2024-06-20 2024, Volume 62 Issue 6

  • Select all
  • Research Article
    Meng Yang , Shu-Feng Zhang , Bin Li , Yun-Xin Lan , Yi-Han Yang , Meng-Jun Liu
    2024, 62(6): 1069-1084. https://doi.org/10.1002/jse.13065

    Jujube (Ziziphus jujuba Mill.), renowned for its nutritional value and health benefits, is believed to have originated in the middle and lower reaches of the Yellow River in China, where it underwent domestication from wild jujube. Nonetheless, the evolutionary trajectory and species differentiation between wild jujube and cultivated jujube still require further elucidation. The chloroplast genome (plastome), characterized by its relatively lower mutation rate compared to the nuclear genome, serves as an excellent model for evolutionary and comparative genomic research. In this study, we analyzed 326 nonredundant plastomes, encompassing 133 jujube cultivars and 193 wild jujube genotypes distributed throughout China. Noteworthy variations in the large single copy region primarily account for the size differences among these plastomes, impacting the evolution from wild jujube to cultivated varieties. Horizontal gene transfer (HGT) unveiled a unique chloroplast-to-nucleus transfer event, with transferred fragments predominantly influencing the evolution of the nuclear genome while leaving the plastome relatively unaffected. Population genetics analysis revealed two distinct evolutionary pathways from wild jujube to cultivated jujube: one driven by natural selection with minimal human interference, and the other resulting from human domestication and cultivation. Molecular dating, based on phylogenetic analysis, supported the likelihood that wild jujube and cultivated jujube fall within the same taxonomic category,Z. jujuba. In summary, our study comprehensively examined jujube plastome structures and HGT events, simultaneously contributing novel insights into the intricate processes that govern the evolution and domestication of jujube species.

  • Research Article
    Qiang He , Yuqing Miao , Xinyuan Zheng , Yaru Wang , Yitao Wang , Zheng Jia , Hongyu Zhang , Yu Wang , Yao Xiao , Cailian Du , Wei Li , Longsheng Xing , Huilong Du
    2024, 62(6): 1085-1102. https://doi.org/10.1002/jse.13068

    Reynoutria multiflora is a widely used medicinal plant in China. Its medicinal compounds are mainly stilbenes and anthraquinones which possess important pharmacological activities in anti-aging, anti-inflammatory and anti-oxidation, but their biosynthetic pathways are still largely unresolved. Here, we reported a near-complete genome assembly of R. multiflora consisting of 1.39 Gb with a contig N50 of 122.91 Mb and only one gap left. Genome evolution analysis revealed that two recent bursts of long terminal repeats (LTRs) contributed significantly to the increased genome size of R. multiflora, and numerous large chromosome rearrangements were observed between R. multiflora and Fagopyrum tataricum genomes. Comparative genomics analysis revealed that a recent whole-genome duplication specific to Polygonaceae led to a significant expansion of gene families associated with disease tolerance and the biosynthesis of stilbenes and anthraquinones in R. multiflora. Combining transcriptomic and metabolomic analyses, we elucidated the molecular mechanisms underlying the dynamic changes in content of medicinal ingredients in R. multiflora roots across different growth years. Additionally, we identified several putative key genes responsible for anthraquinone and stilbene biosynthesis. We identified a stilbene synthase gene PM0G05131 highly expressed in roost, which may exhibit an important role in the accumulation of stilbenes in R. multiflora. These genomic data will expedite the discovery of anthraquinone and stilbenes biosynthesis pathways in medicinal plants.

  • Research Article
    Oyetola Oyebanji , Gregory W. Stull , Rong Zhang , Fabien R. Rahaingoson , De-Zhu Li , Ting-Shuang Yi
    2024, 62(6): 1103-1117. https://doi.org/10.1002/jse.13072

    The Millettioid/Phaseoloid (or the Millettioid) clade is a major lineage of the subfamily Papilionoideae (Fabaceae) that is poorly understood in terms of its diversification and biogeographic history. To fill this gap, we generated a time-calibrated phylogeny for 749 species representing c. 80% of the genera of this clade using nrDNA ITS, plastid matK, and plastome sequence (including 38 newly sequenced plastomes). Using this phylogenetic framework, we explored the clade’s temporal diversification and reconstructed its ancestral areas and dispersal events. Our phylogenetic analyses support the monophyly of the Millettioid/Phaseoloid clade and four of its tribal lineages (Abreae, Desmodieae, Indigofereae, and Psoraleeae), while two tribal lineages sensu lato millettioids and phaseoloids are polyphyletic. The fossil-calibrated dating analysis showed a nearly simultaneous divergence between the stem node (c. 62 Ma) and the crown node (c. 61 Ma) of the Millettioid/Phaseoloid clade in the Paleocene. The biogeographic analysis suggested that the clade originated in Africa and dispersed to Asia, Europe, Australia, and the Americas at different periods in the Cenozoic. We found evidence for shifts in diversification rates across the phylogeny of the Millettioid/Phaseoloid clade throughout the Cenozoic, with a rapid increase in net diversification rates since c. 10 Ma. Possible explanations for the present-day species richness and distribution of the Millettioid/Phaseoloid clade include boreotropical migration, frequent intra- and intercontinental long-distance dispersals throughout the Cenozoic, and elevated speciation rates following the Mid-Miocene Climatic Optimum. Together, these results provide novel insights into major diversification patterns of the Millettioid/Phaseoloid clade, setting the stage for future evolutionary research on this important legume clade.

  • Research Article
    Xin-Lin Yan , Sheng-Long Kan , Mei-Xia Wang , Yong-Yao Li , Luke R. Tembrock , Wen-Chuang He , Li-Yun Nie , Guan-Jing Hu , Dao-Jun Yuan , Xiong-Feng Ma , Zhi-Qiang Wu
    2024, 62(6): 1118-1136. https://doi.org/10.1002/jse.13070

    Cotton (Gossypium spp.) is a vital global source of renewable fiber and ranks among the world’s most important cash crops. While extensive nuclear genomic data of Gossypium has been explored, the organellar genomic resources of allotetraploid cotton, remain largely untapped at the population level. The plastid genome (plastome) is well suited for studying plant species relationships and diversity due to its nonrecombinant uniparental inheritance. Here, we conducted de novo assembly of 336 Gossypium plastomes, mainly from domesticated cultivars, and generated a pan-plastome level resource for population structure and genetic diversity analyses. The assembled plastomes exhibited a typical quadripartite structure and varied in length from 160 103 to 160 597 bp. At the species level, seven allotetraploid species were resolved into three clades, where Gossypium tomentosum and Gossypium mustelinum formed an early diverging clade rooted by diploids, followed by splitting two sister clades of Gossypium darwiniiGossypium barbadense and Gossypium hirsutumGossypium ekmanianumGossypium stephensii. Within the G. hirsutum clade the resolution of cultivated accessions was less polyphyletic with landrace and wild accessions than in G. barbadense suggesting some selection on plastome in the domestication of this adaptable species of cotton. The nucleotide diversity of G. hirsutum was higher than that of G. barbadense. We specifically compared the plastomes of G. hirsutum and G. barbadense to find mutational hotspots within each species as potential molecular markers. These findings contribute a valuable resource for exploring cotton evolution as well as in the breeding of new cotton cultivars and the preservation of wild and cultivated germplasm.

  • Research Article
    Xing-Hao Li , Ru-Fan Li , Fang-Jing Hu , Shuai Zheng , Fu-Qiang Rao , Rong An , Yong-Hong Li , De-Guang Liu
    2024, 62(6): 1137-1149. https://doi.org/10.1002/jse.13079

    The Cucujiformia, with remarkable morphological, ecological, and behavioral diversity, is the most evolutionarily successful group within Coleoptera. However, the phylogenetic relationships among superfamilies within Cucujiformia remain elusive. To address the issues, we conducted a transcriptome-based macro-evolutionary study of this lineage. We sequenced the genomes and transcriptomes of three species from the superfamily Curculionoidea (two from Curculionidae and one from Brentidae), and obtained a data set of more than 569 990 amino acid alignments from 143 species of Cucujiformia. With the most complete collection of whole genomes and transcriptomes so far, we compared the performance of different data matrices with universal-single-copy orthologs (USCO). The resultant trees based on different data sets were consistent for the majority of deep nodes. Two USCO amino acid matrices (i.e., USCO75 and USCO750-abs80) provided well-resolved topology. The analyses confirm that Cucujoidea sensu Robertson et al. 2015 is a nonmonophyletic group, consisting of Erotyloidea, Nitiduloidea, and Cucujoidea sensu Cai et al. 2022. Moreover, Erotyloidea is the early-diverging group, followed by the clade Nitiduloidea. The preferred topologies supported a “basal” split of Coccinelloidea from the remaining superfamilies, and Cleroidea formed the second splitting group. The following phylogeny was supported at the superfamily level in Cucujiformia: (Coccinelloidea, (Cleroidea, ((Lymexyloidea, Tenebrionoidea), (Erotyloidea, (Nitiduloidea, (Cucujoidea, (Chrysomeloidea, Curculionoidea))))))). Our comprehensive analyses recovered well-resolved higher-level phylogenetic relationships within the Cucujiformia, providing a stable framework for comprehending its evolutionary history.

  • Research Article
    Xin Wang , Jiang-Bao Xia , Jun-Hong Bai , Shuo Yin , Wei Wang , Da-Wei Wang , Xin-Xin Yi , Sheng-Hong Dai
    2024, 62(6): 1150-1164. https://doi.org/10.1002/jse.13064

    As an important halophyte in the Yellow River Delta, the Amaranthaceae C3 Suaeda salsa (L.) Pall. has attracted much attention for the “red carpet” landscape, and could be simply divided into red and green phenotypes according to the betacyanin content in the fleshy leaves. However,S. salsa has not been sequenced yet, which limited people’s understanding of this species at the molecular level. We constructed a high-quality chromosome-scale reference genome by combining high-throughput sequencing, PacBio single molecule real-time sequencing, and Hi-C sequencing techniques with a genome size of 445.10 Mb and contigs N50 of 2.94 Mb. Through the annotation of the S. salsa genome, 298.76 Mb of the repetitive sequences and 23 965 protein-coding genes were identified, of which the proportion of long terminal repeats type in the repetitive sequences was the most abundant, about 50.74% of the S. salsa genome. Comparative genomics indicated that S. salsa underwent a whole-genome duplication event about 146.15 million years ago (Ma), and the estimated divergence time between S. salsa and Suaeda aralocaspica was about 16.9 Ma. A total of four betacyanins including betanidin, celosianin II, amaranthin and 6′-O-malonyl-celosianin II were identified and purified in both phenotypes, while two significantly up-regulated betacyanins (celosianin II and amaranthin) may be the main reason for the red color in red phenotype. In addition, we also performed transcriptomics and metabolomics in both phenotypes to explore the molecular mechanisms of pigment synthesis, and a series of structural genes and transcription factors concerning with betacyanin production were selected in S. salsa.

  • Research Article
    Hua Yan , Peng Zhou , Wei Wang , Jian-Fei Ye , Shao-Lin Tan , Chun-Ce Guo , Wen-Gen Zhang , Zi-Wei Zhu , Yi-Zhen Liu , Xiao-Guo Xiang
    2024, 62(6): 1165-1176. https://doi.org/10.1002/jse.13055

    Pterocarya (Juglandaceae) is disjunctly distributed in East Asia and the Caucasus region today, but its fossils are widely distributed in the Northern Hemisphere. We first inferred phylogeny with time estimation of Pterocarya under node-dating (ND) based on plastomes of all eight extant species and tip-dating (TD) based on plastomes and 69 morphological characters of 19 extant and extinct species, respectively. We compared the biogeographical reconstructions on the timetrees from ND and TD, respectively, and then compiled 83 fossil records and 599 current occurrences for predicting the potential distributions for the past and the future. The most recent comment ancestor of Pterocarya is inferred in East Asia at 40.46 Ma (95% highest posterior density [HPD]: 28.04–54.86) under TD and 26.81 Ma (95% HPD: 23.03–33.12) under ND. The current distribution was attributed to one dispersal and one vicariant event without fossils, but as many as six dispersal, six vicariant, and 11 local extinction events when considering fossils. Pterocarya migrated between East Asia and North America via the Bering Land Bridge during the early Oligocene and the early Miocene periods. With the closure of Turgai Strait,Pterocarya dispersed between East Asia and Europe through the Miocene. The potential distribution analyses indicated that Pterocarya preferred warm temperate regions across the Northern Hemisphere since the Oligocene, but the drastic temperature decline caused its extinction in high latitudes. Except for Pterocarya fraxinifolia and Pterocarya stenoptera, suitable habitats for this genus are predicted to contract by 2070 due to climate change.

  • Research Article
    Lone Aagesen , Diego L. Salariato , María A. Scataglini , Juan M. Acosta , Silvia S. Denham , Carolina Delfini
    2024, 62(6): 1177-1192. https://doi.org/10.1002/jse.13067

    In this study, we explored the distributions of grass genera in the Southern Cone (SC) of South America, applying several phylogenetic diversity (PD) metrics and randomization tests. Grasses appear to have been present in South America since their early evolution as tropical understory species more than 60 Ma. During the course of evolution, grasses have adapted to all terrestrial biomes and become one of the most successful plant families on earth. At present, the SC contains nearly all terrestrial biomes and a wide range of humid to arid ecoregions. Analyzing 126.514 point occurrences and four plastid markers for 148 genera (91% of the native grass genera), we found that tropical humid regions hold the highest PD, with no observed bias in branch lengths. These results indicate that niche conservatism dominates the diversity pattern of grasses in the SC. We found significantly low PD in the Dry Chaco and in the Patagonian Steppe, which suggest ecological filtering in both warm and cold arid regions. The Patagonian Steppe also holds significantly longer branches than expected by chance, as the native grass flora is mainly composed of distantly related Pooideae genera with a northern hemisphere origin. Short branches are found in the Uruguayan Savanna, suggesting that these grasslands could be a cradle for grass diversity within the SC. The dated phylogeny supported the current view of a relatively recent evolution of the family within the SC, with most diversification taking place from the middle Miocene and onwards.

  • Research Article
    Bowen Kong , Chungkun Shih , Dong Ren , Yongjie Wang
    2024, 62(6): 1193-1200. https://doi.org/10.1002/jse.13071

    Neuroptera, as a small relic group of Insecta undergoing a rapid species diversification during the Mesozoic Era, is known by diverse extinct endemic lineages preserved as impression fossils and in amber. The current understanding of Mesozoic neuropterans′ diversity has mainly focused on the adults, because the contemporaneous larvae have been fairly rare especially for the Jurassic lacewings. Herein, a new giant lacewing larva,Natator giganteus gen. et sp. nov., is described from the Middle Jurassic Daohugou Beds of China. The remarkable larva is characterized by its impressively large body size, distinctively elongated cervix, and presence of swimming hairs on legs, which provide direct evidence to reveal an aquatic habit for the Jurassic lacewing larva. The morphological analysis indicates this giant larva would have probably inhabited the benthic environments of Jurassic montane rivers and streams. In addition, its morphological specialization suggests that it might have adopted an ambush predation strategy to catch its prey. The finding enhances our knowledge of the species diversity and morphological plasticity for the Jurassic lacewing larvae, and reveals that the aquatic lineages of Neuroptera exhibited dramatically structural and ecological convergence across the evolutionary process.

  • Research Article
    Ryan A. Folk , Aliasghar A. Maassoumi , Carolina M. Siniscalchi , Heather R. Kates , Douglas E. Soltis , Pamela S. Soltis , Michael B. Belitz , Robert P. Guralnick
    2024, 62(6): 1201-1217. https://doi.org/10.1002/jse.13077

    Astragalus (Fabaceae) is astoundingly diverse in temperate, cold arid regions of Earth, positioning this group as a model clade for investigating the distribution of plant diversity in the face of environmental challenges. Here, we identify the spatial distribution of diversity and endemism in Astragalus using species distribution models for 752 species and a phylogenetic tree comprising 847 species. We integrated these to map centers of species richness (SR) and relative phylogenetic diversity (RPD) and used randomization approaches to investigate centers of endemism. We also used clustering methods to identify phylogenetic regionalizations. We then assembled predictor variables of current climate conditions to test environmental factors predicting these phylogenetic diversity results, especially temperature and precipitation seasonality. We find that SR centers are distributed globally at temperate middle latitudes in arid regions, but the Mediterranean Basin is the most important center of RPD. Endemism centers also occur globally, but Iran represents a key endemic area with a concentration of both paleo- and neoendemism. Phylogenetic regionalization recovered an east-west gradient in Eurasia and an amphitropical disjunction across North and South America; American phyloregions are overall most closely related to east and central Asia. SR, RPD, and lineage turnover are driven mostly by precipitation and seasonality, but endemism is driven primarily by diurnal temperature variation. Endemism and regionalization results point to western Asia and especially Iran as a biogeographic gateway between Europe and Asia. RPD and endemism highlight the importance of temperature and drought stress in determining plant diversity and endemism centers.

  • Research Article
    Enzo Jugieau , Victor Talmot , Cybill Staentzel , Sandra Noir , Laurent Hardion
    2024, 62(6): 1218-1226. https://doi.org/10.1002/jse.13075

    The two invasive Reynoutria species,Reynoutria japonica var. japonica and Reynoutria sachalinensis, and their hybrid Reynoutria x bohemica are often misidentified by managers and nonspecialists. The taxonomic confusions are all the more exacerbated by the infraspecific variability of introduced populations in terms of morphology, genetic diversity, and ploidy level. We resolved the identity of North-Eastern French invasive populations using 4582 single-nucleotide polymorphisms (SNPs) from a RADseq analysis, DNA contents estimated by flow cytometry, and 12 vegetative morphometric variables. The SNPs supported only one single genotype for R. japonica over 11 localities, while the nine localities of Reynoutria x bohemica were represented by one genotype each. Estimation of genome size using DAPI staining and flow cytometry revealed only octoploid cytotypes for R. japonica and hexaploid cytotypes for R. x bohemica, whereas R. sachalinensis was represented by tetraploid and hexaploid cytotypes. Among morphometric variables, no single one allows for a clear differentiation of the three taxa. We propose a combination of characters to easily and quickly identify these three invasive taxa based on six vegetative criteria including leaf and apex length, as well as leaf shape, leaf base, and apex shape, and the extrafloral nectaries on the node.

  • Research Article
    Lian-Sheng Xu , Zhu-Qiu Song , Shu-Yuan Liao , You-Sheng Chen
    2024, 62(6): 1227-1237. https://doi.org/10.1002/jse.13066

    The Crepidinae are the largest subtribe of the Cichorieae (Asteraceae). Debate remains over the circumscription and phylogeny of this subtribe, mainly due to its complex morphology and the poor phylogenetic signal provided by traditional Sanger sequencing markers. In this study, a well-resolved phylogeny of the subtribe Crepidinae, consisting of seven highly supported clades, was obtained for the first time using nuclear data with a phylogenomics approach (Hyb-Seq). Using this phylogeny along with other evidence, we propose a new taxonomic framework for the Crepidinae with seven lines and 29 genera, which merges subtribe Chondrillinae with the Crepidinae. We also describe a new monotypic genus,Qineryangia, that is characterized by broad involucres, loose imbricate phyllaries with wavy margins, and thick pappus bristles.

  • Research Article
    Zhi-Fang Liu , Shi-Fang Zhang , Alex D. Twyford , Xiu-Qin Ci , Lang Li , Xiao-Yan Zhang , Jian-Lin Hu , Jia-Chuan Tan , Guang-Da Tang , Sheng-Yuan Qin , Ling Hu , Xin Ding , Hong-Hu Meng , Li-Na Dong , Ting Huang , Hui Ma , Jian-Hua Xiao , Chao-Nan Cai , John G. Conran , Qi Wang , Peter M. Hollingsworth , Jie Li
    2024, 62(6): 1238-1254. https://doi.org/10.1002/jse.13069

    Species delimitation remains a challenge worldwide, especially in highly diverse tropical and subtropical regions. Here, we use an integrative approach that combines morphology, phylogenomics, and species distribution modeling (SDM) to clarify the cryptic differentiation within the enigmatic hemiparasitic love vine Cassytha filiformis (Lauraceae) in China and adjacent regions. We generated complete plastid genomes and nuclear ribosomal sequences for diverse samples from across the species range and compared results with previously published plastid data, recovering two well-supported monophyletic clades. Further, the analysis revealed significant differences in two morphological characters and SDM, indicating distinct environmental factors influencing their distributions. Fossil-calibrated analyses to estimate the origins and diversification patterns for the cryptic species gave divergence age estimates corresponding to the Oligo-Miocene; a period of new ecological opportunities associated with the prevailing East Asian monsoon. Multivariate analyses support the conclusion that southern China and adjacent regions have a different, previously unknown, cryptic lineage of C. filiformis. Our study highlights the importance of using multivariate approach to characterize plant species, as well as the significant role that past climatic changes have played in driving speciation in parasitic plants in tropical and subtropical zones.

  • Research Article
    Qi-Rui Li , Kamran Habib , You-Peng Wu , Si-Han Long , Xu Zhang , Hong-Min Hu , Qian-Zhen Wu , Li-Li Liu , Yan Lin , Xiang-Chun Shen , Ji-Chuan Kang
    2024, 62(6): 1255-1330. https://doi.org/10.1002/jse.13058

    The genus Xylaria comprises a diverse group of fungi with a global distribution and significant ecological importance, known for being a source of bioactive secondary metabolites with antibacterial, antioxidative, anticarcinogenic, and additional properties. In this study, we present a comprehensive taxonomic revision of the species of Xylaria found in some parts of southern China, characterized by an extensive multilocus phylogeny analysis based on internal transcribed spacer (ITS),TUB2 (β-tubulin), and DNA-directed RNA polymerase II subunit 2 (rpb2) gene regions. Morphological examination and detailed comparative analyses of the collected specimens were conducted to determine the distinctiveness of each species. The multilocus phylogeny approach allowed us to infer evolutionary relationships and assess species boundaries accurately, leading to the identification of 40 novel Xylaria species hitherto unknown to science. The newly described species are: X. baoshanensis,X. bawanglingensis,X. botryoidalis,X. dadugangensis,X. doupengshanensis,X. fanglanii,X. glaucae,X. guizhouensis,X. japonica,X. jinghongensis,X. jinshanensis,X. kuankuoshuiensis,X. liboensis,X. negundinis,X. orbiculati,X. ovata,X. pseudoanisopleura,X. pseudocubensis,X. pseudobambusicola,X. pseudoglobosa,X. pseudohemisphaerica,X. pseudohypoxylon,X. puerensis,X. qianensis,X. qiongzhouensis,X. rhombostroma,X. serratifoliae,X. shishangensis,X. shuqunii,X. shuangjiangensis,X. sinensis,X. tongrenensis,X. umbellata,X. xishuiensis,X. yaorenshanensis,X. yinggelingensis,X. yumingii,X. yunnanensis,X. zangmui, and X. zonghuangii. The study’s findings shed light on the distinctiveness of the newly described species, supported by both morphological distinctions and phylogenetic relationships with their close relatives. This taxonomic revision significantly contributes to our understanding the diversity of Xylaria in China and enriches the knowledge of fungal biodiversity worldwide.