Japan Society for the Promotion of Science

36th Recipient (2020)

Recipient

The Committee on the International Prize for Biology of Japan Society
for the Promotion of Science awards the 2020 International Prize for Biology
in the field of "Biology of Environmental Responses" to
Dr. SHIONOZAKI Kazuo,
Senior Advisor, RIKEN Center for Sustainable Resource Science (CSRS)

On August 28, the Committee on the International Prize for Biology (chaired by Dr.BEPPU Teruhiko, Professor Emeritus, The University of Tokyo) decided to award the 36th (2020) International Prize for Biology to Dr. SHINOZAKI Kazuo, Senior Advisor, RIKEN Center for Sustainable Resource Science (CSRS), Japan.This year’s Prize is awarded in the field of the Biology of Environmental Responses.
Photo of SHIONOZAKI Kazuo

SHINOZAKI Kazuo

Education and Professional Positions

1979                     Doctor of Science, Faculty of Science, Nagoya University
1978–1986        Research Associate, Molecular Genetics Division, National Institute of Genetics
1983–1986        Assistant Professor, Division of Biology, Faculty of Science, Nagoya University
1986–1989        Associate Professor, Center for Gene Research, Nagoya University
1989–2005        Chief Scientist, Plant Molecular Biology Laboratory, RIKEN
1999–2005        Project Director, Plant Functional Genomics Research Group, RIKEN Genomic Sciences Center
2005–2013        Director, RIKEN Plant Science Center
2010–2015        Program Director, RIKEN Biomass Engineering Program (concurrent position)
2013–2020        Director, RIKEN CSRS
2020–present  Senior Advisor, RIKEN CSRS and Group Director, Gene Discovery Research Group, CSRS

Awards and Distinctions

1987               Encouragement Prize of the Japanese Biochemical Society Award and Encouragement Award of the Genetics Society of Japan
2000               Thompson Reuters, Most-Cited Award
2003               14th Tsukuba Award
2006               MEXT Minister’s Award Science and Technology
2009               Japanese Society of Plant Physiologists Award
2014–2015  Thompson Reuters, Highly-Cited Researchers List
2015               Enid MacRobbie Corresponding Membership Award, American Society of Plant Biologists (USA)
2016               Person of Cultural Merit Award, Agency for Cultural Affairs of Japan
2016               Medal of Honor with Purple Ribbon, Cabinet Office of Japan
2016–2019  Clarivate Analytics, Highly-Cited Researchers List
2018               Michigan State University (USA), Anton Lang Memorial Award
2020               Elected to the National Academy of Science (USA) as an international member

Research Achievements

Elucidation of plants’ molecular mechanisms for responding to and tolerating environmental stress
Given that plants are immobile, they respond and acquire tolerance to external environmental stresses such as drought, low temperatures, high temperatures, salinity, and so on, in order to survive. Research in the 1980’s on plant responses and adaptation to environmental stresses relied primarily on physiological methods. When Dr. Kazuo Shinozaki joined the Plant Molecular Biology Laboratory at RIKEN in 1989, he was ahead of the world in introducing molecular biology techniques to research on plant response and adaptation to environmental stresses. He discovered numerous important genes related to environmental stress responses and elucidated the functions and regulatory mechanisms of those genes. At the same time, using functional genomic analysis, he has conducted pioneering researches on stress-response gene expression networks and intracellular signal transduction systems that lead from the reception of environmental stress to gene expression. This work has had a major impact on plant molecular biology related to the environmental stress responses and environmental stress tolerance of plants. This is also evident in the fact that Dr. Shinozaki’s works are among the most highly cited in the international plant science community.

Exploration of plant genes related to the response to drought and other environmental stresses and analysis of the expression of those genes
Dr. Shinozaki and his colleagues used the model plant Arabidopsis thaliana to search for genes that were induced in response to the stress of drought and low temperatures and analyzed those genes’ functions. By doing so they discovered that environmental stress tolerance was not connected to a single gene, but rather was comprised of a cluster of genes that had various different functions. While it had been previously known that the plant hormone abscisic acid (ABA) plays an important role in the drought stress response, through their research on the genes induced in response to drought stress and the factors regulating their expression, Dr. Shinozaki and his colleagues showed for the first time that there were ABA-independent regulatory systems in the plant response to drought stress in addition to those that are ABA-dependent, and they discovered various major control regions on DNA sequence and transcription factors of the genes that function in gene expression. In particular, his research elucidating the roles of cis element DRE (Dehydration Responsive Element) in the transcription control region related to drought stress response and the transcription factor DREB (DRE Binding protein) is widely cited in academic papers and is included in numerous plant science textbooks.

Analysis of signal transduction systems related to the environmental stress response of plants
Dr. Shinozaki has elucidated the functions of transcription factors involved in regulating the expression of environmental stress response genes, signal transduction factors, and important regulatory factors related to the reception of osmotic stress. In their research on protein phosphorylation in environmental signal transduction, Dr. Shinozaki and his colleagues identified histidine kinases as the osmotic stress sensor and MAP kinases and SnRK2 kinases as members of the signal transduction system. These discoveries were a significant achievement in the study of signal transduction in environmental stress response. In particular, a series of papers that clarify the function of SnRK2 kinases in relation to signal transduction has been widely cited. Subsequently, he carried out research on important roles of ABA during drought stress, making strides in research on intracellular signal transduction, such as identifying regulation through ABA biosynthesis and degradation, as well as SnRK2 and its upstream factors. With regard to ABA-based transcriptional regulation as well, he identified AREB (ABA Responsive Element Binding protein) as the major transcriptional factor and showed that it was activated by SnRK2. Moreover, he also identified ABCG25 for the first time as an important transporter related to ABA transport between tissues, and clarified the overall picture of the ABA regulatory system in drought stress response.

Identification of long-distance signaling factors from roots to leaves in environmental stress response
When soil becomes dry, plants sense dehydration stress at their roots and adapt to the stress. Information on water deficiency is conveyed from the root up to the portions of the plant above ground through the vascular system of the stem, the leaf stomata close, thereby suppressing moisture evaporation. Dr. Shinozaki and his colleagues discovered that the CLAVATA3/Embryo-Surrounding Region-Related 25 (CLE25) peptide is transported as a long-distance transport signal from the roots to the leaves in a plant’s drought stress response. Decreased water in the roots causes CLE25 to be induced in the vascular bundle of the roots and it is then transported from the roots to the leaves, where it induces ABA synthesis. As a result, the ABA closes the stomata, suppressing evaporation of moisture. This research gained attention as it was the first to elucidate the fact that peptides are involved in the long-distance root-to-leaf signaling network in response to drought stress.

Applied research on improving the drought stress tolerance of crops
Dr. Shinozaki and his colleagues have carried out joint research that uses the Arabidopsis genes involved in environmental stress tolerance and apply them to the development of drought- and cold-tolerant crops, which opened the way to the production of environmental stress tolerant crops. In particular, he is involved in developing drought stress tolerant and salinity stress tolerant rice, soybeans, and other crops and has received many patents related to the use of environmental stress tolerant genes and stress-response promoters. Through joint research with the crop research institute of Consultative Group on International Agriculture Research (CGIAR), he has been working on the development of drought stress tolerant crops, and greater drought tolerance and increased yields have been observed in upland rice grown in arid areas, demonstrating that the Arabidopsis genes related to environmental stress tolerance can in fact be used to develop drought-tolerant crops.

Development of functional genomics research projects and research resources
Dr. Shinozaki and his colleagues have made tremendous contributions to the study of plant functional genomics of the model plant Arabidopsis thaliana. In particular, their ground-breaking findings in the collection of full-length cDNA, which is a copy of a gene transcript, and their pioneering analysis of environmental stress induced gene expression using microarray were highly esteemed. In addition, in order to analyze genome functions, they collected gene knockout mutants and made the research resources public through the RIKEN Bio Resource Center to contribute to the development of plant science. Using the mutant lines, he is conducting phenotypic analysis and made strides in functional analysis of genes through reverse genetics methods. Furthermore, while searching for environmental stress responsive genes through microarray analysis and collecting many stress-inducible genes, he also discovered new gene functions using reverse genetics. Since 2005, as the director of the former RIKEN Plant Science Center, Dr. Shinozaki has received high praise as a project leader, having promoted projects in such areas as functional genomics research, metabolomic research, plant hormone research, environmental stress research, etc. through which he made significant contributions to the development of plant sciences. At the Plant Science Center, he promoted plant science by developing the technical basis for transcriptomic, metabolomic and plant hormone analysis. Meanwhile, he contributed to the launch of the RIKEN Bio Resource Center and promoted the collection and provision of resources (research materials) such as genes and mutants of model plants, which help promote basic plant science research. These resources, which are useful for genetic research on plants, are also being used internationally and have contributed to the publication of many important research findings.

Representative Publications and Literatures:

Original articles
  1. Yamaguchi-Shinozaki K., and Shinozaki K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6: 251-264
  2. Mizoguchi T., Irie K., Hirayama T., Hayashida N., Yamaguchi-Shinozaki K., Matsumoto K., and Shinozaki K. (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA. 93: 765-769
  3. Liu Q., Kasuga M., Sakuma Y., Abe H., Miura S., Yamaguchi-Shinozaki K., and Shinozaki K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low- temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10: 1391-1406
  4. Kasuga M., Liu Q., Miura S., Yamaguchi-Shinozaki K., and Shinozaki K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology 17: 287-291
  5. Urao T., Yakubov B., Satoh R., Yamaguchi-Shinozaki K., Seki M., Hirayama T., and Shinozaki, K. (1999) A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11: 743-754
  6. Seki M., Narusaka M., Kamiya A., Ishida J., Satou M., Sakurai T., Nakajima M., Enju A., Akiyama K., Oono Y., Muramatsu M., Hayashizaki Y., Kawai J., Carninci P., Itoh M., Ishii Y., Arakawa T., Shibata K., Shinagawa A., and Shinozaki K. (2002) Functional annotation of a full-length Arabidopsis cDNA collection. Science 296: 141-145
  7. Yoshida R., Hobo T., Ichimura K., Mizoguchi T., Takahashi F., Aronso, J., Ecker J.R., and Shinozaki K. (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant and Cell Physiology 43: 1473-1483
  8. Umezawa T., Sugiyama N., Mizoguchi M., Hayashi S., Myouga F., Yamaguchi-Shinozaki K., Ishihama Y., Hirayama T., and Shinozaki K. (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences USA 106: 17588-17593
  9. Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y., and Shinozaki K. (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proceedings of the National Academy of Sciences USA 107: 2361-2366
  10. Takahashi F., Mizoguchi T., Yoshida R., Ichimura K., and Shinozaki K. (2011) Calmodulin-dependent activation of MAP kinase for ROS homeostasis in Arabidopsis. Molecular Cell 41: 649-660
  11. Umezawa T., Sugiyama N., Takahashi F., Anderson J.C., Ishihama Y., Peck S.C., and Shinozaki K. (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Science Signaling: 6 rs8
  12. Selvaraj M.G., Ishizaki T., Valencia M., Ogawa S., Dedicova B., Ogata T., Yoshikawa K., Maruyama M., Kusano M., Saito K., Takahashi F., Shinozaki K., Nakashima K., and Ishitani M. (2017) Overexpression of an Arabidopsis thaliana galactinol synthase gene improves drought tolerance in transgenic rice and increased grain yield in the field. Plant Biotechnology Journal 10.1111/pbi 12731
  13. Takahashi F., Suzuki T., Osakabe Y., Betsuyaku S., Kondo Y., Dohmae N., Fukuda H., Yamaguchi-Shinozaki K., and Shinozaki K. (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signaling. Nature 556: 235-238

Review articles and books
  1. Shinozaki K., and Yamaguchi-Shinozaki K. (1997) Gene expression and signal transduction in water-stress response. Plant Physiology 115: 327-334
  2. Yamaguchi-Shinozaki K., and Shinozaki K. (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57: 781-803
  3. Umezawa T., Fujita M., Fujita Y., Yamaguchi-Shinozaki K., and Shinozaki K. (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Current Opinion of Biotechnology 17: 113-122
  4. Hirayama T., and Shinozaki K. (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant Journal 61: 1041-1052
  5. Shinozaki K., Uemura M., Bailey-Serres J., Bray A.E., and Weretilnyk E. (2015) Responses to abiotic stress. In Biochemistry and Molecular Biology of Plants. Second edition. Edited by Buchanan, B., Gruissem, W. and Jones, R.L. American Society of Plant Biologists & Wiley Blackwell. page 1051-1100
  6. Kuromori T., Seo M., and Shinozaki K. (2018) ABA Transport and Plant Water Stress Responses. Trends in Plant Science 23: 513-522
  7. Takahashi F., and Shinozaki K. (2019) Long-distance signaling in plant stress response. Current Opinion of Plant Biology 47:106-111