The pH of the Apoplast: Dynamic Factor with Functional Impact Under Stress

Geilfus, Christoph‐Martin

doi:10.1016/j.molp.2017.09.018

Cited by 162 publications

(143 citation statements)

References 158 publications

(245 reference statements)

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“…Consequently, cc1cc2 mutants exhibited a more acidic apoplast and basic cortical side of the plasma membrane, could acidify a basic growth media faster, and were more sensitive to hygromycin than WT plants (Figs and EV5). Salt stress was reported to alkalinize the apoplast and the cytosol (Gao et al , ; Geilfus, ). This highlights the inverse effect of biotic and abiotic stress on plant cellular pH modulation at the plasma membrane and might explain the opposite phenotypes of cc1cc2 on abiotic and biotic stress.…”

Section: Discussionmentioning

confidence: 99%

“…The activity of Arabidopsis H + -ATPases (AHAs) is essential for plant growth and development under different environmental conditions. Dynamic phosphorylation of specific AHA amino acid residues rapidly regulates proton pump activity in response to external and internal stimuli, such as abiotic and biotic stresses or hormones (Olsson et al, 1998;Gao et al, 2004;Jeworutzki et al, 2010;Stecker et al, 2014;Haruta et al, 2015;Falhof et al, 2016;Geilfus, 2017). The activation of AHAs, for example, is known to require the phosphorylation of their penultimate C-terminal threonine residue (Inoue & Kinoshita, 2017).…”

Section: Introductionmentioning

confidence: 99%

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Pathogen‐inducedpHchanges regulate the growth‐defense balance in plants

et al. 2019

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Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall‐related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation‐based proton pump activation in response to the fungus Fusarium oxysporum immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. In addition, pH seems to influence cellulose structure. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth‐defense balance.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Pathogen‐inducedpHchanges regulate the growth‐defense balance in plants

et al. 2019

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“…The broad pH range (3.5–8.3) experienced by proteins in the apoplast, combined with the rapid pH changes induced by hormones, cell growth, and biotic and abiotic stresses, calls for the use of robust fluorescent tags able to withstand these dynamics (Arsuffi & Braybrook, ; Barbez et al., ; Geilfus, ; Yu et al., ). There are well over 100 FPs available to date, but there is no silver bullet to determine the best FP for any given experiment without trial and error.…”

Section: Discussionmentioning

confidence: 99%

“…5.4 in meristematic cells of Arabidopsis roots) and can vary widely (pH 3.5-8.3; e.g. depending on the tissue/species, if cells are growing, or if they are responding to biotic or abiotic stresses) (Arsuffi & Braybrook, 2018;Barbez, Dunser, Gaidora, Lendl, & Busch, 2017;Geilfus, 2017;Yu, Tang, & Kuo, 2000). This limits the functionality of FPs in the apoplast because acidic conditions reduce FP fluorescence [for an in planta example, see Dean et al (2007)].…”

Section: Introductionmentioning

confidence: 99%

I see the light! Fluorescent proteins suitable for cell wall/apoplast targeting in Nicotiana benthamiana leaves

Stoddard

Rolland

2019

Plant Direct

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Correct subcellular targeting is crucial for protein function. Protein location can be visualized in vivo by fusion to a fluorescent protein ( FP ). Nevertheless, despite intense engineering efforts, most FP s are dim or completely quenched at low pH (<6). This is particularly problematic for the study of proteins targeted to acidic compartments such as vacuoles ( pH ~ 3–6) or plant cell walls ( pH ~ 3.5–8.3). Plant cell walls play important roles (e.g. structural/protective role, control of growth/morphogenesis), are diverse in structure and function, and are highly dynamic (e.g. during cell growth, in response to biotic/abiotic stresses). To study and engineer plant cell walls, it is therefore critical to identify robust tools which can be used to locate proteins expressed in the apoplast. Here we used a transient expression assay in Nicotiana benthamiana leaves to test a range of FP s in vivo , and determined which ones retained strong fluorescence in the acidic environment of the apoplast. We selected 10 fluorescent proteins with a range of in vitro properties; two historical FP s and eight FP s with in vitro properties suggesting lower pH sensitivity or improved brightness, some of which had never been tested in plants prior to our study. We targeted each FP to the cytosol or the apoplast and compared the fluorescence in both compartments, before testing the in vivo pH sensitivity of FP s across a pH 8–4 gradient. Our results suggest that mT urquoise2, mN eonGreen, and mC herry are suited to tracking proteins in the apoplast under dynamic pH conditions. These fluorescent proteins may also be useful in other acidic compartments such as vacuoles.

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“…() for a salt‐induced acidification). Apoplastic pH a is in the moderately acidic range, and values typically range from c. 4.9 to 5.8 (for an overview on the older literature, see Felle (); an update is provided by Geilfus, ). Higher values ( c. pH 6.3) were reported by Gao et al .…”

Section: Evidence For H+ Influx Across the Plasma Membrane Sustained mentioning

confidence: 99%

Biochemical pH clamp: the forgotten resource in membrane bioenergetics

Wegner

Shabala

2019

New Phytologist

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Summary Solute uptake and release by plant cells are frequently energized by coupling to H+ influx supported by the proton motive force (pmf). The pmf results from a stable pH difference between the apoplast and the cytosol, with bulk values ranging from 4.9 to 5.8 and from 7.1 to 7.5, respectively, in combination with a negative electrical membrane potential. The P‐type H+ ATPases pumping H+ from the cytosol into the apoplast at the expense of ATP hydrolysis are generally viewed as the only pmf source, exclusively linking membrane transport to energy metabolism. However, recent evidence suggests that pump activity may be insufficient to energize transport, particularly under stress conditions. Indeed, cytosolic H+ scavenging and apoplastic H+ generation by metabolism (denoted as ‘active’ buffering in contrast to the readily exhausted ‘passive’ matrix buffering) also stabilize the pH gradient. In the cytosol, H+ scavenging is mainly associated with malate decarboxylation catalyzed by malic enzyme, and via the GABA shunt of the tricarboxylic acid (TCA) cycle involving glutamate decarboxylation. In the apoplast, formation of bicarbonate from CO2, the end‐product of respiration, generates H+ at pH ≥ 6. Membrane potential is stabilized by K+ release and/or by anion uptake via ion channels. Finally, thermodynamic aspects of active buffering are discussed.

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The pH of the Apoplast: Dynamic Factor with Functional Impact Under Stress

Cited by 162 publications

References 158 publications

Pathogen‐inducedpHchanges regulate the growth‐defense balance in plants

Pathogen‐inducedpHchanges regulate the growth‐defense balance in plants

I see the light! Fluorescent proteins suitable for cell wall/apoplast targeting in Nicotiana benthamiana leaves

Biochemical pH clamp: the forgotten resource in membrane bioenergetics

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