The Endoplasmic Reticulum Is a Reservoir for WAVE/SCAR Regulatory Complex Signaling in the Arabidopsis Leaf

Chunhua Zhang,Daniel B Szymanski,Simeon O Kotchoni,Sara Reagan,Vitaly P Boyko,Eileen Mallery

doi:10.1104/pp.113.217422

Chunhua Zhang, Daniel B Szymanski + Show 4 more

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https://doi.org/10.1104/pp.113.217422

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Journal: Plant Physiology	Publication Date: Apr 23, 2013
Citations: 37	License type: CC BY 4.0

Affiliation: Purdue University West Lafayette

Abstract

During plant cell morphogenesis, signal transduction and cytoskeletal dynamics interact to locally organize the cytoplasm and define the geometry of cell expansion. The WAVE/SCAR (for WASP family verprolin homologous/suppressor of cyclic AMP receptor) regulatory complex (W/SRC) is an evolutionarily conserved heteromeric protein complex. Within the plant kingdom W/SRC is a broadly used effector that converts Rho-of-Plants (ROP)/Rac small GTPase signals into Actin-Related Protein2/3 and actin-dependent growth responses. Although the components and biochemistry of the W/SRC pathway are well understood, a basic understanding of how cells partition W/SRC into active and inactive pools is lacking. In this paper, we report that the endoplasmic reticulum (ER) is an important organelle for W/SRC regulation. We determined that a large intracellular pool of the core W/SRC subunit NAP1, like the known positive regulator of W/SRC, the DOCK family guanine nucleotide-exchange factor SPIKE1 (SPK1), localizes to the surface of the ER. The ER-associated NAP1 is inactive because it displays little colocalization with the actin network, and ER localization requires neither activating signals from SPK1 nor a physical association with its W/SRC-binding partner, SRA1. Our results indicate that in Arabidopsis (Arabidopsis thaliana) leaf pavement cells and trichomes, the ER is a reservoir for W/SRC signaling and may have a key role in the early steps of W/SRC assembly and/or activation.

Highlights

IntroductionSignal transduction and cytoskeletal dynamics interact to locally organize the cytoplasm and define the geometry of cell expansion
During plant cell morphogenesis, signal transduction and cytoskeletal dynamics interact to locally organize the cytoplasm and define the geometry of cell expansion
Because NAP1 is widely expressed in the shoots (El-Assal et al, 2004), we were able to examine the subcellular distribution of NAP1 extracts prepared from shoots at 16 to 18 d after germination (DAG)

Summary

Introduction

Signal transduction and cytoskeletal dynamics interact to locally organize the cytoplasm and define the geometry of cell expansion. In this scheme for actin-based growth control, the actin network dynamically rearranges at spatial scales that span from approximately 1- to 10-mm subcellular domains that may locally position organelles (Cleary, 1995; Gibbon et al, 1999; Szymanski et al, 1999) to the more than 100-mm actin bundle networks that operate at the spatial scales of entire cells (Gutierrez et al, 2009; Dyachok et al, 2011) It is clear from the work of several laboratories that the W/SRC and ARP2/3 protein complexes are required to organize cortical actin and actin bundle networks in trichomes (Szymanski et al, 1999; Le et al, 2003; Deeks et al, 2004; Zhang et al, 2005) and cylindrical epidermal cells (Mathur et al, 2003b; Dyachok et al, 2008, 2011). A key challenge now is to understand how plant cells deploy these approximately 10- to 20-nm heteromeric protein complexes to influence the patterns of growth at cellular scales

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