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Junko Kusumi Last modified date:2023.09.26

Graduate School
Undergraduate School

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Academic Degree
Doctor of Science
Country of degree conferring institution (Overseas)
Field of Specialization
Molecular evolution, Population Genetics
Outline Activities
Evolutionary genetics (Molecular evolution/population genetics), focusing on the evolutionary changes at the molecular level
Research Interests
  • Co-evolution of the symbiosis system of hydras and their symbionts
    keyword : hydra, green alga, symbiosis
  • Co-evolution, Co-speciation of figs and figwasps
    keyword : Population genetics, Molecular evolution, Molecular phylogeny, Evolution of mutualisms; plant insect interactions,
  • A new model of molecular compensatory evolution
    keyword : compensatory evolution population genetics
  • Population genetic analysis of a widespread coniferous tree Taxodium distichum [L.] Rich. in the Mississippi River Alluvial Valley and Florida
    keyword : Taxodium distichum、genetic diversity, nucleotide polymorphism, microsatellite
Academic Activities
1. Ryo Miyokawa, Hiroyuki J Kanaya, Taichi Q Itoh, Yoshitaka Kobayakawa, Junko Kusumi, Immature symbiotic system between horizontally transmitted green algae and brown hydra., Scientific reports, 10.1038/s41598-021-82489-6, 11, 1, 2921-2921, 2021.02, Some strains of brown hydra (Hydra vulgaris) are able to harbor the green algae Chlorococcum in their endodermal epithelial cells as symbionts. However, the relationship between brown hydra and chlorococcum is considered to be incipient symbiosis because most artificially introduced symbionts are not stable and because symbiotic H. vulgaris strains are rare in the wild. In this study, we compared the gene expression levels of the newly established symbiotic hydra (strain 105G), the native symbiotic strain (J7), and their non-symbiotic polyps to determine what changes would occur at the early stage of the evolution of symbiosis. We found that both the 105G and J7 strains showed comparable expression patterns, exhibiting upregulation of lysosomal enzymes and downregulation of genes related to nematocyte development and function. Meanwhile, genes involved in translation and the respiratory chain were upregulated only in strain 105G. Furthermore, treatment with rapamycin, which inhibits translation activity, induced the degeneration of the symbiotic strains (105G and J7). This effect was severe in strain 105G. Our results suggested that evolving the ability to balance the cellular metabolism between the host and the symbiont is a key requirement for adapting to endosymbiosis with chlorococcum..
2. Junko Kusumi, Motoshi Ichinose, Masaru Iizuka, Effects of gene duplication, epistasis, recombination and gene conversion on the fixation time of compensatory mutations, Journal of Theoretical Biology, 10.1016/j.jtbi.2019.02.001, 467, 134-141, 2019.04, Gene duplication is one of the major mechanisms of molecular evolution. Gene duplication enables copies of a gene to accumulate mutations through functional redundancy. If a gene encodes a specific protein that interacts with other proteins, RNA, or DNA, the relaxation of selective constraints caused by gene duplication might contribute to the fixation of compensatory mutations that occur at the interacting sites. In this study, we investigate the effect of gene duplication, epistasis among the duplicated copies and gene conversion on the fixation time of compensatory mutations by extending the original model of compensatory evolution proposed by Kimura in 1985. Our simulation results reveal that the time to fixation of compensatory mutations can be decreased remarkably by gene duplication if one of the duplicated loci can completely mask the deleterious effects of a mutation that occurs at the other locus. Conversely, the fixation time can be increased by gene duplication if such functional compensation is weak. We also show that the combination of the degree of functional compensation and the rate of gene conversion between duplicate loci have contrasting effects on the time to fixation of compensatory mutations..
3. Natsuki Moriguchi, Kentaro Uchiyama, Ryutaro Miyagi, Etsuko Moritsuka, Aya Takahashi, Koichiro Tamura, Yoshihiko Tsumura, Kosuke M. Teshima, Hidenori Tachida, Junko Kusumi, Inferring the demographic history of Japanese cedar, Cryptomeria japonica, using amplicon sequencing, Heredity, 10.1038/s41437-019-0198-y, 2019.01, The evolution of a species depends on multiple forces, such as demography and natural selection. To understand the trajectory and driving forces of evolution of a target species, it is first necessary to uncover that species’ population history, such as past and present population sizes, subdivision and gene flow, by using appropriate genetic markers. Cryptomeria japonica is a long-lived monoecious conifer species that is distributed in Japan. There are two main lines (omote-sugi and ura-sugi), which are distinguished by apparent differences in morphological traits that may have contributed to their local adaptation. The evolution of these morphological traits seems to be related to past climatic changes in East Asia, but no precise estimate is available for the divergence time of these two lines and the subsequent population dynamics in this species. Here, we analyzed the nucleotide variations at 120 nuclear genes in 94 individuals by using amplicon sequencing in combination with high-throughput sequencing technologies. Our analysis indicated that the population on Yakushima Island, the southern distribution limit of C. japonica in Japan, diverged from the other populations 0.85 million years ago (MYA). The divergence time of the other populations on mainland Japan was estimated to be 0.32 MYA suggesting that the divergence of omote-sugi and ura-sugi might have occurred before the last glacial maximum. Although we found modest levels of gene flow between the present populations, the long-term isolation and environmental heterogeneity caused by climatic changes might have contributed to the differentiation of the lines and their local adaptation..
4. Yuka Ikezaki, Yoshihisa Suyama, Beth A. Middleton, Yoshihiko Tsumura, Kosuke Teshima, Hidenori Tachida, Junko Kusumi, Inferences of population structure and demographic history for Taxodium distichum, a coniferous tree in North America, based on amplicon sequencing analysis, American journal of Botany, 10.3732/ajb.1600046, 103, 11, 2016.12, PREMISE OF THE STUDY: Studies of natural genetic variation can elucidate the genetic basis of phenotypic variation and the past population structure of species. Our study species, Taxodium distichum, is a unique conifer that inhabits the ood plains and swamps of North America. Morphological and eco- logical di erences in two varieties, T. distichum var. distichum (bald cypress) and T. distichum var. imbricarium (pond cypress), are well known, but little is known about the level of genetic di erentiation between the varieties and the demographic history of local populations.
METHODS: We analyzed nucleotide polymorphisms at 47 nuclear loci from 96 individuals collected from the Mississippi River Alluvial Valley (MRAV), and Gulf Coastal populations in Texas, Louisiana, and Florida using high-throughput DNA sequencing. Standard population genetic statistics were calculated, and demographic parameters were estimated using a composite-likelihood approach.
KEY RESULTS: Taxodium distichum in North America can be divided into at least three genetic groups, bald cypress in the MRAV and Texas, bald cypress in Florida, and pond cypress in Florida. The levels of genetic di erentiation among the groups were low but signi cant. Several loci showed the signatures of positive selection, which might be responsible for local adaptation or varietal di erentiation.
CONCLUSIONS: Bald cypress was genetically di erentiated into two geographical groups, and the boundary was located between the MRAV and Florida. This di erentiation could be explained by population expansion from east to west. Despite the overlap of the two varieties’ ranges, they were genetically di erentiated in Florida. The estimated demographic parameters suggested that pond cypress split from bald cypress during the late Miocene..
5. Junko Kusumi, Motoshi Ichinose, Masasuke Takefu, Robert Piskol, Wolfgang Stephan, Masaru Iizuka, A model of compensatory molecular evolution involving multiple sites in RNA molecules, Journal of Theoretical Biology, doi:10.1016/j.jtbi.2015.10.008, 388, 96-107, 2016.01, Consider two sites under compensatory fitness interaction, such as a Watson–Crick base pair in an RNA helix or two interacting residues in a protein. A mutation at any one of these two sites may reduce the fitness of an individual. However, fitness may be restored by the occurrence of a second mutation at the other site. Kimura modeled this process using a two-locus haploid fitness scheme with two alleles at each locus. He predicted that compensatory evolution following this model is very rare unless selection against the deleterious single mutations is weak and linkage between the interacting sites is tight. Here we investigate the question whether the rate of compensatory evolution increases if we take the context of the two directly interacting sites into account. By “context”, we mean the effect of neighboring sites in an RNA helix. Interaction between the focal pair of sites under consideration and the context may lead to so-called indirect compensation. Thus, extending Kimura׳s classical model of compensatory evolution, we study the effects of both direct and indirect compensation on the rate of compensatory evolution. It is shown that the effects of indirect compensation are very strong. We find that recombination does not slow down the rate of compensatory evolution as predicted by the classical model. Instead, compensatory substitutions may be relatively frequent, even if linkage between the focal interacting sites is loose, selection against deleterious mutations is strong, and mutation rate is low. We compare our theoretical results with data on RNA secondary structures from vertebrate introns..
6. Junko Kusumi, Yoshihiko Tsumura, Hidenori Tachida, Evolutionary rate variation in two conifer species, Taxodium distichum (L.) Rich. var. distichum (baldcypress) and Cryptomeria japonica (Thunb. ex L.f.) D. Don (Sugi, Japanese cedar), Genes & Genetic Systems,, 90, 305-315, 2015.12, With the advance of sequencing technologies, large-scale data of expressed sequence tags and full-length cDNA sequences have been reported for several conifer species. Comparative analyses of evolutionary rates among diverse taxa provide insights into taxon-specific molecular evolutionary features and into the origin of variation in evolutionary rates within genomes and between species. Here, we estimated evolutionary rates in two conifer species, Taxodium distichum and Cryptomeria japonica, to illuminate the molecular evolutionary features of these species, using hundreds of genes and employing Chamaecyparis obtusa as an outgroup. Our results show that the mutation rates based on synonymous substitution rates (dS) of T. distichum and C. japonica are approximately 0.67×10-9 and 0.59×10-9/site/year, respectively, which are 15-25 times lower than those of annual angiosperms. We found a significant positive correlation between dS and GC3. This implies that a local mutation bias, such as context dependency of the mutation bias, exists within the genomes of T. distichum and C. japonica, and/or that selection acts on synonymous sites in these species. In addition, the means of the ratios of synonymous to nonsynonymous substitution rate in the two species are almost the same, suggesting that the average intensity of functional constraint is constant between the lineages. Finally, we tested the possibility of positive selection based on the site model, and detected one candidate gene for positive selection..
7. Junko Kusumi, Zhi-Hui Su, Isolation and characterization of 15 polymorphic microsatellite markers for the fig-pollinating wasp, Blastophaga nipponica (Hymenoptera: Agaonidae), Applied Entomology and Zoology, 10.1007/s13355-014-0267-x, 2014.04, We developed microsatellite markers for the fig-pollinating wasp Blastophaga nipponica Grandi using a dual-suppression-PCR technique. Twenty-one candidates of microsatellite loci were obtained, of which 15 yielded scorable patterns. The degree of polymorphism for the 15 loci was further characterized using summary statistics describing the genetic variation in 60 individuals from three natural populations in Japan. All 15 loci were polymorphic and yielded 2–27 alleles per locus. Overall observed heterozygosity (HO) and expected heterozygosity(HE) were 0.465 and 0.631, respectively. As expected,based on the inbreeding tendency of this species, the mean inbreeding coefficient (FIS) was high (= 0.255). These markers will contribute to studies on the population structure of this species..
8. Motoshi Ichinose, Masaru Iizuka, Junko Kusumi, Masasuke Takefu, Models of compensatory molecular evolution: Effects of back mutation, JOURNAL OF THEORETICAL BIOLOGY, 10.1016/j.jtbi.2013.01.011, 323, 1-10, 2013.01, Compensatory mutations are individually deleterious but appropriate combinations of mutants are harmless. For several models of compensatory molecular evolution, we consider the effects of back mutation. It is shown that the effects of back mutation on the rate of compensatory molecular evolution are weak. Further we estimate the values of selection parameter of deleterious single mutants for the models of compensatory molecular evolution both with and without back mutation using sequence data of folded RNA molecules and compare them with previous results..
9. Ayako Tanaka & Masato Ohtani & Yoshihisa Suyama & Nobuyuki Inomata & Yoshihiko Tsumura & Beth A. Middleton & Hidenori Tachida & Junko Kusumi, Population genetic structure of a widespread coniferous tree, Taxodium distichum [L.] Rich. (Cupressaceae), in the Mississippi River Alluvial Valley and Florida, Tree Genetics & Genomes, 2012.03, Studies of genetic variation can elucidate the structure
of present and past populations aswell as the genetic basis
of the phenotypic variability of species. Taxodium distichum is
a coniferous tree dominant in lowland river flood plains and
swamps of the southeastern USA which exhibits morphological
variability and adaption to stressful habitats. This study
provides a survey of the Mississippi River Alluvial Valley
(MAV) and Florida to elucidate their population structure and
the extent of genetic differentiation between the two regions
and sympatric varieties, including bald cypress (var. distichum)
and pond cypress (var. imbricatum). We determined
the genotypes of 12 simple sequence repeat loci totaling 444
adult individuals from 18 natural populations. Bayesian clustering
analysis revealed high levels of differentiation between
the MAV and the Florida regions. Within the MAV region,
there was a significant correlation between genetic and geographical
distances. In addition, we found that there was
almost no genetic differentiation between the varieties. Most
genetic variation was found within individuals (76.73 %),
1.67 % among individuals within population, 15.36 % among
populations within the regions, and 9.23 % between regions
within the variety. Our results suggest that (1) the populations
of theMAVand the Florida regions are divided into two major
genetic groups, which might originate from different glacial
refugia, and (2) the patterns of genetic differentiation and
phenotypic differentiation were not parallel in this species..
10. Junko Kusumi; Hiroshi Azuma; Hsy-Yu Tzeng; Lien-Siang Chou; Yan-Qiong Peng; Keiko Nakamura; Zhi-Hui Su, Phylogenetic analyses suggest a hybrid origin of the figs (Moraceae: Ficus) that are endemic to
the Ogasawara (Bonin) Islands, Japan, Molecular Phylogenetics and Evolution,, 63, 1, 168-179, 2012.01, The Ogasawara Islands are oceanic islands and harbor a unique endemic flora. There are
three fig species (Ficus boninsimae, F. nishimurae and F. iidaiana) endemic to the Ogasawara Islands,
and these species have been considered to be closely related to Ficus erecta, and to have diverged
within the islands. However, this hypothesis remains uncertain. To investigate this issue, we assessed
the phylogenetic relationships of the Ogasawara figs and their close relatives occurring in Japan,
Taiwan and South China based on six plastid genome regions, nuclear ITS region and two nuclear
genes. The plastid genome-based tree indicated a close relationship between the Ogasawara figs and F.
erecta, whereas some of the nuclear gene-based trees suggested this relationship was not so close. In
addition, the phylogenetic analyses of the pollinating wasps associated with these fig species based on
the nuclear 28S rRNA and mitochondrial cytB genes suggested that the fig-pollinating wasps of F.
erecta are not sister to those of the Ogasawara figs. These results suggest the occurrence of an early
hybridization event(s) in the lineage leading to the Ogasawara figs..
11. Junko Kusumi, Zidong, Li, Tomoyuki Kado, Yoshihiko Tsumura, Beth A. Middleton and Hidenori Tachida, Multilocus patterns of nucleotide polymorphism and demographic change in Taxodium distichum (Cupressaceae) in the lower Mississippi River alluvial valley, American journal of botany, 10.3732/ajb.1000082, 97, 11, 1848-1857, 2010.11.
12. Junko Kusumi、Aya Sato、Hidenori Tachida, Relaxation of Functional Constraint on Light-Independent Protochlorophyllide Oxidoreductase in Thuja, Molecular Biology and Evolution, 10.1093/molbev/msj097, 23, 5, 941-948, Relaxation of Functional Constraint on Light-Independent Protochlorophyllide Oxidoreductase in Thuja, 2006.05.
13. Junko Kusumi and Hidenori Tachida, Compositional properties of green-plant plastid genomes., Journal of Molecular evolution, 10.1007/s00239-004-0086-8, 60, 4, 417-425, 2005.04.
14. Junko Kusumi, Yoshihiko Tsumura, Hiroshi Yoshimaru and Hidenori Tachida, Molecular evolution of nuclear genes in Cupressaceae, a group of conifer trees., Molecular biology and evolution, 19, 5, 736-747, 2002.10.
1. Yuka Ikezaki, Yoshihisa Suyama, Beth A. Middleton, Yoshihiko Tsumura, Junko Kusumi, Kosuke Teshima, Hidenori Tachida, Inference of population structure in Taxodium distichum, a coniferous tree in North America, based on amplicon sequence analysis, SMBE Satellite Meeting / NIG International Symposium: The Causes of Genome Evolution, 2014.03, Taxodium distichum is a long-lived coniferous tree widely distributed in southeast North America. It prefers wetlands and has two varieties, bald-cypress and pond-cypress in the United States. These two varieties have clearly different habitats and morphological characteristics. From the results of previous studies, both geographical (between the Florida and Mississippi River regions) and variety specific differentiations were suggested (Tsumura et al., 1999; Lickey and Walker, 2002; Kusumi et al., 2010; Tanaka et al., 2012). The distributions of the two varieties overlapped in the Florida and southern Mississippi River regions, hence the geographical and variety specific differentiations are related in a complex way. Recently, the Next Generation Sequencing (NGS) approach along with amplicon sequence analyses enables us to obtain sequences of many individuals at many loci fairly easily. To infer the detail of population structure of Taxodium, we collected 96 individuals from the two varieties in the Mississippi River, Texas and Florida regions and determined their sequences at 48 nuclear loci using this approach with a GS FLX 454 sequencer. To examine the level of differentiation at neutral loci, we randomly selected genes from an annotated Expressed Sequence Tag (EST) library of Taxodium. The results of a Bayesian clustering analysis and estimated FST values suggested that the populations in the Mississippi River and Texas regions had similar genetic constitution and they are differentiated from the populations in the Florida region though the level of the differentiation was low. The variety specific differentiation was also found, however it was attributed to five loci showing much higher FST values than the other loci. After removing these loci, the Bayesian clustering analysis showed only geographical differentiation. Finally, analyses of the geographical and variety subdivisions assuming the isolation with migration model suggested that the divergence time of the variety subdivision was much older than that of the geographical subdivision (4.6 MYA and 0.2 MYA, respectively). However, a high level of migration from the bald-cypress populations to the pond-cypress populations (2Nu = 10.0) has reduced the level of the variety specific differentiation. On the other hand, the level of migration between the Mississippi-Texas region and Florida region was low (from Mississippi-Texas populations to Florida populations: 0.28; from Florida populations to Mississippi-Texas populations: 0.30), so the level of geographical differentiation seemed to have been increasing. .
2. Junko Kusumi, Motoshi Ichinose, Masasuke Takefu, Wolfgang Stephan, Masaru Iizuka, A model of compensatory molecular evolution with indirect compensation, SMBE Satellite Meeting / NIG International Symposium: The Causes of Genome Evolution, 2014.03, If there is an extra pair of sites that can reduce the deleterious effects of single mutants at directly interacted pair of sites, this reduction is called indirect compensation. This idea was motivated by compensatory molecular evolution of t-RNA secondary structure. [1] A previous study reported that a mutation that destroyed a Watson-Crick pair in a t-RNA stem structure could be compensated by creation of a new pair in the neighborhood. This phenomenon appears in molecular evolution of t-RNAs in mammalian lineages repeatedly. This observation indicates that compensatory evolution could occur not only by a mutation at directly interacted pair of sites but also a mutation at extra sites neighboring the original pair sites by forming a new bond. Here, we considered the effects of “indirect compensation” on the rate of compensatory molecular evolution by introducing a simple mathematical model. Computer simulations demonstrate that the effect of indirect compensation effectively decrease the fixation time of double mutants of direct compensatory sites if mutation is weak (4Nu = 0.01, 0.1) and deleterious effect of selection is strong (4Ns > 3). The degree of reduction of the fixation time depends on the relative ratio of mutation rate to selection intensity. Further, we investigate properties of sample paths by classifying them to, direct pathway, indirect pathway I and indirect pathway II. Each pathway corresponds to no change on indirect compensatory site, the first change on direct compensatory sites and the second change on indirect compensatory site, and the first change on indirect compensatory site and the second change on direct compensatory sites. It is shown that most of the double mutants appear through the indirect pathway II when selection is strong. This pathway enables individuals to complete compensatory molecular evolution without reducing fitness if a mutation at indirect compensation site compensates completely the deleterious effects of single mutants at directly interacted pair of sites. Our results suggest that the compensatory evolution with indirect compensation may be responsible to the molecular evolution of t-RNA secondary structure. .
3. Seedlings of gymnosperms are able to synthesize chlorophyll even in the dark due to dark-operative protochlorophyllide oxidoreductase (DPOR) encoded by chloroplast DNA. In some conifers RNA-editing occurs in mRNA of chlB encoding one of the DPOR subunits resulting in amino acid substitutions in ChlB. These substitutions would be important for the DPOR activity. However, there has been no experimental evidence. In this study the efficiency of RNA-editing in the chlB mRNA was analyzed in black pine seedlings grown in the light and dark. The ratio of edited chlB mRNA to the total chlB mRNA was significantly higher in the dark grown seedlings than that of seedlings grown in the light. In addition, a cyanobacterial ChlB variant corresponding to the unedited mRNA lost the ability to form the catalytic component, NB-protein (hetero tetramer of ChlN and ChlB). This result indicated that the amino acid substitutions by RNA-editing are essential for the formation of NB-protein. It is suggested that black pine seedlings regulates greening process via DPOR activity by RNA-editing in response to environmental light conditions..
4. Figs (Ficus, Moraceae) and their pollinating figwasps (Agaonidae, Chalcidoidea, Hymenoptera) form tight, species-specific obligatory mutualisms, in which neither species can propagate without the other under natural conditions. Figs depend on figwasps for pollen transmission, whereas figwasps complete their growth, development and reproduction within the fig inflorescence. Therefore, dispersal distance and a level of gene flow of one party are expected to affect those of the other party. In this study, we analyzed population structures of Ficus erecta and their pollinating figwasp, Blastophaga nipponica, using SSRs and organelle genome sequence polymorphisms. We used samples from Kansai, Kyushu, Okinawa Island, Yaeyama Islands and Taiwan. Bayesian clustering analyses based on the SSRs data showed that F. erecta and B. nipponica have a similar population structure, which correspond to their locality. In addition, we found a significant correlation between the pairwise Fst values of F. erecta and B. nipponica, suggesting interdependent gene flow of these species. On the other hand, mitochondrial genomic data indicated large genetic differentiations between the Kansai and the other populations in B. nipponica, which is inconsistent to the result of the SSRs data. This may imply that F. erecta and B. nipponica of the Kansai population have different origin-histories. .
5. Taxodium distichum is a coniferous tree that is widely distributed in southeastern North America. Although levels of genetic differentiation between its two varieties, bald-cypress and pond-cypress, are low, genetic differentiation between the Mississippi river coast region and Florida region has been shown using SSR markers. In this study, we determined the sequences of T. distichum at 5 nuclear loci using DNA sampled from populations of the Mississippi river coast and Florida regions. High and significant Fst values were found at two loci: between the two varieties at AMT and between the two regions at Acl5. To investigate whether the high Fst value obtained at the AMT locus reveals variety-specific genetic differentiation, we conducted a preliminary simulation study assuming the neutrality of alleles and a simple population structure. The P-value of the observed value at AMT was 0.0495, suggesting a possible contribution of AMT to the differentiation between varieties..
Membership in Academic Society
  • Society for Molecular Biology &Evolution
  • Society of Evolutionary Studies
  • The genetic society of Japan