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2021 Volume 1
Article Contents
Abstract
Introduction
Amf symbiosis helps the sustainable development of vegetable cultivation
The molecular mechanism of am symbiosis in vegetables
Conclusions and future prospects
Acknowledgments
Conflict of interest
Supplementary information
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References
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ARTICLE   Open Access    

Comparative analysis of the TCP gene family in celery, coriander and carrot (family Apiaceae)

  • 1.

    College of Life Sciences/Center for Genomics and Bio-computing, North China University of Science and Technology, Tangshan 063210, China

  • 2.

    School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China

  • 3.

    Food Science and Technology Department, University of Nebraska-Lincoln, Lincoln, NE 68588, USA

  • 4.

    Faculty of Life Science, Tangshan Normal University, Tangshan 063000, China

  • These authors contributed equally: Qiaoying Pei, Nan Li
More Information
  • Apiaceae is one of the most important families in Apiales and includes many economically important vegetables and medicinal plants. The TEOSINTE BRANCHED 1/CYCLOIDEA/PROLIFERATING CELL FACTOR 1/2 (TCP) gene family plays an important role in regulating plant growth and development, but it has not been widely studied in Apiaceae. In the present study, we identified 215 TCP family genes in six species of plant, of which 122 genes were present in three Apiaceae including 29 in celery (Apium graveolens), 43 in coriander (Coriandrum sativum), and 50 in carrot (Daucus carota). Whole-genome duplication likely contributed to TCP gene family expansion in Apiaceae. There were more paralogs in carrot than in coriander and celery, which was attributable to the greater number of tandem and proximal duplicated genes on chromosome 1. Nine microRNAs were found to regulate 20 TCP genes in the three Apiaceae species, with miR-319 having the most target genes. Several TCP genes showed high expression in the root, petiole and leaf of celery and coriander. These results provide a basis for comparative and functional genomic analyses of TCP genes in Apiaceae and other plants.

  • Introduction

    Vegetables are important food sources for humans, providing fiber, vitamins, carotenes and other nutrients[1]. However, due to limited arable land, many vegetables are cultivated in unfavorable conditions, such as drought and salinity. In addition, some vegetables are repeatedly grown in the same areas for several years in succession, which often causes serious soil-borne diseases. These stresses significantly reduce the yield and the quality of vegetables[2].

    AM (arbuscular mycorrhizal) symbiosis is an important way to enhance the stress tolerance in host plants. More than 72% of terrestrial plants, including many vegetables, can form AM symbiosis with AMF (AM fungi), which belongs to the sub-phylum Glomeromycota[3]. Modern agricultural activities often cause serious environmental pollution partly because farmers tend to over-apply fertilizers to achieve high yield. The application of AM fungi is a good strategy to improve the agricultural environment and ecology during vegetable cultivation, and in particular it has positive effects on vegetable growth under low Pi condition as summarized by two previous reviews[4,5]. However, establishment of AM symbiosis is not always successful in plants and it usually inhibited by high Pi (phosphate) conditions[6−13]. In addition to the optimization of AM fungi application in vegetable cultivation, we can breed new vegetable varieties with stronger ability to establish AM symbiosis. To this end, understanding the molecular mechanism underlying AM symbiosis in different vegetables, as well as in various conditions, will be very helpful. In recent years, the molecular mechanism of AM symbiosis in vegetable studies has emerged, and here we review the important progress in the molecular mechanism of AM symbiosis, with special focus on its application in vegetable growth.

    AMF symbiosis helps the sustainable development of vegetable cultivation

    The extraradical hyphae of AMF can extend the root surface by more than 10 cm, forming an extensive absorbing network beyond the rhizosphere nutrient-depletion zones around roots[14,15]. This allows host plants to access a larger volume of soil than the roots without AMF colonization. The extraradical hyphae of AMF can transfer many elements, such as nitrogen (N), phosphorus (P), sulfur (S) and potassium (K), and H2O, from soil far away to the host roots, which greatly benefits the plant growth (Fig. 1)[3]. It was reported that AMF colonization promoted the accumulation of biomass of Allium L. genus, such as onion and leek[16]. This study showed that the total biomass of Allium cepa inoculated with R. intraradices was at least twice as much as the uninoculated plants[17]. Interestingly, the Allium cepa inoculated with the mixed AMF (F. monosporus, R. clarum, D. nigra and A. laevis) (Table 1) exhibited increased dry weight of shoots, roots and bulbs by 84%, 110%, and 41.6% respectively[18]. However, the promotion effect by AMF varies in different species of Allium cepa. The fresh weight of Allium cepa cv. Karmen inoculated with R. irregularis was just slightly increased compared with Allium cepa cv. Kuba, Sochaczewska and Wolska, although Allium cepa cv. Karmen could also be well colonized by AMF[19]. The total dry weight of Allium fistulosum inoculated with R. intraradices (Table 1) was increased by nearly 150%[17] and the Allium ampeloprasum var. Porrum inoculated with R. irregularis (Table 1) showed an increased biomass of at least 100%[20]. These results suggest that the establishment of AMF can help to achieve the increased yield in Allium L genus without further fertilizer application.

    Figure 1.  The formation of AM symbiosis improves the stress tolerance of host plants. The phosphorus (P), nitrogen (N), potassium (K) and other essential nutrients in soil are transferred to the host plants via extraradical hyphae to increase the quality and yield of host plants. The formation of AM symbiosis also enhances the defense of the host plants against various pathogens and the tolerance to HMs (heavy metals) and salt stresses. The thickness of the gray arrow represents the amount of N leaching.
    DownLoad: Full-Size Img PowerPoint
    Table 1.  The morphological characters of different AM fungi[77, 78].
    Abbreviated nameFull nameNumber of spore wallsMycorrhizal structures stained
    by trypan blue
    A. laevisAcaulospora laevis3V, A, H
    C. claroideumClaroideoglomus claroideum1V, A, H
    C. etunicatumClaroideoglomus etunicatum1V, A, H
    D. nigraDentiscutata nigra3A, H
    F. monosporusFunneliformis monosporus1V, A, H
    F. mosseaeFunneliformis mosseae1V, A, H
    G. albidaGigaspora albida1A, H
    R. clarumRhizoglomus clarum1V, A, H
    R. intraradicesRhizoglomus intraradices1V, A, H
    R. irregularisRhizophagus irregularis1V, A, H
    S. sinuosaSclerocystis sinuosa1V, A, H
    V, vesicles; A, arbuscules; H, hyphae.
     | Show Table
    DownLoad: CSV

    The formation of AM symbiosis is significantly inhibited in the plants supplied with high Pi[6−13]. Therefore, most studies examining the promotion effect by AMF were performed under low Pi conditions, which considerably limits the application of AMF in agriculture[5,21]. Interestingly, field trials showed that potato inoculated with R. intraradices could increase yield by 9.5% under conventional agricultural conditions, including the application of pesticides and fertilizers[22,23]. In addition, Solanum lycopersicum cv. Brioso and var. MicroTom inoculated with R. irregularis were also shown to gain the increased yield and enhanced fruit quality under sufficient Pi condition[24,25].

    Drought and soil salinity are the frequently occurred stresses that limit crop production in agriculture[26]. The tolerance of host plants against drought and soil salinity can be greatly enhanced by AMF (Fig. 1)[21]. The mixture of AM-fungal spores (R. intraradices, C. etunicatum, F. mosseae, F. geosporum, and C. claroideum) (Table 1) was still shown to increase the tolerance of Solanum lycopersicum cv. Syta seedlings to salt-stress under sufficient Pi conditions[27]. In addition, the inoculation with AMF can boost the plant defense responses to pathogen and disease under low Pi condition (Fig. 1)[20]. Under sufficient Pi condition, the inoculation with S. sinuosa and G. albida (Table 1) enables Phaseolus vulgaris cv. French bean survive the root-rot incidence, resulting in the yield increase by nearly 100%[28]. In Capsicum annuum cv. Charliston Bagci addition, the inoculation with F. mosseae and C. etunicatum (Table 1) alleviates the symptoms of Phytophthora blight[29].

    Usually crops can only take up half of the nutrients in the applied chemical fertilizers, while the other half are leached into ground water and surface water, leading to eutrophication and loss of biodiversity[30]. N, a major nutrient in fertilizers, can also be lost from soil as a potent greenhouse gas, including N2O (nitrous oxide) and N2 (dinitrogen gas)[31−34]. Interestingly, the inoculation with R. irregularis in Solanum lycopersicum cv. 76R decreased losses of NO−3 by 54%[35].

    Heavy metal pollution is a worldwide problem. AMF has been emerging as a cost-effective and environmently friendly strategy to assist alleviation of heavy metal phytotoxicity[36]. The previous study showed that Cajanus cajan cv. Millsp inoculated with F. mosseae significantly decreased Cd uptake (by 20%) in the root[37]. This result indicates the potential value of AMF for cultivating vegetables in soil slightly polluted by heavy metal. In addition to the alleviation of heavy metal phytotoxicity, AMF can also enhance the plant tolerance to cold, which has been well summarized in a previous review[5].

    The molecular mechanism of AM symbiosis in vegetables

    SLs (Strigolactones) are a group of carotenoid-derived compounds synthesized in plant roots and secreted into the rhizosphere where SLs activate mitochondria and energy metabolism of AMF to promote spore germination and prime the branching of extraradical hyphae[38]. Pea shoots branching mutants (rms (RAMOSUS)1-6) were obtained many years ago by ethylmethanesulfonate mutagenesis[39], but until recently, researchers confirmed the causive genes in the mutants (rms1-5) are involved in the biosynthesis and perception of SLs and the reduced AM symbiosis was observed in these mutants (Fig. 2a, Table 2)[40−43]. In tomato, the function of SlCCD7 (Carotenoid Cleavage Dioxygenase 7), the enzyme involved in the biosynthesis of SLs, is essential for the formation of AM symbiosis[44]. Other genes that affect SLs pathway, such as SlIAA7 was also shown to regulate AM symbiosis (Fig. 2a, Table 2)[45].

    Figure 2.  The molecular mechanism of AM symbiosis in vegetables. (a) RMS1/4/5 are involved in biosynthesis of SLs that promote the spore germination and prime the branching of extraradical hyphae. SlLYK10 binds to COs/LCOs that are secreted by AMF to regulate AM symbiosis. CSSP is required for the early invasion of intra-hyphae and branching of arbuscule. PvRbohB negatively affects the early invasion of intra-hyphae by controlling ROS levels in beans. GmPAP33 negatively regulates the arbuscule degeneration by promoting the hydrolysion of phosphatidylcholine and phosphatidic acid. (b) Many proteins located on PAM, such as SlPT4, SlHA8, SlHAK10 and GmAMT4.1, are required for the exchange of the nutrients and signals between AM and host plants. In addition, GRAS proteins, such as DELLA, RAM1 and RAD1, can regulate the formation of arbuscule.
    DownLoad: Full-Size Img PowerPoint
    Table 2.  The genes involved in the formation of AM symbiosis in different crop species.
    GeneOrganismGene functionMutant phenotype involved in AM symbiosisReference
    RMS1PeaRequired for the biosynthesis of SLsReduced the colonization levels of AM symbiosis[40]
    RMS4PeaRequired for the biosynthesis of SLsReduced the colonization levels of AM symbiosis[41]
    RMS5PeaRequired for the biosynthesis of SLsReduced the colonization levels of AM symbiosis[40]
    NAPeaRequired for the biosynthesis of GAsIncreased the colonization levels of AM symbiosis[46]
    SlCCD7TomatoRequired for the biosynthesis of SLsReduced the colonization levels of AM symbiosis[44]
    SlIAA7TomatoRequired for the biosynthesis of SLsReduced the colonization levels of AM symbiosis[45]
    SlLYK10TomatoRequired for the perception of LCOsReduced the colonization levels of AM symbiosis[48]
    SlLYK12TomatoRequired for the perception of LCOsReduced the colonization levels of AM symbiosis[49]
    SlCCaMKTomatoRequired for the calcium ion spiking in the nuclearReduced the early invasion of intra-hyphae and the branching of arbuscule[48]
    SlCYCLOPSTomatoRequired for the induction of RAM1Reduced the early invasion of intra-hyphae and the branching of arbuscule[51]
    GmSYMRKα/βSoybeanRequired for the calcium ion spiking in the nuclearReduced the early invasion of intra-hyphae[52]
    PvRbohBBeanRequired for the production of ROSIncreased the early invasion of intra-hyphae[53]
    CRY/LA
    (DELLA)    		PeaRequired for the induction of RAM1 and interacted with MYB1Inhibited the branching and the degeneration of arbuscule[46]
    SlDLK2TomatoRemains unknownIncreased the colonization levels of AM symbiosis[60]
    SlPT4TomatoRequired for the transporting of phosphateReduced the colonization levels of AM symbiosis[54]
    SlHA8TomatoRequired for the generation of H+ gradientInhibited the branching of arbuscule[57]
    SlHAK10TomatoRequired for the transporting of potassiumReduced the colonization levels of AM symbiosis[56]
    TSBTomatoMicrotubules-associated geneReduced the colonization levels of AM symbiosis[62]
    GmPAP33SoybeanRequired for the promotion of hydrolysis of phosphatidylcholine and phosphatidic acidIncreased the percentage of small arbuscule[63]
     | Show Table
    DownLoad: CSV

    In contrast to the rms1-5 mutants in pea, the Gibberellin acids (GAs)-deficient pea mutant (na-1) showed a significant increase of AM symbiosis (Table 2), suggesting GAs have a negative effect on AM symbiosis[46]. This GA-mediated negative effect on AM symbiosis was also confirmed in other species, including rice, Medicago truncatula and Lotus japonicus[37]. Besides SLs and GAs, other phytohormones can also affect AM symbiosis and their roles in AM symbiosis have been previously reviewed[46].

    AMF can produce short chain chitooligosaccharides (COs) and lipo-chitooligosaccharides (LCOs), which are bound by LYSIN MOTIF RECEPTOR KINASE (LYK) to activate Ca2+ spiking and initiate AM symbiosis[47]. In tomato, SlLYK10 and SlLYK12 are required for AM symbiosis and SlLYK10 can bind to LCOs (Fig. 2a, Table 2)[48−50]. Besides the perception of signals from AMF, the common symbiosis signaling pathway (CSSP) is activated in the host plants to initiate the formation of AM symbiosis and nodulation in legume (Fig. 2a, Table 2)[3]. In tomato, CCaMK (Calcium/Calmodulin-dependent protein Kinase) and CYCLOPS were shown to be indispensible for the early invasion of intra-hyphae (Fig. 2a, Table 2)[48,51]. In soybean, the ancestor of SYMRK (Symbiosis Receptor-like Kinase), also belonging to CSSP, gave rise to two paralogous genes GmSYMRKα and GmSYMRKβ, both of which are required for the early invasion of intra-hyphae (Fig. 2a, Table 2)[52]. In addition, the influencing factors also include ROS (reactive oxygen species) as PvRbohB has been shown to negatively regulate the early invasion of intra-hyphae by affecting ROS levels in beans (Fig. 2a, Table 2)[53].

    The intra-hyphae enter into the cortical cells of the host plants to form arbuscule, which is then enveloped by the cell membrane called PAM (Periarbuscular Membrane) (Fig. 2b)[3]. Many PAM locating proteins, such as SlPT4 (Phosphate Transporter 4), SlHA8 (H+-ATPase 8), SlHAK10 (High-affinity K+ Transporter 10) and GmAMT4.1 (Ammonium Transporter 4.1), are required for the exchange of the nutrients and signals and AM symbiosis (Fig. 2b, Table 2)[54−57]. The arbuscule is also regulated by many TFs (Transcriptional Factors), such as RAM1 (Reduced Arbuscular Mycorrhiza 1) and RAD1 (Required for Arbuscule Development 1), both of which belong to GRAS family[57]. The loss-of-function of DELLA, another GRAS family gene, caused impaired AM symbiosis in pea[46]. The follow-up studies further showed that DELLA interacted with CYCLOPS to enhance the expression of RAM1[58]. Interestingly, SlDELLA was also shown to interact with SlDLK2 (DWARF14-Like 2), a negative regulator of AM symbiosis, but the function of SlDLK2-SlDELLA complex is unclear yet (Table 2)[59]. The study in tomato suggested that many GRAS family TFs function redundantly to regulate AM symbiosis (Fig. 2b, Table 2)[60].

    The formation of arbuscule is also accompanied by the morphological and physiological changes of the arbuscule-containing cortical cells, partly due to the affected cytoskeletons[47]. A recent study showed that tsb (tomato similar to SB401) gene clustered into the same group as microtubules-associated proteins of Solanaceae species, providing further evidence supporting the roles of cytoskeletons in the arbuscule formation (Table 2)[61]. The arbuscule can usually survive for 7−14 d before the final degeneration, which is accompanied by the gradual disappearance of the PAM and matrix[58]. Previous studies showed that MYB1 induced the expression of hydrolase genes by forming a complex with GRAS family transcription factors DELLA and NSP1, and GmPAP33 (Purple Acid Phosphatase 33) inhibited the arbuscule degeneration by promoting the hydrolysis of phosphatidylcholine and phosphatidic acid (Fig. 2b, Table 2)[62,63].

    The formation of AM symbiosis is influenced by environmental conditions. Previous studies showed that high N and P both inhibited the formation of AM symbiosis[6−13, 64−68]. Recently, a study in tomato found that the FAB (fasciated and branched) and FIN (fasciated inflorescence), homologous genes to PsNARK (Nodule Autoregulation Receptor Kinase) and PsRDN1 (ROOT DETERMINED NODULATION 1) that are involved in autoregulation of nodulation, were required for the suppression of AM symbiosis by high N[68]. We found that conseved SPX-PHR module regulated the formation of AM symbiosis in response to different phoaphate conditions[69]. SlPHR1/4/10/11/12 were localized in the arbuscule-containing cells to transactivate the expression of AM maker genes. SlSPX1 interacted with them to inhibit their transactivity and negatively regulate the formation of AM symbiosis under medium and replete phoaphate conditions. The elevated atmospheric carbon dioxide (CO2) concentration, which causes problems to the global climate, has increasingly raised concerns. A recent study showed that the rise of atmospheric carbon dioxide could promote the formation of AM symbiosis by triggering the redox-auxin-strigolactone systemic signaling cascade[70].

    Conclusions and future prospects

    Accumulating evidence has shown that AMF can enhance the tolerance of host plants (including vegetables and crops) under abiotic and biotic stresses. However, the mechanism behind this AMF-mediated stress tolerance is not entirely clear. Microbiome has been emerging as an important way to dissect the underlying mechanism[71]. A few studies showed that AM symbiosis shaped the rhizosphere microbiota and some bacteria such as Streptomyces were beneficial to plants under different stresses[72−74]. In future, recently developed microbiome approaches will drive the progress in understanding whether AM symbiosis recruits the beneficial microbe during the defense against the abiotic and biotic stresses.

    Another major issue in the study of AM symbiosis is the effect of external environmental conditions, such as high N and P, which limit the application of AMF in vegetable cultivation[6−13,64−68]. The future studies of the molecular mechanism that limits AM symbiosis under different environmental conditions will benefit the breeding for cultivars with stronger stress resistance. Recently, we uncovered the mechanism behind the inhibition of AM symbiosis by repleted Pi condition in tomato and the key role of SlSPX1 in this process[69]. It is interesting to further examine how AM fungi help Slspx1 mutants to cope with abiotic and biotic stresses under replete Pi conditions, and this will provide the basis for the application of AM fungi in modern agriculture.

    The application of AM fungi in vegetables can also benefit from the studies in other crops as many genes involved in the formation of AM symbiosis are conserved in different species. In rice, it has been shown that the natural variation of OsCERK1 enhanced the colonization of AM symbiosis[75]. It is possible to modify the amino acid sequence of such genes, including the homologs of OsCERK1 in vegetables, to enhance the AM colonization in vegetable growth. Technical advancement can also facilitate this purpose. A recent study showed that the expression of the target gene can be up-regulated by a donor-DNA-free CRISPR/Cas-based approach[76], so the specific increase of the expresssion of target genes, such as SlPT4, SlHAK10 and SlHA8 that localize at PAM, to enhance the absorption of N, P and K form AM fungi is theoretically feasible.

    Acknowledgments

    This work is supported by the Natural Science Foundation of Fujian Province (2019J01418) and the Prominent Subject Foundation of Fujian Province (712018011) to Dehua Liao.

  • Shuang Wu is the Editorial Board member of journal Vegetable Research. He is blinded from reviewing or making decisions on the manuscript. The article was subject to the journal's standard procedures, with peer-review handled independently of this Editorial Board member and his research groups.

  • Supplemental Table S1 The TCP gene family members and their abbreviation name in celery, coriander, carrot, lettuce, grape, and Arabidopsis.
    Supplemental Table S2 The summary of TCP gene family members in  A.  graveolens , C. sativum, D. carota and compared with  A. thaliana .
    Supplemental Table S3 The list of orthologous TCP gene pairs between A. graveolens,  C. sativum, and  D. carota.
    Supplemental Table S4 The list of paralogous TCP gene pairs in each of other examined species.
    Supplemental Table S5 Ka/Ks calculation and divergent time of the orthologous  gene pairs between A. graveolens, C. sativum, and  D. carota.
    Supplemental Table S6 The duplicated type of TCP genes in A. graveolens,C. sativum and D. carota. The 0 to 4 indicate the singleton, dispersed, proximal, tandem, WGD duplication type, respectively.
    Supplemental Table S7 The prediction of target TCP family genes of miRNA in carrot, coriander, and celery.
    Supplemental Table S8 The expression level of the TCP genes in root, leaf and petiole for A. graveolens and C. savitum.  The gene expression was determined by the RNA-Seq data (RPKM).
    Supplemental Fig. S1 The gene structure of TCP gene family in three Apiaceae species.
    Supplemental Fig. S2 The circle plot of paralogous TCP gene pairs among three Apiaceae species.
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  • Cite this article

    Pei Q, Li N, Bai Y, Wu T, Yang Q, et al. 2021. Comparative analysis of the TCP gene family in celery, coriander and carrot (family Apiaceae). Vegetable Research 1: 5 doi: 10.48130/VR-2021-0005
    Pei Q, Li N, Bai Y, Wu T, Yang Q, et al. 2021. Comparative analysis of the TCP gene family in celery, coriander and carrot (family Apiaceae). Vegetable Research 1: 5 doi: 10.48130/VR-2021-0005
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Comparative analysis of the TCP gene family in celery, coriander and carrot (family Apiaceae)

  • 1.

    College of Life Sciences/Center for Genomics and Bio-computing, North China University of Science and Technology, Tangshan 063210, China

  • 2.

    School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 610054, China

  • 3.

    Food Science and Technology Department, University of Nebraska-Lincoln, Lincoln, NE 68588, USA

  • 4.

    Faculty of Life Science, Tangshan Normal University, Tangshan 063000, China

  • Received: 05 January 2021
  • Accepted: 11 June 2021
  • Published online: 22 June 2021
Vegetable Research  1,  Article number: 5  (2021)  |  Cite this article

Abstract: Apiaceae is one of the most important families in Apiales and includes many economically important vegetables and medicinal plants. The TEOSINTE BRANCHED 1/CYCLOIDEA/PROLIFERATING CELL FACTOR 1/2 (TCP) gene family plays an important role in regulating plant growth and development, but it has not been widely studied in Apiaceae. In the present study, we identified 215 TCP family genes in six species of plant, of which 122 genes were present in three Apiaceae including 29 in celery (Apium graveolens), 43 in coriander (Coriandrum sativum), and 50 in carrot (Daucus carota). Whole-genome duplication likely contributed to TCP gene family expansion in Apiaceae. There were more paralogs in carrot than in coriander and celery, which was attributable to the greater number of tandem and proximal duplicated genes on chromosome 1. Nine microRNAs were found to regulate 20 TCP genes in the three Apiaceae species, with miR-319 having the most target genes. Several TCP genes showed high expression in the root, petiole and leaf of celery and coriander. These results provide a basis for comparative and functional genomic analyses of TCP genes in Apiaceae and other plants.

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    INTRODUCTION

    • The Apiaceae family of plants includes more than 400 genera and 3,000 species[1,2]. Several Apiaceae species such as carrot (Daucus carota), celery (Apium graveolens), and coriander (Coriandrum sativum) are cultivated as a vegetable or for medicinal purposes worldwide[3,4].

      Celery is an annual or biennial herbage species originating from the Mediterranean and Middle East[5,6]. Besides being a vegetable, celery is also used as a medicinal plant[7]. Coriander, which is also known as cilantro, is a popular herb and a major ingredient of curry powder[8]. Carrot is an economically important vegetable with a high nutritional value[9]. All three of these plants are diploid species although their chromosome number and genome size differ: celery and coriander each have 22 chromosomes (2n = 2x = 22) whereas carrot has 18 (2n = 2x = 18)[3,10,11], and the assembled genome size of celery is 3.33 Gb, which is larger than coriander (2.11 Gb) and carrot (421.5 Mb)[3,11,12].

      The TCP gene family in plants is named after the first identified members—ie, TEOSINTE BRANCHED 1 (TB1) in maize (Zea mays)[13], CYCLOIDEA (CYC) in snapdragon (Antirrhinum majus)[14], and PROLIFERATING CELL FACTOR 1 (PCF1) and PCF2 in rice (Oryza sativa)[15]. TCP genes regulate multiple processes in plant growth and development such as shoot branching[16], seed germination[17,18], gametophyte development[19,20], leaf development[21−25], leaf senescence[26−28], mitochondrial biogenesis[29], flower development[30−32] and cell cycle[29,33]. There are 24 TCP genes in Arabidopsis thaliana[34], 22 in rice[34], 24 in tomato[35], 19 in plum[26], 42 in switchgrass[36], 36 in carrot[37], and 32 in celery[38]. However, to date, no TCP genes have been identified in coriander. High-quality genome sequences of celery, carrot and coriander were recently released[3,11,12], which can facilitate comparative analyses of specific genes in Apiaceae.

      In this study, we identified and characterized TCP genes in celery, coriander and carrot and performed comparisons with genes in Lactuca sativa (lettuce), Vitis vinifera (grape), and Arabidopsis. We mapped the TCP genes to chromosomes, identified orthologs and paralogs, detected collinearity and gene expansion or loss, and analyzed their expression patterns in plant tissues. Our results provide a basis for comparative studies on the function and evolution of TCP genes in plants.

    MATERIALS AND METHODS

      Identification of TCP family genes in celery, coriander and carrot

    • The genome sequences of coriander and celery were downloaded from the coriander genome database (http://cgdb.bio2db.com) and celery genome database (http://celerydb.bio2db.com), respectively[3,10]. The Arabidopsis genome sequence was retrieved from The Arabidopsis Information Resource (TAIR10; http://www.arabidopsis.org). The sequences of carrot (version 2), lettuce (version 5), and grape (Genoscope.12X) were downloaded from Phytozome (https://phytozome.jgi.doe.gov/pz/portal.html)[11,39,40]. The Pfam database (https://pfam.sanger.ac.uk) was used to identify TCP family genes with the identifier PF03634 (E value < 1e−4)[41]. The Simple Modular Architecture Research Tool (SMART v9.0) database and Conserved Domains Database (CDD) were used for domain validation[42,43].

      Phylogenetic analysis of TCP gene family

    • To analyze the evolutionary relationships of TCP genes in Apiaceae, multiple sequence alignment of the TCP amino acid sequences of Arabidopsis, grape, lettuce, carrot, coriander and celery was performed with ClustalW software (v2.0)[44] and a phylogenetic tree was constructed with the neighborhood-joining method (bootstrap = 1,000) using MEGA X[45]. The reconstructed TCP gene tree was compared to the actual species tree using Notung v2.9 software with default parameters[46,47].

      Chromosome location, gene structure and conserved motif analysis

    • The location of coriander, celery and carrot TCP genes on chromosomes was drawn using Tbtools software and the files were saved in general feature format (gff)[48]. Gene structure was determined using Gene Structure Display Server 2.0 (https://gsds.cbi.pku.edu.cn)[49]. Conserved motifs were analyzed using Multiple Expectation maximizations for Motif Elicitation suite 5.2.0 (http://meme-suite.org)[50].

      Analysis of orthologs and paralogs

    • Orthologous and paralogous TCP gene pairs in celery, coriander and carrot were analyzed using OrthoMCL software v2.0 (https://orthomcl.org/orthomcl)[51]. The relationships of the genes among the three species was depicted using Circos software (v0.69)[52].

      Identification of collinear blocks and duplication types

    • MCScanX was used to identify collinear blocks and duplication types of the TCP genes[53]. Whole-genome sequences were searched against themselves using BLASTp (E value < 1e−5). We extracted TCP genes located in the collinear blocks using Perl scripts. The duplication type of TCP genes was estimated using the subprogram duplicate_gene_classifier.

      Calculation of Ka/Ks and estimation of divergence time

    • The nonsynonymous rate (Ka), synonymous rate (Ks), their ratio (Ka/Ks) and divergence time among orthologous gene pairs of the three species were calculated using KaKs_Calculator 2.0[54]. The coding sequence of orthologous gene pairs were aligned using ClustalW (v2.0)[44]; AXTconvertor software (v1.0) was then used to convert the alignment file to axt format. Lastly, the Ka value, Ks value and their ratio were calculated based on the Nei–Gojobori method[54]. Ks was used to estimate the divergence time based on the formula T = Ks/2r, where r indicates neutral substitutions (5.2 × 10−9 for Apiaceae)[12].

      Analysis of selective pressures

    • We used the maximum likelihood method and codon substitution models to determine the likelihood ratio of positive selection. We analyzed each branch of the phylogenetic tree to infer ω (the ratio of nonsynonymous to synonymous distances) using CodeML implemented in PAML4.9[47,55]. We adopted a complete deletion method for analyzing alignments with gaps and eliminated sequences with gaps in over 40% of their length. The likelihood ratio test between M0 and M1 and between M7 and M8 models were used to determine variation sites.

      Identification of micro (mi)RNA target genes in the TCP gene family

    • Mature miRNA sequences of A. thaliana were downloaded from miRBase (release 22.1; http://www.mirbase.org)[56]. TCP genes that are miRNA targets were predicted using psRNATarget Schema v2 (2017 release)[57] with maximum expectation ≤ 3 and other default parameters. A miRNA–TCP gene network was constructed using Cytoscape v3.7.2 software[58].

      Expression of TCP genes

    • TCP gene expression data in celery and coriander were extracted from RNA sequencing (RNA-seq) datasets previously published by our group[3,10] using Perl script; the values were normalized as reads per kilobase per million reads (RKPM). An expression heatmap was created using TBtools software (v1.0)[48].

    RESULTS

      Identification of TCP genes in three Apiaceae species

    • We identified 29 TCP genes in the genome of celery, 43 in coriander, and 50 in carrot (Supplemental Table S1 and S2). Additionally, 24 TCP genes were identified in Arabidopsis along with 20 in grape and 49 in lettuce (Supplemental Table S2). Thus, a total of 215 TCP genes were identified in the six species for further analysis.

      Phylogenetic and functional analyses of TCP gene family

    • To classify the TCP gene family in plants, we constructed a phylogenetic tree of all 215 amino acid sequences from the six abovementioned species using MEGA X (Fig. 1). Consistent with the phylogenetic relationships described in Arabidopsis and grape, the phylogenetic tree had three groups according to the type of TCP protein domain including the PCF, CINCINNATA (CIN), and CYC/TB1 classes.

      Figure 1.  Phylogenetic tree of TCP family genes in three Apiaceae species (carrot, celery and coriander) and lettuce, grape and Arabidopsis. The topology of the phylogenetic tree was determined using IQ-TREE with maximum likelihood (ML) based on the JTT+F+R8 model. The bootstrap was set to 1,000 replicates, and values > 40% are shown. The three classes were identified based on bootstrap values and phylogenetic topology.

      In class PCF, there were ten AgTCP, 26 CsTCP, and 36 DcTCP genes; in class CYC/TB1, there were eight AgTCP, seven CsTCP, and seven DcTCP genes; and in class CIN, there were 11 AgTCP, ten CsTCP and seven DcTCP genes (Fig. 1 and Supplemental Table S2). Notably, in coriander and carrot there were more TCP genes in class PCF than in the other two classes.

      The functions of most TCP family genes have been well studied in the model plant Arabidopsis. We inferred the function of homologous genes within the same taxonomic group in the phylogenetic tree in order to clarify the function of TCP genes in Apiaceae. For example, AT1G53230.1 (AtTCP3) is known to suppress the expression of CUP-SHAPED COTYLEDON (CUC), resulting in cotyledon fusion[24]. We identified three TCP genes—namely, DcTCP34, AgTCP2, and CsTCP6—that clustered together with AtTCP3 (Fig. 1), suggesting that they are also related to cotyledon fusion. It may also be possible to deduce the function of other Apiaceae TCP genes based on the function of the homologous genes in Arabidopsis.

      TCP gene family structure and conserved motifs

    • We carried out a gene structure analysis of TCP family genes to identify exons, introns and untranslated regions (Supplemental Fig. S1). Of the 122 TCP genes in Apiaceae, 94—including all 50 DcTCP genes—lacked introns. Most TCP genes had a single exon, although there were some exceptions. For example, CsTCP15 (class CIN) had four exons and DcTCP11 (class PCF) had three. In general, genes in the same class or subclass had similar gene structure and size.

      As gene structure varied among genes, we performed a motif analysis to examine the structure in greater detail. We compared five motifs in Apiaceae species and found that motif 3 was found at the beginning of most genes, followed by motif 1 and motif 2 (Fig. 2). However, motif 2 was located at the start of the CsTCP7, DcTCP15, CsTCP23, CsTCP36, and CsTCP2 and motif 5 was present at the beginning of DcTCP11. Almost all TCP genes had motif 1 except for DcTCP and CsTCP in class PCF, indicating that this motif is highly conserved and plays an important role in Apiaceae. Motif 3 was also present in most TCP genes and is likely conserved in Apiaceae.

      Figure 2.  Conversed motifs in TCP family genes of three Apiaceae species.

      Most genes in classes CYC/TB1 and CIN lacked motif 2 except for DcTCP17 and CsTCP79. Only five genes in class CIN had motif 4, which was present in all class CYC/TB1 genes. Motif 5 was only found in class PCF and not in other classes. Interestingly, DcTCP14 (class PCF) did not have any of the 5 motifs, suggesting that they were lost during the course of the evolution of carrot. Thus, genes in the same class had similar motif composition, indicating that they are functionally similar.

      Chromosomal distribution of TCP genes in Apiaceae species

    • In celery, 27/29 TCP genes mapped to nine chromosomes (Fig. 3a and Supplemental Table S1). Two celery TCP genes did not map to any chromosomes, and no TCP family gene was found on chromosomes Agr6 and Agr10. There were five genes that mapped to chromosomes Agr3, Agr5, and Agr11 while only one was located on chromosomes Agr1 and Agr2.

      Figure 3.  Distribution of TCP transcription factors on each chromosome in three Apiaceae species. (a) Celery, (b) Coriander, (c) Carrot.

      In coriander, 35/43 TCP genes mapped to nine chromosomes (Fig. 3b and Supplemental Table S1); none were found on chromosome Csa8. Chromosome Csa9 had the most TCP genes (10), followed by chromosomes Csa7 (6) and Csa1 (5). Chromosomes Csa2 and Csa3 each had just one TCP gene.

      The 50 carrot TCP genes were unevenly distributed across nine chromosomes (Dca1–9) (Fig. 3c and Supplemental Table S1). Interestingly, TCP gene expansion was observed on chromosome 1, which had 16 genes. Additionally, 15 genes (DcTCP1–15) were clustered together, mainly through tandem and proximal duplication.

      Identification of orthologous and paralogous TCP genes in Apiaceae

    • We examined orthologous and paralogous gene pairs in Apiaceae and found that there were 22 orthologous gene pairs between any two of celery, coriander and carrot (Fig. 4 and Supplemental Table S3), indicating a close phylogenetic relationship between these species. There were only three paralogous gene pairs in celery and coriander (Supplemental Fig. S2 and Supplemental Table S4) but 29 were found in carrot.

      Figure 4.  Circle plot of orthologous TCP gene pairs among three Apiaceae species.

      The Ks value was calculated to estimate the divergence time of orthologous TCP gene pairs among celery, coriander and carrot (Fig. 5 and Supplemental Table S5). The divergence time ranged from 14.03 to 116.15 million years between celery and coriander TCP genes, 24.94 to 81.44 million years between celery and carrot, and 22.59 to 94.72 million years between coriander and carrot orthologous TCP gene pairs. Therefore, the divergence time of most TCP genes was earlier than that of any two species (celery vs coriander, 11–13 Mya; carrot vs celery or coriander, 20–23 Mya)[4].

      Figure 5.  Ks and divergence time of TCP orthologs. Ks values (a) and divergence time estimation (b) of orthologous gene pairs between any two of three Apiaceae species.

      Detection of duplication type for TCP family genes in Apiaceae

    • Various types of gene duplication can lead to the expansion of a gene family. We examined five types of gene duplication in celery, coriander and carrot (Fig. 6a, Table 1 and Supplemental Table S6)—namely, singleton, dispersed, proximal, tandem and whole-genome duplication (WGD). There were no singleton TCP gene in the three species of Apiaceae (Table 1). Dispersed and tandem duplications were the predominant types in celery and coriander. In celery, the percentage of genes showing dispersed duplication and WGD was 48.1% and 40.7%, respectively; in coriander, the percentages were 40.0% and 45.7%, respectively. WGD was also the predominant type in carrot (32.0%), which had a lower percentage of dispersed duplication (24.0%) than celery and coriander. Moreover, the percentage of the tandem type was higher in carrot (30.0%) than in celery (11.1%) and coriander (11.4%). These results demonstrate that WGD played an important role in TCP gene expansion in celery, coriander and carrot, which is supported by the previous suggestion that they underwent two WGD events since their divergence from lettuce[3].

      Figure 6.  Duplication and loss of TCP family genes. (a) Percentage of duplication types for TCP family genes and genes in the whole genome of three Apiaceae species. (b) Duplication (+) or loss (−) of TCP family genes in three Apiaceae species and three other representative species. Numbers after '+' and '−' are the number of genes. Agr, Apium graveolens (celery); Ath, Arabidopsis thaliana (Arabidopsis); Csa, Coriandrum sativum (coriander); Dca, Daucus carota (carrot); Lsa, Lactuca sativa (lettuce); Vvi, Vitis vinifera (grape).

      Table 1.  The identification of duplicated type for TCP family genes and all genes in A. graveolens, C. sativum and D. carota.

      Duplication typea Categoryb A. graveolens C. sativum D. carota
      Singleton All genes 3,028 3,577 3,543
      TCP 0 0 0
      Percentage (%) 0 0 0
      Dispersed All genes 15,258 14,963 13,378
      TCP 13 14 12
      Percentage (%) 48.15 40 24
      Proximal All genes 1,167 2,161 1,428
      TCP 0 1 7
      Percentage (%) 0 2.86 14
      Tandem All genes 2,426 3,032 3,501
      TCP 3 4 15
      Percentage (%) 11.11 11.43 30
      WGD/segmental All genes 7,787 10,200 8,974
      TCP 11 16 16
      Percentage (%) 40.74 45.71 32
      Total All genes 29,666 33,933 30,824
      TCP 27 35 50
      Note: a the classification of duplicate genes was conducted using the MCScanX program. WGD/segmental duplicates were inferred by the anchor genes in collinear blocks. Tandem duplicates were defined as paralogs that were adjacent to each other on chromosomes. Proximal duplicates were paralogs near each other, while interrupted by several other genes. Dispersed duplicates were paralogs that were neither near each other on chromosomes, nor do they showed conserved synteny. b TCP indicated the TCP family genes. Percentage (%) indicated the percentage of TCP family gene number among all genes.

      TCP gene loss and duplication during the evolution of Apiaceae

    • We compared species and gene trees in celery, coriander and carrot to identify gene losses and duplications during the evolution of the TCP gene family. There were more gene losses in celery (20) than in coriander (7) and carrot (17) but more gene duplications in carrot (18) than in coriander (4) and celery (3). In the common ancestor of coriander, celery and carrot, there were 20 gene duplications and 14 gene losses (Fig. 6b).

      Positive selection of TCP family genes in Apiaceae

    • We analyzed natural selection in the evolution of TCP genes in Apiaceae (Fig. 7). Strong positive selection was observed at the major nodes of the phylogenetic tree, which may have contributed to the functional divergence of Apiaceae species. We detected 35 positive selection sites overall; most were in class PCF (29), followed by class CYC/TB1 (5) and class CIN (1), indicating that TCP genes in class PCF underwent greater positive selection in the evolution of Apiaceae.

      Figure 7.  Positive selection of TCP family genes in celery, coriander and carrot. Red stars represent branches in which positive selection occurred. The maximum likelihood (ML) phylogenetic tree was constructed using PhyML software.

      miRNA target TCP genes in Apiaceae

    • We next sought to identify TCP family genes in Apiaceae that are regulated by miRNAs. We found nine miRNAs that regulated 20 TCP family genes including five genes in celery, nine in coriander and six in carrot (Supplemental Table S7 and Fig. 8). Of the nine miRNAs, miR-319 had the most target genes (11), followed by miR-172 (3) and miR-181 (3) (Fig. 8). Specifically, miR-319 regulated four TCP family genes in celery, four in coriander, and three in carrot. Our results are supported by other studies demonstrating that miR-319 regulates TCP family genes[31,59−61]. We also found that four genes were regulated by more than one miRNA: DcTCP20 was regulated by miR-319 and miR-837, CsTCP33 was regulated by miR-319 and miR-8181, and AgTCP26 and AgTCP27 were regulated by miR-319 and miR-8181 (Supplemental Table S7 and Fig. 8).

      Figure 8.  Interaction network of miRNAs and target TCP family genes in carrot, celery and coriander.

      Expression of TCP family genes in celery and coriander

    • We analyzed the expression patterns of TCP genes in root, petiole and leaf tissues of celery and coriander. In celery, all TCP family genes in class CYC/TB1 had relatively low expression in the three tissues (Fig. 9a and Supplemental Table S8) whereas AgTCP22 had the highest expression level (RPKM > 60), suggesting a key role in celery growth and development. In coriander and celery, all TCP family genes in class CYC/TB1 were expressed at a relatively low level in the three tissues (Fig. 9b and Supplemental Table S8); meanwhile, several genes including CsTCP39, CsTCP14, CsTCP12, CsTCP31, and CsTCP40 had high expression. CsTCP6 and CsTCP30 were more highly expressed in leaf than in the other two tissues.

      Figure 9.  Expression of TCP family genes in three replicates of plant tissues including root (R1, R2 and R3), petiole (P1, P2 and P3), and leaf (L1, L2 and L3). Hierarchical gene expression clustering of TCP genes in celery (a) and coriander (b). Expression levels were calculated based on RPKM.

    DISCUSSION

    • Celery, coriander and carrot are typical members of the Apiaceae family. The draft genomes of these three species were recently released[3,11,12] and there have been several studies on TCP family genes in carrot and celery based on the sequences[37,38,62,63]. The latest versions of the celery, coriander and carrot genomes are of high quality with chromosomal-level assembly, allowing us to accurately and comprehensively analyze the TCP gene family in Apiaceae. To date there have been no reports on TCP genes in coriander. In this study, we identified 43 TCP genes in coriander as well as 29 in celery and 50 in carrot. Our results provide a resource for future studies on the TCP gene family in Apiaceae or related species.

      TCP transcription factors have a 59-amino acid basic helix-loop-helix (bHLH) motif that is involved in DNA binding and protein–protein interaction[64]. The bHLH-like domain of TCP differs from the canonical bHLH in its basic region[34,65]. PCF1 and PCF2 interact with DNA-binding proteins that specifically bind to the PROLIFERATING CELL NUCLEAR ANTIGEN (PCNA) promoter[15]. Our analyses of gene structure and motifs of TCP genes in Apiaceae revealed similarities within the same class or subclass.

      Gene duplication is the main mechanism underlying the evolution of complex phenotypes[66]. Many duplicated genes in plants were produced by WGD or whole-genome triplication[67−70]. Most duplicated genes were functionally redundant and had one of four fates during the course of evolution namely: conservation, neofunctionalization, subfunctionalization and specialization[67,71]. In conservation, the ancestral function was maintained in both copies, thus preserving gene dosage[71]. In neofunctionalization, one copy retained the original function while the other acquired a novel function[71,72]. In subfunctionalization, both copies were required to preserve the ancestral gene function[71,73,74]. In specialization, subfunctionalization and neofunctionalization acted cooperatively, producing two gene copies that were functionally distinct from each other and from the ancestral gene[71,75]. Functional redundancies of TCP genes have been reported in Arabidopsis[76]. In carrot, 15 TCP genes were clustered on chromosome 1, and the number of paralogous gene pairs was greater in carrot (29) than in celery (3) and coriander (3). Although there were more gene losses than duplications in the evolution of celery, coriander and carrot, we found that WGD made a major contribution to TCP gene family expansion in Apiaceae, which is similar to what has been reported in most other gene families in higher plants[47,77−80].

      The broad range of functions of TCP family genes in plants can be attributed to the diverse structures of different members. Most TCP genes are highly expressed in meristematic tissues, suggesting that their main function is to promote plant proliferation and growth[81]. However, some TCP genes, such as CIN and CYC/TB1, are known to negatively regulate plant proliferation and development[82] (lateral organ development for CIN genes and flower and lateral shoot development for CYC/TB1 genes)[26]. Our gene expression analysis showed that TCP gene expression in celery (AgTCP22) and coriander (CsTCP12) was nearly 2x higher in root and petiole than in leaf, suggesting roles in plant growth and development.

      In conclusion, we identified and characterized TCP genes in three Apiaceae species. We described their chromosomal location, exon–intron structure, motifs, collinearity, positive selection and expression patterns in plant tissues. These results provide a basis for investigations on the molecular networks regulating growth and development in Apiaceae and other plants.

      Acknowledgments
      • This work was supported by the National Natural Science Foundation of China (31801856), China Postdoctoral Science Foundation (2020M673188), Hebei Province Higher Education Youth Talents Program (BJ2018016), and Key Science Research and Development Program of Tangshan (19150206E).
      Conflict of interest
      • The authors declare that they have no conflict of interest.
      Supplementary information
      • Supplemental Table S1 The TCP gene family members and their abbreviation name in celery, coriander, carrot, lettuce, grape, and Arabidopsis.
      • Supplemental Table S2 The summary of TCP gene family members in  A.  graveolens , C. sativum, D. carota and compared with  A. thaliana .
      • Supplemental Table S3 The list of orthologous TCP gene pairs between A. graveolens,  C. sativum, and  D. carota.
      • Supplemental Table S4 The list of paralogous TCP gene pairs in each of other examined species.
      • Supplemental Table S5 Ka/Ks calculation and divergent time of the orthologous  gene pairs between A. graveolens, C. sativum, and  D. carota.
      • Supplemental Table S6 The duplicated type of TCP genes in A. graveolens,C. sativum and D. carota. The 0 to 4 indicate the singleton, dispersed, proximal, tandem, WGD duplication type, respectively.
      • Supplemental Table S7 The prediction of target TCP family genes of miRNA in carrot, coriander, and celery.
      • Supplemental Table S8 The expression level of the TCP genes in root, leaf and petiole for A. graveolens and C. savitum.  The gene expression was determined by the RNA-Seq data (RPKM).
      • Supplemental Fig. S1 The gene structure of TCP gene family in three Apiaceae species.
      • Supplemental Fig. S2 The circle plot of paralogous TCP gene pairs among three Apiaceae species.
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      • Copyright: © 2021 by the author(s). Exclusive Licensee Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
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    Cite this article
    Pei Q, Li N, Bai Y, Wu T, Yang Q, et al. 2021. Comparative analysis of the TCP gene family in celery, coriander and carrot (family Apiaceae). Vegetable Research 1: 5 doi: 10.48130/VR-2021-0005
    Pei Q, Li N, Bai Y, Wu T, Yang Q, et al. 2021. Comparative analysis of the TCP gene family in celery, coriander and carrot (family Apiaceae). Vegetable Research 1: 5 doi: 10.48130/VR-2021-0005
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  • Introduction
  • Materials and methods

  • Identification of tcp family genes in celery, coriander and carrot

  • Phylogenetic analysis of tcp gene family

  • Chromosome location, gene structure and conserved motif analysis

  • Analysis of orthologs and paralogs

  • Identification of collinear blocks and duplication types

  • Calculation of ka/ks and estimation of divergence time

  • Analysis of selective pressures

  • Identification of micro (mi)rna target genes in the tcp gene family

  • Expression of tcp genes

  • Results

  • Identification of tcp genes in three apiaceae species

  • Phylogenetic and functional analyses of tcp gene family

  • tcp gene family structure and conserved motifs

  • Chromosomal distribution of tcp genes in apiaceae species

  • Identification of orthologous and paralogous tcp genes in apiaceae

  • Detection of duplication type for tcp family genes in apiaceae

  • tcp gene loss and duplication during the evolution of apiaceae

  • Positive selection of tcp family genes in apiaceae

  • Mirna target tcp genes in apiaceae

  • Expression of tcp family genes in celery and coriander

  • Discussion
  • Acknowledgments
  • Conflict of interest
  • Supplementary information
  • Rights and permissions
  • About this article
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