Kyushu University [kensuke kusumi (Lecturer) Faculty of Sciences, Department of Biology]

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kensuke kusumi
Lecturer
Informational biology
Department of Biology
Faculty of Sciences
Last modified date：2023.12.06

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Department of Systems Life Sciences
Graduate School of Systems Life Sciences

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Department of Biology
School of Sciences

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Plant Frontier Research Center

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1.	Kazuhiro Ito, Doshun Ito, Mina Goto, Sae Suzuki, Shinji Masuda, Koh Iba, Kensuke Kusumi, Regulation of ppGpp synthesis and its impact on chloroplast biogenesis during early leaf development in rice, Plant and Cell Physiology, 10.1093/pcp/pcac053, 63, 7, 919-931, 2022.04, [URL], Guanosine tetraphosphate (ppGpp) is known as an alarmone that mediates bacterial stress responses. In plants, ppGpp is synthesized in chloroplasts from GTP and ATP and functions as a regulator of chloroplast gene expression to affect photosynthesis and plant growth. This observation indicates that ppGpp metabolism is closely related to chloroplast function, but the regulation of ppGpp and its role in chloroplast differentiation are not well understood. In rice, ppGpp directly inhibits plastidial guanylate kinase (GKpm), a key enzyme in GTP biosynthesis. GKpm is highly expressed during early leaf development in rice, and the GKpm-deficient mutant, virescent-2 (v2), develops chloroplast-deficient chlorotic leaves under low-temperature conditions. To examine the relationship between GTP synthesis and ppGpp homeostasis, we generated transgenic rice plants over-expressing RSH3, a protein known to act as a ppGpp synthase. When RSH3 was overexpressed in v2, the leaf chlorosis was more severe. Although the RSH3 overexpression in the wild type caused no visible effects, pulse amplitude modulation fluorometer measurements indicated that photosynthetic rates were reduced in this line. This finding implies that the regulation of ppGpp synthesis in rice is involved in the maintenance of the GTP pool required to regulate plastid gene expression during early chloroplast biogenesis. We further investigated changes in the expressions of RelA/SpoT Homolog (RSH) genes encoding ppGpp synthases and hydrolases during the same period. Comparing the expression of these genes with the cellular ppGpp content suggests that the basal ppGpp level is determined by the antagonistic action of multiple RSH enzymatic activities during early leaf development in rice..
2.	Wataru Yamori, Kensuke Kusumi, Koh Iba, Ichiro Terashima, Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice, Plant Cell and Environment, 10.1111/pce.13725, 2020.01, A close correlation between stomatal conductance and the steady-state photosynthetic rate has been observed for diverse plant species under various environmental conditions. However, it remains unclear whether stomatal conductance is a major limiting factor for the photosynthetic rate under naturally fluctuating light conditions. We analysed a SLAC1 knockout rice line to examine the role of stomatal conductance in photosynthetic responses to fluctuating light. SLAC1 encodes a stomatal anion channel that regulates stomatal closure. Long exposures to weak light before treatments with strong light increased the photosynthetic induction time required for plants to reach a steady-state photosynthetic rate and also induced stomatal limitation of photosynthesis by restricting the diffusion of CO<sub>2</sub> into leaves. The slac1 mutant exhibited a significantly higher rate of stomatal opening after an increase in irradiance than wild-type plants, leading to a higher rate of photosynthetic induction. Under natural conditions, in which irradiance levels are highly variable, the stomata of the slac1 mutant remained open to ensure efficient photosynthetic reaction. These observations reveal that stomatal conductance is important for regulating photosynthesis in rice plants in the natural environment with fluctuating light..
3.	Kensuke Kusumi, Ayana Hashimura, Yoshiko Yamamoto, Juntaro Negi, Koh Iba, Contribution of the S-type anion channel SLAC1 to stomatal control and its dependence on developmental stage in rice, Plant and Cell Physiology, 10.1093/pcp/pcx142, 58, 12, 2085-2094, 2017.06, Rice production depends on water availability and carbon fixation by photosynthesis. Therefore, optimal control of stomata, which regulate leaf transpiration and CO₂ absorption, is important for high productivity. SLOW ANION CHANNEL-ASSOCIATED 1 (SLAC1) is an S-type anion channel protein that controls stomatal closure in response to elevated CO₂. Rice slac1 mutants showed significantly increased stomatal conductance (g_s) and enhanced CO₂ assimilation. To discern the contribution of stomatal regulation to rice growth, we compared g_s in the wild type (WT) and two mutants, slac1 and the dominant-positive mutant SLAC1-F461A, which expresses a point mutation causing an amino acid substitution (F461A) in SLAC1, at different growth stages. Because the side group of F461 is estimated to function as the channel gate, stomata in the SLAC1-F461A mutant are expected to close constitutively. All three lines had maximum g_s during the tillering stage, when the g_s values were 50% higher in slac1 and 70% lower in SLAC1-F461A, compared with the WT. At the tillering stage, the g_s values were highest in the first leaves at the top of the stem and lower in the second and third leaves in all three lines. Both slac1 and SLAC1-F461A retained the ability to change g_s in response to the day–night cycle, and showed differences in tillering rate and plant height compared with the WT, and lower grain yield. These observations show that SLAC1 plays a crucial role in regulating stomata in rice at the tillering stage..
4.	Kensuke Kusumi, Koh Iba, Establishment of the chloroplast genetic system in rice during early leaf development and at low temperatures, Frontiers in Plant Science, 10.3389/fpls.2014.00386, 5, 386, 2014.07, [URL], Chloroplasts are the central nodes of the metabolic network in leaf cells of higher plants, and the conversion of proplastids into chloroplasts is tightly coupled to leaf development. During early leaf development, the structure and function of the chloroplasts differ greatly from those in a mature leaf, suggesting the existence of a stage-specific mechanism regulating chloroplast development during this period. Here, we discuss the identification of the genes affected in low temperature-conditional mutants of rice (Oryza sativa). These genes encode factors involved in chloroplast rRNA regulation (NUS1), and nucleotide metabolism in mitochondria, chloroplasts and cytosol (V2, V3, ST1). These genes are all preferentially expressed in the early leaf developmental stage P4, and depleting them causes altered chloroplast transcription and translation, and ultimately leaf chlorosis. Therefore, it is suggested that regulation of cellular nucleotide pools and nucleotide metabolism is indispensable for chloroplast development under low temperatures at this stage. This review summarizes the current understanding of these factors and discusses their roles in chloroplast biogenesis..
5.	Yuhta Nomura, Atsushi Izumi, Yoshinori Fukunaga, Kensuke Kusumi, Koh Iba, Seiya Watanabe, Yoichi Nakahira, Andreas P. M. Weber, Akira Nozawa, Yuzuru Tozawa, Diversity in Guanosine 3′,5′-Bisdiphosphate (ppGpp) Sensitivity Among Guanylate Kinases of Bacteria and Plants. , Journal of Biological Chemistry, 10.1074/jbc.M113.534768., 289, 15631-15641, 2014.04, [URL], The guanosine 3′,5′-bisdiphosphate (ppGpp) signaling system is shared by bacteria and plant chloroplasts, but its role in plants has remained unclear. Here we show that guanylate kinase (GK), a key enzyme in guanine nucleotide biosynthesis that catalyzes the conversion of GMP to GDP, is a target of regulation by ppGpp in chloroplasts of rice, pea, and Arabidopsis. Plants have two distinct types of GK that are localized to organelles (GKpm) or to the cytosol (GKc), with both enzymes being essential for growth and development. We found that the activity of rice GKpm in vitro was inhibited by ppGpp with a Ki of 2.8 μM relative to the substrate GMP, whereas the Km of this enzyme for GMP was 73 μM. The IC50 of ppGpp for GKpm was ~10 μM. In contrast, the activity of rice GKc was insensitive to ppGpp, as was that of GK from baker′s yeast, which is also a cytosolic enzyme. These observations suggest that ppGpp plays a pivotal role in the regulation of GTP biosynthesis in chloroplasts through specific inhibition of GKpm activity, with the regulation of GTP biosynthesis in chloroplasts thus being independent of that in the cytosol. We also found that GKs of Escherichia coli and Synechococcus elongatus PCC 7942 are insensitive to ppGpp, in contrast to the ppGpp sensitivity of the Bacillus subtilis enzyme. Our biochemical characterization of GK enzymes has thus revealed a novel target of ppGpp in chloroplasts and has uncovered diversity among bacterial GKs with regard to regulation by ppGpp..
6.	Mimi Hashimoto-Sugimoto, Juntaro Negi, Kensuke Kusumi, Koh Iba, New Approaches to the Biology of Stomatal Guard Cells, 10.1093/pcp/pct145, 55, 2, 241-250, 2014.02, [URL], CO2 acts as an environmental signal that regulates stomatal movements. High CO2 concentrations reduce stomatal aperture, whereas low concentrations trigger stomatal opening. In contrast to our advanced understanding of light and drought stress responses in guard cells, the molecular mechanisms underlying stomatal CO2 sensing and signaling are largely unknown. Leaf temperature provides a convenient indicator of transpiration, and can be used to detect mutants with altered stomatal control. To identify genes that function in CO2 responses in guard cells, CO2-insensitive mutants were isolated through high-throughput leaf thermal imaging. The isolated mutants are categorized into three groups according to their phenotypes: (i) impaired in stomatal opening under low CO2 concentrations; (ii) impaired in stomatal closing under high CO2 concentrations; and (iii) impaired in stomatal development. Characterization of these mutants has begun to yield insights into the mechanisms of stomatal CO2 responses. In this review, we summarize the current status of the field and discuss future prospects..
7.	Negi, J., Moriwaki, K., Konishi, M., Yokoyama, R., Nakano, T., Kusumi, K., Hashimoto-Sugimoto, M., Schroeder, J.I., Nishitani, K., Yanagisawa, S. and Iba, K. , A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis., Current Biology, 10.1093/pcp/pct145, 55, 241-250, 2013.02, Stomata are highly specialized organs that consist of pairs of guard cells and regulate gas and water vapor exchange in plants [1-3]. Although early stages of guard cell differentiation have been described [4-10] and were interpreted in analogy to processes of cell type differentiation in animals [11], the downstream development of functional stomatal guard cells remains poorly understood. We have isolated an Arabidopsis mutant, stomatal carpenter 1 (scap1), that develops irregularly shaped guard cells and lacks the ability to control stomatal aperture, including CO2-induced stomatal closing and light-induced stomatal opening. SCAP1 was identified as a plant-specific Dof-type transcription factor expressed in maturing guard cells, but not in guard mother cells. SCAP1 regulates the expression of genes encoding key elements of stomatal functioning and morphogenesis, such as K(+) channel protein, MYB60 transcription factor, and pectin methylesterase. Consequently, ion homeostasis was disturbed in scap1 guard cells, and esterification of extracellular pectins was impaired so that the cell walls lining the pores did not mature normally. We conclude that SCAP1 regulates essential processes of stomatal guard cell maturation and functions as a key transcription factor regulating the final stages of guard cell differentiation..
8.	Kusumi, K., Hirotsuka, S., Kumamaru, T. and Iba, K. , Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1, a guard cell anion channel protein., Journal of Experimental Botany, 10.1093/jxb/ers216, 63, 15, 5635-5644, 2012.08, [URL], In rice (Oryza sativa L.), leaf photosynthesis is known to be highly correlated with stomatal conductance; however, it remains unclear whether stomatal conductance dominantly limits the photosynthetic rate. SLAC1 is a stomatal anion channel protein controlling stomatal closure in response to environmental [CO2]. In order to examine stomatal limitations to photosynthesis, we isolated and characterized a SLAC1-deficient mutant of rice. A TILLING screen of NMU-derived mutant lines was conducted for the rice SLAC1 ortholog gene Os04g0674700, and four mutant lines containing mutations within the open reading frame were obtained. A second screen using an infrared thermography camera revealed that one of the mutants, named slac1, had a constitutive low-leaf-temperature phenotype. Measurement of leaf gas exchange showed that slac1 plants grown in the greenhouse had significantly higher stomatal conductance (gs), rates of photosynthesis (A) and ratios of internal [CO2] to ambient [CO2] (Ci/Ca) compared to wild-type plants, whereas there was no significant difference in the response of photosynthesis to internal [CO2] (A/Ci curves). These observations demonstrate that in well-watered conditions, stomatal conductance is a major determinant of photosynthetic rate in rice. .
9.	Kusumi, Kensuke; Sakata, Chikako; Nakamura, Takahiro; Kawasaki, Shinji; Yoshimura, Atsushi; Iba, Koh, A plastid protein NUS1 is essential for build-up of the genetic system for early chloroplast development under cold stress condition, The Plant Journal, 2011.09.
10.	Kusumi, K., Hirotsuka, S., Shimada, H., Chono, Y., Matsuda, O. and Iba, K., Contribution of chloroplast biogenesis to carbon-nitrogen balance during early leaf development in rice, J. Plant Res. , 123, 4, 617-622, 2010.01.
11.	Yoo, S-C., Cho, S-H., Sugimoto, H., Li, Jinjie., Kusumi, K., Koh, H-J., Iba, K. and Paek, N-C. , Rice Virescent-3 and Stripe-1 encoding the large and small subunits of ribonucleotide reductase are required for chloroplast biogenesis during early leaf development., Plant Physiol. , 150: 388-401, 2009.05.
12.	Sugimoto, H., Kusumi, K., Noguchi, K., Yano, M., Yoshimura, A., and Iba, K., The rice nuclear gene, VIRESCENT 2, is essential for chloroplast development and encodes a novel type of guanylate kinase targeted to plastids and mitochondria., Plant Journal, 52: 512-527, 2007.11.
13.	Kusumi, K., Yaeno, T., Kojo, K., Hirayama, M., Hirokawa, D., Yara, A., and Iba, K., The role of salicylic acid in the glutathione-mediated protection against photo-oxidative stress in rice, Physiol. Plant., 128: 651-661, 2006.12.
14.	K. Kusumi, A. Yara, N. Mitsui, Y. Tozawa, and K. Iba, Characterization of a rice nuclear-encoded plastid RNA polymerase gene OsRpoTp, Plant Cell Physiol., 10.1093/pcp/pch133, 45, 9, 1194-1201, 45 (9) : 1194-1201 (2004), 2004.09.

1.	sORF, sorfc03, associated with Nitrogen metabolism in Arabidopsis.
2.	The stringent response regulator ppGpp contributes to the regulation of plastidial GTP pool during chloroplast differentiation in rice.
3.	Arabidopsis short ORF, SORFC03 is involved in the repression of lateral root growth under high-nitrogen conditions.
4.	sORF, sorfc03, associated with Nitrogen metabolism in Arabidopsis.
5.	Kazuhiro Ito, Yuki Hisanaga, Kousuke Hanada, Koh Iba, Kensuke Kusumi, An Arabidopsis short ORF, SORFC03, is involved in the regulation of nitrogen-dependent lateral root developmen, The International Conference on Arabidopsis Research (ICAR), 2021.06, Nitrogen (N) is an important factor for the basis of metabolism for plant growth. While knowledge and understanding of N metabolism has improved considerably over the last several decades, most of the key factors involved in these processes still remain uncharacterized. Recently, short open reading frames (sORFs) were found in the known intergenic regions in eukaryotes. In Arabidopsis, about 8,000 sORFs have already been identified, however, most of them remain uncharacterized. In this study, we characterized one of these sORFs, sorfc03, which is suggested to be involved in the regulation of lateral root (LR) development associated with N metabolism..
6.	sORFs associated with Nitrogen metabolism in Arabidopsis.
7.	sORFs associated with Nitrogen metabolism in Arabidopsis.
8.	sORFs associated with Nitrogen metabolism in Arabidopsis.
9.	sORFs associated with Nitrogen metabolism in Arabidopsis.
10.	sORFs associated with Nitrogen metabolism in Arabidopsis.
11.	sORFs associated with Nitrogen metabolism in Arabidopsis.
12.	sORFs associated with CO2 adaptation in Arabidopsis.
13.	楠見健介, 橋村綾菜, 射場厚, Contribution of guard cell SLAC1 anion channel to the growth stage-dependent stomatal regulation in rice , 17th International Congress on Photosynthesis Research, 2016.08, [URL], Rice cultivation mainly depends on soil water availability as well as on carbon fixation by photosynthesis. Therefore, optimal control of stomata, which regulates leaf respiration and CO2 absorption simultaneously, is crucial for healthy growth. SLAC1 is a stomatal anion channel protein controlling stomatal closure in response to environmental [CO2]. SLAC1-deficient mutant of rice, slac1, exhibited significant increase in stomatal conductance (gs) with enhanced CO2 assimilation, showing that this channel plays a major role in stomatal closure in rice. In this study, in order to clarify contribution of the SLAC1 to stomatal regulation, we investigated changes in the stomatal conductance during the vegetative growth stage of rice, and compared them among the wild type (WT), slac1 and SLAC1-F461A, which expressed a dominant point mutation (F461A) causing constitutive stomatal closure. .
14.	SLAC1 is a stomatal anion channel protein controlling stomatal closure. We previously reported that the SLAC1-deficient mutant of rice, slac1, had constitutively higher stomatal conductance compared to wild type. On the other hand, change in the stomatal conductance in response to some environmental cues, such as day-night cycle and change in the external [CO2], still remained in slac1, suggesting the possible existence of SLAC1-independent mechanism regulating stomatal closure. In this study, we examined transgenic rice, SLAC1-F461A, which expressed a point mutation causing an amino acid substitution (F461A) in SLAC1. Because side group of F461 is estimated to function as the channel gate, stomata in the SLAC1-F461A are expected to close constitutively. SLAC1-F461A plant had a high-leaf-temperature phenotype, and measurement of leaf transpiration showed that the stomatal conductance of young leaves of the SLAC1-F461A was about 70% lower than that of wild type. These indicate that in the SLAC1-F461A SLAC1 channels are always open and the stomata close constitutively. We will discuss the effect of the mutation on the growth and photosynthesis and contribution of SLAC1 to stomatal regulation during rice growth..
15.	Short open reading frames associated with CO2 adaptation in Arabidopsis.
16.	SLAC1 is a stomatal anion channel protein controlling stomatal closure. We previously reported that the SLAC1-deficient mutant of rice, slac1, had constitutively higher stomatal conductance compared to wild type. On the other hand, change in the stomatal conductance in response to some environmental cues, such as day-night cycle and change in the external [CO2], still remained in slac1, suggesting the possible existence of SLAC1-independent mechanism regulating stomatal closure. In this study, we examined transgenic rice, SLAC1-F461A, which expressed a point mutation causing an amino acid substitution (F461A) in SLAC1. Because side group of F461 is estimated to function as the channel gate, stomata in the SLAC1-F461A are expected to close constitutively. SLAC1-F461A plant had a high-leaf-temperature phenotype, and measurement of leaf transpiration showed that the stomatal conductance of young leaves of the SLAC1-F461A was about 70% lower than that of wild type. These indicate that in the SLAC1-F461A SLAC1 channels are always open and the stomata close constitutively. We will discuss the effect of the mutation on the growth and photosynthesis and contribution of SLAC1 to stomatal regulation during rice growth..
17.	楠見健介, 射場厚, Modulation and maintenance of chloroplast genetic system during early leaf development and at low temperatures in rice, Japanese-Finnish Seminar 2014 "Design of Superior Machinery of Light Energy Conversion in Photosynthetic Organisms", 2014.10, Chloroplast biogenesis is most significant during the changes in cellular organization associated with leaf development in higher plants. During early leaf development, the structure and function of the chloroplasts differ greatly from those in a mature leaf, suggesting the existence of a stage-specific mechanism regulating chloroplast development during this period. We have analyzed genes involved specifically in early chloroplast biogenesis by using low temperature-conditional mutants of rice (Oryza sativa). These genes encode factors involved in chloroplast rRNA regulation (NUS1), and nucleotide metabolism in mitochondria, chloroplasts and cytosol (V2, V3, ST1). These are all preferentially expressed in the early leaf developmental stage P4, and depleting them causes altered chloroplast transcription and translation, and ultimately leaf chlorosis. Accordingly, regulation of cellular nucleotide pools and nucleotide metabolism is likely to be involved in the chloroplast biogenesis under low temperatures at this stage. Current understanding of these factors and organization of them during early leaf development will be discussed..
18.	SLAC1 is a stomatal anion channel protein controlling stomatal closure in response to environmental [CO2]. Our previous study showed that the SLAC1-deficient mutant of rice, slac1, had higher stomatal conductance, higher rates of photosynthesis and lower leaf temperature compared to the wild-type plants, revealing that SLAC1 was involved in stomatal closure in rice, as was observed in Arabidopsis. On the other hand, change in the stomatal conductance in response to day-night cycle as well as to the external [CO2] still remained in the slac1 mutant, suggesting the possible existence of SLAC1-independent mechanism regulating stomatal closure. To estimate the contribution of SLAC1 to stomatal closure, we examined the effect of different developmental stage and different leaf position on SLAC1 gene expression and the stomatal conductance in the slac1 mutant and wild-type plants. Our data suggest the tissue-specificity and age-dependency of SLAC1 function in the stomatal closure in rice..
19.	In rice (Oryza sativa L.), leaf photosynthesis is known to be highly correlated with stomatal conductance. Hower, it remains unclear whether stomatal conductance dominantly limits the photosynthetic rate. SLAC1 is a stomatal anion channel protein controlling stomatal closure in response to environmental [CO2]. In order to examine stomatal limitations to photosynthesis, we isolated and characterized a SLAC1-deficient mutant of rice, slac1. The slac1 plant had a constitutive low-leaf-temperature phenotype. Measurement of leaf gas exchange showed that slac1 plants had significantly higher stomatal conductance (gs), rates of photosynthesis (A) and ratios of internal [CO2] to ambient [CO2] (Ci/Ca) compared to wild-type plants, whereas there was no significant difference in the response of photosynthesis to internal [CO2] (A/Ci curves). These observations demonstrate that stomatal conductance is a major determinant of photosynthetic rate in rice..
20.	Characterization of SLAC1-deficient mutant of rice.
21.	Regulation of chloroplast biogenesis during early stages of leaf development in rice., [URL].