Curriculum Vitaes

Suzuki Nobuhiro

  (鈴木 伸洋)

Profile Information

Affiliation
Associate Professor, Faculty of Science and Technology, Department of Materials and Life Sciences, Sophia University
Degree
学士(香川大学)
修士(香川大学)
Ph.D(University of Nevada Reno)
博士(生物化学及び分子生物学)(ネバダ大学リノ校)

Researcher number
50735925
J-GLOBAL ID
201401089213197583
researchmap Member ID
7000007565

2004-2010 University of Nevada, Reno
Molecular mechanisms regulating heat stress response of plants

2010-2014 University of North Texas
Reactive oxygen species signal underlying systemic acquired acclimation of plants to abiotic stresses

2014- Sophia University Faculty of Science and Technology
Signal networks regulating different types of abiotic stress responses in plants

(Subject of research)
Molecular mechanisms regulating different types of heat stress responses in plants
Response of plants to stress combinations


Papers

 38
  • Lingxiao Ji, Zhengfeng Zhang, Shuang Liu, Liyan Zhao, Qiang Li, Benze Xiao, Nobuhiro Suzuki, David J Burks, Rajeev K Azad, Guosheng Xie
    The Plant journal : for cell and molecular biology, 117(1) 72-91, Jan, 2024  
    Lipocalins constitute a conserved protein family that binds to and transports a variety of lipids while fatty acid desaturases (FADs) are required for maintaining the cell membrane fluidity under cold stress. Nevertheless, it remains unclear whether plant lipocalins promote FADs for the cell membrane integrity under cold stress. Here, we identified the role of OsTIL1 lipocalin in FADs-mediated glycerolipid remodeling under cold stress. Overexpression and CRISPR/Cas9 mediated gene edition experiments demonstrated that OsTIL1 positively regulated cold stress tolerance by protecting the cell membrane integrity from reactive oxygen species damage and enhancing the activities of peroxidase and ascorbate peroxidase, which was confirmed by combined cold stress with a membrane rigidifier dimethyl sulfoxide or a H2 O2 scavenger dimethyl thiourea. OsTIL1 overexpression induced higher 18:3 content, and higher 18:3/18:2 and (18:2 + 18:3)/18:1 ratios than the wild type under cold stress whereas the gene edition mutant showed the opposite. Furthermore, the lipidomic analysis showed that OsTIL1 overexpression led to higher contents of 18:3-mediated glycerolipids, including galactolipids (monoglactosyldiacylglycerol and digalactosyldiacylglycerol) and phospholipids (phosphatidyl glycerol, phosphatidyl choline, phosphatidyl ethanolamine, phosphatidyl serine and phosphatidyl inositol) under cold stress. RNA-seq and enzyme linked immunosorbent assay analyses indicated that OsTIL1 overexpression enhanced the transcription and enzyme abundance of four ω-3 FADs (OsFAD3-1/3-2, 7, and 8) under cold stress. These results reveal an important role of OsTIL1 in maintaining the cell membrane integrity from oxidative damage under cold stress, providing a good candidate gene for improving cold tolerance in rice.
  • Tomoki Oshita, Joongeun Sim, Taufika Islam Anee, Hanako Kiyono, Chihiro Nozu, Nobuhiro Suzuki
    Journal of plant physiology, 281 153915-153915, Jan 17, 2023  Peer-reviewedCorresponding author
    Due to recent global warming, heat stress can simultaneously occur with cadmium (Cd) stress in regions suffering from metal pollution. In this study, we investigated the effects of heat, Cd and their combination on the growth and physiological characteristics of Arabidopsis thaliana. Arabidopsis plants were more susceptible to a combination of heat and Cd stress than to each stress applied individually, although the accumulation of Cd in shoots was comparable between plants subjected to Cd stress and the combined stress. Plants subjected to this stress combination showed a dramatic reduction in the accumulation of the photosynthetic reaction center proteins in photosystem II as well as a tendency toward enhanced lipid peroxidation, suggesting that the negative effects of a combination of heat and Cd stresses might be caused by oxidative damage accompanied by damage to the photosynthetic apparatus. Interestingly, aos and lox3 mutants deficient in jasmonic acid (JA) synthesis showed attenuation of the negative effects caused by a combination of heat and Cd stresses on the growth and maximum quantum efficiency of photosystem II. The roles of JA might be altered when heat stress is combined with Cd stress, despite its significance in the tolerance of plants to Cd stress when individually applied, which has been shown in previous studies.
  • Nobuhiro Suzuki
    International journal of molecular sciences, 24(2), Jan 10, 2023  Peer-reviewedInvitedLead authorCorresponding author
    Heat stress severely affects plant growth and crop production. It is therefore urgent to uncover the mechanisms underlying heat stress responses of plants and establish the strategies to enhance heat tolerance of crops. The chloroplasts and mitochondria are known to be highly sensitive to heat stress. Heat stress negatively impacts on the electron transport chains, leading to increased production of reactive oxygen species (ROS) that can cause damages on the chloroplasts and mitochondria. Disruptions of photosynthetic and respiratory metabolisms under heat stress also trigger increase in ROS and alterations in redox status in the chloroplasts and mitochondria. However, ROS and altered redox status in these organelles also activate important mechanisms that maintain functions of these organelles under heat stress, which include HSP-dependent pathways, ROS scavenging systems and retrograde signaling. To discuss heat responses associated with energy regulating organelles, we should not neglect the energy regulatory hub involving TARGET OF RAPAMYCIN (TOR) and SNF-RELATED PROTEIN KINASE 1 (SnRK1). Although roles of TOR and SnRK1 in the regulation of heat responses are still unknown, contributions of these proteins to the regulation of the functions of energy producing organelles implicate the possible involvement of this energy regulatory hub in heat acclimation of plants.
  • Nobuhiro Suzuki, Shunsuke Shigaki, Mai Yunose, Nicholas Raditya Putrawisesa, Sho Hogaki, Maria Carmela Di Piazza
    Biomimetics (Basel, Switzerland), 7(2), Jun 19, 2022  Peer-reviewedLead authorCorresponding author
    In this paper, the main features of systems that are required to flexibly modulate energy states of plant cells in response to environmental fluctuations are surveyed and summarized. Plant cells possess multiple sources (chloroplasts and mitochondria) to produce energy that is consumed to drive many processes, as well as mechanisms that adequately provide energy to the processes with high priority depending on the conditions. Such energy-providing systems are tightly linked to sensors that monitor the status of the environment and inside the cell. In addition, plants possess the ability to efficiently store and transport energy both at the cell level and at a higher level. Furthermore, these systems can finely tune the various mechanisms of energy homeostasis in plant cells in response to the changes in environment, also assuring the plant survival under adverse environmental conditions. Electrical power systems are prone to the effects of environmental changes as well; furthermore, they are required to be increasingly resilient to the threats of extreme natural events caused, for example, by climate changes, outages, and/or external deliberate attacks. Starting from this consideration, similarities between energy-related processes in plant cells and electrical power grids are identified, and the potential of mechanisms regulating energy homeostasis in plant cells to inspire the definition of new models of flexible and resilient electrical power grids, particularly microgrids, is delineated. The main contribution of this review is surveying energy regulatory mechanisms in detail as a reference and helping readers to find useful information for their work in this research field.
  • Kazuma Katano, Nobuhiro Suzuki
    Plant signaling & behavior, 1-7, Sep 22, 2021  Peer-reviewed
    Pollination is one of the critical processes that determines crop yield and quality. Thus, it is an urgent need to elucidate the mechanisms underlying pollination. Our previous research has revealed a novel phenomenon that pollen attachment to stigma caused stigma shrinkage, whereas failure of pollen attachment to stigma due to the environmental stress induced elongation of stigmatic papillae. However, little is known about the mechanisms of these morphological alterations in stigmatic papillae. Since the RLK-ROPGEF-ROP network is a common mechanism for the elongation of pollen tubes and root hairs, this network may be also involved in the elongation of papillae in the stigma. In this review, we will discuss the known mechanisms regulating pollen tube growth and root hair elongation and attempt to propose an elongation mechanism of stigmatic papillae. In addition, we will suggest that the degradation of F-actin by a significant increase in Ca2+ induced by the components of pollen coat might be a putative molecular mechanism of stigmatic papillae shrinkage during pollen adhesion.
  • Hanako Kiyono, Kazuma Katano, Nobuhiro Suzuki
    Plants (Basel, Switzerland), 10(8), Aug 11, 2021  Peer-reviewedCorresponding author
    To thrive on the earth, highly sophisticated systems to finely control reproductive development have been evolved in plants. In addition, deciphering the mechanisms underlying the reproductive development has been considered as a main research avenue because it leads to the improvement of the crop yields to fulfill the huge demand of foods for the growing world population. Numerous studies revealed the significance of ROS regulatory systems and carbohydrate transports and metabolisms in the regulation of various processes of reproductive development. However, it is poorly understood how these mechanisms function together in reproductive tissues. In this review, we discuss mode of coordination and integration between ROS regulatory systems and carbohydrate transports and metabolisms underlying reproductive development based on the hitherto findings. We then propose three mechanisms as key players that integrate ROS and carbohydrate regulatory systems. These include ROS-dependent programmed cell death (PCD), mitochondrial and respiratory metabolisms as sources of ROS and energy, and functions of arabinogalactan proteins (AGPs). It is likely that these key mechanisms govern the various signals involved in the sequential events required for proper seed production.
  • Plant Signal Behav, 15(8) 1778919, Aug 2, 2020  Peer-reviewedCorresponding author
  • Front Plant Sci, 11 989, Jul 30, 2020  Peer-reviewedCorresponding author
  • Kazuma Katano, Kohey Honda, Nobuhiro Suzuki
    International journal of molecular sciences, 19(11), Oct 28, 2018  Peer-reviewedInvitedCorresponding author
    Because of their sessile lifestyle, plants cannot escape from heat stress and are forced to alter their cellular state to prevent damage. Plants, therefore, evolved complex mechanisms to adapt to irregular increases in temperature in the natural environment. In addition to the ability to adapt to an abrupt increase in temperature, plants possess strategies to reprogram their cellular state during pre-exposure to sublethal heat stress so that they are able to survive under subsequent severe heat stress. Such an acclimatory response to heat, i.e., acquired thermotolerance, might depend on the maintenance of heat memory and propagation of long-distance signaling. In addition, plants are able to tailor their specific cellular state to adapt to heat stress combined with other abiotic stresses. Many studies revealed significant roles of reactive oxygen species (ROS) regulatory systems in the regulation of these various heat responses in plants. However, the mode of coordination between ROS regulatory systems and other pathways is still largely unknown. In this review, we address how ROS regulatory systems are integrated with other signaling networks to control various types of heat responses in plants. In addition, differences and similarities in heat response signals between different growth stages are also addressed.
  • Nobuhiro Suzuki, Kazuma Katano
    Frontiers in plant science, 9 490-490, 2018  Peer-reviewedInvitedCorresponding author
    Regulatory systems of reactive oxygen species (ROS) are known to be integrated with other pathways involving Ca2+ signaling, protein kinases, hormones and programmed cell death (PCD) pathways to regulate defense mechanisms in plants. Coordination between ROS regulatory systems and other pathways needs to be flexibly modulated to finely tune the mechanisms underlying responses of different types of tissues to heat stress, biotic stresses and their combinations during different growth stages. Especially, modulation of the delicate balance between ROS-scavenging and producing systems in reproductive tissues could be essential, because ROS-dependent PCD is required for the proper fertilization, despite the necessity of ROS scavenging to prevent the damage on cells under heat stress and biotic stresses. In this review, we will update the recent findings associated with coordination between multiple pathways under heat stress, pathogen attack and their combinations. In addition, possible integrations between different signals function in different tissues via ROS-dependent long-distance signals will be proposed.
  • Katano K, Kataoka R, Fujii M, Suzuki N
    Plant Physiol Biochem, 123 288-296, Dec 13, 2017  Peer-reviewedCorresponding author
  • Ryo Kataoka, Misato Takahashi, Nobuhiro Suzuki
    Plant Signal Behav, 12(11) e1376159, Nov, 2017  Peer-reviewedCorresponding author
  • Nobuhiro Suzuki
    Plant signaling & behavior, 11(11) e1247139, Nov, 2016  Peer-reviewedLead authorCorresponding author
    As sessile organisms, plants are continuously exposed to various environmental stresses. In contrast to the controlled conditions employed in many researches, more than one or more abiotic and/or biotic stresses simultaneously occur and highly impact growth of plants and crops in the field environments. Therefore, an urgent need to generate crops with enhanced tolerance to stress combinations exists. Researchers, however, focused on the mechanisms underlying acclimation of plants to combined stresses only in recent studies. Plant hormones might be a key regulator of the tailored responses of plants to different stress combinations. Co-ordination between different hormone signaling, or hormone signaling and other pathways such as ROS regulatory mechanisms could be flexible, being altered by timing and types of stresses, and could be different depending on plant species under the stress combinations. In this review, update on recent studies focusing on complex-mode of hormone signaling under stress combinations will be provided.
  • Simon Gilroy, Maciej Białasek, Nobuhiro Suzuki, Magdalena Górecka, Amith R Devireddy, Stanisław Karpiński, Ron Mittler
    Plant physiology, 171(3) 1606-15, Jul, 2016  Peer-reviewedInvited
  • Nobuhiro Suzuki, Elias Bassil, Jason S. Hamilton, Madhuri A. Inupakutika, Sara Izquierdo Zandalinas, Deesha Tripathy, Yuting Luo, Erin Dion, Ginga Fukui, Ayana Kumazaki, Ruka Nakano, Rosa M. Rivero, Guido F. Verbeck, Rajeev K. Azad, Eduardo Blumwald, Ron Mittler
    PLOS ONE, 11(1) e0147625, Jan, 2016  Peer-reviewedLead authorCorresponding author
    Abiotic stresses such as drought, heat or salinity are a major cause of yield loss worldwide. Recent studies revealed that the acclimation of plants to a combination of different environmental stresses is unique and cannot be directly deduced from studying the response of plants to each of the different stresses applied individually. Here we report on the response of Arabidopsis thaliana to a combination of salt and heat stress using transcriptome analysis, physiological measurements and mutants deficient in abscisic acid, salicylic acid, jasmonic acid or ethylene signaling. Arabidopsis plants were found to be more susceptible to a combination of salt and heat stress compared to each of the different stresses applied individually. The stress combination resulted in a higher ratio of Na+/K+ in leaves and caused the enhanced expression of 699 transcripts unique to the stress combination. Interestingly, many of the transcripts that specifically accumulated in plants in response to the salt and heat stress combination were associated with the plant hormone abscisic acid. In accordance with this finding, mutants deficient in abscisic acid metabolism and signaling were found to be more susceptible to a combination of salt and heat stress than wild type plants. Our study highlights the important role abscisic acid plays in the acclimation of plants to a combination of two different abiotic stresses.
  • J. S. Hamilton, E. L. Gorishek, P. M. Mach, D. Sturtevant, M. L. Ladage, N. Suzuki, P. A. Padilla, R. Mittler, K. D. Chapman, G. F. Verbeck
    JOURNAL OF ANALYTICAL ATOMIC SPECTROMETRY, 31(4) 1030-1033, 2016  Peer-reviewed
    The advent of laser ablation coupled to inductively coupled plasma-mass spectrometry has allowed for the elemental analysis of solid samples in their native state, or with little sample preparation required. Furthermore, with the addition of a cooled ablation cell spatially resolved elemental imaging of soft and semi-soft samples, specifically biological tissues, is attainable. A new single Peltier element laser ablation cell is described and a demonstration of its applicability to biological sampling is discussed to evaluate its performance. Through the analysis of three different biological tissues the device is shown to provide spatially resolved images of mapped elements while maintaining the structural integrity of the tissues during the hours long sampling times.
  • Nobuhiro Suzuki, Amith R. Devireddy, Madhuri A. Inupakutika, Aaron Baxter, Gad Miller, Luhua Song, Elena Shulaev, Rajeev K. Azad, Vladimir Shulaev, Ron Mittler
    PLANT JOURNAL, 84(4) 760-772, Nov, 2015  Peer-reviewedLead author
    The acclimation of plants to changes in light intensity requires rapid responses at several different levels. These include biochemical and biophysical responses as well as alterations in the steady-state level of different transcripts and proteins. Recent studies utilizing promoter:: reporter constructs suggested that transcriptional responses to changes in light intensity could occur within seconds, rates for which changes in mRNA expression are not routinely measured or functionally studied. To identify and characterize rapid changes in the steady-state level of different transcripts in response to light stress we performed RNA sequencing analysis of Arabidopsis thaliana plants subjected to light stress. Here we report that mRNA accumulation of 731 transcripts occurs as early as 20-60 sec following light stress application, and that at least five of these early response transcripts play an important biological role in the acclimation of plants to light stress. More than 20% of transcripts accumulating in plants within 20-60 sec of initiation of light stress are H2O2- and ABA-response transcripts, and the accumulation of several of these transcripts is inhibited by transcriptional inhibitors. In accordance with the association of rapid response transcripts with H2O2 and ABA signaling, a mutant impaired in ABA sensing (abi-1) was found to be more tolerant to light stress, and the response of several of the rapid response transcripts was altered in mutants impaired in reactive oxygen metabolism. Our findings reveal that transcriptome reprogramming in plants could occur within seconds of initiation of abiotic stress and that this response could invoke known as well as unknown proteins and pathways.
  • Simon Gilroy, Nobuhiro Suzuki, Gad Miller, Won-Gyu Choi, Masatsugu Toyota, Amith R Devireddy, Ron Mittler
    Trends in plant science, 19(10) 623-30, Oct, 2014  Peer-reviewed
    Systemic signaling pathways enable multicellular organisms to prepare all of their tissues and cells to an upcoming challenge that may initially only be sensed by a few local cells. They are activated in plants in response to different stimuli including mechanical injury, pathogen infection, and abiotic stresses. Key to the mobilization of systemic signals in higher plants are cell-to-cell communication events that have thus far been mostly unstudied. The recent identification of systemically propagating calcium (Ca(2+)) and reactive oxygen species (ROS) waves in plants has unraveled a new and exciting cell-to-cell communication pathway that, together with electric signals, could provide a working model demonstrating how plant cells transmit long-distance signals via cell-to-cell communication mechanisms. Here, we summarize recent findings on the ROS and Ca(2+) waves and outline a possible model for their integration.
  • Nobuhiro Suzuki, Rosa M Rivero, Vladimir Shulaev, Eduardo Blumwald, Ron Mittler
    The New phytologist, 203(1) 32-43, Jul, 2014  Peer-reviewedInvited
    Environmental stress conditions such as drought, heat, salinity, cold, or pathogen infection can have a devastating impact on plant growth and yield under field conditions. Nevertheless, the effects of these stresses on plants are typically being studied under controlled growth conditions in the laboratory. The field environment is very different from the controlled conditions used in laboratory studies, and often involves the simultaneous exposure of plants to more than one abiotic and/or biotic stress condition, such as a combination of drought and heat, drought and cold, salinity and heat, or any of the major abiotic stresses combined with pathogen infection. Recent studies have revealed that the response of plants to combinations of two or more stress conditions is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Moreover, the simultaneous occurrence of different stresses results in a high degree of complexity in plant responses, as the responses to the combined stresses are largely controlled by different, and sometimes opposing, signaling pathways that may interact and inhibit each other. In this review, we will provide an update on recent studies focusing on the response of plants to a combination of different stresses. In particular, we will address how different stress responses are integrated and how they impact plant growth and physiological traits.
  • Aaron Baxter, Ron Mittler, Nobuhiro Suzuki
    Journal of experimental botany, 65(5) 1229-40, Mar, 2014  
    Reactive oxygen species (ROS) play an integral role as signalling molecules in the regulation of numerous biological processes such as growth, development, and responses to biotic and/or abiotic stimuli in plants. To some extent, various functions of ROS signalling are attributed to differences in the regulatory mechanisms of respiratory burst oxidase homologues (RBOHs) that are involved in a multitude of different signal transduction pathways activated in assorted tissue and cell types under fluctuating environmental conditions. Recent findings revealed that stress responses in plants are mediated by a temporal-spatial coordination between ROS and other signals that rely on production of stress-specific chemicals, compounds, and hormones. In this review we will provide an update of recent findings related to the integration of ROS signals with an array of signalling pathways aimed at regulating different responses in plants. In particular, we will address signals that confer systemic acquired resistance (SAR) or systemic acquired acclimation (SAA) in plants.
  • Nobuhiro Suzuki, Gad Miller, Carolina Salazar, Hossain A. Mondal, Elena Shulaev, Diego F. Cortes, Joel L. Shuman, Xiaozhong Luo, Jyoti Shah, Karen Schlauch, Vladimir Shulaev, Ron Mittler
    PLANT CELL, 25(9) 3553-3569, Sep, 2013  
    Being sessile organisms, plants evolved sophisticated acclimation mechanisms to cope with abiotic challenges in their environment. These are activated at the initial site of exposure to stress, as well as in systemic tissues that have not been subjected to stress (termed systemic acquired acclimation [SAA]). Although SAA is thought to play a key role in plant survival during stress, little is known about the signaling mechanisms underlying it. Here, we report that SAA in plants requires at least two different signals: an autopropagating wave of reactive oxygen species (ROS) that rapidly spreads from the initial site of exposure to the entire plant and a stress-specific signal that conveys abiotic stress specificity. We further demonstrate that SAA is stress specific and that a temporal-spatial interaction between ROS and abscisic acid regulates rapid SAA to heat stress in plants. In addition, we demonstrate that the rapid ROS signal is associated with the propagation of electric signals in Arabidopsis thaliana. Our findings unravel some of the basic signaling mechanisms underlying SAA in plants and reveal that signaling events and transcriptome and metabolome reprogramming of systemic tissues in response to abiotic stress occur at a much faster rate than previously envisioned.
  • Song Luhua, Alicia Hegie, Nobuhiro Suzuki, Elena Shulaev, Xiaozhong Luo, Diana Cenariu, Vincent Ma, Stephanie Kao, Jennie Lim, Meryem Betul Gunay, Teruko Oosumi, Seung Cho Lee, Jeffery Harper, John Cushman, Martin Gollery, Thomas Girke, Julia Bailey-Serres, Rebecca A. Stevenson, Jian-Kang Zhu, Ron Mittler
    Physiologia Plantarum, 148(3) 322-333, Jul, 2013  
  • Nobuhiro Suzuki, Gad Miller, Hiroe Sejima, Jeffery Harper, Ron Mittler
    JOURNAL OF EXPERIMENTAL BOTANY, 64(1) 253-263, Jan, 2013  
    Reactive oxygen species play a key role in the response of plants to abiotic stress conditions. Their level is controlled in Arabidopsis thaliana by a large network of genes that includes the H2O2-scavenging enzymes cytosolic ascorbate peroxidase (APX) 1 and 2. Although the function of APX1 has been established under different growth conditions, genetic evidence for APX2 function, as well as for the mode of cooperation between APX1 and APX2, is very limited. This study characterized the response of Arabidopsis mutants deficient in APX1, APX2, and APX1/APX2 to heat, salinity, light, and oxidative stresses. The findings reveal that deficiency in APX2 resulted in a decreased tolerance to light stress, as well as an enhanced tolerance to salinity and oxidative stresses. Interestingly, plants lacking APX2 were more sensitive to heat stress at the seedling stage, but more tolerant to heat stress at the reproductive stage. Cooperation between APX1 and APX2 was evident during oxidative stress, but not during light, salinity, or heat stress. The findings demonstrate a role for APX2 in the response of plants to light, heat, salinity, and oxidative stresses. The finding that plants lacking APX2 produced more seeds under prolonged heat stress conditions suggests that redundant mechanisms activated in APX2-deficient plants during heat stress play a key role in the protection of reproductive tissues from heat-related damage. This finding is very important because heat-associated damage to reproductive tissues in different crops is a major cause for yield loss in agriculture production worldwide.
  • Nobuhiro Suzuki, Ron Mittler
    Free radical biology & medicine, 53(12) 2269-76, Dec 15, 2012  
    Animals and plants evolved sophisticated mechanisms that regulate their responses to mechanical injury. Wound response in animals mainly promotes wound healing processes, nerve cell regeneration, and immune system responses at the vicinity of the wound site. In contrast, wound response in plants is primarily directed at sealing the wound site via deposition of various compounds and generating systemic signals that activate multiple defense mechanisms in remote tissues. Despite these differences between animals and plants, recent studies have shown that reactive oxygen species (ROS) play very common signaling and coordination roles in the wound responses of both systems. This review provides an update on recent findings related to ROS-regulated coordination of intercellular communications and signal transduction during wound response in plants and animals. In particular, differences and similarities in H2O2-dependent long-distance signaling between zebrafish and Arabidopsis thaliana are discussed.
  • Nobuhiro Suzuki, Shai Koussevitzky, Ron Mittler, Gad Miller
    Plant, cell & environment, 35(2) 259-70, Feb, 2012  
    The redox state of the chloroplast and mitochondria, the two main powerhouses of photosynthesizing eukaryotes, is maintained by a delicate balance between energy production and consumption, and affected by the need to avoid increased production of reactive oxygen species (ROS). These demands are especially critical during exposure to extreme environmental conditions, such as high light (HL) intensity, heat, drought or a combination of different environmental stresses. Under these conditions, ROS and redox cues, generated in the chloroplast and mitochondria, are essential for maintaining normal energy and metabolic fluxes, optimizing different cell functions, activating acclimation responses through retrograde signalling, and controlling whole-plant systemic signalling pathways. Regulation of the multiple redox and ROS signals in plants requires a high degree of coordination and balance between signalling and metabolic pathways in different cellular compartments. In this review, we provide an update on ROS and redox signalling in the context of abiotic stress responses, while addressing their role in retrograde regulation, systemic acquired acclimation and cellular coordination in plants.
  • Nobuhiro Suzuki, Gad Miller, Jorge Morales, Vladimir Shulaev, Miguel Angel Torres, Ron Mittler
    Current opinion in plant biology, 14(6) 691-9, Dec, 2011  
    Reactive oxygen species (ROS) play a key signal transduction role in cells. They are involved in the regulation of growth, development, responses to environmental stimuli and cell death. The level of ROS in cells is determined by interplay between ROS producing pathways and ROS scavenging mechanisms, part of the ROS gene network of plants. Recent studies identified respiratory burst oxidase homologues (RBOHs) as key signaling nodes in the ROS gene network of plants integrating a multitude of signal transduction pathways with ROS signaling. The ability of RBOHs to integrate calcium signaling and protein phosphorylation with ROS production, coupled with genetic studies demonstrating their involvement in many different biological processes in cells, places RBOHs at the center of the ROS network of cells and demonstrate their important function in plants.
  • Ron Mittler, Sandy Vanderauwera, Nobuhiro Suzuki, Gad Miller, Vanesa B Tognetti, Klaas Vandepoele, Marty Gollery, Vladimir Shulaev, Frank Van Breusegem
    Trends in plant science, 16(6) 300-9, Jun, 2011  
    Reactive oxygen species (ROS) play a multitude of signaling roles in different organisms from bacteria to mammalian cells. They were initially thought to be toxic byproducts of aerobic metabolism, but have now been acknowledged as central players in the complex signaling network of cells. In this review, we will attempt to address several key questions related to the use of ROS as signaling molecules in cells, including the dynamics and specificity of ROS signaling, networking of ROS with other signaling pathways, ROS signaling within and across different cells, ROS waves and the evolution of the ROS gene network.
  • Nobuhiro Suzuki, Hiroe Sejima, Rachel Tam, Karen Schlauch, Ron Mittler
    PLANT JOURNAL, 66(5) 844-851, Jun, 2011  
    P>Brief periods of heat stress of even a few days can have a detrimental effect on yield production worldwide, causing devastating economic and societal impacts. Here we report on the identification of a new heat-response regulon in plants controlled by the multiprotein bridging factor 1c (MBF1c) protein of Arabidopsis thaliana. Members of the highly conserved MBF1 protein family function as non-DNA-binding transcriptional co-activators involved in regulating metabolic and development pathways in different organisms from yeast to humans. Nonetheless, our studies suggest that MBF1c from Arabidopsis functions as a transcriptional regulator which binds DNA and controls the expression of 36 different transcripts during heat stress, including the important transcriptional regulator DRE-binding protein 2A (DREB2A), two heat shock transcription factors (HSFs), and several zinc finger proteins. We further identify CTAGA as a putative response element for MBF1c, demonstrate that the DNA-binding domain of MBF1c has a dominant-negative effect on heat tolerance when constitutively expressed in plants, and show that constitutive expression of MBF1c in soybean enhances yield production in plants grown under controlled growth conditions without causing adverse effects on growth. Our findings could have a significant impact on improving heat tolerance and yield of different crops subjected to heat stress.
  • Sandy Vanderauwera, Nobuhiro Suzuki, Gad Miller, Brigitte van de Cotte, Stijn Morsa, Jean-Luc Ravanat, Alicia Hegie, Christian Triantaphylides, Vladimir Shulaev, Marc C. E. Van Montagu, Frank Van Breusegem, Ron Mittler
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 108(4) 1711-1716, Jan, 2011  
    Eukaryotic organisms evolved under aerobic conditions subjecting nuclear DNA to damage provoked by reactive oxygen species (ROS). Although ROS are thought to be a major cause of DNA damage, little is known about the molecular mechanisms protecting nuclear DNA from oxidative stress. Here we show that protection of nuclear DNA in plants requires a coordinated function of ROS-scavenging pathways residing in the cytosol and peroxisomes, demonstrating that nuclear ROS scavengers such as peroxiredoxin and glutathione are insufficient to safeguard DNA integrity. Both catalase (CAT2) and cytosolic ascorbate peroxidase (APX1) play a key role in protecting the plant genome against photorespiratory-dependent H(2)O(2)-induced DNA damage. In apx1/cat2 double-mutant plants, a DNA damage response is activated, suppressing growth via a WEE1 kinase-dependent cell-cycle checkpoint. This response is correlated with enhanced tolerance to oxidative stress, DNA stress-causing agents, and inhibited programmed cell death.
  • Gad Miller, Nobuhiro Suzuki, Sultan Ciftci-Yilmaz, Ron Mittler
    Plant, cell & environment, 33(4) 453-67, Apr, 2010  
    Water deficit and salinity, especially under high light intensity or in combination with other stresses, disrupt photosynthesis and increase photorespiration, altering the normal homeostasis of cells and cause an increased production of reactive oxygen species (ROS). ROS play a dual role in the response of plants to abiotic stresses functioning as toxic by-products of stress metabolism, as well as important signal transduction molecules. In this review, we provide an overview of ROS homeostasis and signalling in response to drought and salt stresses and discuss the current understanding of ROS involvement in stress sensing, stress signalling and regulation of acclimation responses.
  • Gad Miller, Arik Honig, Hanan Stein, Nobuhiro Suzuki, Ron Mittler, Aviah Zilberstein
    JOURNAL OF BIOLOGICAL CHEMISTRY, 284(39) 26482-26492, Sep, 2009  
    The two-step oxidation of proline in all eukaryotes is performed at the inner mitochondrial membrane by the consecutive action of proline dehydrogenase (ProDH) that produces Delta(1)-pyrroline-5-carboxylate (P5C) and P5C dehydrogenase (P5CDH) that oxidizes P5C to glutamate. This catabolic route is down-regulated in plants during osmotic stress, allowing free Pro accumulation. We show here that overexpression of MsProDH in tobacco and Arabidopsis or impairment of P5C oxidation in the Arabidopsis p5cdh mutant did not change the cellular Pro to P5C ratio under ambient and osmotic stress conditions, indicating that P5C excess was reduced to Pro in a mitochondrial-cytosolic cycle. This cycle, involving ProDH and P5C reductase, exists in animal cells and now demonstrated in plants. As a part of the cycle, Pro oxidation by the ProDH-FAD complex delivers electrons to the electron transport chain. Hyperactivity of the cycle, e. g. when an excess of exogenous L-Pro is provided, generates mitochondrial reactive oxygen species (ROS) by delivering electrons to O-2, as demonstrated by the mitochondria-specific MitoSox staining of superoxide ions. Lack of P5CDH activity led to higher ROS production under dark and light conditions in the presence of Pro excess, as well as rendered plants hypersensitive to heat stress. Balancing mitochondrial ROS production during increased Pro oxidation is therefore critical for avoiding Pro-related toxic effects. Hence, normal oxidation of P5C to Glu by P5CDH is key to prevent P5C-Pro intensive cycling and avoid ROS production from electron run-off.
  • Shai Koussevitzky, Nobuhiro Suzuki, Serena Huntington, Leigh Armijo, Wei Sha, Diego Cortes, Vladimir Shulaev, Ron Mittler
    JOURNAL OF BIOLOGICAL CHEMISTRY, 283(49) 34197-34203, Dec, 2008  
    Within their natural habitat plants are subjected to a combination of different abiotic stresses, each with the potential to exacerbate the damage caused by the others. One of the most devastating stress combinations for crop productivity, which frequently occurs in the field, is drought and heat stress. In this study we conducted proteomic and metabolic analysis of Arabidopsis thaliana plants subjected to a combination of drought and heat stress. We identified 45 different proteins that specifically accumulated in Arabidopsis in response to the stress combination. These included enzymes involved in reactive oxygen detoxification, malate metabolism, and the Calvin cycle. The accumulation of malic enzyme during the combined stress corresponded with enhanced malic enzyme activity, a decrease in malic acid, and lower amounts of oxaloacetate, suggesting that malate metabolism plays an important role in the response of Arabidopsis to the stress combination. Cytosolic ascorbate peroxidase 1 (APX1) protein and mRNA accumulated during the stress combination. When exposed to heat stress combined with drought, an APX1-deficient mutant (apx1) accumulated more hydrogen peroxide and was significantly more sensitive to the stress combination than wild type. In contrast, mutants deficient in thylakoid or stromal/mitochondrial APXs were not more sensitive to the stress combination than apx1 or wild type. Our findings suggest that cytosolic APX1 plays a key role in the acclimation of plants to a combination of drought and heat stress.
  • Nobuhiro Suzuki, Sunil Bajad, Joel Shuman, Vladimir Shulaev, Ron Mittler
    JOURNAL OF BIOLOGICAL CHEMISTRY, 283(14) 9269-9275, Apr, 2008  
    The ability of an organism to acclimate to its environment is a key determinant in its global distribution and capacity to compete with other organisms. The heat stress response, a highly conserved environmental and developmental program in eukaryotic and prokaryotic organisms, is an important component of the acclimation response of plants. Previous studies have shown that heat shock transcription factors play an important role in thermotolerance in plants and other organisms, controlling the expression of different heat shock proteins and detoxifying enzymes. In contrast, although several other pathways, involving ethylene, salicylic acid ( SA), and trehalose, were recently shown to play a central role in thermotolerance in plants, a key regulator of these responses was not identified. Here we report that the highly conserved transcriptional coactivator, MBF1c ( multiprotein bridging factor 1c), is a key regulator of thermotolerance in Arabidopsis thaliana. MBF1c protein accumulates rapidly and is localized to nuclei during heat stress. MBF1c is required for thermotolerance and functions upstream to SA, trehalose, ethylene, and pathogenesis-related protein 1 during heat stress. In contrast, MBF1c is not required for the expression of transcripts encoding HSFA2 and different heat shock proteins. Interestingly, MBF1c interacts with TPS5 ( trehalose phosphate synthase 5), which is also heat-inducible, and mutants deficient in TPS5 are thermosensitive. Our results provide evidence for the existence of a tightly coordinated heat stress-response network, involving trehalose- ,SA-, and ethylene-signaling pathways, that is under the control of MBF1c.
  • Gad Miller, Nobuhiro Suzuki, Ludmila Rizhsky, Alicia Hegie, Shai Koussevitzky, Ron Mittler
    PLANT PHYSIOLOGY, 144(4) 1777-1785, Aug, 2007  
    Reactive oxygen species (ROS) play a key signaling role in plants and are controlled in cells by a complex network of ROS metabolizing enzymes found in several different cellular compartments. To study how different ROS signals, generated in different cellular compartments, are integrated in cells, we generated a double mutant lacking thylakoid ascorbate peroxidase (tylapx) and cytosolic ascorbate peroxidase1 (apx1). Our analysis suggests that two different signals are generated in plants lacking cytosolic APX1 or tylAPX. The lack of a chloroplastic hydrogen peroxide removal enzyme triggers a specific signal in cells that results in enhanced tolerance to heat stress, whereas the lack of a cytosolic hydrogen peroxide removal enzyme triggers a different signal, which results in stunted growth and enhanced sensitivity to oxidative stress. When the two signals are coactivated in cells (i.e. tylapx/apx1), a new response is detected, suggesting that the integration of the two different signals results in a new signal that manifests in late flowering, low protein oxidation during light stress, and enhanced accumulation of anthocyanins. Our results demonstrate a high degree of plasticity in ROS signaling in Arabidopsis (Arabidopsis thaliana) and suggest the existence of redundant pathways for ROS protection that compensate for the lack of classical ROS removal enzymes such as cytosolic and chloroplastic APXs. Further investigation of the enhanced heat tolerance in plants lacking tylAPX, using mutants deficient in chloroplast-to-nuclei retrograde signaling, suggests the existence of a chloroplast-generated stress signal that enhances basal thermotolerance in plants.
  • N Suzuki, L Rizhsky, HJ Liang, J Shuman, Shulaev, V, R Mittler
    PLANT PHYSIOLOGY, 139(3) 1313-1322, Nov, 2005  
    Abiotic stresses cause extensive losses to agricultural production worldwide. Acclimation of plants to abiotic conditions such as drought, salinity, or heat is mediated by a complex network of transcription factors and other regulatory genes that control multiple defense enzymes, proteins, and pathways. Associated with the activity of different transcription factors are transcriptional coactivators that enhance their binding to the basal transcription machinery. Although the importance of stress-response transcription factors was demonstrated in transgenic plants, little is known about the function of transcriptional coactivators associated with abiotic stresses. Here, we report that constitutive expression of the stress-response transcriptional coactivator multiprotein bridging factor 1c (MBF1c) in Arabidopsis (Arabidopsis thaliana) enhances the tolerance of transgenic plants to bacterial infection, heat, and osmotic stress. Moreover, the enhanced tolerance of transgenic plants to osmotic and heat stress was maintained even when these two stresses were combined. The expression of MBF1c in transgenic plants augmented the accumulation of a number of defense transcripts in response to heat stress. Transcriptome profiling and inhibitor studies suggest that MBF1c expression enhances the tolerance of transgenic plants to heat and osmotic stress by partially activating, or perturbing, the ethylene-response signal transduction pathway. Present findings suggest that MBF1 proteins could be used to enhance the tolerance of plants to different abiotic stresses.
  • N Suzuki, S Taketa, M Ichii
    PLANT AND SOIL, 255(1) 9-17, Aug, 2003  
    This paper reports morphological and physiological characteristics of a first root-hairless mutant (RH2) of rice ( Oryza sativa L.), which can be useful in advancing knowledge on the role of root hairs in water and nutrient uptake, and genetics of root hairs. The mutant was selected among NaN3 mutagenized progeny of the rice cultivar Oochikara. Microscopic observations showed absence of root hairs in RH2. At the seedling stage, RH2 showed shorter seedling height and shorter roots compared to the wild type variety Oochikara. Because of the differences in seedling growth, all comparisons between Oochikara and RH2 in uptake-related characters were made on the basis of values adjusted by the dry weight of either the shoot or the root. When grown at low water potential in soil, Oochikara and RH2 were similar in shoot water content and transpiration per unit shoot dry weight, and similarly, at low water potential in solution culture, there was no significant difference between Oochikara and RH2 in transpiration per unit shoot dry weight. These results suggest that at the seedling stage, root hairs do not significantly contribute to uptake of water. In solution culture, Oochikara and RH2 did not significantly differ in phosphate uptake per unit root dry weight. This result supports the previous work that root hairs do not contribute to phosphate uptake in solution culture. Regarding to response to plant hormones, RH2 showed a higher level of resistance to two synthetic auxins, 2,4-dichlorophenoxyacetic acid ( 2,4-D) and 1-naphthaleneacetic acid (NAA) than Oochikara. NAA treatment induced very short root hairs in RH2, suggesting that the absence of root hairs in RH2 may be due to a shortage of endogenous auxin. Genetic analysis showed that the root hairless character in RH2 is inherited as a single recessive gene.

Misc.

 14
  • Wetland Research, 10 37-46, 2020  Peer-reviewedLead authorCorresponding author
  • Katano K, Honda K, Suzuki N
    Int J Mol Sci, 19(11) E3370, Oct 28, 2018  Peer-reviewedInvited
  • Nobuhiro Suzuki, Kazuma Katano
    Frontiers in Plant Science, 9 490, Apr 16, 2018  
    Regulatory systems of reactive oxygen species (ROS) are known to be integrated with other pathways involving Ca2+ signaling, protein kinases, hormones and programmed cell death (PCD) pathways to regulate defense mechanisms in plants. Coordination between ROS regulatory systems and other pathways needs to be flexibly modulated to finely tune the mechanisms underlying responses of different types of tissues to heat stress, biotic stresses and their combinations during different growth stages. Especially, modulation of the delicate balance between ROS-scavenging and producing systems in reproductive tissues could be essential, because ROS-dependent PCD is required for the proper fertilization, despite the necessity of ROS scavenging to prevent the damage on cells under heat stress and biotic stresses. In this review, we will update the recent findings associated with coordination between multiple pathways under heat stress, pathogen attack and their combinations. In addition, possible integrations between different signals function in different tissues via ROS-dependent long-distance signals will be proposed.
  • Simon Gilroy, Maciej Bialasek, Nobuhiro Suzuki, Magdalena Gorecka, Amith R. Devireddy, Stanislaw Karpinski, Ron Mittler
    PLANT PHYSIOLOGY, 171(3) 1606-1615, Jul, 2016  Peer-reviewed
  • Nobuhiro Suzuki
    PLANT SIGNALING & BEHAVIOR, 11(11) e1247139, 2016  Peer-reviewedInvited
    As sessile organisms, plants are continuously exposed to various environmental stresses. In contrast to the controlled conditions employed in many researches, more than one or more abiotic and/or biotic stresses simultaneously occur and highly impact growth of plants and crops in the field environments. Therefore, an urgent need to generate crops with enhanced tolerance to stress combinations exists. Researchers, however, focused on the mechanisms underlying acclimation of plants to combined stresses only in recent studies. Plant hormones might be a key regulator of the tailored responses of plants to different stress combinations. Co-ordination between different hormone signaling, or hormone signaling and other pathways such as ROS regulatory mechanisms could be flexible, being altered by timing and types of stresses, and could be different depending on plant species under the stress combinations. In this review, update on recent studies focusing on complex-mode of hormone signaling under stress combinations will be provided.

Books and Other Publications

 3

Presentations

 21

Research Projects

 5

Industrial Property Rights

 1