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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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.
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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