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Auxin- and pH-induced guttation in Phycomyces sporangiophores: relation between guttation and diminished elongation growth

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Abstract

Guttation, the formation of exudation water, is widespread among plants and fungi, yet the underlying mechanisms remain largely unknown. We describe the conditions for inducing guttation in sporangiophores of the mucoracean fungus, Phycomyces blakesleeanus. Cultivation on peptone-enriched potato dextrose agar elicits vigorous guttation mainly below the apical growing zone, while sporangiophores raised on a glucose-mineral medium manifest only moderate guttation. Mycelia do not guttate irrespective of the employed media. The topology of guttation droplets allows identifying the non-growing part of the sporangiophore as a guttation zone, which responds to humidity and medium composition in ways that become relevant for turgor homeostasis and thus the sensor physiology of the growing zone. Apparently, the entire sporangiophore, rather than exclusively the growing zone, participates in signal reception and integration to generate a common growth output. Exogenous auxin applied to the growing zones elicits two correlated responses: (i) formation of guttation droplets in the growing and transition zones below the sporangium and (ii) a diminution of the growth rate. In sporangiophore populations, guttation-induction by exogenous control buffer occurs at low frequencies; the bias for guttation increases with increasing auxin concentration. Synthetic auxins and the transport inhibitor NPA suppress guttation completely, but leave growth rates largely unaffected. Mutants C2 carA and C148 carA madC display higher sensitivities for auxin-induced guttation compared to wild type. A working model for guttation includes aquaporins and mechanosensitive ion channels that we identified in Phycomyces by sequence domain searches.

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All data were derived from experimental work and analyzed in this study. Data files can be provided on demand.

Abbreviations

ABCB:

Plant ATP-binding cassette transporter B

APW:

Artificial pond water

AQP:

Aquaporin

BA:

Benzoic acid

2,4-D:

2,4-Dichlorophenoxyacetic acid

DMSO:

Dimethyl sulfoxide

GR:

Growth rate

GUZ:

Guttation zone

GZ:

Growing zone of the sporangiophore

IAA:

Indole-3-acetic acid

MES:

2-(N-Morpholino)ethanesulfonic acid

MIP:

MAJOR INTRINSIC PROTEIN (aquaporin)

MP:

Membrane potential

MSC:

Mechanosensitive ion channel

MSL:

MECHANOSENSITIVE CHANNEL OF SMALL CONDUCTANCE-LIKE

MYC:

Malt agar enriched with yeast extract and casamino acids

1-NAA:

1-Naphthaleneacetic acid

2-NAA:

2-Naphthaleneacetic acid

NIP:

Nodulin 26-like intrinsic protein, plant aquaporin

NPA:

N-1-Naphthylphtalamic acid

PDA:

Potato dextrose agar

PDAPE:

Potato dextrose agar enriched with peptone

PIEZO:

Mechanosensitive ion channel

PIN:

PIN-FORMED, auxin efflux transporter

PIP:

Plasma membrane intrinsic protein, plant aquaporin

RAS-GAP:

Rat sarcoma GTPase-activating protein

RH:

Relative humidity

SIV:

Mineral-glucose solid medium

TIP:

Tonoplast intrinsic protein, aquaporin

TZ:

Transition zone of the sporangiophore

Tris:

Tris(hydroxymethyl)aminomethane

VP:

Variation potential

WAT1:

WALLS ARE THIN1, EamA-like transporter

XIP:

X-intrinsic protein, family of plant aquaporin

ZIP:

Plant aquaporin

References

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Acknowledgements

The authors are grateful to Prof. Rainer Hertel for encouragement and helpful discussions, and Nevena Živković for assistance in image processing.

Funding

This work was supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Contract No. 451–03-68/2022–14/200053); the initial phase of the project was funded by the Deutsche Forschungsgemeinschaft (GA 173/13–1).

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Authors and Affiliations

  1. Institute for Multidisciplinary Research, University of Belgrade, Kneza Višeslava 1, 11030, Belgrade, Serbia

    Branka D. Živanović & Sladjana Z. Spasić

  2. Max Planck Institute for Evolutionary Biology, Department of Evolutionary Biology, August Thienemann Str. 2, 24306, Plön, Germany

    Kristian Ullrich

  3. Singidunum University, Danijelova 32, 11010, Belgrade, Serbia

    Sladjana Z. Spasić

  4. Faculty of Biology, Philipps-University Marburg, Karl-Von-Frisch Str. 8, 35032, Marburg, Germany

    Paul Galland

Authors
  1. Branka D. Živanović
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  2. Kristian Ullrich
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  3. Sladjana Z. Spasić
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  4. Paul Galland
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Contributions

BŽ and PG designed research, analyzed data, and wrote the manuscript. BŽ performed the experiments. SS created mathematical methods for calculations and statistical data analysis. KU did the sequence domain analyses. All authors read and approved the manuscript.

Corresponding author

Correspondence to Branka D. Živanović.

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The authors declare no competing interests.

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Handling Editor: Peter Nick

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Main conclusion

At high humidity and on peptone-enriched growth media, Phycomyces blakesleeanus generates guttation droplets on the entire sporangiophore surface, i.e., sporangium, growing- and transition zones, and most prominently, the basal parts; mycelia do not display guttation. Exogenous auxin applied to the growing zones elicits in 2 min guttation and a diminution of the growth rates.

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Živanović, B.D., Ullrich, K., Spasić, S.Z. et al. Auxin- and pH-induced guttation in Phycomyces sporangiophores: relation between guttation and diminished elongation growth. Protoplasma 260, 1109–1133 (2023). https://doi.org/10.1007/s00709-022-01833-3

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  • DOI: https://doi.org/10.1007/s00709-022-01833-3

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