Apiaceae, Lindl.

Sousa, Rose Marie O. F., Cunha, Ana C. & Fernandes-Ferreira, Manuel, 2021, The potential of Apiaceae species as sources of singular phytochemicals and plant-based pesticides, Phytochemistry (112714) 187, pp. 1-32 : 2-3

2. The Apiaceae family

Apiaceae Lindl. (= Umbelliferae Juss. ) is one of the most numerous plant family. It includes several vegetable and herbs of high economic and medicinal value ( Olle and Bender, 2010). The most economically important Apiaceae crops cultivated for food, culinary spices/herbs and/or EO(s) production are listed in Table 1 . Apiaceae species are readily identifiable flowering plants with obvious distinctive characters ( Pimenov and Leonov, 1993; Downie et al., 2000), but their identification to the genus and species levels is of known difficulty ( Plunkett and Downie, 1999). Umbellifers exhibit a remarkable array of morphological and anatomical modifications of their fruits, many of which are adaptations for various modes of seed dispersal ( Downie et al., 2000). Drude (1898) traditionally divided the Apiaceae into 3 subfamilies (Hydrocotyloideae Link, Saniculoideae Burnett and Apioideae Drude ). This division system almost exclusively based on fruit anatomical characters (traditionally viewed as stable) was widely adopted and has been used by many authors (e.g., Pimenov and Leonov, 1993; Plunkett and Downie, 1999). Nevertheless, the almost exclusive use of morphological-based criteria to delimit suprageneric groups has ambiguous interpretations and has caused considerable controversy surrounding affiliations at the tribal level ( Berenbaum, 1990). Therefore, the resolution of the family classification has been difficult. Since Pimenov and Leonov’ s classification (1993), several authors have proposed a few taxonomic changes within the family based on hypothesized phylogenetic relationships established from a combination of morphological and molecular data (e.g., Downie et al., 2001; Spalik and Downie, 2001; Calvino ˜et al., 2008).

Apioideae is the most taxonomically complex of the three subfamilies ( Downie and Katz-Downie, 1996). Besides being the largest (consisting of 1800–3000 herbaceous plants of temperate climate encompassed in 250–400 genera), Apioideae is also the best-known subfamily of Apiaceae ( Plunkett and Downie, 1999) . Currently, species of the subfamily Apioideae show a cosmopolitan distribution ( Downie et al., 2000; Nicolas and Plunkett, 2014), being largely distributed in Africa, the Mediterranean region and throughout Eurasia ( Nicolas and Plunkett, 2014). These may be distinguished from those of the other subfamilies with basis on morphological (1), biological (2) and chemical (3) distinctive characters:

(1) Presence of compound umbels; finely divided leaves; two oneseeded mericarps attached to a central bifurcate carpophore; a terminal style; absence of stipule and presence of well-developed schizogenous secretory canals ( Downie and Katz-Downie, 1996; Downie et al., 2010). Schizogenous secretory canals are composed of an epithelium which surrounds a central cavity ( Bosabalidis, 1996). Regarding their ontogenesis, the formation of the duct central cavity occurs predominantly through a schizogenous process (separation of two epithelial mother cells along the common wall), although lysigenous ducts (spaces resulting from the dissolution of cells) may also be found. Later, epithelial cells lining the central cavity differentiate into secretory cells ( Bosabalidis, 1996).

(2) A relatively distinctive insect fauna and insect specialists, namely Depressaria spp. (Elachistidae) and Papilio spp. (Papilionidae) ( Berenbaum, 1990).

(3) The occurrence of some classes of compounds, namely, furanocoumarins ( Fig. 1 ), phenylpropenes ( Fig. 2 ), methylated flavonoids, flavones, etc. ( Berenbaum, 1990).

3. Phytochemicals from Apiaceae species

In addition to their popularity and high commercial relevance, umbelliferous crops are important sources of bioactive compounds. The Apiaceae family is rich in specialized metabolites, yielding distinctive compounds such as sesquiterpenic lactones, furanocoumarins, monoterpene coumarins, polyacetylenes, volatile phenylpropenes, phthalides, etc. (Hadaˇcek et al., 1994; El-Razek et al., 2001a, b; Christensen and Brandt, 2006; Evergetis et al., 2012). Species of the carrot family, namely Ferula and Peucedanum species exhibit a remarkable variety of chemicals of interest to the pharmaceutical industry (see reviews of Nazari et al., 2011; Sahebkar and Iranshahi, 2011; and Sarkhail, 2014). Several Apiaceae extracts and/or compounds have been described as antimicrobials ( Ozçelik et al., 2004; Khalil et al., 2018), antioxidants ( Momin and Nair, 2002; Singh et al., 2006a, 2006b; Zhang et al., 2006), anti-inflammatory ( Tabanca et al., 2007), vasorelaxants ( Ko et al., 1991), chemopreventive agents (Zheng et al., 1992), and phytoestrogens (Yoshikawa et al., 2000; Başer et al., 2007). For example, a group of aliphatic C 17 polyacetylenes identified in carrot, celery, parsley and parsnip have revealed interesting anti-tumor (namely antileukemic), anti-inflammatory and antiplatelet aggregatory effects in mammals ( Konoshima and Lee, 1986; Christensen and Brandt, 2006; Chen et al., 2015). Furthermore, the linear furanocoumarin psoralen ( Fig. 1 ) has been successfully used in the treatment of skin disorders (eczema, psoriasis) by means of a combination of oral ingestion and UV-A treatment ( Croteau et al., 2000). The ethnomedicinal value and the various therapeutic properties exhibited by some Apiaceae fruits were recently reviewed ( Sayed-Ahmad et al., 2017).

Nonetheless, the Apiaceae family also ascribes renowned deadly poisonous species such as fool’ s parsley ( Aethusa cynapium L.), hemlock water-dropwort ( Oenanthe crocata L.), poison hemlock ( Conium maculatum L.) and water hemlock ( Cicuta virosa L.). Some conjugated polyacetylenes (viz. cicutoxin, oenanthotoxin, virol A, virol B, virol C, etc.), which are produced by species of the Oenanthe ( O. crocata ) and Cicuta genera [ C. virosa , C. maculata L., C. douglasii (DC.) J.M. Coult. & Rose ], have been identified amongst the strongest plant neurotoxins (Uwai et al., 2000). Conium maculatum has been known since ancient times for its acute narcotic neurotoxic effect. Its toxicity is due to the strong phytotoxins piperidinic alkaloids [viz. conmaculatin, γ- coniceine, (S)-(+)-coniine, (R)-()-coniine and N-methylconiine]. Besides its acute effects, C. maculatum have been found to induces a chronic teratogenic activity on livestock and humans (Lopez´et al., 1999; Radulovic´et al., 2012). Nonetheless, the carrot family comprises very few alkaloid-producing species, with alkaloids showing a very erratic distribution ( Berenbaum, 1990).

3.1. Essential oils (EOs) and volatile constituents as added value products

Nowadays, EOs or volatile constituents are gaining high popularity and extending their prospect for application, mostly on account of the growing consumer awareness concerning its health benefits, and as a result of the generalized trend to ‘green consumerism’ ( Dubey et al., 2011). In 2018, the global EOs market demand was 226.9 kilotons ( Grand View Research, 2019). With the rising demand for this type of plant-derived product and the diversification of their appliance, it is expected that the global EO market demand will grow significantly (CAGR of 8.6% from 2019 to 2025), likely reaching 403.06 kilotons by 2025 ( Grand View Research, 2019).

For the last three decades, these plant-derived products have received a great deal of attention from scientists, corporations, and society in general. EOs have been widely employed as therapeutic and biochemical controlling agents (as bactericidal, virucidal, fungicidal, antiparasitic, insecticidal, etc.) ( Bakkali et al., 2008). Because of their varied properties, EOs and plant volatiles constituents show a myriad of applications, particularly as pharmaceutics, agrochemicals, anti-microbial agents, flavoring agents, cosmetics and fragrances ( Bakkali et al., 2008; Schwab et al., 2008; Regnault-Roger et al., 2012). Owing to the GRAS status of certain EOs, plant-derived EO products, in general, are eligible for minimum-risk pesticide products ( Cloyd et al., 2009; Tripathi et al., 2009). Most EOs constituents are relatively non-toxic to mammals and fish in toxicological tests ( Koul et al., 2008). From the chemical perspective, EOs 1 are complex natural heterogeneous mixtures composed of various terpenoids of low molecular weight, as well as non-terpenoid volatile compounds ( Başer and Demirci, 2007). Simultaneously, EOs are phytochemically diverse (i.e. containing many biosynthetically different compounds) and redundant (i.e. containing many analogs of one class) ( Regnault-Roger et al., 2012). Along with compounds belonging to the class of terpenoids, predominantly monoterpenoids and sesquiterpenoids (rarely diterpenes), other volatile specialized metabolites of distinct biosynthetic origin may be detected in EOs mixtures, namely aromatic and aliphatic constituents (Weisshaar and Jenkins, 1998; Sangwan et al., 2001). Volatiles constituents of EOs can be found in variable amounts in different plant organs (e.g., flowers, leaves, stems, fruits, seeds, bark roots and/or rhizomes) depending on the species ( Tisserand and Young, 2013). EO bearing plants belong to many different botanical families, and specific types of secretory structures, as well as their location, have been associated to some plant families ( Figueiredo et al., 2008). In the Apiaceae family the accumulation of EOs is delimited to specialized structures located along plants vegetative and reproductive organs, known as secretory duct (or oil duct) and vittae, respectively ( Franz and Novak, 2009). These secretory structures form a highly interconnected network of tubular intercellular spaces extending throughout plants phloem ( Senalik and Simon, 1986; Bosabalidis, 1996). Investigations on the localization of biologically active specialized products in Apiaceae have revealed that these inner secretory structures might be the place of synthesis and/or storage of different classes of compounds, including terpenoids ( Senalik and Simon, 1986), lipids ( Atia et al., 2009), phenolics, namely flavonoids ( Reinold and Hahlbrock, 1997; Atia et al., 2009) furanocoumarins (Zobel and March 1993; Reinold and Hahlbrock, 1997) and phenylpropenes ( Gersbach and Reddy, 2002; Gross et al., 2006), and in some rare cases alkaloids ( Corsi and Biasci, 1998).

EOs and oleoresins can be extracted from roots, herbs and fruits of several Apiaceae species with suitable yields (> 10 L/hectare). Apiaceae being trade internationally as EO-producing crops are limited to a handful of species ( Table 1 ), despite the existence of a vast range of EObearing Apiaceae already documented and characterized ( Chizzola, 2010; Baser and Kirimer, 2014). Coriander EOs (from fruits and leaves), fennel fruits EO (sweet and bitter fennel), alongside with dill EO (fruits and leaves), are the leading products from Apiaceae , followed by other species such as celery, caraway, anise, ajowan, parsley, cumin, carrot, and angelica ( Lawrence, 1993). Evergetis and Haroutounian (2014) and Evergetis et al. (2015) identified about 18 Apiaceae species from the Greek flora showing EOs producing potential at the industrial scale (estimated yields ranging from 11 to 35 L per hectare), plus Bupleurum fruticosum L. that showed an exceptional yield of 522 L per hectare. Most of the species included in the former studies could constitute viable sources of several fine chemicals, which is a strong argument to advocate their valorization and production ( Evergetis and Haroutounian, 2014).

Figures

Fig. 1. Type of bioactive coumarins, furanocoumarins and furanochromones found in Apiaceae species showing allelopathic and/or pesticidal activity.

Fig. 2. Examples of volatile bioactive phenylpropene-derivatives and their occurrence in Apiaceae species: (A) allylbenzenes and (B) propenylbenzenes (Sources: Duke, 1992; Baser et al., 2007).