The Emerging Role of Reactive Oxygen Species Signaling during Lateral Root Development

Manzano, Concepción; Pallero-Baena, Mercedes; Casimiro, Ilda; Rybel, Bert De; Orman-Ligeza, Beata; Isterdael, Gert Van; Beeckman, Tom; Draye, Xavier; Casero, P. J.; Pozo, Juan C. del

doi:10.1104/pp.114.238873

Cited by 122 publications

(118 citation statements)

References 49 publications

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“…It has been supported that lateral root primordium specification involves auxin-induced transcriptional regulation but not ROS signaling (Manzano et al 2014). Although our data cannot unambiguously answer the previous question, the altered pattern of auxin accumulation in H 2 O 2 -treated leaves suggests an early, auxin-induced, SMC specification.…”

Section: Ros and Asymmetrical Smc Divisioncontrasting

confidence: 51%

Deliberate ROS production and auxin synergistically trigger the asymmetrical division generating the subsidiary cells in Zea mays stomatal complexes

2015

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Subsidiary cell generation in Poaceae is an outstanding example of local intercellular stimulation. An inductive stimulus emanates from the guard cell mother cells (GMCs) towards their laterally adjacent subsidiary cell mother cells (SMCs) and triggers the asymmetrical division of the latter. Indole-3-acetic acid (IAA) immunolocalization in Zea mays protoderm confirmed that the GMCs function as local sources of auxin and revealed that auxin is polarly accumulated between GMCs and SMCs in a timely-dependent manner. Besides, staining techniques showed that reactive oxygen species (ROS) exhibit a closely similar, also time-dependent, pattern of appearance suggesting ROS implication in subsidiary cell formation. This phenomenon was further investigated by using the specific NADPH-oxidase inhibitor diphenylene iodonium, the ROS scavenger N-acetyl-cysteine, menadione which leads to ROS overproduction, and H2O2. Treatments with diphenylene iodonium, N-acetyl-cysteine, and menadione specifically blocked SMC polarization and asymmetrical division. In contrast, H2O2 promoted the establishment of SMC polarity and subsequently subsidiary cell formation in "younger" protodermal areas. Surprisingly, H2O2 favored the asymmetrical division of the intervening cells of the stomatal rows leading to the creation of extra apical subsidiary cells. Moreover, H2O2 altered IAA localization, whereas synthetic auxin analogue 1-napthaleneacetic acid enhanced ROS accumulation. Combined treatments with ROS modulators along with 1-napthaleneacetic acid or 2,3,5-triiodobenzoic acid, an auxin efflux inhibitor, confirmed the crosstalk between ROS and auxin functioning during subsidiary cell generation. Collectively, our results demonstrate that ROS are critical partners of auxin during development of Z. mays stomatal complexes. The interplay between auxin and ROS seems to be spatially and temporarily regulated.

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Section: Ros and Asymmetrical Smc Divisioncontrasting

confidence: 51%

Deliberate ROS production and auxin synergistically trigger the asymmetrical division generating the subsidiary cells in Zea mays stomatal complexes

2015

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“…The ROS signaling function of AtPIP2;1 may also be relevant in other tissues or organs where AtPIP2;1 operates such as bundle sheaths (36) or roots (37). In the latter case, AtPIP2;1 was shown to facilitate the emergence of lateral roots, a process known to involve ROS (38). These ideas are not exclusive of other cell signaling functions of AtPIP2;1, such as extracellular CO 2 transport and signaling in guard cells (25).…”

Section: Discussionmentioning

confidence: 91%

Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure

Rodrigues

Reshetnyak

Grondin

et al. 2017

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

259

216

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Stomatal movements are crucial for the control of plant water status and protection against pathogens. Assays on epidermal peels revealed that, similar to abscisic acid (ABA), pathogen-associated molecular pattern (PAMP) flg22 requires the AtPIP2;1 aquaporin to induce stomatal closure. Flg22 also induced an increase in osmotic water permeability (P f ) of guard cell protoplasts through activation of AtPIP2;1. The use of HyPer, a genetic probe for intracellular hydrogen peroxide (H 2 O 2 ), revealed that both ABA and flg22 triggered an accumulation of H 2 O 2 in wild-type but not pip2;1 guard cells. Pretreatment of guard cells with flg22 or ABA facilitated the influx of exogenous H 2 O 2 . Brassinosteroid insensitive 1-associated receptor kinase 1 (BAK1) and open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6) were both necessary to flg22-induced P f and both phosphorylated AtPIP2;1 on Ser121 in vitro. Accumulation of H 2 O 2 and stomatal closure as induced by flg22 was restored in pip2;1 guard cells by a phosphomimetic form (Ser121Asp) but not by a phosphodeficient form (Ser121Ala) of AtPIP2;1. We propose a mechanism whereby phosphorylation of AtPIP2;1 Ser121 by BAK1 and/or OST1 is triggered in response to flg22 to activate its water and H 2 O 2 transport activities. This work establishes a signaling role of plasma membrane aquaporins in guard cells and potentially in other cellular context involving H 2 O 2 signaling.aquaporin | pathogen | guard cell signaling | hydrogen peroxide | stomatal movement

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“…So far, no per mutants have been reported to have defective polar growth in pollen tubes, probably due to the high degree of genetic redundancy between the 71 encoded apo PER III proteins in Arabidopsis (Francoz et al, 2015). Some apo PER III proteins appear to harden the cell wall structure, while others impact cell wall loosening during plant development (Passardi et al, 2006;Jin et al, 2011;Pedreira et al, 2011;Herrero et al, 2013;Kunieda et al, 2013;Shigeto et al, 2013;Manzano et al, 2014). It is unclear how these two opposite effects on cell wall polymers that are mediated by apo PER III are coordinated during the oscillatory growth cycles of these cells.…”

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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The Emerging Role of Reactive Oxygen Species Signaling during Lateral Root Development

Cited by 122 publications

References 49 publications

Deliberate ROS production and auxin synergistically trigger the asymmetrical division generating the subsidiary cells in Zea mays stomatal complexes

Deliberate ROS production and auxin synergistically trigger the asymmetrical division generating the subsidiary cells in Zea mays stomatal complexes

Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure

ROS Regulation of Polar Growth in Plant Cells

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