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SQUAMOSA promoter-binding protein-like 7 mediates copper deficiency response in the presence of high nitrogen in Arabidopsis thaliana

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Abstract

Key message

SQUAMOSA promoter-binding protein-like 7 mediates copper deficiency response in the presence of high nitrogen even with the sufficient level of copper in Arabidopsis thaliana.

Abstract

Under copper (Cu) deficiency, accumulation of mRNA encoding two Cu/Zn superoxide dismutases, CSD1 and CSD2, is downregulated to save Cu for plastocyanin. This downregulation depends on miR398 and is under the control of SQUAMOSA promoter-binding protein-like7 (SPL7). Arabidopsis seedlings are routinely cultured on Murashige and Skoog medium. However, the high nitrogen (N) content of the medium (60 mM) has been shown to induce a similar response to Cu deficiency. The mRNA and protein levels of CSD1 and CSD2 are reduced under high N conditions, even if the Cu concentration in the medium is sufficient (0.1–0.5 µM). In this study, we show that this symptom, similar to the Cu deficiency, occurred in the presence of high N largely depending on SPL7, suggesting that plants actually sensed Cu deficiency. However, a change in N concentration in the medium did not influence the total Cu concentration in shoots or roots. High N did not increase the protein content in leaves but facilitated rapid seedling growth. We speculate that this rapid growth causes a continuous Cu deficiency mainly because of high Cu uptake by mesophyll cells in the leaves. This idea was supported by the observation that plastocyanin did not overaccumulate at the range of 0.1–0.5 µM Cu with 30 mM N. In contrast, in the presence of 5 µM Cu with 30 mM N, plants accumulate more Cu in plastocyanin in the thylakoid lumen, resulting in a slight Cu deficiency in the chloroplast stroma. This process is independent of SPL7.

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Abbreviations

CRR1:

Copper response regulator 1

Cyt:

Cytochrome

MS:

Murashige and Skoog

PC:

Plastocyanin

qRT-PCR:

Quantitative reverse transcription-polymerase chain reaction

RT:

Room temperature

SBP:

SQUAMOSA promoter-binding protein

SD:

Standard deviation

SOD:

Superoxide dismutase

SPL7:

SQUAMOSA promoter-binding protein-like 7

WT:

Wild-type

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Acknowledgements

The authors thank Dr. Amane Makino for the antibody. We also thank Dr. Naoyuki Sotta for his advice on the statistical analysis.

Funding

This work was supported by the NC-CARP/GRENE project; the Japan Science and Technology Agency [CREST program to TS]; and the Japanese Society for the Promotion of Science [16H06555 to TS].

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Authors and Affiliations

  1. Graduate School of Science, Kyoto University, Kyoto, 606-8502, Japan

    Mélanie Mermod, Mari Takusagawa & Toshiharu Shikanai

  2. Graduate School of Agriculture, Kyushu University, Fukuoka, 812-8581, Japan

    Teruyuki Kurata

  3. Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657, Japan

    Takehiro Kamiya & Toru Fujiwara

Authors
  1. Mélanie Mermod
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  2. Mari Takusagawa
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  3. Teruyuki Kurata
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  4. Takehiro Kamiya
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  5. Toru Fujiwara
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  6. Toshiharu Shikanai
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Contributions

MM, MT and TS conceived and designed research. MM, MT and TK conducted experiments. TK and TF contributed to the metal analysis. MM and TS wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Toshiharu Shikanai.

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Communicated by Manju Gupta.

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Fig. S1

Increasing N mimics a Cu deficiency response in RNA accumulation. Relative transcript levels of FSD1 (a), CSD1 (b), and CSD2 (c) were determined by qRT-PCR analysis in 3-week old WT shoots cultured on the MS medium without sucrose. Shoots from 5-6 seedlings per condition were pooled for RNA isolation. Three independent biological replicates were analyzed. Transcript levels were normalized to EF1a as a constitutively expressed control gene. Means ± SD, Tukey HSD (p < 0.05). Different alphabets mean statistically significant differences

Table S1

Primers used in this study

Table S2

Summary of regression analysis

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Mermod, M., Takusagawa, M., Kurata, T. et al. SQUAMOSA promoter-binding protein-like 7 mediates copper deficiency response in the presence of high nitrogen in Arabidopsis thaliana. Plant Cell Rep 38, 835–846 (2019). https://doi.org/10.1007/s00299-019-02422-0

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  • DOI: https://doi.org/10.1007/s00299-019-02422-0

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