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Flower nectar trichome structure of carnivorous plants from the genus butterworts Pinguicula L. (Lentibulariaceae).

ABSTRACT: Pinguicula (Lentibulariaceae) is a genus comprising around 96 species of herbaceous, carnivorous plants, which are extremely diverse in flower size, colour and spur length and structure as well as pollination strategy. In Pinguicula, nectar is formed in the flower spur; however, there is a gap in the knowledge about the nectary trichome structure in this genus. Our aim was to compare the nectary trichome structure of various Pinguicula species in order to determine whether there are any differences among the species in this genus. The taxa that were sampled were Pinguicula moctezumae, P. moranensis, P. rectifolia, P. emarginata and P. esseriana. We used light microscopy, histochemistry, scanning and transmission electron microscopy to address those aims. We show a conservative nectary trichome structure and spur anatomy in various Mexican Pinguicula species. The gross structural similarities between the examined species were the spur anatomy, the occurrence of papillae, the architecture of the nectary trichomes and the ultrastructure characters of the trichome cells. However, there were some differences in the spur length, the size of spur trichomes, the occurrence of starch grains in the spur parenchyma and the occurrence of cell wall ingrowths in the terminal cells of the nectary trichomes. Similar nectary capitate trichomes, as are described here, were recorded in the spurs of species from other Lentibulariaceae genera. There are many ultrastructural similarities between the cells of nectary trichomes in Pinguicula and Utricularia.

SUBMITTER: Lustofin K

PROVIDER: S-EPMC6982637 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Flower nectar trichome structure of carnivorous plants from the genus butterworts Pinguicula L. (Lentibulariaceae).

Lustofin Krzysztof K Świątek Piotr P Miranda Vitor F O VFO Płachno Bartosz J BJ

Protoplasma 20190819 1

Pinguicula (Lentibulariaceae) is a genus comprising around 96 species of herbaceous, carnivorous plants, which are extremely diverse in flower size, colour and spur length and structure as well as pollination strategy. In Pinguicula, nectar is formed in the flower spur; however, there is a gap in the knowledge about the nectary trichome structure in this genus. Our aim was to compare the nectary trichome structure of various Pinguicula species in order to determine whether there are any differen ...[more]

PMID: 31428856

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Project description:Earlier phylogenetic studies in the genus Pinguicua (Lentibulariaceae) suggested that the species within a geographical region was rather monophyletic, although the sampling was limited or was restricted to specific regions. Those results conflicted with the floral morphology-based classification, which has been widely accepted to date. In the current study, one nuclear ribosomal DNA (internal transcribed spacer; ITS) and two regions of chloroplast DNA (matK and rpl32-trnL), from up to ca. 80% of the taxa in the genus Pinguicula, covering all three subgenera, were sequenced to demonstrate the inconsistency and explore a possible evolutionary history of the genus. Some incongruence was observed between nuclear and chloroplast topologies and the results from each of the three DNA analyses conflicted with the morphology-based subgeneric divisions. Both the ITS tree and network, however, corresponded with the biogeographical patterns of the genus supported by life-forms (winter rosette or hibernaculum formation) and basic chromosome numbers (haploidy). The dormant strategy evolved in a specific geographical region is a phylogenetic constraint and a synapomorphic characteristic within a lineage. Therefore, the results denied the idea that the Mexican group, morphologically divided into the three subgenera, independently acquired winter rosette formations. Topological incongruence among the trees or reticulations, indicated by parallel edges in phylogenetic networks, implied that some taxa originated by introgressive hybridisation. Although there are exceptions, species within the same geographical region arose from a common ancestor. Therefore, the classification by the floral characteristics is rather unreliable. The results obtained from this study suggest that evolution within the genus Pinguicula has involved; 1) ancient expansions to geographical regions with gene flow and subsequent vicariance with genetic drift, 2) acquirement of a common dormant strategy within a specific lineage to adapt a local climate (i.e., synapomorphic characteristic), 3) recent speciation in a short time span linked to introgressive hybridisation or multiplying the ploidy level (i.e., divergence), and 4) parallel evolution in floral traits among lineages found in different geographical regions (i.e., convergence). As such, the floral morphology masks and obscures the phylogenetic relationships among species in the genus.

Project description:Background and aimsFloral 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.MethodsThe 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 resultsNo 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.ConclusionFloral 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.

Project description:The carnivorous plants of the family Lentibulariaceae have attained recent attention not only because of their interesting lifestyle, but also because of their dynamic nuclear genome size. Lentibulariaceae genomes span an order of magnitude and include species with the smallest genomes in angiosperms, making them a powerful system to study the mechanisms of genome expansion and contraction. However, little is known about mitochondrial DNA (mtDNA) sequences of this family, and the evolutionary forces that shape this organellar genome. Here we report the sequencing and assembly of the complete mtDNA from the endemic terrestrial Brazilian species Utricularia reniformis. The 857,234bp master circle mitochondrial genome encodes 70 transcriptionaly active genes (42 protein-coding, 25 tRNAs and 3 rRNAs), covering up to 7% of the mtDNA. A ltrA-like protein related to splicing and mobility and a LAGLIDADG homing endonuclease have been identified in intronic regions, suggesting particular mechanisms of genome maintenance. RNA-seq analysis identified properties with putative diverse and important roles in genome regulation and evolution: 1) 672kbp (78%) of the mtDNA is covered by full-length reads; 2) most of the 243kbp intergenic regions exhibit transcripts; and 3) at least 69 novel RNA editing sites in the protein-coding genes. Additional genomic features are hypothetical ORFs (48%), chloroplast insertions, including truncated plastid genes that have been lost from the chloroplast DNA (5%), repeats (5%), relics of transposable elements mostly related to LTR retrotransposons (5%), and truncated mitovirus sequences (0.4%). Phylogenetic analysis based on 32 different Lamiales mitochondrial genomes corroborate that Lentibulariaceae is a monophyletic group. In summary, the U. reniformis mtDNA represents the eighth largest plant mtDNA described to date, shedding light on the genomic trends and evolutionary characteristics and phylogenetic history of the family Lentibulariaceae.

Project description:Lentibulariaceae is the richest family of carnivorous plants spanning three genera including Pinguicula, Genlisea, and Utricularia. Utricularia is globally distributed, and, unlike Pinguicula and Genlisea, has both aquatic and terrestrial forms. In this study we present the analysis of the chloroplast (cp) genome of the terrestrial Utricularia reniformis. U. reniformis has a standard cp genome of 139,725bp, encoding a gene repertoire similar to essentially all photosynthetic organisms. However, an exclusive combination of losses and pseudogenization of the plastid NAD(P)H-dehydrogenase (ndh) gene complex were observed. Comparisons among aquatic and terrestrial forms of Pinguicula, Genlisea, and Utricularia indicate that, whereas the aquatic forms retained functional copies of the eleven ndh genes, these have been lost or truncated in terrestrial forms, suggesting that the ndh function may be dispensable in terrestrial Lentibulariaceae. Phylogenetic scenarios of the ndh gene loss and recovery among Pinguicula, Genlisea, and Utricularia to the ancestral Lentibulariaceae cladeare proposed. Interestingly, RNAseq analysis evidenced that U. reniformis cp genes are transcribed, including the truncated ndh genes, suggesting that these are not completely inactivated. In addition, potential novel RNA-editing sites were identified in at least six U. reniformis cp genes, while none were identified in the truncated ndh genes. Moreover, phylogenomic analyses support that Lentibulariaceae is monophyletic, belonging to the higher core Lamiales clade, corroborating the hypothesis that the first Utricularia lineage emerged in terrestrial habitats and then evolved to epiphytic and aquatic forms. Furthermore, several truncated cp genes were found interspersed with U. reniformis mitochondrial and nuclear genome scaffolds, indicating that as observed in other smaller plant genomes, such as Arabidopsis thaliana, and the related and carnivorous Genlisea nigrocaulis and G. hispidula, the endosymbiotic gene transfer may also shape the U. reniformis genome in a similar fashion. Overall the comparative analysis of the U. reniformis cp genome provides new insight into the ndh genes and cp genome evolution of carnivorous plants from Lentibulariaceae family.

Dataset Information

Flower nectar trichome structure of carnivorous plants from the genus butterworts Pinguicula L. (Lentibulariaceae).

Publications

Flower nectar trichome structure of carnivorous plants from the genus butterworts Pinguicula L. (Lentibulariaceae).

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