Suzuki Nobuhiro

Although positive effects of microwave irradiation on plants have been reported, their underlying mechanisms remain unknown. In this study, we investigated the effects of low microwave irradiation on Arabidopsis thaliana. Interestingly, we found low output (23 W) with oscillating condition (not continuous irradiation) promoted plant growth. The microwave irradiation neither raised the plants' temperature nor induced heat responsive gene expression. Furthermore, overall transcriptome profile in microwave irradiation treated plants were significantly different from heat treated plants, suggesting that growth promotion might be attributed to non-thermal effects of microwave. Transcriptome and metabolome analysis indicated that microwave irradiation altered circadian clock as well as hormonal response especially in auxin and gibberellin, which promoted plant growth by inducing amino acid biosynthesis and stress tolerance, and reducing cell wall thickness. This finding potentially contributes to develop new approach to increase food production through accelerating crop yield in environmentally friendly way.

Abstract Salt stress and waterlogging are two of the most common abiotic stresses in nature, often occurring concurrently. However, our understanding of the mechanisms underlying responses of plants to a combination of these stresses remains limited. In this study, we investigated growth, physiological and biochemical responses of Solanum lycopersicum cv. Micro‐Tom to salt stress, waterlogging and the combination of both. Under waterlogging individually, plants showed increased plant height and longer root length. However, they exhibited a significantly smaller leaf area, fewer leaves, reduced fresh and dry weights, and lower relative water content compared to plants grown under controlled conditions. These effects were more severe than those caused by salt stress alone. Interestingly, the growth inhibition from waterlogging was alleviated under combined salt and waterlogging stress. This attenuation may be associated with decreased accumulation of H₂O₂ and oxidized lipids, along with increased proline and photosynthetic pigment contents compared with waterlogging individually applied. However, ROS accumulations and contents of photosynthetic pigments were not straightforwardly linked to the activity of photosynthesis. In addition, activities of various antioxidant enzymes such as CAT, GPX and GST as well as those involved in the AsA‐GSH cycle were differently altered by salt stress and waterlogging, individually and in combination. Taken together, these results suggest that the response of tomato plants to salt stress and waterlogging, individually and in combination, can be differently modulated via fine‐tuning of acclimation mechanisms to oxidative stress.

Flooding causes severe yield losses worldwide, making it urgent to enhance crop tolerance to this stress. Since natural flooding often involves physical flow, we hypothesized that the effects of submergence on plants could change when combined with physical flow. In this study, we analyzed the growth and transcriptome of Arabidopsis thaliana exposed to submergence or flooding with physical flow. Plants exposed to flooding with physical flow had smaller rosette diameters, especially at faster flow rates. Transcriptome analysis revealed that “defense response” transcripts were highly up-regulated in response to flooding with physical flow. In addition, up-regulation of transcripts encoding ROS-producing enzymes, SA synthesis, JA synthesis, and ethylene signaling was more pronounced under flooding with physical flow when compared to submergence. Although H2O2 accumulation changed in response to submergence or flooding with physical flow, it did not lead to lipid peroxidation, suggesting a role for ROS as signaling molecules under these conditions. Multiple regression analysis indicated possible links between rosette diameter under flooding with physical flow and the expression of Rbohs and SA synthesis transcripts. These findings suggest that pathogen defense responses, regulated by SA and ROS signaling, play crucial roles in plant responses to flooding with physical flow.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.