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Allium crop breeding remains severely hindered due to the lack of high-quality reference genomes. Here we report high-quality chromosome-level genome assemblies for three key Allium crops (Welsh onion, garlic and onion), which are 11.17 Gb, 15.52 Gb and 15.78 Gb in size with the highest recorded contig N50 of 507.27 Mb, 109.82 Mb and 81.66 Mb, respectively. Beyond revealing the genome evolutionary process of Allium species, our pathogen infection experiments and comparative metabolomic and genomic analyses showed that genes encoding enzymes involved in the metabolic pathway of Allium -specific flavor compounds may have evolved from an ancient uncharacterized plant defense system widely existing in many plant lineages but extensively boosted in alliums. Using in situ hybridization and spatial RNA sequencing, we obtained an overview of cell-type categorization and gene expression changes associated with spongy mesophyll cell expansion during onion bulb formation, thus indicating the functional roles of bulb formation genes. Chromosome-level genome assemblies of three Allium crops (onion, garlic and Welsh onion) and spatial RNA sequencing provide insights into Allium trait evolution and gene expression patterns during onion bulb formation.

The genus Allium L., one of the largest monocotyledonous genera and one that includes many economically important crops with nutritional and medicinal value, has been the focus of classification or phylogeny studies for centuries. Recent studies suggested that the genus can be divided into 15 subgenera and 72 sections, which were further classified into three evolutionary lineages. However, the phylogenetic relationships reconstructed by one or two loci showed weaker support, especially for the third evolutionary lineage, which might not show the species relationships very clearly and could hinder further adaptive and evolutionary study. In this study, a total of 39 complete chloroplast genomes of Allium (covering 12 Allium subgenera) were collected, and combining these with 125 species of plastomes from 19 other families of monocots, we reconstructed the phylogeny of the genus Allium, estimated the origin and divergence time of the three evolutionary lineages and investigated the adaptive evolution in this genus and related families. Our phylogenetic analysis confirmed the monophyly and three evolutionary lineages of Allium, while new species relationships were detected within the third evolutionary lineage. The divergence time of the three evolutionary lineages was estimated to be in the early Eocene to the middle Miocene, and numerous positive selected genes (PSGs) and PSGs with high average Ka/Ks values were found in Allium species. Our results detected a well-supported phylogenetic relationship of Allium. The PSGs and PSGs with high Ka/Ks values, as well as diversified morphologies, complicated chromosome characteristics and unique reproductive modes may play important roles in the adaptation and evolution of Allium species. This is the first study that conducted phylogenetic and evolutionary analyses on the genus Allium combined with the plastome and morphological and cytological data. We hope that this study can contribute to further analysis of Allium for other researchers.

The Allium genus is cultivated globally as vegetables, condiments, or medicinal plants and is characterized by large genomes and strong pungency. However, the genome evolution and genomic basis underlying their unique flavor formation remain poorly understood. Herein, we report an 11.27-Gb chromosome-scale genome assembly for bunching onion ( A. fistulosum ). The uneven bursts of long-terminal repeats contribute to diversity in genome constituents, and dispersed duplication events largely account for gene expansion in Allium genomes. The extensive duplication and differentiation of alliinase and lachrymatory factor synthase manifest as important evolutionary events during flavor formation in Allium crops. Furthermore, differential selective preference for flavor-related genes likely lead to the variations in isoalliin content in bunching onions. Moreover, we reveal that China is the origin and domestication center for bunching onions. Our findings provide insights into Allium genome evolution, flavor formation and domestication history and enable future genome-assisted breeding of important traits in these crops. Genome evolution of Allium genus and genomic basis underlying the pungency flavor formation remain poorly understood. Here, the authors assemble the genome of bunching onion and conduct population genetics analyses to reveal Allium genome evolution, flavor formation and domestication history.

The genus Allium is one of the largest monocotyledonous genera, containing over 850 species, and most of these species are found in temperate climates of the Northern Hemisphere. Furthermore, as a large number of new Allium species continue to be identified, phylogenetic classification based on morphological characteristics and a few genetic markers will gradually exhibit extremely low discriminatory power. In this study, we present the use of complete chloroplast genome sequences in genome-scale phylogenetic studies of Allium . We sequenced and assembled four Allium chloroplast genomes and retrieved five published chloroplast genomes from GenBank. All nine chloroplast genomes were used for genomic comparison and phylogenetic inference. The chloroplast genomes, ranging from 152,387 bp to 154,482 bp in length, exhibited conservation of genomic structure, and gene organization and order. Subsequently, we observed the expansion of IRs from the basal monocot Acorus americanus to Allium , identified 814 simple sequence repeats, 131 tandem repeats, 154 dispersed repeats and 109 palindromic repeats, and found six highly variable regions. The phylogenetic relationships of the Allium species inferred from the chloroplast genomes obtained high support, indicating that chloroplast genome data will be useful for further resolution of the phylogeny of the genus Allium .

Allium species are valued for their culinary and medicinal applications, with flowering and bulbing being key developmental processes regulated by photoperiod and temperature. In short-day, many Allium species exhibit limited floral induction, hindering their potential in breeding programs. The present study aimed to (i) develop a methodology to induce flowering under non-inductive conditions and (ii) elucidate the molecular mechanisms regulating florogenesis and bulbing in A. cepa , A. sativum , and A. tuberosum. A photoperiod extension system (10 h daylight followed by 8 h artificial light) coupled with gibberellic acid (GA 3 ; 50, 100, 200 mg/L) treatment was standardized and applied to wild Allium species ( A. tuberosum , A. fasciculatum , A. macranthum A. schoenoprasum ). Results revealed that 200 mg/L GA 3 combined with an 18-hrs photoperiod significantly promoted early scape emergence and flowering in A. tuberosum. In contrast, scape induction was not observed in other species under any treatment combinations. In our parallel experiment, expression profiling through qRT-PCR indicated that FT1, FT3, and FT4 genes were associated with bulbing, while FT2, CO, and LFY were key regulators of flowering. High expression of LFY, AP1, SEP3, and PI in A. cepa and A. tuberosum was correlated with successful floral transition, whereas their suppression in A. sativum underpinned its non-flowering phenotype. Additionally, the flowering repressor FLC was up-regulated during bulbing but down-regulated during flowering, reinforcing its antagonistic role in florogenesis. This work provides new insights into the florogenesis and bulbing regulatory network under short-day conditions and underscores the pivotal role of LFY in promoting flowering in Allium species. The findings offer a framework for future genetic manipulation strategies, including LFY overexpression to induce flowering in sterile garlic cultivars and LFY knockdown to control bolting in bulb onions.

The genus Allium is a rich source of steroidal saponins, and its medicinal properties have been attributed to these bioactive compounds. The saponin compounds with diverse structures play a pivotal role in Allium's defense mechanism. Despite numerous studies on the occurrence and chemical structure of steroidal saponins, their biosynthetic pathway in Allium species is poorly understood. The monosomic addition lines (MALs) of the Japanese bunching onion (A. fistulosum, FF) with an extra chromosome from the shallot (A. cepa Aggregatum group, AA) are powerful genetic resources that enable us to understand many physiological traits of Allium. In the present study, we were able to isolate and identify Alliospiroside A saponin compound in A. fistulosum with extra chromosome 2A from shallot (FF2A) and its role in the defense mechanism against Fusarium pathogens. Furthermore, to gain molecular insight into the Allium saponin biosynthesis pathway, high-throughput RNA-Seq of the root, bulb, and leaf of AA, MALs, and FF was carried out using Illumina's HiSeq 2500 platform. An open access Allium Transcript Database (Allium TDB, http://alliumtdb.kazusa.or.jp) was generated based on RNA-Seq data. The resulting assembled transcripts were functionally annotated, revealing 50 unigenes involved in saponin biosynthesis. Differential gene expression (DGE) analyses of AA and MALs as compared with FF (as a control) revealed a strong up-regulation of the saponin downstream pathway, including cytochrome P450, glycosyltransferase, and beta-glucosidase in chromosome 2A. An understanding of the saponin compounds and biosynthesis-related genes would facilitate the development of plants with unique saponin content and, subsequently, improved disease resistance.

Satellite DNA (satDNA) is a family of tandemly repeated non-coding sequences in eukaryotic genomes involved in shaping genome architecture and regulation of various biological functions. Within a species, all satDNA families collectively form the satellitome. Satellitomes of Allium species has been explored only superficially, largely due to enormous genome sizes, high transposable element content, and a general lack of reference genomic resources. The emergence of reference genome assemblies now makes it possible to conduct a more in-depth study. Here, we applied a comprehensive bioinformatics approach to study the satellitomes of Allium cepa and Allium fistulosum. Using two complementary bioinformatics pipelines along with available reference genome assemblies, we have created the most complete collection of consensus satDNA sequences of A. cepa and A. fistulosum so far, consisting of 83 and 97 consensus sequences, respectively. The in silico analysis of the genomic distribution allowed the identification of 11 novel candidates for cytogenetic marker panels, including chromosome-specific satDNA families. Validation of satDNA using PCR and FISH confirmed the reliability of the created satellitomes. Furthermore, comparative analysis of satDNA genomic organization and abundance provided insights into the evolution of these species satellitomes. These findings provide a foundational resource that will help illuminate the evolutionary dynamics of Allium satellitomes and pave the way for future cytogenetic studies of Allium species.

BACKGROUND AND AIMS: The genus Allium comprises more than 800 species, placing it among the largest monocotyledonous genera. It is a variable group that is spread widely across the Holarctic region. Previous studies of Allium have been useful in identifying and assessing its evolutionary lineages. However, there are still many gaps in our knowledge of infrageneric taxonomy and evolution of Allium. Further understanding of its phylogeny and biogeography will be achieved only through continued phylogenetic studies, especially of those species endemic to China that have often been excluded from previous analyses. Earlier molecular studies have shown that Chinese Allium is not monophyletic, so the goal of the present study was to infer the phylogeny and biogeography of Allium and to provide a classification of Chinese Allium by placement of Chinese species in the context of the entire phylogeny. METHODS: Phylogenetic studies were based on sequence data of the nuclear ribosomal internal transcribed spacer (ITS) and chloroplast rps16 intron, analysed using parsimony and Bayesian approaches. Biogeographical patterns were conducted using statistical dispersal-vicariance analysis (S-DIVA). KEY RESULTS: Phylogenetic analyses indicate that Allium is monophyletic and consists of three major clades. Optimal reconstructions have favoured the ancestors of Amerallium, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum as originating in eastern Asia. CONCLUSIONS: Phylogenetic analyses reveal that Allium is monophyletic but that some subgenera are not. The large genetic distances imply that Allium is of ancient origin. Molecular data suggest that its evolution proceeded along three separate evolutionary lines. S-DIVA indicates that the ancestor of Amerallium, Anguinum, Vvedenskya, Porphyroprason and Melanocrommyum originated from eastern Asia and underwent different biogeographical pathways. A taxonomic synopsis of Chinese Allium at sectional level is given, which divides Chinese Allium into 13 subgenera and 34 sections.

Asparagales, the largest monocot order, is renowned for its ecological, economic, and medicinal significance. Here, we leverage transcriptome data from 455 Asparagales species to explore the phylogeny of Asparagales. Moreover, we investigate the evolutionary patterns of the genes involved in allium flavor formation. We not only establish a robust bifurcating phylogeny of Asparagales but also explore their reticulate relationships. Notably, we find that eight genes involved in the biosynthesis of allium flavor compounds underwent expansion in Allium species. Furthermore, we observe Allium -specific mutations in one amino acid within alliinase and three within lachrymatory factor synthase. Overall, our findings highlight the role of gene expansion, increased expression, and amino acid mutations in driving the evolution of Allium -specific compounds. These insights not only deepen our understanding of the phylogeny of Asparagales but also illuminate the genetic mechanisms underpinning specialized compounds. Asparagales is the largest monocot order. Here, the authors produce the phylogeny of Asparagales with transcriptomic data from 455 species and investigate the evolution of genes involved with allium flavor biosynthesis.

The photoperiod marks a varied set of behaviors in plants, including bulbing. Bulbing is controlled by inner signals, which can be stimulated or subdued by the ecological environment. It had been broadly stated that phytohormones control the plant development, and they are considered to play a significant part in the bulb formation. The past decade has witnessed significant progress in understanding and advancement about the photoperiodic initiation of bulbing in plants. A noticeable query is to what degree the mechanisms discovered in bulb crops are also shared by other species and what other qualities are also dependent on photoperiod. The FLOWERING LOCUS T (FT) protein has a role in flowering; however, the FT genes were afterward reported to play further functions in other biological developments (e.g., bulbing). This is predominantly applicable in photoperiodic regulation, where the FT genes seem to have experienced significant development at the practical level and play a novel part in the switch of bulb formation in Alliums. The neofunctionalization of FT homologs in the photoperiodic environments detects these proteins as a new class of primary signaling mechanisms that control the growth and organogenesis in these agronomic-related species. In the present review, we report the underlying mechanisms regulating the photoperiodic-mediated bulb enlargement in Allium species. Therefore, the present review aims to systematically review the published literature on the bulbing mechanism of Allium crops in response to photoperiod. We also provide evidence showing that the bulbing transitions are controlled by phytohormones signaling and FT-like paralogues that respond to independent environmental cues (photoperiod), and we also show that an autorelay mechanism involving FT modulates the expression of the bulbing-control gene. Although a large number of studies have been conducted, several limitations and research gaps have been identified that need to be addressed in future studies.