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Biological processes in clusters 1 and 2 (see Figure 4), as revealed by analysis of GO term distribution using Blast2GO and REVIGO algorithms. GO terms are represented by circles and are plotted according to semantic similarities to other GO terms (adjoining circles are most closely related). Circle size is proportional to the abundance of the GO term in the cluster, while color indicates semantic similarities. Only GO terms with higher than 1% frequency in the cluster are shown. (A) Cluster 1. Main patterns are related to the general development of reproductive tissues, metabolism, microsporogenesis and cell-division processes and specific related fertility processes. (B) Cluster 2. Main patterns are related to energy-consuming activities and/or response to stress.
Source publication
Commercial cultivars of garlic, a popular condiment, are sterile, making genetic studies and breeding of this plant challenging. However, recent fertility restoration has enabled advanced physiological and genetic research and hybridization in this important crop. Morphophysiological studies, combined with transcriptome and proteome analyses and qu...
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Citations
... Normal tapetum function requires the properly timed initiation and progression of programmed cell death (PCD) (Papini et al., 1999;Kawanabe et al., 2006;Ji et al., 2013). Non-regulated PCD of the tapetum can lead to energy deficiency and consequent pollen abortion in garlic (Shemesh-Mayer et al., 2015). Abnormal tapetal development has been previously described as a possible cause of male sterility in garlic (Novak, 1972;Shemesh-Mayer et al., 2015), onion (Allium cepa) (Holford et al., 1991), lily (Lilium Asiatic) (Wang et al., 2019) and Arabidopsis thaliana (Chaudhury et al., 1994). ...
... Non-regulated PCD of the tapetum can lead to energy deficiency and consequent pollen abortion in garlic (Shemesh-Mayer et al., 2015). Abnormal tapetal development has been previously described as a possible cause of male sterility in garlic (Novak, 1972;Shemesh-Mayer et al., 2015), onion (Allium cepa) (Holford et al., 1991), lily (Lilium Asiatic) (Wang et al., 2019) and Arabidopsis thaliana (Chaudhury et al., 1994). ...
... Cultivated garlic is a natural male-sterile material and an ideal female parent for hybrid production. Limited by the availability of male-fertile garlic cultivars, research has mainly focused on the analysis of organ-and tissue-specific gene expression in garlic (Allium sativum L.) using transcriptome data (Kamenetsky et al., 2015;Shemesh-Mayer et al., 2015;Havey and Ahn, 2016). The release of the garlic genome (Sun et al., 2020;Hao et al., 2023), and especially the availability of a fertile garlic cultivar G398, which has been identified and maintained by our group for more than 20 years, provide a strong foundation for a systematic analysis of the molecular mechanisms underlying the sterility of garlic cultivars. ...
Garlic cultivars are predominantly characterized by their sterility and reliance on asexual reproduction, which have traditionally prevented the use of hybrid breeding for cultivar improvement in garlic. Our investigation has revealed a notable exception in the garlic line G398, which demonstrates the ability to produce fertile pollen. Notably, at the seventh stage of anther development, callose degradation in the sterile line G390 was impeded, while G398 exhibited normal callose degradation. Transcriptome profiling revealed an enhanced expression of the callose-degrading gene, AsaNRF1, in the mature flower buds of the fertile line G398 compared to the sterile line G390. An insertion in the promoter of AsaNRF1 in G390 was identified, which led to its reduced expression at the tetrad stage and consequently delayed callose degradation, potentially resulting in the male sterility of G390. A discriminatory marker was developed to distinguish between fertile G398 and sterile G390, facilitating the assessment of male fertility in garlic germplasm resources. This study introduces a practical approach to harnessing garlic hybridization, which can further facilitate the breeding of new cultivars and the creation of novel male-fertile garlic germplasm using modern molecular biology methods.
... These accessions were obtained from local markets or national institutions in each country. Detailed information regarding these accessions was reported by Etoh [27] and Hirata et al. [28]. 'White-roppen' black garlic was processed in a rice cooker using warm mode for two weeks. ...
To investigate the bioactivities of fresh garlic and its processed product, black garlic, we conducted comparative analyses of antioxidant, anti-inflammatory, innate immune activation, and anti-cancer activities in addition to the chemical composition (sugar, amino acid, and polyphenol contents) of these materials. Simultaneous assay using neutrophil-like cells showed that fresh garlic exhibited antioxidant and innate immunostimulatory activities, whereas black garlic displayed a potent anti-inflammatory effect. The antioxidant activity index was correlated with phenol and flavonoid contents, while the innate immunostimulatory activity was correlated with fructan content. Furthermore, some black garlics with low fructose content were found to inhibit the proliferation of UM-UC-3 cancer cells, while other black garlics rich in fructose increased UM-UC-3 cell proliferation. It was shown that the processing of fresh garlic could change the composition of sugars, antioxidants, and amino acids, which have different effects on neutrophil-like cells and UM-UC-3 cells, as well as on bioactivities.
... Based on the literature and our previous research [13,17,35,[64][65][66], we surveyed flowering pathways and specific genes conceivably involved in the various stages of garlic floral development, e.g., meristem transition, floral scape elongation, differentiation of flowers, and floral organs. This survey resulted in a list of 543 candidate genes (Table S4). ...
Garlic, originating in the mountains of Central Asia, has undergone domestication and subsequent widespread introduction to diverse regions. Human selection for adaptation to various climates has resulted in the development of numerous garlic varieties, each characterized by specific morphological and physiological traits. However, this process has led to a loss of fertility and seed production in garlic crops. In this study, we conducted morpho-physiological and transcriptome analyses, along with whole-genome resequencing of 41 garlic accessions from different regions, in order to assess the variations in reproductive traits among garlic populations. Our findings indicate that the evolution of garlic crops was associated with mutations in genes related to vernalization and the circadian clock. The decline in sexual reproduction is not solely attributed to a few mutations in specific genes, but is correlated with extensive alterations in the genetic regulation of the annual cycle, stress adaptations, and environmental requirements. The regulation of flowering ability, stress response, and metabolism occurs at both the genetic and transcriptional levels. We conclude that the migration and evolution of garlic crops involve substantial and diverse changes across the entire genome landscape. The construction of a garlic pan-genome, encompassing genetic diversity from various garlic populations, will provide further insights for research into and the improvement of garlic crops.
... This large size is a common property among other Allium species, making it challenging to study. Prior to genome sequencing, some studies provided information on the transcriptome (the expressed part of the genome) of various tissues, such as meristems and other organs [67][68][69][70][71]. In addition to efforts to characterize the gene content of the garlic genome, efforts have also been made since 2015 to identify genes in phylogenetically close species, such as onion [72], bunching onions [73] and Chinese chives [74]. ...
... The study of garlic genes will further our understanding, at the molecular level, of the main problems faced by this crop, such as the infertility. Some transcriptomic studies aimed at understanding its molecular basis and might help to restore the production of true seeds in some varieties [8,71]. Other studies have focused on the relationship between storage temperatures and bulb formation [75]. ...
Citation: Parreño, R.; Rodríguez-Alcocer, E.; Martínez-Guardiola, C.; Carrasco, L.; Castillo, P.; Arbona, V.; Jover-Gil, S.; Candela, H. Turning Garlic into a Modern Crop: State of the Art and Perspectives. Plants 2023, 12, 1212. Abstract: Garlic is cultivated worldwide for the value of its bulbs, but its cultivation is challenged by the infertility of commercial cultivars and the accumulation of pathogens over time, which occurs as a consequence of vegetative (clonal) propagation. In this review, we summarize the state of the art of garlic genetics and genomics, highlighting recent developments that will lead to its development as a modern crop, including the restoration of sexual reproduction in some garlic strains. The set of tools available to the breeder currently includes a chromosome-scale assembly of the garlic genome and multiple transcriptome assemblies that are furthering our understanding of the molecular processes underlying important traits like the infertility, the induction of flowering and bulbing, the organoleptic properties and resistance to various pathogens.
... Further, Shemesh-Mayer et al. (2015a) also suggested that the sterility in garlic is governed by genetic factors as it was not restored by temperature changes. RNAseq and proteomic studies indicated the energy deficiency caused due to respiratory restrictions or non-regulated programmed cell death led to the pollen abortion in the male-sterile genotype (Shemesh-Mayer et al., 2015b). The genes for the restorer of fertility factor (Rf) have been identified in several species and are found to be a member of the pentatricopeptide repeat family of proteins (PPR). ...
Alliums are not considered breeder-friendly crops due to their complex nature, breeding behaviour and large genome. The study of trait genetics and breeding of Allium crops is challenging due to some inherent characteristics such as a high degree of cross-pollination, inbreeding depression and biannual life cycle in many alliaceous crops. Hence, despite their nutritional and economic importance, only limited genetic and genomic information is available. The challenging task of working with large genome size (10–30 pg/IC)(Ricroch et al., 2005) leads to difficulty in sequencing, limited markers availability and, eventually, hampered mapping and genomics-assisted breeding in these crops. The present chapter reviews genetic studies of important traits in alliums.
... (C) Tissue-specific expression patterns of garlic PEBP genes in vegetative and reproductive organs and seeds. The expression values were computed as FPKM based on transcriptome analyses of vegetative and reproductive organs and seeds [11,12,19,52]. FPKM values were used to create a heat map by one minus Pearson correlation, with MORPHEUS [53] . ...
... includes only 166 bp, located between nucleotide positions 318,450,068 and 318,450,234 (Table 1). We analyzed the expression patterns of this sequence in the transcriptome catalog of developing garlic flowers [52] and found that the expression extends both upstream (from 318,449,800) and downstream (to 318,450,400); thus, the actual gene might be longer than 500 bp ( Figure 2B). ...
... Table 1). The gray boxes represent the reads for expression of the transcriptome sequence of the individual flowers [52] upstream and downstream of the genomic sequence of AsLFY2. (C) Transcriptome analysis of AsLFYs in vegetative and reproductive tissues and seeds of garlic [11,12,19,52]. ...
Commercial cultivars of garlic are sterile, and therefore efficient breeding of this crop is impossible. Recent restoration of garlic fertility has opened new options for seed production and hybridization. Transcriptome catalogs were employed as a basis for garlic genetic studies, and in 2020 the huge genome of garlic was fully sequenced. We provide conjoint genomic and transcriptome analysis of the regulatory network in flowering garlic genotypes. The genome analysis revealed phosphatidylethanolamine-binding proteins (PEBP) and LEAFY (LFY) genes that were not found at the transcriptome level. Functions of TFL-like genes were reduced and replaced by FT-like homologs, whereas homologs of MFT-like genes were not found. The discovery of three sequences of LFY-like genes in the garlic genome and confirmation of their alternative splicing suggest their role in garlic florogenesis. It is not yet clear whether AsLFY1 acts alone as the “pioneer transcription factor” or AsLFY2 also provides these functions. The presence of several orthologs of flowering genes that differ in their expression and co-expression network advocates ongoing evolution in the garlic genome and diversification of gene functions. We propose that the process of fertility deprivation in garlic cultivars is based on the loss of transcriptional functions of the specific genes.
... (C) Tissue-specific expression patterns of garlic PEBP genes in vegetative and reproductive organs and seeds. The expression values were computed as FPKM based on transcriptome analyses of vegetative and reproductive organs and seeds [11,12,19,52]. FPKM values were used to create a heat map by one minus Pearson correlation, with MORPHEUS [53]. ...
... includes only 166 bp, located between nucleotide positions 318,450,068 and 318,450,234 (Table 1). We analyzed the expression patterns of this sequence in the transcriptome catalog of developing garlic flowers [52] and found that the expression extends both upstream (from 318,449,800) and downstream (to 318,450,400); thus, the actual gene might be longer than 500 bp ( Figure 2B). Table 1). ...
... Table 1). The gray boxes represent the reads for expression of the transcriptome sequence of the individual flowers [52] upstream and downstream of the genomic sequence of AsLFY2. (C) Transcriptome analysis of AsLFYs in vegetative and reproductive tissues and seeds of garlic [11,12,19,52]. ...
Background
Commercial cultivars of garlic produce neither flowers nor seeds, and therefore efficient breeding of this important vegetable and medicinal crop is impossible. New avenues for hybridization and seed production were recently opened by the restoration of garlic fertility. The huge genome of garlic was fully sequenced in 2020 but, before that, transcriptome catalogs had been employed as a basis for garlic genetic studies. Here, we provide the conjoint genomic and transcriptome analysis of the regulatory network in flowering garlic genotypes.
Results
Our genome-wide analysis revealed phosphatidylethanolamine-binding proteins (PEBP) and LEAFY (LFY) genes that were not previously observed at the transcriptome level. Functions of TFL-like genes were reduced and probably replaced by FT-like homologs, whereas homologs of MFT-like genes were not found in the garlic genome. The discovery of three sequences of LFY-like genes in the garlic genome and confirmation of their alternative splicing suggest their key role in garlic florogenesis. It is not yet clear whether only one gene—AsLFY1—acts alone as the "pioneer transcription factor" or AsLFY2 also provides these functions.
Conclusions
The garlic genome, including key flowering genes, is highly repetitive. The presence of several orthologs of flowering genes that differ in their temporal and spatial expression and co-expression network advocates ongoing evolution in the garlic genome and diversification of gene functions. We propose that the process of fertility deprivation in garlic cultivars is based on the loss of transcriptional functions of the specific genes. Further comparisons of the genome and transcriptome factors in flowering and non-flowering garlic genotypes will clarify the possible evolution of their reproductive traits and contribute to fertility restoration and efficient breeding of this important crop.
... A. sativum cultivars have a somatic chromosome number 2n = 16 with a karyotypic formula of six metacentric chromosomes, four submetacentric chromosomes, and six acrocentric chromosomes (Jo et al. 2012) and its genome size is estimated at 15.9 Gbp, which is 32 folds larger than the rice genome (Shemesh-Mayer et al. 2015) and thus, obvious to infer that full sequencing of the garlic genome remains a challenging task . Unusually, garlic was continued to consider as a sexually sterile and its sterility barred the enhancement of garlic genetic potency through cross-hybridization (Lampasona et al. 2003). ...
‘Garlic’ (Allium sativum L.) is the second most important cultivated Allium known throughout the world. It is known for its versatile use as a spice, condiment, vegetable and an intended medicinal panacea. Its clove contains sulphur-based compound ‘Alliin’ (S-allyl-L-cysteine sulfoxide) predominantly as an active ingredient, which on physical injury to the clove becomes ‘Allicin’. Alliin and allicin both are devoid of lachrymatory factor so, it does not make one tears-up while chopping garlic cloves. Origin, history, phylogeny, different types with classification, propagation, bulbils, flowering potential, studies with fertile clones, germplasm, improvement efforts along with the worth knowing well-researched facts about garlic are consolidated in the present paper. This review aims to convey an amalgamated overview of garlic and necessarily provides a retrospect of garlic’s past to have a rear-view and helps to understand the status quo from the research standpoint further. It is an attempt to speculate garlic’s research dimensions.
... Through transcriptome analysis and global gene-expression profiling, Shemesh-Mayer et al. (2015) showed that more than 16,000 genes are differentially expressed in the developing flowers of fertile garlic plants compared with male-sterile ones. Genes associated with the fertility-related pathways such as starch and glycerol-3-phosphate metabolism, hexose biosynthesis, fatty-acyl-CoA transport, naringenin-chalcone synthase activity, Ras and Rab GTPase activity were found to be differentially expressed. ...
... Comparative proteome analysis of fertile and male sterile garlic lines through 2D protein maps has shown 36 protein spots differing significantly, of which nine were present only in the male-sterile line (Shemesh-Mayer et al., 2015). Dufoo-Hurtado et al. (2015) have shown that the low-temperature conditioning of garlic seed cloves at 5°C for 5 weeks changes the sprouts proteome. ...
Families Cucurbitaceae and Amaryllidaceae accommodate important vegetable crops such as gourds, melons, and onions, which all have received substantial quantum of breeding efforts. These crops have been in pace with the sequential developments in omics, beginning from the development of molecular markers and marker-assisted selection, genome sequencing and analysis, transcriptome and gene expression analysis, proteome and target protein analysis, metabolome analysis, and in seeking the roles of microRNAs in functional and developmental biology. Bioinformatics tools have also been extensively supporting their breeding programs. This chapter consolidates the progress made in Cucurbitaceous and Amaryllidaceous vegetables, through omics approaches.
... Although fertility restoration of garlic has been achieved, the commercial garlic varieties are still sterile due to pollen degeneration and reproduced vegetatively by planting individual cloves or bulbils (Pooler and Simon, 1994;Etoh and Simon, 2002;Simon and Jenderek, 2003;Shemesh Mayer et al., 2013;Shemesh-Mayer and Kamenetsky-Goldstein, 2021), and consequently, the classical hybridization in breeding strategy and genetic studies of this economically important crop has been strictly hindered for a long time (Shemesh-Mayer et al., 2015). Its germplasm resources for improvement are severely lacking. ...
Garlic (Allium sativum L.) is a compelling horticultural crop with high culinary and therapeutic values. Commercial garlic varieties are male-sterile and propagated asexually from individual cloves or bulbils. Consequently, its main breeding strategy has been confined to the time-consuming and inefficient selection approach from the existing germplasm. Polyploidy, meanwhile, plays a prominent role in conferring plants various changes in morphological, physiological, and ecological properties. Artificial polyploidy induction has gained pivotal attention to generate new genotype for further crop improvement as a mutational breeding method. In our study, efficient and reliable in vitro induction protocols of autotetraploid garlic were established by applying different antimitotic agents based on high-frequency direct shoot organogenesis initiated from inflorescence explant. The explants were cultured on solid medium containing various concentrations of colchicine or oryzalin for different duration days. Afterward, the ploidy levels of regenerated plantlets with stable and distinguished characters were confirmed by flow cytometry and chromosome counting. The colchicine concentration at 0.2% (w/v) combined with culture duration for 20 days was most efficient (the autotetraploid induction rate was 21.8%) compared to the induction rate of 4.3% using oryzalin at 60 μmol L–1 for 20 days. No polymorphic bands were detected by simple sequence repeat analysis between tetraploid and diploid plantlets. The tetraploids exhibited a stable and remarkable dwarfness effect rarely reported in artificial polyploidization among wide range of phenotypic variations. There are both morphological and cytological changes including extremely reduced plant height, thickening and broadening of leaves, disappearance of pseudostem, density reduction, and augmented width of stomatal. Furthermore, the level of phytohormones, including, indole propionic acid, gibberellin, brassinolide, zeatin, dihydrozeatin, and methyl jasmonate, was significantly lower in tetraploids than those in diploid controls, except indole acetic acid and abscisic acid, which could partly explain the dwarfness in hormonal regulation aspect. Moreover, as the typical secondary metabolites of garlic, organosulfur compounds including allicin, diallyl disulfide, and diallyl trisulfide accumulated a higher content significantly in tetraploids. The obtained dwarf genotype of autotetraploid garlic could bring new perspectives for the artificial polyploids breeding and be implemented as a new germplasm to facilitate investigation into whole-genome doubling consequences.
