NADPH oxidase involvement in cellular integrity

Macpherson, Neil; Takeda, Seiji; Shang, Zhonglin; Dark, Adeeba; Mortimer, Jenny C.; Brownlee, Colin; Dolan, Liam; Davies, Julia M.

doi:10.1007/s00425-008-0716-2

Cited by 32 publications

(22 citation statements)

References 20 publications

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“…These seemingly diverse pathways may nonetheless share certain functional themes. For instance, with the well-established role of apoplastic ROS in controlling wall stiffness and extensibility (14,(43)(44)(45), it is conceivable that FER would mediate a ROS environment that weakens the pollen tube wall, whereas ANX1 and ANX2 would do so to maintain its integrity. Given the role of NADPH oxidasederived ROS in secondary cell wall synthesis and that RAC/ROPs have been implicated as regulating this process (46), it is conceivable for ROS to be involved in the THE1-mediated cell wall integrity-dependent growth regulatory process.…”

Section: Discussionmentioning

confidence: 99%

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

Duan¹,

Kita

Li³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

569

752

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Plant RHO GTPases (RAC/ROPs) mediate multiple extracellular signals ranging from hormone to stress and regulate diverse cellular processes important for polarized cell growth, differentiation, development, reproduction, and responses to the environment. They shuttle between the GDP-bound inactive state and the GTP-bound activated state and their activation is predominantly mediated by a family of guanine nucleotide exchange factors (GEFs) referred to as ROPGEFs. Using the Arabidopsis ROPGEF1 as bait, we identified members of a receptor-like kinase (RLK) family as potential upstream regulators for RAC/ROP signaling. NADPH oxidase-derived reactive oxygen species (ROS) are emerging as important regulators for growth and development and play a crucial role in mediating RAC/ROP-regulated root hair development, a polarized cell growth process. We therefore screened T-DNA insertion mutants in these RLKs for root hair defects and found that mutations in one of them, At3g51550 encoding the FERONIA (FER) receptor-like kinase, induced severe root hair defects. We show that the fer phenotypes correlated with reduced levels of active RAC/ ROPs and NADPH oxidase-dependent, auxin-regulated ROS accumulation in roots and root hairs and that up-regulating RAC/ROP signaling in fer countered the mutant phenotypes. Taken together, these observations strongly support FER as an upstream regulator for the RAC/ROP-signaled pathway that controls ROS-mediated root hair development. Moreover, FER was pulled down by ROP2 GTPase in a guanine nucleotide-regulated manner implying a dynamic signaling complex involving FER, a ROPGEF, and a RAC/ROP.

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Section: Discussionmentioning

confidence: 99%

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

Duan¹,

Kita

Li³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

569

752

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“…ATP is released by Arabidopsis in response to hyperand hypo-osmotic stress (Jeter et al, 2004). AtRBOHC is implicated in the response to hypo-osmotic shock (Macpherson et al, 2008), and AtMPK3 is known to be involved in hypo-osmotic and moderately hyperosmotic stress responses, where its transcription is dependent on Ca 2+ influx (Droillard et al, 2002). The results obtained here for roots, and previously for the Ca 2+ influx-dependent ATP induction of AtMPK3 transcription in leaves (Song et al, 2006), identify extracellular ATP, released during stress, as a regulator of the MPK cascade.…”

Section: Discussionmentioning

confidence: 99%

Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca²⁺channels

Demidchik¹,

Shang²,

Shin³

et al. 2009

The Plant Journal

Self Cite

187

247

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SUMMARYExtracellular ATP regulates higher plant growth and adaptation. The signalling events may be unique to higher plants, as they lack animal purinoceptor homologues. Although it is known that plant cytosolic free Ca 2+ can be elevated by extracellular ATP, the mechanism is unknown. Here, we have studied roots of Arabidopsis thaliana to determine the events that lead to the transcriptional stress response evoked by extracellular ATP. Root cell protoplasts were used to demonstrate that signalling to elevate cytosolic free Ca 2+ is determined by ATP perception at the plasma membrane, and not at the cell wall. Imaging revealed that extracellular ATP causes the production of reactive oxygen species in intact roots, with the plasma membrane NADPH oxidase AtRBOHC being the major contributor. This resulted in the stimulation of plasma membrane Ca 2+-permeable channels (determined using patch-clamp electrophysiology), which contribute to the elevation of cytosolic free Ca 2+ . Disruption of this pathway in the AtrbohC mutant impaired the extracellular ATP-induced increase in reactive oxygen species (ROS), the activation of Ca 2+ channels, and the transcription of the MAP kinase3 gene that is known to be involved in stress responses. This study shows that higher plants, although bereft of purinoceptor homologues, could have evolved a distinct mechanism to transduce the ATP signal at the plasma membrane.

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“…This was suggested to occur in growing root hairs (Velasquez et al, 2015). By contrast, the apo ROS produced by the activity of apo PER III (in hydroxylic cycles) would enhance polysaccharide cleavage and act as a wall-loosening agent that promotes growth (Fry, 1998;Schopfer et al, 2002;Dunand et al, 2007;Macpherson et al, 2008) independently of Ca 2+ signaling. Recently, two PER proteins (PER44 and PER75) were found to be repressed at the transcriptional level under low-gravity conditions.…”

Section: Apo Ros Homeostasis Is Regulated By Plasma Membrane Noxs Andmentioning

confidence: 99%

ROS Regulation of Polar Growth in Plant Cells

2016

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ORCID ID: 0000-0001-6332-7738 (J.M.E.).Root hair cells and pollen tubes, like fungal hyphae, possess a typical tip or polar cell expansion with growth limited to the apical dome. Cell expansion needs to be carefully regulated to produce a correct shape and size. Polar cell growth is sustained by oscillatory feedback loops comprising three main components that together play an important role regulating this process. One of the main components are reactive oxygen species (ROS) that, together with calcium ions (Ca 2+ ) and pH, sustain polar growth over time. Apoplastic ROS homeostasis controlled by NADPH oxidases as well as by secreted type III peroxidases has a great impact on cell wall properties during cell expansion. Polar growth needs to balance a focused secretion of new materials in an extending but still rigid cell wall in order to contain turgor pressure. In this review, we discuss the gaps in our understanding of how ROS impact on the oscillatory Ca 2+ and pH signatures that, coordinately, allow root hair cells and pollen tubes to expand in a controlled manner to several hundred times their original size toward specific signals.

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NADPH oxidase involvement in cellular integrity

Cited by 32 publications

References 20 publications

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca²⁺channels

ROS Regulation of Polar Growth in Plant Cells

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NADPH oxidase involvement in cellular integrity

Cited by 32 publications

References 20 publications

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development

Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca2+channels

ROS Regulation of Polar Growth in Plant Cells

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Plant extracellular ATP signalling by plasma membrane NADPH oxidase and Ca²⁺channels