The role of<i>Arabidopsis SCAR</i>genes in ARP2-ARP3-dependent cell morphogenesis

Uhrig, Joachim F.; Mutondo, Moola; Zimmermann, Ilona; Deeks, Michael J.; Machesky, Laura M.; Thomas, Philipp; Uhrig, Silke; Rambke, Claudia; Hussey, Patrick J.; Hülskamp, Martin

doi:10.1242/dev.02792

Cited by 95 publications

(105 citation statements)

References 63 publications

(103 reference statements)

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“…There was a strong association between inducible expression of the toxins and the appearance of trichomes with severe trichome swelling and reduced branch number phenotypes (Singh et al, 2012). Although the exact mechanism of ROP-dependent control of W/SRC remains to be determined, the results described above in combination with the detection of direct interactions between the ROPGEF SPK1, active forms of ROP, and W/SRC subunits (Basu et al, , 2008Uhrig et al, 2007) strongly suggest that W/SRC is a ROP effector complex.…”

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confidence: 88%

“…Many of the components and regulatory relationships among the complexes were discovered based on the stage-specific cell-swelling and -twisting phenotypes of the distorted class of Arabidopsis (Arabidopsis thaliana) trichome mutants (Szymanski et al, 1999;Zhang et al, 2005Zhang et al, , 2008Djakovic et al, 2006;Le et al, 2006;Uhrig et al, 2007). However, in both maize (Zea mays) and Arabidopsis, W/SRC and/or ARP2/3 are required for normal pavement cell morphogenesis (Frank and Smith, 2002;Mathur et al, 2003b;Brembu et al, 2004).…”

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confidence: 99%

“…For example, mutant complementation tests indicate that human W/SRC and ARP2/3 complex subunits can substitute for the Arabidopsis proteins (Mathur et al, 2003b). Furthermore, biochemical assays of Arabidopsis W/SRC El-Assal et al, 2004;Frank et al, 2004;Le et al, 2006;Uhrig et al, 2007) and ARP2/ 3 assembly (Kotchoni et al, 2009) have shown that the binary interactions among W/SRC subunits and ARP2/3 complex assembly mechanisms are indistinguishable from those that have been observed for human W/SRC (Gautreau et al, 2004) and yeast ARP2/3 (Winter et al, 1999). After an initial period of controversy concerning the biochemical control of W/SRC, it is now apparent that vertebrate W/SRC (Derivery et al, 2009;Ismail et al, 2009), like the ARP2/3 complex (Machesky et al, 1999), is intrinsically inactive and requires positive regulation by Rac and other factors to fully activate ARP2/3 (Ismail et al, 2009;Lebensohn and Kirschner, 2009;Chen et al, 2010).…”

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confidence: 99%

“…The endoplasmic reticulum (ER) may also be involved in W/SRC regulation. The ER-localized DOCK family ROPGEF SPK1 (Zhang et al, 2010) physically associates with multiple W/SRC proteins (Uhrig et al, 2007;Basu et al, 2008) and, based on genetic criteria, is an upstream, positive regulator of the W/SRC-ARP2/3 pathway (Basu et al, 2008). In the leaf, one function of SPK1 is to promote normal trafficking between the ER and Golgi; however, arp2/3 mutants do not share ER-stress phenotypes with spk1 (Zhang et al, 2010), making it unclear if SPK1 and the ER are directly involved in W/SRC signaling.…”

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confidence: 99%

“…This paper focuses on the localization and control of the W/SRC subunit NAP1/GNARLED/NAPP/HEM1/ 2. Arabidopsis NAP1 directly interacts with the ROP/ Rac effector subunit SRA1/PIROGI/KLUNKER/PIRP El-Assal et al, 2004;Uhrig et al, 2007). Based on the equally severe syndrome of nap1 and arp2/3 null phenotypes, and double mutant analyses, the only known function of NAP1 is to positively regulate ARP2/3 (Brembu et al, 2004;Deeks et al, 2004;El-Din El-Assal et al, 2004;Li et al, 2004).…”

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

et al. 2013

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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.

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

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Plant Actin Biology

Deeks

Hussey

2009

Encyclopedia of Life Sciences

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Actin is a major component of the plant cytoskeleton. Filamentous actin (F‐actin) contributes to the maintenance of the internal architecture of the cell, drives cytoplasmic streaming (the movement of components around the cytosol) and contributes to the process of cell division. The biochemistry of plant actin has many similarities to that of yeast and animals, but has developed its own strategies and molecular machinery to organize actin filaments. F‐actin provides tracks for myosin molecular motors to transport organelles at high velocities and actin is required for specific stages of vesicle trafficking that underpin cell growth and development. The means by which plant cells control the nucleation of new actin filaments from G‐actin have diverged considerably from yeast and metazoans. The unique aspects of the plant actin cytoskeleton are likely to have arisen from a combination of the environmental challenges to a sessile multicellular existence and a complex evolutionary history. Key concepts The basic principles of actin biochemistry applicable to animals, fungi and protists are conserved in plants but there are a number of specific modifications as plants do not possess the full complement of animal actin‐binding proteins. Actin filaments in plants have to fulfil unique functions. Actin focuses on the expansion of tip growing cells, maintains cytoarchitecture and responds to the environment (e.g. polarizing in response to pathogen stimulation). During cell division actin filaments participate in all major plant‐specific arrays. A stationary cell is NOT a physically inactive cell. Actin cables are exploited for organelle transport. Actin‐based transport tends to dominate over microtubule‐based movement. Plants utilize the fastest known type V myosin (known in plants as type XI) within the eukaryote kingdom. Polymerization dynamics are thought to add to trafficking capabilities as low levels of antiactin drugs disrupt vesicle delivery and fusion during cell growth yet preserve myosin‐mediated transport. New proteins and new domain combinations have become established in plants to regulate the actin cytoskeleton in accordance with the unusual demands placed on them. Importantly, these radical adaptations should not be considered purely in terms of a response to a sedentary way of life as the fungal kingdom has achieved such a conversion using arguably less radical cytoskeletal solutions. Consequently the impact of other unique facets of plant evolutionary history and niches must be considered.

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Plant Actin Biology

Deeks

Hussey

2016

Encyclopedia of Life Sciences

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Actin is a major component of the plant cytoskeleton. Filamentous actin (F‐actin) contributes to the maintenance of the internal architecture of the cell, drives cytoplasmic streaming (the movement of components around the cytosol) and contributes to the process of cell division. The biochemistry of plant actin has many similarities to that of yeast and animals, but has developed its own strategies and molecular machinery to organise actin filaments. F‐actin provides tracks for myosin molecular motors to transport organelles at high velocities, and actin is required for specific stages of vesicle trafficking that underpin cell growth and development. The means by which plant cells control the nucleation of new actin filaments from G‐actin have diverged considerably from yeast and metazoans. The unique aspects of the plant actin cytoskeleton are likely to have arisen from a combination of the environmental challenges to a sessile multicellular existence and an ancient diversification from the ancestors of the Opisthokonta and Amoebozoa model organisms from which the majority of eukaryote cytoskeletal paradigms have been established. Key Concepts The basic principles of actin biochemistry applicable to animals, fungi and protists are conserved in plants but there are a number of specific modifications as plants do not possess the full complement of animal actin‐binding proteins. Actin filaments in plants have to fulfil unique functions. Actin focuses on the expansion of tip growing cells, maintains cytoarchitecture and responds to the environment (e.g. polarising in response to pathogen stimulation). During cell division actin filaments participate in all major plant‐specific arrays. A stationary cell is NOT a physically inactive cell. Actin cables are exploited for organelle transport. Actin‐based transport tends to dominate over microtubule‐based movement. Plants utilise the fastest known type V myosin (known in plants as type XI) within the eukaryote kingdom. Polymerisation dynamics are thought to add to trafficking capabilities as low levels of antiactin drugs disrupt vesicle delivery and fusion during cell growth yet preserve myosin‐mediated transport. Plant‐specific proteins and novel domain combinations have become established in plants to regulate the actin cytoskeleton in accordance with the demands of sessile multicellular photosynthetic autotrophy. These cytoskeletal adaptations to sedentary life within a cell wall are distinct from fungi, possibly reflecting the ancient diversification between the opisthokonts and plants.

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The role ofArabidopsis SCARgenes in ARP2-ARP3-dependent cell morphogenesis

Cited by 95 publications

References 63 publications

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

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

Plant Actin Biology

Plant Actin Biology

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