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Extreme environments and plants thriving in them, known as extremophytes, offer promising platforms for studying the diverse adaptive mechanisms that have evolved in plants. However, research on adaptation to extreme environments is still limited to those environments where model species or their relative can survive. Fumarole fields, an extreme environment often overlooked, are characterized by multi-hazardous abiotic stressors, including atmospheric contamination (high concentration of H2S, SO2, and CO2), high soil temperature (~60℃), and strong soil acidification (pH=2-3). These conditions make fumarole fields a rich source for studying stress tolerance mechanisms in plants. In this review, we highlight the recent ecological, physiological, and genomic advances involved in fumarole field adaptation, and discuss the forward avenues. The studies outlined in this paper demonstrate that the extreme levels of abiotic stressors found in fumarole fields make them unparalleled field laboratories for studying the unknown stress tolerance mechanisms, warranting further genomic assessments. Some studies succeeded in identifying genes associated with fumarole field adaptation and shedding light on evolutionary implications; however, they have also encountered challenges such as limited genome resources and high genetic differentiation from related species and/or neighboring populations. To overcome such difficulties, we propose integrating ecophysiological and genomic approaches, drawing from the recent studies in other extreme environments. We expect that further studies in the fumarole fields will contribute to broadening our general knowledge of the limits of life., (© The Author(s) 2024. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site–for further information please contact journals.permissions@oup.com.)

Background and Aims: Hybridization is the main driver of plant diversification, and gene flow via hybridization has multifaceted effects on plant evolution. Carex angustisquama is an extremophyte that grows on soils heavily acidified by volcanism. Despite its habitat distinct from that of other species, this species is known to form interspecific hybrids, implying interspecific gene flow. It is crucial to verify the extent and direction of interspecific gene flow between C. angustisquama and closely related species to understand the evolutionary process of an extremophyte in solfatara fields., Methods: In this study, expressed sequence tag-simple sequence repeat markers were utilized to infer the extent and direction of interspecific gene flow between C. angustisquama and closely related species., Key Results: Bayesian clustering and simulation analyses revealed that all individuals of the three hybrid species were classified into the first hybrid generation or first backcross to C. angustisquama; therefore, current interspecific gene flow is limited. Moreover, in the Bayesian inference of historical gene flow based on multispecies samples, the model that assumed no interspecific gene flow was the most strongly supported across all species pairs, including phylogenetically close but ecologically distinctive species pairs., Conclusions: Our results revealed that interspecific gene flow between C. angustisquama and its related species has been limited both currently and historically. Moreover, our results of Bayesian inference of historical gene flow indicated that extrinsic, rather than intrinsic, factors probably act as isolating barriers between Carex species, with hybrid breakdown via microhabitat segregation being the probable potential barrier. Overall, our findings provide insights into the evolutionary process of an extremophyte in solfatara fields and offer an important example of the mechanisms of diversification of the speciose genus Carex., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Variation in partner quality is commonly observed in diverse cooperative relationships, despite the theoretical prediction that selection favoring high-quality partners should eliminate such variation. Here, we investigated how genetic variation in partner quality could be maintained in the nitrogen-fixing mutualism between Lotus japonicus and Mesorhizobium bacteria. We reconstructed de novo assembled full-genome sequences from nine rhizobial symbionts, finding massive variation in the core genome and the similar symbiotic islands, indicating recent horizontal gene transfer (HGT) of the symbiosis islands into diverse Mesorhizobium lineages. A cross-inoculation experiment using 9 sequenced rhizobial symbionts and 15 L. japonicus accessions revealed extensive quality variation represented by plant growth phenotypes, including genotype-by-genotype interactions. Variation in quality was not associated with the presence/absence variation in known symbiosis-related genes in the symbiosis island; rather, it showed significant correlation with the core genome variation. Given the recurrent HGT of the symbiosis islands into diverse Mesorhizobium strains, local Mesorhizobium communities could serve as a major source of variation for core genomes, which might prevent variation in partner quality from fixing, even in the presence of selection favoring high-quality partners. These findings highlight the novel role of HGT of symbiosis islands in maintaining partner quality variation in the legume-rhizobia symbiosis., (© The Author(s) 2020. Published by Oxford University Press on behalf of FEMS.)

Background and Aims: Clines, the gradual variation in measurable traits along a geographical axis, play a major role in evolution and can contribute to our understanding of the relative roles of selective and neutral process in trait variation. Using genetic and morphological analyses, the relative contributions of neutral and non-neutral processes were explored to infer the evolutionary history of species of the series Sakawanum (genus Asarum), which shows significant clinal variation in calyx lobe length., Methods: A total of 27 populations covering the natural geographical distribution of the series Sakawanum were sampled. Six nuclear microsatellite markers were used to investigate genetic structure and genetic diversity. The lengths of calyx lobes of multiple populations were measured to quantify their geographical and taxonomic differentiation. To detect the potential impact of selective pressure, morphological differentiation was compared with genetic differentiation (QCT-FST comparison)., Key Results: Average calyx lobe length of A. minamitanianum was 124.11 mm, while that of A. costatum was 13.80 mm. Though gradually changing along the geographical axis within series, calyx lobe lengths were significantly differentiated among the taxa. Genetic differentiation between taxa was low (FST = 0.099), but a significant geographical structure along the morphological cline was detected. Except for one taxon pair, pairwise QCT values were significantly higher than the neutral genetic measures of FST and G'ST., Conclusions: Divergent selection may have driven the calyx lobe length variation in series Sakawanum taxa, although the underlying mechanism is still not clear. The low genetic differentiation indicates recent divergence and/or gene flows between geographically close taxa. These neutral processes would also affect the clinal variation in calyx lobe lengths. Overall, this study implies the roles of population history and divergent selection in shaping the current cline of a flower trait in the series Sakawanum., (© The Author(s) 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Background and Aims: Recent biogeographic studies have illustrated that Quaternary climatic changes and historical orogenies have driven the development of high levels of biodiversity. In this context, phylogenetic niche conservatism may play a role as a major precursor of allopatric speciation. However, the effects of niche evolution on the diversification patterns of plant species under rapid habitat changes are still unknown. Here, Primula section Reinii, one of the few primroses endemic to the Japanese Archipelago, was investigated. This study aimed to clarify the phylogenetic position and relationships of section Reinii, interpret the biogeographic and diversification patterns of this group and gain a better understanding of the role of climatic niche evolution in the Japanese endemic primroses., Methods: Dated phylogeny for Primula section Reinii is presented based on the sequences of six chloroplast genes and one nuclear gene. Biogeographic history was reconstructed using statistical dispersal-vicariance analysis. Macro-evolutionary modelling of the climatic niche was combined with biogeographic inferences., Key Results: Section Reinii was shown to be monophyletic based on chloroplast and nuclear sequences. Fossil-calibrated dating analysis estimated that this section diverged from its sister taxon, sect. Cortusoides, around 1.82 million years ago, and intraspecific diversification occurred within the last million years. This time frame was characterized by Quaternary climatic oscillations and uplift of high mountains in Japan. Biogeographic inference suggested that this section originated at the northern end of the Japanese Archipelago and then dispersed southward to other islands. Models of climatic niche evolution indicated that the closely related species P. reinii and P. tosanensis have contrasting niche optima and rates of niche evolution., Conclusion: Our results highlight that spatiotemporal heterogeneity in the Japanese islands may play a significant role in the biogeographic history of Japanese endemic primroses. Contrasting evolutionary processes found in closely related species illustrate the effects of climatic niche evolution on species' diversification patterns., (© The Author 2017. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please email: journals.permissions@oup.com)

Background and Aims: Investigating intraspecific karyotypic and genetic variations jointly can provide unique insights into how historical, ecological and cytogenetic factors influence microevolution. A coastal herb, Lysimachia mauritiana, exhibits extensive karyotypic polymorphism and displays a complex cytogeographic pattern across the Ryukyus. To explore whether a similar degree of chromosomal variation exists south of the Ryukyus, and in an attempt to ascertain the mechanisms that may have generated the patterns, comprehensive sampling was conducted in Taiwan., Methods: Karyotypes were analysed at mitotic metaphase for 550 individuals from 42 populations throughout Taiwan Proper and its adjacent islands. In addition, genetic variation was estimated using 12 allozymes (21 loci) of 314 individuals sampled from 12 localities., Key Results: Four chromosome numbers and eight cytotypes, including four endemic cytotypes, were detected. Cytotype distributions were highly structured geographically, with single cytotypes present in most populations and four major cytotypes dominating the north, east and south of Taiwan and the Penghu Archipelago. Allozyme variation was very low and F-statistics indicated an extremely high level of population differentiation, implying limited gene flow among populations. Cluster analysis of allozyme variation uncovered four geographic groups, each corresponding perfectly to the four dominant cytotypes. The geographic structure of cytotype distribution and allozyme variation probably resulted from severe genetic drift triggered by genetic bottlenecks, suggesting that Taiwanese populations were likely to be derived from four independent founder events. In the few localities with multiple cytotypes, cytogeographic patterns and inferences of chromosomal evolution revealed a trend of northward dispersal, consistent with the course of the Kuroshio Current that has been influential in shaping the coastal biota of the region., Conclusions: The data elucidate the patterns of colonization and the effects of the Kuroshio Current on the distribution of L. mauritiana in Taiwan. These inferences are highly relevant to other coastal plant species in the region and will stimulate further studies.

The diversity of cyanobacterial species within the coralloid roots of an individual and populations of Cycas revoluta was investigated based on 16S rRNA gene sequences. Sixty-six coralloid roots were collected from nine natural populations of cycads on Kyushu and the Ryukyu Islands, covering the entire distribution range of the species. Approximately 400 bp of the 5'-end of 16S rRNA genes was amplified, and each was identified by denaturing gradient gel electrophoresis. Most coralloid roots harbored only one cyanobiont, Nostoc, whereas some contained two or three, representing cyanobiont diversity within a single coralloid root isolated from a natural habitat. Genotypes of Nostoc within a natural population were occasionally highly diverged and lacked DNA sequence similarity, implying genetic divergence of Nostoc. On the other hand, Nostoc genotypes showed no phylogeographic structure across the distribution range, while host cycads exhibited distinct north-south differentiation. Cycads may exist in symbiosis with either single or multiple Nostoc strains in natural soil habitats., (© 2012 Federation of European Microbiological Societies. Published by Blackwell Publishing Ltd. All rights reserved.)

Understanding the role of habitat-associated adaptation in reducing gene flow resulting in population differentiation and speciation is a major issue in evolutionary biology. We demonstrate a significant role for habitat divergence in species isolation between two naturally hybridizing riparian and nonriparian plants, Ainsliaea faurieana and A. apiculata (Asteraceae), on Yakushima Island, Japan. By analyzing the fine-scale population structure at six sympatric sites, we found that variations in leaf shape, geography, light conditions, and genotype were strongly correlated across riverbank-forest transitions. No evidence of effective gene flow was found between the two species across the majority of the transition zones, although the NewHybrid clustering analysis confirmed interspecific hybridization. However, a relatively high level of gene flow was observed across one zone with a more diffuse ecotone and intermediate flooding and light conditions, possibly generated by human disturbances. These results suggest that the barriers to gene flow between the riparian and forest species are primarily ecological. Additional common garden experiments indicated that the two species are adaptively differentiated to contrasting flooding and light environments. Overall, our study suggests that adaptations to different habitats can lead to the formation of reproductive isolating barriers and the maintenance of distinct species boundaries., (© 2010 The Author(s). Evolution© 2010 The Society for the Study of Evolution.)

Background and Aims: Farfugium (Asteraceae) is a small genus that contains the two species F. japonicum and F. hiberniflorum and is distributed along a long archipelago in east Asia. The common taxon, F. japonicum, includes three varieties associated with a wide range of habitats, including forest understorey (sciophytes), coastal crag (heliophytes) and riverbed (rheophytes). Leaf shape is an important taxonomic character within this genus and is associated with the habitat., Methods: Twenty populations that included all Farfugium taxa were collected throughout its range. Leaf morphology was measured to determine differences amongst the taxa. Phylogenetic analyses based on sequences of the internal transcribed spacer of nuclear rDNA and four plastid DNA regions (matK, trnL-trnF, trnH-psbA and rpl20-rps12) were conducted separately., Key Results: Leaf morphology was significantly different amongst taxa, but morphological variations were partly explained by adaptation to certain environmental conditions that each population inhabited. Molecular phylogenies for the nDNA internal transcribed spacer and cpDNA were consistent in classifying F. hiberniflorum and the Taiwanese var. formosanum, whilst suggesting polyphyletic origins for the rheophyte, sciophyte and heliophyte taxa. All samples from the southern Ryukyus (Japan) and Taiwan clustered into a monophyletic group, which corroborates the land configuration theory involving Quaternary land-bridge formation and subsequent fragmentation into islands. The incongruence between the two DNA datasets may imply traces of introgressive hybridization and/or incomplete lineage sorting., Conclusions: The occurrence of rheophyte, sciophyte and heliophyte plants within Farfugium may be attributable to their isolation on islands and subsequent adaptation to the riparian, coastal crag and forest understorey environments, following their migration over the Quaternary land-bridge formation along their distribution range. Nearly identical DNA sequences coupled with highly divergent morphologies amongst these taxa suggest that diversification was rapid.

The Pleistocene was characterized by a cyclic pattern of cold and warm climatic periods, or climatic oscillations, which caused fluctuations in the distributions of organisms. This resulted in drastic changes in demography, thereby accelerating the genetic divergence of populations. Phylogeographic studies have elucidated the history of populations during the Pleistocene. However, given the lack of model-based analysis of population histories, previous phylogeographic studies could not adequately evaluate the effect of these Pleistocene climatic oscillations on the genetic divergence and migration events between populations. Populations of Japanese alpine plants in central and northern Japan are highly differentiated, and a history of isolation between regions during the Pleistocene was inferred. Using sequences of 10 nuclear genes (ca. approximately 7,000 bp in total) from Cardamine nipponica (Brassicaceae), we applied an isolation with migration (IM) model to test the significance of the isolation history between central and northern Japan and to assess whether range shifts during the Pleistocene climatic oscillations were involved in the genetic differentiation between regions. The estimated divergence time indicates that the two regions were separated about 100,000-110,000 years ago. The exclusive occurrence of closely related haplotypes within each region (parsimony network) and the high level of genetic differentiation between the regions (mean F(ST) = 0.417) indicate that genetic divergence occurred following the isolation of the two regions. Therefore, the genetic differentiation between regions was shaped during the Pleistocene, especially during the last glacial and inter and postglacial periods. In addition, our multilocus analysis showed that populations in central and northern Japan were completely isolated after they split. Geographic separation and subsequent restricted migration events among mountains could explain this isolation history between regions. Furthermore, genetic drift in the reduced populations would remove evidence of occasional migration, emphasizing the isolation history. Therefore, our application of a demographic model demonstrated the Pleistocene origin of geographic differentiation statistically and provided a plausible migration history for C. nipponica.

Given that plants are sessile organisms, traits involved in adapting to local environments and/or in monitoring the surrounding environment, such as having photoreceptors, are significant targets of natural selection in plant evolution. To assess the intraspecific adaptive evolution of photoreceptors, we investigated sequence variations in four phytochrome genes (PHYA-C and PHYE) of Cardamine nipponica (Brassicaceae), an endemic Japanese alpine plant. The genealogies of haplotypes and genetic differentiations showed inconsistent patterns of evolution across phytochromes, suggesting that evolutionary forces were distinct in phytochromes of C. nipponica. An overall low level of nucleotide diversity in phytochrome genes suggests that the evolution of phytochromes is constrained by purifying selection within C. nipponica, which is consistent with previous findings on phytochromes. However, PHYE alone exhibited a non-neutral pattern of polymorphisms (Tajima's D = 1.91, P < 0.05) and an accumulation of nonsynonymous substitutions between central and northern Japan. In particular, the PHY domain, which plays an important role in stabilizing the active form (Pfr) of phytochromes, harbored a specific nonsynonymous fixation between regions. Thus, our finding indicates that local adaptation is involved in the evolution of PHYE in C. nipponica and is the first to suggest the involvement of PHYE in local adaptation.

Background and Aims: The flora of the Sino-Japanese plant region of eastern Asia is distinctively rich compared with other floristic regions in the world. However, knowledge of its floristic evolution is fairly limited. The genus Ainsliaea is endemic to and distributed throughout the Sino-Japanese region. Its interspecific phylogenetic relationships have not been resolved. The aim is to provide insight into floristic evolution in eastern Asia on the basis of a molecular phylogenetic analysis of Ainsliaea species., Methods: Cladistic analyses of the sequences of two nuclear (ITS, ETS) and one plastid (ndhF) regions were carried out individually and using the combined data from the three markers., Key Results: Phylogenetic analyses of three DNA regions confirmed that Ainsliaea is composed of three major clades that correspond to species distributions. Evolution of the three lineages was estimated to have occurred around 1.1 MYA during the early Pleistocene., Conclusions: The results suggest that Ainsliaea species evolved allopatrically and that the descendants were isolated in the eastern (between SE China and Japan, through Taiwan and the Ryukyu Islands) and western (Yunnan Province and its surrounding areas, including the Himalayas, the temperate region of Southeast Asia, and Sichuan Province) sides of the Sino-Japanese region. The results suggest that two distinct lineages of Ainsliaea have independently evolved in environmentally heterogeneous regions within the Sino-Japanese region. These regions have maintained rich and original floras due to their diverse climates and topographies.