Kyushu University Academic Staff Educational and Research Activities Database
List of Papers
Akiko Maruyama-Nakashita Last modified date:2021.06.16

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

1. Y. Nakai, A. Maruyama-Nakashita, Biosynthesis of Sulfur-Containing Small Biomolecules in Plants., Int. J. Mol. Sci., 10.3390/ijms21103470, 21, 3470, 2019.05.
2. A. Allahham, S. Kanno, L. Zhang, A. Maruyama-Nakashita, Sulfur deficiency increases phosphate accumulation, uptake, and transport in Arabidopsis thaliana., Int. J. Mol. Sci., 10.3390/ijms21082971, 21, 2971, 2019.04.
3. T. Morikawa-Ichinose, D. Miura, L. Zhang, S.-J. Kim, A. Maruyama-Nakashita, Involvement of BGLU30 in glucosinolate catabolism in the Arabidopsis leaf under dark conditions., Plant and Cell Physiology,, 61, 1095-1106, 2019.06.
4. Miyuki Kusajima, Moeka Fujita, Hiromoto Yamakawa, Tsukasa Ushiwatari, Takamasa Mori, Kazuki Tsukamoto, Hiroshi Hayashi, Akiko Maruyama-Nakashita, Fang Sik Che, Hideo Nakashita, Characterization of plant immunity-activating mechanism by a pyrazole derivative, Bioscience, Biotechnology and Biochemistry, 10.1080/09168451.2020.1750341, 2020.01, A newly identified chemical, 4-{3-[(3,5-dichloro-2-hydroxybenzylidene)amino]propyl}-4,5-dihydro-1H-pyrazol-5-one (BAPP) was characterized as a plant immunity activator. BAPP enhanced disease resistance in rice against rice blast disease and expression of a defense-related gene without growth inhibition. Moreover, BAPP was able to enhance disease resistance in dicotyledonous tomato and Arabidopsis plants against bacterial pathogen without growth inhibition, suggesting that BAPP could be a candidate as an effective plant activator. Analysis using Arabidopsis sid2-1 and npr1-2 mutants suggested that BAPP induced systemic acquired resistance (SAR) by stimulating between salicylic acid biosynthesis and NPR1, the SA receptor protein, in the SAR signaling pathway..
5. Liu Zhang, Ryota Kawaguchi, Tomomi Morikawa-Ichinose, Alaa Allahham, Sun Ju Kim, Akiko Maruyama-Nakashita, Sulfur deficiency-induced glucosinolate catabolism attributed to two β-glucosidases, bglu28 and bglu30, is required for plant growth maintenance under sulfur deficiency, Plant and Cell Physiology, 10.1093/pcp/pcaa006, 61, 4, 803-813, 2020.04, Sulfur (S) is an essential element for plants, and S deficiency causes severe growth retardation. Although the catabolic process of glucosinolates (GSLs), the major S-containing metabolites specific to Brassicales including Arabidopsis, has been recognized as one of the S deficiency (S) responses in plants, the physiological function of this metabolic process is not clear. Two β-glucosidases (BGLUs), BGLU28 and BGLU30, are assumed to be responsible for this catabolic process as their transcript levels were highly upregulated byS. To clarify the physiological function of BGLU28 and BGLU30 and their roles in GSL catabolism, we analyzed the accumulation of GSLs and other S-containing compounds in the single and double mutant lines of BGLU28 and BGLU30 and in wild-type plants under different S conditions. GSL levels were highly increased, while the levels of sulfate, cysteine, glutathione and protein were decreased in the double mutant line of BGLU28 and BGLU30 (bglu28/30) underfiS. Furthermore, transcript level of Sulfate Transporter1;2, the main contributor of sulfate uptake from the environment, was increased in bglu28/30 mutants underfiS. With these metabolic and transcriptional changes, bglu28/30 mutants displayed obvious growth retardation underfiS. Overall, our results indicate that BGLU28 and BGLU30 are required for-S-induced GSL catabolism and contribute to sustained plant growth underfiS by recycling sulfate to primary S metabolism..
6. Chisato Yamaguchi, Soudthedlath Khamsalath, Yuki Takimoto, Akiko Suyama, Yuki Mori, Naoko Ohkama-Ohtsu and Akiko Maruyama‐Nakashita, SLIM1 Transcription Factor Promotes Sulfate Uptake and Distribution to Shoot,Along with Phytochelatin Accumulation, Under Cadmium Stress in Arabidopsis thaliana, Plants, doi:10.3390/plants9020163, 9, 163, 2020.01.
7. Takatsugu Nakajima, Yusuke Kawano, Iwao Ohtsu, Akiko Maruyuama-Nakashita, Alaa Allahham, Muneo Sato, Yuji Sawada, Masami Yokota Hirai, Tadashi Yokoyama and Naoko Ohkama-Ohtsu, Effects of Thiosulfate as a Sulfur Source on Plant Growth, Metabolites Accumulation and Gene Expression in Arabidopsis and Rice, Plant and Cell Physiology, doi:10.1093/pcp/pcz082, 2019.04.
8. Yuki Kimura, Tsukasa Ushiwatari, Akiko Suyama, Rumi Tominaga‐Wada, Takuji Wada and Akiko Maruyama‐Nakashita, Contribution of Root Hair Development to Sulfate Uptake in Arabidopsis, Plants, doi:10.3390/plants8040106, 8, 106, 2019.04.
9. Tomomi Morikawa-Ichinose, Sun-Ju Kim, Alaa Allahham, Ryota Kawaguchi and Akiko Maruyama-Nakashita, Glucosinolate Distribution in the Aerial Parts of sel1-10, a Disruption Mutant of the Sulfate Transporter SULTR1;2, in Mature Arabidopsis thaliana Plants, Plants, doi:10.3390/plants8040095, 8, 2019.04.
10. Ye-Jin Park, Jin-Hyuk Chun, Hyunnyung Woo, Akiko Maruyama-Nakashita, Sun-Ju Kim, Effects of different sulfur ion concentration in nutrient solution and light source on glucosinolate contents in
kale sprouts (Brassica oleracea var. acephala), Korean Journal of Agricultural Science,, 44, 261-271, 2017.06.
11. Akiko Maruyama-Nakashita, Metabolic changes sustain the plant life in low-sulfur environments, Current Opinion in Plant Biology,, 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..
12. 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,, 2017.05.
13. 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.
14. 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..
15. 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..
16. 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.
17. Naoko Yoshimoto, Tatsuhiko Kataoka, Akiko Maruyama-Nakashita, Hideki Takahashi, Measurement of Uptake and Root-to-Shoot Distribution of Sulfate in Arabidopsis Seedlings., Bio-protocol,, 6, e1700, 6: e1700, 2016.03.
18. Akiko Maruyama-Nakashita, Auxin Response Factors and Aux/IAA proteins potentially control –S responsive expression of SULTR1;1, Molecular Physiology and Ecophysiology of Sulfur. The Proceedings for 9th International Plant Sulfur Workshop, 2015.10.
19. 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..
20. Akiko Maruyama-Nakashita, Sulfate Uptake, Cysteine and GSH contents are increased by 5-aminolevulinic acid in Arabidopsis thaliana., Conference Proceedings of the 8th International Workshop on Plant Sulfur Metabolism, 2012.10.
21. A. Maruyama-Nakashita, MY. Hirai, S. Funada, S. Fueki , Exogenous application of 5-aminolevulinic acid increases transcript levels of sulfur transport and assimilatory genes, sulfate uptake, and cysteine and glutathione contents in Arabidopsis thaliana. , Soil Sci. Plant Nutr. , 56: 281-288., 2010.04.
22. 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.
23. Toru Fujiwara, Akiko Maruyama-Nakashita, Yoko Ide, Masami Yokota Hirai, Toward comprehensive understanding of regulatory network of sulfur metabolism.
, Conference Proceedings of the 7th International Workshop on Plant Sulfur Metabolism, 2009.10.
24. 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.
25. H. Goda, E. Sasaki, K. Akiyama, A. Maruyama-Nakashita, K. Nakabayashi, W. Li, M. Ogawa, Y. Yamauchi, J. Preston, K. Aoki, T. Kiba, S. Takatsuto, S. Fujioka, T. Asami, T. Nakano, H. Kato, T. Mizuno, H. Sakakibara, S. Yamaguchi, E. Nambara, Y. Kamiya, H. Takahashi, M. Yokota Hirai, T. Sakurai, K. Shinozaki, K. Saito, S. Yoshida, Y. Shimada , The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access., The Plant J. , 55, 526-542., 2008.04.
26. A. Maruyama-Nakashita, E. Inoue, K. Saito, H. Takahashi , Potential use of sulfur-responsive promoter of sulfate transporter gene for detection and quantification of selenate and chromate in the environment. , Plant Biotech. , 24: 261-263., 2007.05.
27. 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.
28. 丸山 明子, Transcriptional regulation of SULTR1;1 and SULTR1;2 in Arabidopsis root., Sulfur Transport and Assimilation in Plants in the Post Genomic Era (Conference Proceedings of the 6th International Workshop on Plant Sulfur Metabolism), 43-44, 2005.10.
29. 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.
30. A. Maruyama-Nakashita, Y. Nakamura, T. Yamaya, H. Takahashi , Regulation of high-affinity sulfate transporters in plants: towards systematic analysis of sulfur signaling and regulation. , J. Exp. Bot. , 55: 1843-1849., 2004.05.
31. 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.
32. A. Maruyama-Nakashita, Y. Nakamura, A. Watanabe-Takahashi, T. Yamaya, H. Takahashi , Induction of SULTR1;1 sulfate transporter in Arabidopsis roots involves protein phosphorylation/dephosphorylation circuit for transcriptional regulation. , Plant Cell Physiol. , 45: 340-345., 2004.03.
33. 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.
34. 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.
35. Y. Hatzfeld, A. Maruyama, A. Schmidt, M. Noji, K. Ishizawa and K. Saito , ß-Cyanoalanine synthase is a mitochondrial cysteine synthase-like protein in spinach and Arabidopsis thaliana. , Plant Physiol. , 123: 1163-1172., 2000.05.
36. 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.
37. A. Maruyama, R. Hasegawa, K. Ishizawa and Y. Esashi , Involvement of ß-cyanoalanine synthase in germination of cocklebur seeds. , Progress in Seed Research (Conference Proceedings of the 2nd ICSST) , 25-30., 1998.10.
38. A. Maruyama, K. Ishizawa, T. Takagi and Y. Esashi , Cytosolic ß-cyanoalanine synthase activity attributed to cysteine synthases in cocklebur seeds. Purification and characterization of cytosolic cysteine synthases. , Plant Cell Physiol. , 39: 671-680., 1998.05.
39. A. Maruyama, M. Yoshiyama, Y. Adachi, H. Nanba, R. Hasegawa and Y. Esashi , Possible participation of ß-cyanoalanine synthase in increasing the amino acid pool of cocklebur seeds in response to ethylene during the pre-germination period. , Aust. J. Plant. Physiol. , 24: 751-757., 1997.05.
40. R. Hasegawa, A. Maruyama, H. Sasaki, T. Tada and Y. Esashi, Possible involvement of ethylene-activated ß-cyanoalanine synthase in the regulation of cocklebur seed germination., J. Exp. Bot. , 46, 551-556., 1995.02.
41. R. Hasegawa, A. Maruyama, M. Nakaya, S. Tsuda and Y. Esashi, The presence of two types of ß-cyanoalanine synthase in germinating seeds and their responses to ethylene., Physiol. Plant., 93, 713-718, 1995.06.
42. M. Yoshiyama, A. Maruyama, T. Atsumi and Y. Esashi, Mechanism of action of C2H4 in promoting the germination of cocklebur seeds. 3. A further enhancement of priming effect with nitrogenous compounds and C2H4 responsiveness of seeds., Aust. J. Plant. Physiol. , 23, 519-525, 23: 519-525., 1996.05.
43. Y. Esashi, A. Maruyama, S. Sasaki, A. Tani and M. Yoshiyama, Involvement of cyanogens in the promotion of germination of cocklebur seeds in response to various nitrogenous compounds, inhibitors of respiratory and ethylene., Plant Cell Physiol. , 37: 545-549., 1996.05.
44. A. Maruyama, M. Yoshiyama, Y. Adachi, A. Tani, R. Hasegawa, and Y. Esashi , Promotion of cocklebur seed germination by allyl, sulfur and cyanogenic compounds. , Plant Cell Physiol. , 37: 1054-1058., 1996.05.