Welcome to the Maruta group!
Our research group is seeking national and international students who relish collaborative research. For international students, one avenue of joining our group is to secure a MEXT scholarship (but it is not an easy way...) and I will serve as the host laboratory. If you exhibit a strong passion and motivation for the research we conduct, please feel free to reach out to Maruta at any time. Although Matsue, our current residence, is not a metropolis, it boasts a lush natural landscape surrounded by picturesque seas and mountains. In comparison to urban areas, the cost of housing is relatively affordable and there are numerous supermarkets and tourist destinations, making it a highly hospitable location to reside. Shimane University also has a significant population of international students.
Photo: Welcome party for new members (2022)
We are a very small group, but we all work together harmoniously, happily, and energetically. The best way to enjoy and advance research is through active discussion, and for this reason, it is important to facilitate communication within the team through team-building activities. We are waiting for you.
Research Backgrounds
I am conducting research focused on the acclimation of plants to their surroundings, with a particular emphasis on the interplay between vitamin C (ascorbate) and reactive oxygen species (ROS). One of the central scientific questions that continue to intrigue me is the reason why plants exhibit high concentrations of vitamin C. While it is widely recognized that plants serve as a crucial source of vitamin C for human consumption, it remains enigmatic as to why plants themselves require such substantial quantities of this compound. To unravel this mystery, it is imperative to comprehend the intricate relationship between ascorbate and ROS. Previously, ROS were perceived as toxic molecules that were generated in response to stress in plant cells. However, with the advancement of research on oxidative stress, it is now widely acknowledged that plants possess a remarkable ability to precisely regulate ROS levels and employ them as signals for various physiological processes, including stress acclimation. Ascorbate acts as a potent antioxidant, and through evolution, plants have developed ascorbate peroxidase (APX), which allows them to utilize ascorbate for scavenging H2O2. The idea that plants accumulate ascorbate to mitigate oxidative damage caused by ROS is well established. However, does the high accumulation of ascorbate disrupt the signaling function of ROS? If the answer is yes, ascorbate may impede plant acclimation to the environment. Conversely, if the answer is no, then plants must possess a mechanism that allows them to maintain ROS signaling function while simultaneously accumulating high concentrations of ascorbate. At present, the answer to this question remains elusive, but I firmly believe that obtaining a clear understanding of this issue is crucial for breeding crops with high-stress tolerance. Plants possess multiple unique ascorbate metabolic pathways not found in other organisms, enabling them to utilize this compound as an exceptional redox buffer. I am systematically elucidating these elegant pathways' molecular mechanisms and physiological significance to advance our knowledge of the functional interactions between ascorbate and ROS.
1) Plant-Specific Ascorbate Metabolism
• Ascorbate Biosynthesis
Our research on the biosynthesis of ascorbate has been conducted in collaboration with Professor Ishikawa (within the same laboratory). We have made substantial contributions to the clarification of biosynthetic pathways in plants. Recently, our focus has been on the control mechanism of biosynthesis by light, and we are currently conducting further investigations. Our recent review article (Maruta, 2022, Biosci Biotechnol Biochem) provides more detailed information on this topic, including our research background and current issues.
• Ascorbate Peroxidase
Ascorbate Peroxidase (APX) is a distinctive enzyme, commonly observed in eukaryotic photosynthetic organisms, that utilizes ascorbate as an electron donor to eliminate H2O2. Although the reaction between ascorbate and H2O2 is inherently slow, the presence of APX in plants facilitates the metabolic process of H2O2 utilization through ascorbate. Higher plants exhibit various isoforms of APX, distributed in the cytosol, mitochondria, peroxisomes, and chloroplasts (stroma and thylakoid membranes). Historically, the predominant view of ROS was as mere cytotoxic molecules, resulting in a focus on APX's role as a protective enzyme against oxidative stress. While this perspective is not entirely erroneous, recent findings suggest that plants possess redundant defense mechanisms against oxidative stress and APX is merely one of them (e.g., Kameoka & Okayasu et al., 2021, Plant J). Rather, the prevailing view is that APX regulates H2O2 signaling (see Maruta et al., 2016, Plant Cell Physiol). Furthermore, it has been suggested that its role as an ascorbate oxidase, rather than as an H2O2 scavenging enzyme, may be crucial in orchestrating H2O2 signaling (in preparation). We have recently paid particular attention to the function of the APX from this perspective. Additionally, we are also interested in investigating the functional overlap and differentiation between APX and other peroxidases in chloroplasts.
• Ascorbate Recycling
As described above, plants utilize ascorbate as a potent antioxidant and electron donor for APX to preserve cellular redox balance. This means the rapid rate of oxidation of ascorbate in plant cells. Given the instability of oxidized forms of ascorbate, recycling ascorbate from the oxidized forms is crucial to accumulate substantial concentrations of the antioxidant. The recycling process of ascorbate in plants encompasses the participation of monodehydroascorbate reductase (MDAR) and dehydroascorbate reductase (DHAR). MDAR reduces monodehydroascorbate (MDHA) to ascorbate using NAD(P)H, whereas DHAR utilizes glutathione (GSH) to reduce dehydroascorbate (DHA). The isoforms of these enzymes operate within the intracellular compartment in which APX is located and uphold its function. The redundancy of these enzymes establishes a robust ascorbate recycling system and enables elevated accumulation of ascorbate. Despite its significance, the physiological importance of these enzymes has yet to be fully explored. One of our recent topics is the non-enzymatic reduction of DHA by GSH, which supplements the DHAR enzymatic reaction. In essence, the cooperation between DHAR and GSH determines the capacity to recycle ascorbate, particularly in chloroplasts (Terai et al., 2020, Plant Physiol; Hamada et al., 2023, Plant J). The physiological role of MDAR remains unclear (see Tanaka & Takahashi et al., 2021, Antioxidants), so our current focus is the interplay between the MDAR and GSH-dependent pathways.
• Ascorbate Degradation
With our advancing comprehension of the ascorbate redox cycle in plant cells, our focus has shifted to the investigation of ascorbate degradation. Ascorbate degradation commences with dehydroascorbate (DHA) and is anticipated to be influenced by the redox turnover of ascorbate inside and outside the cell. Of particular interest is the observation that ascorbate degradation is pronounced in the dark, which may have a close association with senescence. We are also interested in the potential physiological functions and the fate of the degradation products of ascorbate. To address these issues, we are utilizing the knowledge and techniques we have acquired through our studies of the ascorbate redox cycle. We anticipate that these studies will furnish strategies to mitigate the decrease in vitamin C content in vegetable post-harvest.
• Functional Relationship between Ascorbate and Other Antioxidants
Ascorbate constitutes the preeminent water-soluble antioxidant in plants, yet other antioxidants also play a substantial role in the preservation of cellular redox homeostasis. Such antioxidants include glutathione and tocopherol. Plants also abound with flavonoids, whose function as antioxidants in plants remains a matter of debate. Nonetheless, they exert a shielding effect on ultraviolet and visible light, reducing the incidence of light stress injury. These antioxidants do not operate in isolation but are interconnected; for instance, glutathione is implicated in the recycling of ascorbate, and ascorbate is necessary for the regeneration of tocopherols. We have recently commenced studying the interplay and redundancy of these antioxidants and are also investigating the extent to which they contribute to the dissipation of reducing power.
2) ROS Signaling and Stress Acclimation
• Chloroplast-to-Nucleus H2O2 Signaling
Chloroplasts constitute the primary source of reactive oxygen species (ROS) in plant cells. It has been demonstrated that ROS derived from chloroplasts can act as retrograde signals from chloroplast to the nucleus, thereby modulating the expression of nuclear-encoded genes. In this context, hydrogen peroxide (H2O2), which is comparatively stable and permeable to membranes, plays a crucial role as a mobile signal. Our team has contributed to the elucidation of the regulatory mechanism of gene expression by chloroplast-derived H2O2, using a conditional expression repressor system of tAPX (see Maruta et al., 2012, J. Biol. Chem.). While we are not currently investigating this aspect, we are devising strategies to unveil the regulatory mechanisms and targets of H2O2 signaling in chloroplasts.
• Oxidative Stress-Induced Programmed Cell Death
Oxidative stress elicits programmed cell death, which is notably observed in Arabidopsis mutants (cat2) deficient in the major catalase. I have previously worked with Professor Frank Van Breusegem at Ghent University/VIB to unravel the molecular mechanisms of cell death in cat2, and our collaboration on this project is ongoing. Specifically, we have identified several genes required for cell death in cat2 using forward and reverse genetic approaches and are currently investigating their physiological function. One of our interests is the molecular mechanism underlying glutathione oxidation that occurs in cat2 and its downstream signaling events.