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Easton Gray
Easton Gray

Apium Graveolens


Collenchyma is a type of supporting tissue commonly found in stems, petioles, leaves and floral segments of many herbaceous and woody plants, particularly in eudicotyledons [1, 2]. This tissue is commonly located peripherally in organs, where it may occur either immediately below the epidermis, or separated by several layers of parenchyma cells (Additional file 1: Figure S1). In addition to its peripheral location, collenchyma is often associated with vascular bundles [1,2,3]. A predominant feature of collenchyma cells is their unevenly thickened walls that are usually regarded as primary [2]. Based on the positions of the wall thickenings, collenchyma can be divided into four main types: angular collenchyma, which is the commonest type and has thickening mainly in the cell corners, e. g. in the petioles of celery (Apium graveolens), stems of potato (Solanum tuberosum) and deadly nightshade (Atropa belladonna) [4]; tangential collenchyma has the inner and outer tangential walls thickened more heavily than the radial ones, e.g. in stems of elder (Sambucus nigra) [5]; annular collenchyma has the walls uniformly thickened, e.g. in the petioles of cow parsnip (Heracleum lanatum) and petioles of sweetgum (Liquidamber styraciflua) [6]; lacunar collenchyma has intercellular spaces adjacent to the thickened walls, e.g. in the petioles of winter heliotrope (Petasites fragrans) [6].




apium graveolens


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Celery (Apium graveolens L.) is an annual or biennial herbaceous plant in the Apiaceae family that originated in the Mediterranean and the Middle East. It is a popular vegetable crop and is widely cultivated in Europe, East Asia, southeastern Oceania, and southern Africa (Fig. 1a). The whole celery plant exhibits aromatic flavor, and its leaf blades and petioles are the main edible organs (Fig. 1b). In addition to containing common nutrients such as vitamins, proteins and carbohydrates, celery contains flavonoids, carotenoids, terpenoids, and unsaturated fatty acids that exhibit biological activity and physiological functions in human beings1,2,3,4.


To build the phylogenetic tree, redundant sequences (90% identity or more) from the same organism were removed using CD-HIT42. Then, homolog clusters were predicted by comparing each pair of the nine plant genomes (A. graveolens, D. carota, M. guttatus, S. tuberosum, S. lycopersicum, Oryza sativa, Coffea canephora, Actinidia chinensis, and A. thaliana) using OrthoMCL. The protein sequences for clusters containing a single-copy gene of each species were aligned with MUSCLE v3.8.3143. Then, positions showing poor alignment were eliminated with G blocks (version 0.91b). All alignments were subsequently concatenated to one super alignment. The phylogeny was reconstructed by the neighbor-joining method using the Jones-Taylor-Thornton model44. The reliability of the tree topology was measured by bootstrapping (1000 replications). Evolutionary analysis was conducted in MEGA745. The species divergence time in the phylogenetic tree was estimated via the Bayesian relaxed molecular clock (BRMC) method using the program MULTIDIVTIME, which was implemented in the Thornian Time Traveller (T3) package46,47. To estimate the synonymous substitutions per synonymous site (Ks), all paralogous gene pairs were analyzed with the maximum likelihood method in the PAML program48.


Apium graveolens L. (family Apiaceae), originated from the Mediterranean basin, is a biennial species grown worldwide. There are three distinct taxonomic varieties, var. dulce (celery), var. rapaceum (celeriac), and var. secalinum (smallage) [1]. Celery is the most widely grown variety and it was spread to China in the Han Dynasty (the second century B. C.). After a long period of domestication, cultivars with slender petiole known as Chinese celery or local celery came into being [2]. Celery is rich in a variety of nutrients like vitamins, minerals and proteins and it has many pharmacological efficacies, which make it an increasing popular vegetable to consumers [3], [4]. In China, celery growing area has been increased from 0.54 million hectare in 2004 to 0.57 million hectare in 2006 according to the data statistics, almost accounting for 3% of the total vegetable planting area throughout the country. So it is essential to breed new celery varieties and enrich commercial species.


During the last decades, large amounts of transcriptomic and genomic sequences have been available in many model organisms. For Apium graveolens, only about 2,000 ESTs were deposited in GenBank database. Therefore, extensive genomic or transcriptomic sequences are badly needed for Apium graveolens, which can be used for new genes discovery, molecular markers development, gene localization, and comparative genomics and so on. Given that the celery is a diploid with a large genome (3109 bp) and a high degree of heterozygosity, it is infeasible to consider whole genome sequencing because of the high costs and time-consuming. Fortunately, the advent of transcriptome sequencing provides an alternative to the whole genome sequencing. Transcriptome sequences exclude non-coding DNA, thus the sequences obtained must contain a high content of functional information [14], [15] and are beneficial to reveal the molecular mechanism of functional genes [16].


The polymorphic SSR markers were then used to perform genetic correlation analysis among the 31 different A. graveolens accessions, and dendrograms were constructed from the genetic similarity matrix (Figure 8). At the genetic distance of 0.6, cultivated and wild species were separated. Within the cultivated species, almost all lines of A. graveolens L. var. dulce formed a cluster, except that five lines (C111, C67, C114, C123, and C163) were classified into a group with A. graveolens L. var.rapaceum (C163). The lines belonging to A. graveolens L. var. dulce were further classified into local celery (cultivars developed through ancient introductions) and celery (modern cultivars introduced from Europe and America). And most local celery formed one group with the remaining scattered in the celery group.


Male C57BL/6 mice treated with MPTP were orally dosed with A. graveolens extract daily for 21 days. Behavioral tests, including a rotarod apparatus, a narrow beam test, a drag test, a grid walk test, a swimming test, and a resting tremor evaluation, were performed. Thereafter, the mice were sacrificed, and monoamine oxidase A and B activity, lipid peroxidation activity, and superoxide anion levels were measured. Immunohistochemical staining of tyrosine hydroxylase was performed to identify dopaminergic neurons.


We speculated that A. graveolens ameliorated behavioral performance by mediating neuroprotection against MPTP-induced PD via antioxidant effects, related neurotransmitter pathways and an increase in the number of dopaminergic neurons.


Apium graveolens L., a.k.a. celery, is a traditional Chinese medicine prescribed to treat hypertension, gout, and diabetes [17,18,19]. Its stem, root, and leaf extracts can promote differentiation of neuronal stem cells to neurons and supportive cells such as astrocytes and oligodendrocytes [20]. Apigenin, a compound that can be isolated from celery stems, can promote mature neurons in model systems, both in vitro and in vivo [21]. Moreover, high concentrations of luteolin, another compound found in A. graveolens, can inhibit lipopolysaccharide (LPS), which reduces DA recycling and disturb tyrosine hydroxylase (TH) enzyme function in the DA synthesis pathway of neuronal and glial cells in vitro. Apart from these effects, the inhibition of LPS by luteolin can activate supportive cells and expression of tumor necrosis factor-α, nitric oxide and superoxide [22]. Given all the aforementioned effects of A. graveolens constituents, we conducted this study to determine the neuroprotective effect of A. graveolens extract through its antioxidant effect and related neurotransmitter pathway and investigate whether A. graveolens has the capacity to inhibit MPTP neurotoxicity and protect DA neurons.


Whole A. graveolens plants were harvested and dried at Lampang Herb Conservation, Lampang, Thailand, then authenticated by the Forest Herbarium, Bangkok, Thailand (BKF number 188856) and used to prepare a methanolic extract by Dr. Wanida Sukketsiri, Department of Pharmacology, Faculty of Science, Prince of Songkla University, Thailand. The coarse power was exhaustively extracted with 70% methanol (1:1) for 72 h. The methanolic extract was filtrated through Whatman No. 1 filter paper and concentrated under vacuum in a rotary evaporator. Finally, the A. graveolens methanolic extract (AGME) was lyophilized with a freeze dryer, placed in a tight container and stored in a cool place until use. All AGME came from the same lot with previous publications [23, 24]. Each vial contained 1 g of dried extract from whole A. graveolens plants. The percent yield (w/w) of the methanolic extract was 16.0%; characterization of AGME has previously been reported by our group [23, 24]. To guarantee the quality of AGME, HPLC was performed on the methanolic extract and luteoin and apigenin were used as standard markers. Our HPLC result analysis of AGME displayed the active compounds of apigenin 0.031% w/w and luteolin 0.030% w/w, respectively compared to standards [24]. The dried extract was freshly prepared throughout the day at the time of each experiment by dissolving it in normal saline solution (NSS) for once-daily oral gavage.


Drug therapy of PD with L-DOPA has adverse side effects after a long duration of treatment. These effects consist of dyskinesia, sleep disturbance, and depression [16]; the combination of this drug with other drugs to increase the bio-availability or retention time magnifies this challenge [43]. For example, Tidomet Plus is a combination of levodopa and carbidopa with the purpose of inhibiting peripheral elimination of L-DOPA. Nonetheless, previous research has found that levodopa may be neurotoxic and promote the degeneration of nigrostriatal projections [44]. In addition, prolonged DA treatment is associated with the intracellular accumulation of oxidative stress [45]. To circumvent these drawbacks, the field of herbal medicine has focused on natural products, searching for a low-cost alternative treatment with less severe side effects. A. graveolens, especially the well-known variety called Chinese celery, has been used as a spice and a cooked vegetable in the Asia-Pacific region for a long time. The general beneficial effects of this herb are abundant; for example, it is used to treat gout, diabetes, and hypertension [17, 18, 46]. Despite its versatility, the neuroprotective effect of this plant extract in a PD model has not yet been investigated in detail. 041b061a72


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