ИСТИНА

Extrafloral nectaries (EFNs) is a common plant-defence trait widespread in vascular plants. EFNs are plant glands secreting nectar and located outside the flower. Weber & Keeler (2013) analysed records of EFNs published over the last 135 years. EFNs have been reported in 3941 species representing 745 genera and 108 families, about 1–2 % of vascular plant species and 21 % of families. Foliar nectaries are known in four of 36 fern families, but unknown in gymnosperms. EFNs have not been found yet in early angiosperms and magnoliids. They occur in monocotyledons, but most EFNs are found within eudicots, especially in rosids. Phylogenetic analyses revealed the repeated gain and loss of EFNs across plant clades, especially in more derived dicot families, and imply that EFNs are found in a minimum of 457 independent lineages. The number of unreported cases of EFNs may be comparable to the number of species already reported (Weber and Keeler, 2013). Weber and Keeler (2013) formulated several hypotheses concerning the evolution of EFN such as “EFNs are tropical adaptations”, “EFNs evolve in response to resource availability”, “EFNs are more likely to evolve in vines”, that need additional testing. Biogeographic distribution. EFN-bearing plants occur in a wide range of habitats, mainly in tropics and subtropics, less often in temperate regions. EFNs from deserts and other arid lands are insufficiently studied (Marazzi et al., 2013). Location on plant. Almost any above-ground plant part can bear EFNs, from vegetative parts such as leaves and stipules, to parts of the inflorescences, and even the outer floral organs not directly involved in pollination (Marazzi et al., 2013). EFN location in Fabales includes leaves, petioles, stipules, stems, pedicels, peduncles or stems of inflorescence, as well as sepals/calyx/perianth/tepals/floral bracts/cataphylls; EFNs located on the last group of organs are sometimes termed ‘extrasoral’, not ‘extrafloral’ (Marazzi et al., 2013). EFNs may vary in abundance and distribution on a plant during ontogeny (Marazzi et al., 2013). Function. EFNs are not directly related to pollination. Ants are their main visitors. The benefits of plants that may be caused by the EFN related activity of ants and other small arthropods are: reducing leaf herbivory and twig destruction, increasing fruit and seed production, reducing of ant visitation to floral nectaries, thereby enhancing the pollination success and reducing seed predation (Bentley, 1977; Koptur, 1979; Guimarães Jr. et al., 2006). Methods of detection and analysis. The majority of EFN studies include morphological and anatomical analyses, some studies also involve analysis of ultrastructure using SEM and TEM. Additionally, histochemical detection of reducing sugars using Fehling’s reagent, measurement of nectar concentration with sugar hand-held refractometers (Díaz-Catelazo et al., 2005) and paper (Davis et al., 1988) or thin-layer chromatography (Paiva, 2009) were applied. Morphology. EFNs can vary from simple glandular trichomes and cryptic non-structural or structural secretory tissue enclosed within EFN-bearing plant parts, to prominent, complex vascularized or non-vascularized glands on the surface of the EFN-bearing organ (Marazzi et al., 2013). Melo et al. (2010) distinguish two categories of EFNs: 1) substitutive nectaries, which are common structures (e.g., stipules, floral pedicels), that have evolved to function like EFNs; 2) non-substitutive EFNs which are glandular structures that have developed specifically to be EFNs. Substitutive EFNs may indicate a recent evolutionary acquisition (Melo et al., 2010). Anatomy. In anatomically specialized EFNs, three kinds of tissues can be recognized: the epidermis, the nectary parenchyma, and the subnectary parenchyma (including the vascular bundles branching off from the leaf vasculature). In some EFN-bearing legumes, an additional fourth structure of one or two layers of cells can be observed between the nectary and the subnectary parenchyma (Melo et al., 2010; Marazzi et al., 2013). TEM ultrastructure of EFNs was studied in several Papilionoideae species, e.g. Vicia faba (Davis et al., 1988) and Erythrina speciosa (Paiva, 2009). Some similarities in structure of nectaries and patterns of nectar secretion were found between floral nectaries and EFNs: secretory epidermal cells of structural nectaries possess cell wall ingrowth and developed membrane system (endoplasmic reticulum (ER), dictyosomes, vacuoles); head cells of secretory trichomes have large nuclei, dense cytoplasm with dictyosomes, ER, mitochondria (MT), plastids (PL), and ribosomes (RS); in vascularized nectaries sieve elements and companion cells play significant role in nectar secretion mechanism; cell wall ingrowth was observed in phloem companion cells; both apoplastic and symplastic pathways may be included in nectar secretion. Alternative theories have been proposed to explain nectar secretion mechanism, that can be applied to EFNs, i.e. granulocrine theory (Davis et al., 1988; Paiva, 2009) and pressure-driven mass flow mechanism (Vassilyev, 2010). The legume family (Fabaceae) is known for its diverse interactions with ants and stands out among other plant families, with 30 % of the EFN-bearing species (Marazzi et al., 2013). EFNs in Papilionoideae. EFNs are more common for Caesalpinioideae (incl. Mimosoideae) (EFNs found in 89 of 148 genera) and less common for Papilionoideae, however found in 50 of 503 genera (Marazzi, oral talk on 7ILC, 2018). EFNs in Papilionoideae vary in structure, they can be substitutive or non-substitutive. Below several examples of EFNs described in various tribes of Papilionoideae, taken from literature, are presented. Tribal position of species is given according to Lewis et al. (2005). EFNs are mainly distributed within tribes Vicieae, Phaseoleae, Crotalarieae. Tribe Vicieae(=Fabeae). In Vicia faba EFNs are brown spots on abaxial surface of each stipule (Bhattacharyya & Maheshwari, 1970; Davis et al., 1988; Heneidak & Hasan, 2007). They consist of densely gathered clavate glandular hairs and unicellular hairs, aggregated in shallow depression. Glandular hairs are capitated trichomes consisting of four-celled secretory head, one stalk cell and a basal cell. Both xylem and phloem are present in the stipule beneath the extrafloral nectary (Davis et al., 1988). Similar EFNs were described for Vicia narbonensis, V. peregrina, V. sativa, V. angustifolia, V. sepium and V. grandiflora. In Vicia subgenus Vicilla (V. ervilia, V. montana) EFNs are absent (Heneidak & Hasan, 2007). In V. angustifolia nectarines were also located on calyx surface. Tribe Phaseoleae. EFNs are found in Calopogonium, Canavalia, Erythrina, Galactia, Macroptilium, Phaseolus, Rhynchosia, Vigna (Bhattacharyya & Maheshwari, 1970; Díaz-Castelazo et al., 2005; Kost & Heil, 2005; Paiva, 2009; Melo et al., 2010; Gonzalez & Marazzi, 2018). The majority of recorded species are from tropical regions. EFNs located on leaf parts (stipules, stipels, rachis, leaf surfaces) were described in M. atropurpureum, P. lunatus, E. velutina, Rhynchosia species. In M. atropurpureum and Rhynchosia these EFNs are represented by capitated trichomes. EFNs developing in inflorescences on the nodes, floral pedicels or from aborted floral buds were recorded in V. candida, V. peduncularis, M. prostratum, M. atropurpureum, G. latisiliqua, Canavalia rosea, E. velutina. Anatomical structure of EFNs shaped as swollen scars on abscission site of aborted floral buds: secretory epidermis absent, the central abscission region is modified for nectar secretion and consists of several layers (cell remains of aborted bud, nectary and subnectary parenchyma), vascularization by one or two vascular bundles (Gonzalez & Marazzi, 2018). Substitutive EFNs of E. velutina located on leaf rachis and floral pedicels, comprised of a uniseriate epidermis, parenchyma cells, starch storage cavities and vascular bundles randomly arranged in the parenchyma. Exudation occurs through glandular trichomes which are grouped in the EFN secretory region (Melo et al., 2010). Erythrina speciosa possesses pericarpal nectaries (PNs). PN is represented by a single hyaline trichome that consists of a basal cell, stalk cell(s) and a small secretory multicellular head. The apical stalk cell shows inner periclinal and anticlinal walls impregnated by lipids and lignin and has dense cytoplasm with with abundance of MT and ER. The secretory cells show large nuclei and dense cytoplasm, which predominantly has dictyosomes, rough ER, plastids, MT and free RS. At the secretory stage the periplasmic space is prominent and contains secretion residues (Paiva, 2009). Tribe Crotalarieae. In a pantropical weed Crotalaria pallida EFNs are located in the racemes, at the base of each flower or pod (Guimaraes Jr. et al., 2006). In Crotalaria incana EFNs are scars of fallen stipules and aborted buds as well as unicellular trichomes with secretory basal cell (Diaz-Castelazo et al., 2005). Other tribes. EFNs were also reported in members of tribes Galegeae, Trifolieae, Dalbergieae, Genisteae and Loteae (Bhattacharyya & Maheshwari, 1970), however without detailed description. Extrafloral glands are common in Lotus and related genera, sometimes they are treated as EFNs (Magne et al., 2018), but their structure and secreted substances are unknown. EFN are apparently absent in tribes Swartzieae, Sophoreae, Podalyrieae (Bhattacharyya & Maheshwari, 1970). The study is supported by grant 19-04-00883a from the Russian Fund of Fundamental Research.