that the tip-localized Rop1 is a central component of these mechanisms and have allowed us to develop a model for a Rop-dependent network in the control of tip growth (Figure 3). Our unpublished data suggest that PM-localized Rop1 is activated by an unknown localized cue and that the active Rop1 promotes the localization of Rop1 to the PM, forming a positive feedback loop of Rop activation and recruitment. The localized activation of this loop and subsequent lateral amplification and global inhibition of this loop allows the formation of a tip-high gradient of active Rop (Figure 3). This active Rop gradient defines the tip growth domain and controls localized exocytosis. Our evidence suggests that Rop controls localized exocytosis through both actin dynamics and cytoslic calcium accumulation at the tip. This model will be further tested by addressing the following questions: 1) What is the localized cue? 2) How does it activate Rop1 and how does active Rop promote Rop recruitment? 3) How does active Rop regulate actin dynamics and calcium accumulation?

Figure 2. The pollen tube as a model system for cell polarity studies. A. In vitro-cultured pollen tubes show uniformly cylindrically-shaped cells. B. Schematics showing polar distribution of the cytoplasm in pollen tubes. Note the apex contains dynamic F-actin and Golgi vesicles.
Figure 3. A model for spatial regulation of a Rop signaling network and its role in the control of tip growth in pollen tubes. A. The localization of GFP-tagged RIC1 indicating the distribution of active Rop as a tip-high gradient in the plasma membrane of pollen tubes. The localization coincides with the tip growth domain (see Figure 2). B. This Rop activity gradient is formed by an elaborate spatial regulation of Rop recruitment and activation at the tip, defines the tip growth domain, and controls polar exocytosis.

Rop signaling to cell shape formation during organogenesis.

The Rop-dependent tip growth mechanism provides a paradigm for understanding cell polarity control and cell shape formation in plants. By investigating the role of Rop signaling in various other cell types, including root hairs (also tip-growing cells) and various non-tip-growing cells in intact tissue, we conclude that Rop signaling provides a general mechanism for the control of cell polarity and cell shape formation. Furthermore, we have demonstrated that cell shape formation in intact tissues involves two phases with distinct mechanisms. In the Rop-dependent early phase cell expansion occurs in various directions defined by the localization of cortical fine actin as in tip growth, whereas in the Rop-independent late phase cells expand only the longitudinal direction that is determined by transverse cortical microtubules. Cell expansion in developing tissues is controlled by developmental and hormonal signals and likely involves inter-cellular communication between neighboring cells. Using epidermal pavement cells with unique wavy shape and combined genetic and biochemical approaches, we are identifying signals that regulate Rop-dependent directional cell expansion and other components in the Rop-dependent pathways.

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Selected Publications, Invited Reviews and Book Chapters (Bibliography page)

The Yang Group

Yang's group was conducting research (retreat) in Yosemite in Sept. 2001. Left to right: Shundai, Ying Gu, Ying Fu, Vanessa, Zhenbiao, John.

Postdoctoral Associates:

  • Fang Bao, since 03/02, Rop signaling in hormone action.
  • Jae-Ung Huang, since 03/02, Rop signaling in pollen tube tip growth.
  • Vanessa Vernoud, since 05/00, genetic screen for pollen tube mutants and Rop1 enhancers and suppressors.
  • John (Zhi-Liang) Zheng, since 12/99, Rop signaling in ABA responses and nutrient stress.
  • Ying Fu, since 11/99, Rop regulation of cytoskeletal dynamics in pollen tube growth and cell shape formation.

Graduate Students:

  • Ying Fu, since 1998, genetic studies of RICs and Rop1 targets in pollen tubes.
  • Shundai (co-supervised by Betty Lord), since 2000, actin dynamics in pollen tubes/actin nucleation factors.

Staff Research Associate

  • Avin Tam, since 10/01, biochemistry of RICs

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