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Akiko Maruyama-Nakashita Last modified date:2019.06.15

Associate Professor / Bioscience & Biotechnology, Graduate School of Bioresource and Bioenvironmental Sciences
Department of Bioscience and Biotechnology
Faculty of Agriculture


Graduate School


E-Mail
Phone
092-802-4712
Fax
092-802-4712
Academic Degree
Ph.D
Country of degree conferring institution (Overseas)
No
Field of Specialization
Plant Science, Plant Nutrition
Total Priod of education and research career in the foreign country
00years00months
Outline Activities
I conduct education of plant nutrition and the related subject to graduate and undergraduate students. I conduct the research about the molecular machinery of sulfate uptake, sulfur assimilation and sulfur metabolism in plants. Social activities through research and education are conducted.
Research
Research Interests
  • Effects of sulfur deficiency on the uptake and transport of other nutrients in plants
    keyword : sulfate, phosphate, nitrate, transport, vascular tissues
    2011.04~2020.03.
  • Regulatory mechanism of glucosinolates catabolism in plants
    keyword : glucosinolates、synthesis、signal transduction
    2016.04~2020.03.
  • Role of sulfur metabolism in plant response and adaptation to environmental stress
    keyword : sulfur metabolism, environmental stress
    2010.05~2027.05.
  • Essentiality of selenium for plants and plant tolerance to selenate
    keyword : selenium, selenate, essentiality, tolerance
    2007.05~2027.05.
  • Effects of heavy metal treatment on sulfur assimilation and metabolism, and the physiological meaning of the effects.
    keyword : Cadmium, Sulfur, Transport, Sulfate
    2010.05~2027.05.
  • Regulatory mechanism of sulfur assimilation and metabolism in plants
    keyword : Sulfur, Sulfate transporter, Sulfur containing compounds, Transcriptional regulation, Signal transduction
    2010.07~2023.07.
  • Identification and characterization of the sulfur response mutants to identify novel regulatory proteins of sulfur assimilation and metabolism
    keyword : sulfur response mutants, regulatory proteins of sulfur assimilation and metabolism
    2001.05~2014.05.
  • Transcriptional regulation of sulfate transporters in response to sulfur nutritional status
    keyword : Sulfate transporter, Transcriptional control, Transcription factor, cis-acting element
    2001.05~2027.05.
  • Molecular mechanism of sulfate uptake and translocation in plants
    keyword : Sulfate, uptake, translocation
    2001.04~2014.05.
  • Functional identification of the proteins which transcript accumulation are regulated by sulfur level
    keyword : Functional identification、sulfur responsive genes
    2001.05~2014.05.
  • Regulatory mechanism of glucosinolates synthesis in plants
    keyword : glucosinolates、synthesis、signal transduction
    2001.04~2014.05.
Academic Activities
Books
1. Akiko Maruyama-Nakashita, Naoko Ohkama-Ohtsu, Glutathione in plant growth, development and stress tolerance (Eds, MA Hossain, MG Mostofa, PD Vivancos, DJ Burritt, M. Fujita, LS Phan Tran), Springer, 2017.05, Sulfur Assimilation and Glutathione Metabolism in Plants.
Reports
1. A. Maruyama-Nakashita, Metabolic changes sustain the plant life in low-sulfur environments, Current Opinion in Plant Biology, http://dx.doi.org/10.1016/j.pbi.2017.06.015, 2017.11, Plants assimilate inorganic sulfate into various organic sulfur (S) compounds, which contributes to the global sulfur cycle in the environment as well as the nutritional supply of this essential element to animals. Plants, to sustain their lives, adapt the flow of their S metabolism to respond to external S status by activating S assimilation and catabolism of stored S compounds, and by repressing the synthesis of secondary S metabolites like glucosinolates. The molecular mechanism of this response has been gradually revealed, including the discovery of several regulatory proteins and enzymes involved in S deficiency responses. Recent progress in this research area and the remaining issues are reviewed here..
Papers
1. Akiko Maruyama-Nakashita, Metabolic changes sustain the plant life in low-sulfur environments, Current Opinion in Plant Biology, http://dx.doi.org/10.1016/j.pbi.2017.06.015, 93, 144-151, 2017.11, Plants assimilate inorganic sulfate into various organic sulfur (S)
compounds, which contributes to the global sulfur cycle in the
environment as well as the nutritional supply of this essential
element to animals. Plants, to sustain their lives, adapt the flow
of their S metabolism to respond to external S status by
activating S assimilation and catabolism of stored S
compounds, and by repressing the synthesis of secondary S
metabolites like glucosinolates. The molecular mechanism of
this response has been gradually revealed, including the
discovery of several regulatory proteins and enzymes involved
in S deficiency responses. Recent progress in this research
area and the remaining issues are reviewed here..
2. Chisato Yamaguchi, Naoko Ohkama-Ohtsu, Takuro Shinano, Akiko Maruyama-Nakashita, Plants prioritize phytochelatin synthesis during cadmium exposure even under reduced sulfate uptake caused by the disruption of SULTR1;2., Plant Signaling & Behavior, http://dx.doi.org/10.1080/15592324.2017.1325053, 2017.05.
3. Akiko Maruyama-Nakashita, Akiko Suyama, Hideki Takahashi, 5′-non-transcribed flanking region and 5′-untranslated region play distinctive roles in sulfur deficiency induced expression of SULFATE TRANSPORTER 1;2 in Arabidopsis roots, Plant Biotechnology, DOI: 10.5511/plantbiotechnology.16.1226a, 34, 51-55, 2017.03.
4. Chisato Yamaguchi, Yuki Takimoto, Naoko Ohkama-Ohtsu, Akiko Hokura, Takuro Shinano, Toshiki Nakamura, Akiko Suyama, Akiko Maruyama-Nakashita, Effects of Cadmium Treatment on the Uptake and Translocation of Sulfate in Arabidopsis thaliana., Plant and Cell Physiology, 57, 2353-2366, 2016.11, Cadmium (Cd) is a highly toxic and non-essential element
for plants, whereas phytochelatins and glutathione are lowmolecular-
weight sulfur compounds that function as chelators
and play important roles in detoxification. Cadmium
exposure is known to induce the expression of sulfurassimilating
enzymes and sulfate uptake by roots.
However, the molecular mechanism underlying Cd-induced
changes remains largely unknown. Accordingly, we analyzed
the effects of Cd treatment on the uptake and translocation
of sulfate and accumulation of thiols in Arabidopsis thaliana.
Both wild type (WT) and null mutant (sel1-10 and sel1-18)
plants of the sulfate transporter SULTR1;2 exhibited growth
inhibition when treated with CdCl2. However, the mutant
plants exhibited a lower growth rate and lower Cd accumulation.
Cadmium treatment also upregulated the transcription
of SULTR1;2 and sulfate uptake activity in WT plants,
but not in mutant plants. In addition, the sulfate, phytochelatin
and total sulfur contents were preferentially accumulated
in the shoots of both WT and mutant plants treated
with CdCl2, and sulfur K-edge XANES spectra suggested that
sulfate was the main compound responsible for the
increased sulfur content in the shoots of CdCl2-treated
plants. Our results demonstrate that Cd-induced sulfate
uptake depends on SULTR1;2 activity, and that CdCl2 treatment
greatly shifts the distribution of sulfate to shoots, increases
the sulfate concentration of xylem sap and
upregulates the expression of SULTRs involved in root-toshoot
sulfate transport. Therefore, we conclude that root-toshoot
sulfate transport is stimulated by Cd and suggest that
the uptake and translocation of sulfate in CdCl2-treated
plants are enhanced by demand-driven regulatory networks..
5. Fayezeh Aarabi, Miyuki Kusajima, Takayuki Tohge, Tomokazu Konishi, Tamara Gigolashvili, Makiko Takamune, Yoko Sasazaki, Mutsumi Watanabe, Hideo Nakashita, Alisdair R. Fernie, Kazuki Saito, Hideki Takahashi, Hans-Michael Hubberten, Rainer Hoefgen, Akiko Maruyama-Nakashita, Sulfur deficiency–induced repressor proteins optimize glucosinolate biosynthesis in plants, Science Advances, 2, e1601087, 2016.10, Glucosinolates (GSLs) in the plant order of the Brassicales are sulfur-rich secondary metabolites that harbor antipathogenic and antiherbivory plant-protective functions and have medicinal properties, such as carcinopreventive and antibiotic activities. Plants repress GSL biosynthesis upon sulfur deficiency (−S); hence, field performance and medicinal quality are impaired by inadequate sulfate supply. The molecular mechanism that links –S to GSL biosynthesis has remained understudied. We report here the identification of the –S marker genes sulfur deficiency induced 1 (SDI1) and SDI2 acting as major repressors controlling GSL biosynthesis in Arabidopsis under –S condition.
SDI1 and SDI2 expression negatively correlated with GSL biosynthesis in both transcript and metabolite
levels. Principal components analysis of transcriptome data indicated that SDI1 regulates aliphatic GSL biosynthesis as part of –S response. SDI1 was localized to the nucleus and interacted with MYB28, a major transcription factor that promotes aliphatic GSL biosynthesis, in both yeast and plant cells. SDI1 inhibited the transcription of aliphatic GSL biosynthetic genes by maintaining the DNA binding composition in the form of an SDI1-MYB28 complex, leading to down-regulation of GSL biosynthesis and prioritization of sulfate usage for primary metabolites under sulfur-deprived conditions..
6. Akiko Maruyama-Nakashita, Combinatorial use of sulfur-responsive regions of sulfate transporters provides a highly sensitive plant-based system for detecting selenate and chromate in the environment, Soil Science and Plant Nutrition, 62, 2016.03.
7. Akiko Maruyama-Nakashita, Akiko Watanabe-Takahashi, Eri Inoue, Tomoyuki Yamaya, Kazuki Saito, Hideki Takahashi, Sulfur-responsive elements in the 3’-non-transcribed intergenic region are essential for the induction of Sulfate Transporter 2;1 gene expression in Arabidopsis roots under sulfur deficiency., The Plant Cell, 27, 1279-1296, 2015.04, Under sulfur deficiency (–S), plants induce expression of the sulfate transport systems in roots to increase uptake and root-to-shoot transport of sulfate. The low-affinity sulfate transporter SULTR2;1 is predominantly expressed in xylem parenchymaand pericycle cells in Arabidopsis thaliana roots under –S. The mechanisms underlying –S-inducible expression of SULTR2;1
in roots have remained unclear, despite the possible significance of SULTR2;1 for acclimation to low-sulfur conditions. In this investigation, examination of deletions and base substitutions in the 3'-intergenic region of SULTR2;1 revealed novel sulfur-responsive elements, SURE21A (5'-CAATGTATC-3') and SURE21B (5'-CTAGTAC-3'), located downstream of the SULTR2;1
3'-untranslated region. SURE21A and SURE21B effectively induced reporter gene expression from fusion constructs under –S in combination with minimal promoters or promoters not inducible by –S, suggesting their versatility in controlling transcription. T-DNA insertions near SURE21A and SURE21B abolished –S-inducible expression of SULTR2;1 in roots and reduced the uptake and root-to-shoot transport of sulfate. In addition, these mutations partially suppressed SULTR2;1 expression in shoots, without changing its –S-responsive expression. These findings indicate that SULTR2;1 contributes to the increase in uptake and internal translocation of sulfate driven by gene expression induced under the control of sulfur-responsive elements in the 3'-nontranscribed intergenic region of SULTR2;1..
8. C. Kawashima, N. Yoshimoto, A. Maruyama-Nakashita, Y. Tsuchiya, K. Saito, H. Takahashi, T. Dalamy , Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. , The Plant J. , 57, 313 – 321, 2009.05.
9. M. Yasuda, A. Ishikawa, Y. Jikumaru, M. Seki, T. Umezawa, T. Asami, A. Maruyama-Nakashita, T. Kudo, K. Shinozaki, S. Yoshida, H. Nakashita , Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. , The Plant Cell. , 2008.06.
10. A. Maruyama-Nakashita, Y. Nakamura, T. Tohge, K. Saito, H. Takahashi , Central transcriptional regulator of plant sulfur response and metabolism. , The Plant Cell , 18: 3235-3251., 2006.11.
11. A. Maruyama-Nakashita, Y. Nakamura, A. Watanabe-Takahashi, E. Inoue, T. Yamaya, H. Takahashi, Identification of a novel cis-acting element conferring sulfur deficiency response in Arabidopsis roots. , The Plant J. , 42: 305-314., 2005.05.
12. A. Maruyama-Nakashita, Y. Nakamura, T. Yamaya, H. Takahashi , A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. , The Plant J. , 38: 779-789., 2004.05.
13. A. Maruyama-Nakashita, E. Inoue, A. Watanabe-Takahashi, T. Yamaya, H. Takahashi , Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways., Plant Physiol. , 132: 597-605., 2003.05.
14. A. Maruyama, K. Ishizawa and K. Saito , ß-Cyanoalanine synthase and cysteine synthase from potato: molecular cloning, biochemical characterization, and spatial and hormonal regulation. , Plant Mol. Biol. , 46: 749-760., 2001.05.
15. A. Maruyama, K. Ishizawa and T. Takagi , Purification and characterization of ß-cyanoalanine synthase and cysteine synthases from potato tubers. ß-Cyanoalanine synthase and mitochondrial cysteine synthase are the same enzyme? , Plant Cell Physiol. , 41: 200-208., 2000.05.
Presentations
1. 丸山明子, 草島美幸, 高宗万希子, 光田展隆, 木村侑希, 仲下英雄, 髙橋秀樹, 硫黄欠乏下での硫酸イオン吸収の増加に寄与するWRKY転写因子, 第59回日本植物生理学会, 2018.03.
2. Akiko Maruyama-Nakashita, Sulfur deficiency responses in plants: Regulation of sulfate transport and Trade-off of the primary and secondary sulfur metabolism in Arabidopsis
, 2016.09.
3. 丸山 明子, 草島 美幸, Tamara Gigolashvili, 小西 智一, 仲下 英雄, SDI1 inhibits aliphatic GSL biosynthesis through the interaction with MYB28, 第58回日本植物生理学会, 2017.03.
4. Akiko Maruyama-Nakashita, Detection and Quantification of Selenate and Chromate Using Sulfur-Responsive Regions of Sulfate Transporters
, The 5th SULPHYTON WORKSHOP, 2016.09.
5. Akiko Maruyama-Nakashita, Sulfur deficiency response in plants: Trade-off of the primary and secondary sulfur metabolism , The 5th SULPHYTON WORKSHOP, 2016.09.
6. Chisato Yamaguchi, Yuki Takimoto, Naoko Ohkama-Ohtsu, Akiko Hokura, Takuro Shinano, Toshiki Nakamura, Akiko Suyama, Akiko Maruyama-Nakashita, Effects of Cadmium Treatment on the Uptake and Translocation of Sulfate in Arabidopsis thaliana, The 5th SULPHYTON WORKSHOP, 2016.09.
7. Akiko Maruyama-Nakashita, Akiko Watanabe-Takahashi, Eri Inoue, Tomoyuki Yamaya, Kazuki Saito, Hideki Takahashi, Sulfur-Responsive Elements in 3’-Non-Transcribed Region of SULFATE TRANSPORTER 2;1 : Essential Role in Transcriptional Regulation, Sulfate Uptake and Translocation in Arabidopsis Roots under Sulfur-Deficient Conditions., The 27th International Conference on Arabidopsis Research, 2016.07.
8. Chisato Yamaguchi, Yuki Takimoto, Akiko Hokura, Naoko Ohkama-Ohtsu, Takuro Shinano, Akiko Suyama, Akiko Maruyama-Nakashita, Effects of Cadmium Treatment on Uptake and Translocation of Sulfate in Arabidopsis thaliana
, The 27th International Conference on Arabidopsis Research, 2016.07.
9. Akiko Maruyama-Nakashita, Yuki Takimoto, Eri Inoue, Kazuki Saito, Hideki Takahashi, Detection and Quantification of Selenate and Chromate Using Sulfur-Responsive Regions of Sulfate Transporters, 13th International Conference on the Biogeochemistry of Trace Elements, ICOBTE 2015 FUKUOKA, 2015.07.
10. Chisato Yamaguchi, Yuki Takimoto, Takuro Shinano, Akiko Hokura, Akiko Maruyama-Nakashita, Effects of Cadmium Treatment on Uptake and Translocation of Sulfate in Arabidopsis thaliana, 13th International Conference on the Biogeochemistry of Trace Elements, ICOBTE 2015 FUKUOKA, 2015.07.
11. Akiko Maruyama-Nakashita, Hiromi Makino, Akiko Suyama, Ryuichi Nishihama, Kimitsune Ishizaki, Takayuki Kohchi, Sulfate transporters in Marchantia polymorpha: Molecular species and the responses to sulfur nutrition, Marchantia Workshop 2014, 2014.12.
12. Hiromi Makino, Yuka Maeda, Yuuki Jodoi, Akiko Suyama, Sakiko Ishida, Akiko Maruyama-Nakashita, Kimitsune Ishizaki, Ryuichi Nishihama, Takayuki Kohchi, Functional analysis of MpEIL in relation to ethylene and sulfur nutrition response, Marchantia Workshop 2014, 2014.12.
13. 丸山 明子, Makiko Takamune, Yuki Kimura, Yumiko Nakamura, Kazuki Saito, Hideki Takahashi, A novel cis-acting element and transcription factor involved in the induction of SULTR1;2 expression and sulfate uptake activity under sulfur limitation in Arabidopsis roots, 9th International Workshop SULFUR METABOLISM IN PLANTS, 2014.04, Background:
When plants become sulfur deficient (-S), they increase sulfate uptake capacity as one of the acclimation processes. In Arabidopsis, the transcript level of SULTR1;2, a high-affinity sulfate transporter facilitates sulfate uptake from the environment, is highly induced under –S condition (1, 2). The –S response of SULTR1;2 is controlled by SLIM1 transcription factor (3). To determine the how sulfate uptake activity is induced by -S, we tried to identify the cis-acting element and transcription factors involved in the –S-response of SULTR1;2.

Methods:
SULTR1;2 promoter region was dissected by deletion and base substitution analysis in transgenic Arabidopsis using luciferase as a reporter. Luciferase activities in the roots of transgenic plants grown under sulfur sufficient (+S) and –S conditions were analyzed and the regions indispensable for the –S response were determined.
WRKY transcription factors which transcript levels were induced by –S in SLIM1-dependent manner were collected using microarray data (3). Transcript levels of SULTR1;2 and sulfate uptake activity were analyzed as described in 3.

Results:
The results of deletion analysis indicated that –S-responsive expression of SULTR1;2 requires the regions from –371 to –360 and –328 to –323. The –371/–360 region contained a WRKY binding sequence (TGAC), and the -328/-323 region contained a SEF4 motif (AAAAAT), respectively.
There were 3 WRKY transcription factors which transcript levels were induced by –S in wild-type plants but not in slim1 mutants. Then we isolated T-DNA insertion mutants of the 3 WRKYs, and analyzed SULTR1;2 expression and sulfate uptake activity under +S and –S conditions. Significant down-regulation was observed in a mutant under –S condition, suggesting the involvement of the WRKY transcription factor in –S-inducible expression of SULTR1;2 and sulfate uptake.

Conclusion
A novel cis-acting element and a WRKY transcription factor involved in –S response of SULTR1;2 was determined.

References
1) Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP. Plant J. 29, 475-486.
2) Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K. Plant J. 29, 465-473.
3) Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H Plant Cell, 18, 3235-3251.
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Membership in Academic Society
  • Japan Society for Bioscience, Biotechnology and Agrochemistry
  • Japan Transporter Research Association: JTRA
  • Japanese Society for Plant Cell and Molecular Biology
  • Japanese Society of Soil Science and Plant Nutrition
  • The Japanese Society of Plant Physiologists
Educational
Educational Activities
For education I'm conducting the education related to Plant Nutrition and the related subject to graduate and undergraduate students.
Class for under graduate: Experimental course, Plant Physiology and Biochemistry, Scientific English, Molecular Biology, Challenges in agricultural science and technology of plants
Class for under graduate: Advanced Course of Molecular Biosciences, Advanced Course of Plant Physiology and Biochemistry
Other Educational Activities
  • 2012.04.
  • 2009.04.