Do food trichomes occur inPinguicula(Lentibulariaceae) flowers?

Abstract

Background and Aims Floral food bodies (including edible trichomes) are a form of floral reward for pollinators. This type of nutritive reward has been recorded in several angiosperm families: Annonaceae, Araceae, Calycanthaceae, Eupomatiaceae, Himantandraceae, Nymphaeaceae, Orchidaceae, Pandanaceae and Winteraceae. Although these bodies are very diverse in their structure, their cells contain food material: starch grains, protein bodies or lipid droplets. In Pinguicula flowers, there are numerous multicellular clavate trichomes. Previous authors have proposed that these trichomes in the Pinguicula flower play the role of ‘futterhaare’ (‘feeding hairs’) and are eaten by pollinators. The main aim of this study was to investigate whether the floral non-glandular trichomes of Pinguicula contain food reserves and thus are a reward for pollinators. The trichomes from the Pinguicula groups, which differ in their taxonomy (species from the subgenera: Temnoceras, Pinguicula and Isoloba) as well as the types of their pollinators (butterflies/flies and bees/hummingbirds), were examined. Thus, it was determined whether there are any connections between the occurrence of food trichomes and phylogeny position or pollination biology. Additionally, we determined the phylogenetic history of edible trichomes and pollinator evolution in the Pinguicula species. Methods The species that were sampled were: Pinguicula moctezumae, P. esseriana, P. moranensis, P. emarginata, P. rectifolia, P. mesophytica, P. hemiepiphytica, P. agnata, P. albida, P. ibarrae, P. martinezii, P. filifolia, P. gigantea, P. lusitanica, P. alpina and P. vulgaris. Light microscopy, histochemistry, and scanning and transmission electron microscopy were used to address our aims with a phylogenetic perspective based on matK/trnK DNA sequences. Key Results No accumulation of protein bodies or lipid droplets was recorded in the floral non-glandular trichomes of any of the analysed species. Starch grains occurred in the cells of the trichomes of the bee-/fly-pollinated species: P. agnata, P. albida, P. ibarrae, P. martinezii, P. filifolia and P. gigantea, but not in P. alpina or P. vulgaris. Moreover, starch grains were not recorded in the cells of the trichomes of the Pinguicula species that have long spurs, which are pollinated by Lepidoptera (P. moctezumae, P. esseriana, P. moranensis, P. emarginata and P. rectifolia) or birds (P. mesophytica and P. hemiepihytica), or in species with a small and whitish corolla that self-pollinate (P. lusitanica). The results on the occurrence of edible trichomes and pollinator syndromes were mapped onto a phylogenetic reconstruction of the genus. Conclusion Floral non-glandular trichomes play the role of edible trichomes in some Pinguicula species (P. agnata, P. albida, P. ibarrae, P. martinezii, P. filifolia and P. gigantea), which are mainly classified as bee-pollinated species that had originated from Central and South America. It seems that in the Pinguicula that are pollinated by other pollinator groups (Lepidoptera and hummingbirds), the non-glandular trichomes in the flowers play a role other than that of a floral reward for their pollinators. Edible trichomes are symplesiomorphic for the Pinguicula species, and thus do not support a monophyletic group such as a synapomorphy. Nevertheless, edible trichomes are derived and are possibly a specialization for fly and bee pollinators by acting as a food reward for these visitors.

Arabinogalactan Proteins in the Digestive Glands of Dionaea muscipula J.Ellis Traps

“…For the SEM, the material was fixed and later processed as described in Lustofin et al [35], and then dehydrated and dried using supercritical CO 2 . The material was then sputter-coated with gold and examined at an accelerating voltage of 20 kV using a Hitachi S-4700 scanning electron microscope, which is housed at the Institute of Geological Sciences, Jagiellonian University in Kraków, Poland.…”

Comparative Floral and Pollen Micromorphology of Leonurus japonicus and L. macranthus (Lamiaceae)

“…Thus, the high density of non-glandular and glandular trichomes, especially on the abaxial side of the calyx and lip, may have several roles in the two Leonurus species, including physical protection and deterrence of herbivory. Recent investigations have also suggested that edible floral non-glandular trichomes, which contain starch, may act as a food reward for visitors and pollinators [65,66], and that most lamiacean plants produce and store aromatic com-pounds, essential oils, or floral scents-which may increase the attractiveness of flowers to insects [67][68][69][70][71]-in glandular trichomes, especially the peltate and capitate glands on the calyx and corolla [23,30,[67][68][69]. Thus, field surveys and histochemical studies are necessary to explore whether the floral non-glandular trichomes of Leonurus can be provided as a food material to pollinators and to describe secondary metabolic compounds.…”

On the infrageneric classification of Pinguicula

“…(Casper 1966, p. 59). However, Casper's assumption of "floral functional stability" has proven fundamentally wrong in the light of evolutionary concepts, as certain flower characters can be switched quickly during evolution in adaptation to new pollinator groups or when new floral syndromes evolve, especially in young evolutionary lineages that are still in the process of biological radiation -this holds true for any group of plants, including Pinguicula (Cieslak et al 2005;Fleischmann 2016;Fleischmann & Roccia 2018;Lustofin et al 2020;Shimai et al 2021). This can result in closely related species displaying quite different, diverging floral morphology (= divergent evolution), but also in rather distantly related species that show strikingly similar flower shapes (= convergent or parallel evolution) -both can be visualized in Figure 3.…”

“…1). However, all molecular phylogenetic studies that included these two taxa independently show that both are closely related sister species Lustofin et al 2020;Shimai et al 2021), which exposes their different subgeneric/sectional classification based on flower morphology as artificial, so it does not mirror their natural affinity. There are several more examples where morphology-based concepts and phylogenetic results are in conflict.…”

“…3). Certainly, these long-spurred, funnel-tubed flowers (which additionally show bright red, purple, or magenta colors) evolved in these species in adaptation to hummingbird pollination (Lampard et al 2016;Lustofin et al 2020). And obviously P. laueana and P. hemiepiphytica are much more closely related to P. moranensis (which, based on the morphological concept, was placed in a different section, P. section Orchidopsis), than they are to the other species (P. crassifolia, P. utricularioides, P. calderoniae) they have been associated with in section Longitubus.…”