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Plant Molecular Biology

, Volume 101, Issue 1–2, pp 21–40 | Cite as

Arabidopsis mlo3 mutant plants exhibit spontaneous callose deposition and signs of early leaf senescence

  • Stefan Kusch
  • Susanne Thiery
  • Anja Reinstädler
  • Katrin Gruner
  • Krzysztof Zienkiewicz
  • Ivo Feussner
  • Ralph PanstrugaEmail author
Article

Abstract

Key message

Arabidopsis thaliana mlo3 mutant plants are not affected in pathogen infection phenotypes but—reminiscent of mlo2 mutant plants—exhibit spontaneous callose deposition and signs of early leaf senescence.

Abstract

The family of Mildew resistance Locus O (MLO) proteins is best known for its profound effect on the outcome of powdery mildew infections: when the appropriate MLO protein is absent, the plant is fully resistant to otherwise virulent powdery mildew fungi. However, most members of the MLO protein family remain functionally unexplored. Here, we investigate Arabidopsis thaliana MLO3, the closest relative of AtMLO2, AtMLO6 and AtMLO12, which are the Arabidopsis MLO genes implicated in the powdery mildew interaction. The co-expression network of AtMLO3 suggests association of the gene with plant defense-related processes such as salicylic acid homeostasis. Our extensive analysis shows that mlo3 mutants are unaffected regarding their infection phenotype upon challenge with the powdery mildew fungi Golovinomyces orontii and Erysiphe pisi, the oomycete Hyaloperonospora arabidopsidis, and the bacterial pathogen Pseudomonas syringae (the latter both in terms of basal and systemic acquired resistance), indicating that the protein does not play a major role in the response to any of these pathogens. However, mlo3 genotypes display spontaneous callose deposition as well as signs of early senescence in 6- or 7-week-old rosette leaves in the absence of any pathogen challenge, a phenotype that is reminiscent of mlo2 mutant plants. We hypothesize that de-regulated callose deposition in mlo3 genotypes might be the result of a subtle transient aberration of salicylic acid-jasmonic acid homeostasis during development.

Keywords

MLO (Mildew resistance Locus O) Salicylic acid (SA) Callose Senescence Phytohormone Systemic acquired resistance (SAR) 

Abbreviations

bp

Base pair

CFU

Colony forming units

dpi

Days post inoculation

FW

Fresh weight

GO

Gene ontology

GUS

β-glucuronidase

Hpa

Hyaloperonospra arabidopsidis

hpi

Hours post inoculation

JA

Jasmonic acid

JA-Ile

Jasmonic acid isoleucine

MAMP

Microbe-associated molecular pattern

MS

Murashige and Skoog

Psm

Pseudomonas syringae pv. maculicola

Pst

Pseudomonas syringae pv. tomato

RH

Relative humidity

rpm

rounds per minute

RLU

Relative light units

RT-PCR

Reverse transcriptase polymerase chain reaction

SA

Salicylic acid

SAG

Salicylic acid glucoside

SAR

Systemic acquired resistance

T-DNA

Transfer-DNA

UPLC-nano ESI–MS/MS

Ultrahigh-pressure liquid chromatography-tandem mass spectrometry

YFP

Yellow fluorescent protein

Notes

Acknowledgements

This study was supported by the German Research Foundation (Deutsche Forschungsgemeinschaft; DFG) [Grant PA861/11-1 to R.P. and Grant INST 186/822-1 to I.F.]. H. arabidopsidis Noco2 was kindly provided by Jane Parker (Max Planck Institute for Plant Breeding Research, Cologne, Germany). The two P. syringae pv. maculicola strains were kindly provided by Jürgen Zeier (Heinrich Heine University, Düsseldorf, Germany). This work would not have been possible without coffee and chocolate.

Author contributions

S.K. and S.T. performed the pathogen assays, K.G. did the SAR experiments. S.K. and A.R. conducted callose, senescence, GUS and osmotic stress assays. Phytohormone measurements were performed by K.Z., and K.Z. and I.F. analyzed the data. S.K. did the expression analysis, statistical testing, and plotting of the data. R.P. and S.K. designed the project and wrote the manuscript. All authors have read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary material

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Supplementary material 1 (PDF 681 kb)
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Supplementary material 8 (PDF 251 kb)
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Supplementary material 9 (DOCX 29 kb)
11103_2019_877_MOESM10_ESM.xlsx (202 kb)
Supplementary material 10—Co-expressed genes of AtMLO1, AtMLO2, and AtMLO3 after ATTED-II release v2017.12.14 (XLSX 202 kb)
11103_2019_877_MOESM11_ESM.txt (66 kb)
Supplementary material 11—GO terms of the 79 genes from the common co-expression network of AtMLO2 and AtMLO3 (TXT 66 kb)
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Supplementary material 12—Cis-regulatory elements of the 79 genes from the common co-expression network of AtMLO2 and AtMLO3 predicted by AthaMap (XLSX 240 kb)
11103_2019_877_MOESM13_ESM.xlsx (41 kb)
Supplementary material 13—Cis-regulatory elements of the 79 genes from the common co-expression network of AtMLO2 and AtMLO3 predicted by MEME v5.0.4 (XLSX 41 kb)

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© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Unit of Plant Molecular Cell Biology, Institute for Biology IRWTH Aachen UniversityAachenGermany
  2. 2.Department of Plant Biochemistry, Göttingen Center for Molecular Biosciences (GZMB), Albrecht-von-Haller-Institute for Plant SciencesUniversity of GöttingenGöttingenGermany
  3. 3.Service Unit for Metabolomics and Lipidomics, Göttingen Center for Molecular Biosciences (GZMB)University of GöttingenGöttingenGermany

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