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Carnivorous Plants: Phylogeny and Structural Evolution
Abstract
The carnivorous habit in flowering plants represents a grade of structural organization. Different morphological features associated with the attraction, trapping, and digestion of prey characterize a diversity of specialized forms, including the familiar pitcher and flypaper traps. Phylogenetic analysis of nucleotide sequence data from the plastic rbcL gene indicates that both carnivory and stereotyped trap forms have arisen independently in different lineages of angiosperms. Furthermore, these results demonstrate that flypaper traps share close common ancestry with all other trap forms. Recognition of these patterns of diversification may provide ideal, naturally occurring systems for studies of developmental processes underlying macromorphological evolution in angiosperms.
Supplementary resources (12)
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... The first Sanger-sequenced molecular phylogeny using the plastid rbcL gene across all major angiosperm lineages provided an opportunity to map the evolution of carnivory, and uncovered evidence of at least five independent origins of carnivorous plants [1]. Since that study, additional cases of carnivory have been verified for members of the Poales families Bromeliaceae (Brocchinia hechtiodes, B. reducta [2,3], Catopsis beteronianum [4]) and Eriocaulaceae (Paepalanthus bromelioides [5]), in the Ericales (Roridula gorgonias) [6], and Lamiales (Plantaginaceae; Philcoxia spp. ...
... Albert et al. [1] provided the first molecular phylogenetic insight into the origins of carnivorous plants using the rbcL plastid marker with a broad sampling across angiosperm families. The Darlingtonia, Heliamphora and Sarracenia genera formed a monophyletic Sarraceniaceae, sister to the proto-carnivorous Rordidula (Roridulaceae), and together this clade was sister to two accessions from the Ericaceae (Ericales). ...
... Carnivory evolved once in the Oxidales, specifically within the monotypic Cephalotaceae family, which is endemic to a few coastal sites in southwestern Western Australia [27]. The earliest molecular phylogeny to include Cephalotus placed it as sister to Oxalis [1]. Subsequent studies found that it is nested within Oxidales, with some placing it as sister to Brunelliaceae [29,40,59], while others found a sister relationship with Elaeocarpaceae [60]. ...
Plastid molecular phylogenies that broadly sampled angiosperm lineages imply that car-nivorous plants evolved at least 11 times independently in 13 families and 6 orders. Within and between these clades, the different prey capture strategies involving flypaper and pitfall structures arose in parallel with the subsequent evolution of snap traps and suction bladders. Attempts to discern the deep ontological history of carnivorous structures using multigene phylogenies have provided a plastid-level picture of sister relationships at the family level. Here, we present a molecular phylogeny of the angiosperms based on nuclear target sequence capture data (Angiosperms-353 probe set), assembled by the Kew Plant Trees of Life initiative, which aims to complete the tree of life for plants. This phylogeny encompasses all carnivorous and protocarnivorous families, although certain genera such as Philcoxia (Plantaginaceae) are excluded. This study offers a novel nuclear gene-based overview of relationships within and between carnivorous families and genera. Consistent with previous broadly sampled studies, we found that most carnivorous families are not affiliated with any single family. Instead, they emerge as sister groups to large clades comprising multiple non-carnivorous families. Additionally, we explore recent genomic studies across various carnivorous clades that examine the evolution of the carnivorous syndrome in relation to whole-genome duplication, subgenome dominance, small-scale gene duplication, and convergent evolution. Furthermore, we discuss insights into genome size evolution through the lens of carnivorous plant genomes.
... Carnivorous plants that produce a pitfall-formed trap are called "pitcher plants", including Sarraceniaceae, Cephalotaceae, and Nepenthaceae [15]. The Nepenthes (Nepenthaceae) create jug-shaped traps that acquire arthropods and other small animals [16]. ...
Simple Summary
Traps of Nepenthes (pitcher plants), often referred to as an “external stomach”, conduct a unique process of external digestion. In this process in pitcher plants, reactive oxygen species (ROS) primarily act positively, whereas they are considered as “evil characters” in humans. Reactive nitrogen species (RNS) have a dual role, which depends on their concentration and the place of their generation. The digestive process in Nepenthes is influenced by reactive oxygen and nitrogen species (RONS), which serve as regulators in both plant and human systems.
Abstract
Carnivorous plants attract animals, trap and kill them, and absorb nutrients from the digested bodies. This unusual (for autotrophs) type of nutrient acquisition evolved through the conversion of photosynthetically active leaves into specialised organs commonly called traps. The genus Nepenthes (pitcher plants) consists of approximately 169 species belonging to the group of carnivorous plants. Pitcher plants are characterised by specialised passive traps filled with a digestive fluid. The digestion that occurs inside the traps of carnivorous plants depends on the activities of many enzymes. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) also participate in the digestive process, but their action is poorly recognised. ROS and RNS, named together as RONS, exhibit concentration-dependent bimodal functions (toxic or signalling). They act as antimicrobial agents, participate in protein modification, and are components of signal transduction cascades. In the human stomach, ROS are considered as the cause of different diseases. RNS have multifaceted functions in the gastrointestinal tract, with both positive and negative impacts on digestion. This review describes the documented and potential impacts of RONS on the digestion in pitcher plant traps, which may be considered as an external stomach.
... Due to this unique adaptation they are commonly called pitcher plants, although pitcher-shaped carnivorous leaves have evolved convergently in at least two other lineages (Nepenthes L., Cephalotus Labill.) (Albert et al., 1992). Most Sarracenia species occur sympatrically with at least one other species, and all species pairs can produce fertile hybrids (Bell, 1952). ...
Introgression can produce novel genetic variation in organisms that hybridize. Sympatric species pairs in the carnivorous plant genus Sarracenia L. frequently hybridize, and all known hybrids are fertile. Despite being a desirable system for studying the evolutionary consequences of hybridization, the extent to which introgression occurs in the genus is limited to a few species in only two field sites. Previous phylogenomic analysis of Sarracenia estimated a highly resolved species tree from 199 nuclear genes, but revealed a plastid genome that is highly discordant with the species tree. Such cytonuclear discordance could be caused by chloroplast introgression (i.e. chloroplast capture) or incomplete lineage sorting (ILS). To better understand the extent to which introgression is occurring in Sarracenia, the chloroplast capture and ILS hypotheses were formally evaluated. Plastomes were assembled de-novo from sequencing reads generated from 17 individuals in addition to reads obtained from the previous study. Assemblies of 14 whole plastomes were generated and annotated, and the remaining fragmented assemblies were scaffolded to these whole-plastome assemblies. Coding sequence from 79 homologous genes were aligned and concatenated for maximum-likelihood phylogeny estimation. The plastome tree is extremely discordant with the published species tree. Plastome trees were simulated under the coalescent and tree distance from the species tree was calculated to generate a null distribution of discordance that is expected under ILS alone. A t-test rejected the null hypothesis that ILS could cause the level of discordance seen in the plastome tree, suggesting that chloroplast capture must be invoked to explain the discordance. Due to the extreme level of discordance in the plastome tree, it is likely that chloroplast capture has been common in the evolutionary history of Sarracenia.
... July 2023 Volume 89 Issue 710.1128/aem.00812-23 ...
Plants use different strategies to obtain the nutrients that they need to grow. Some plants access their nitrogen directly from the soil, while others rely on microbes to access the nitrogen for them.
... Carnivorous plants are polyphyletic and represented by approximately 850 carnivorous plant species [40]. Carnivorous syndromes have evolved independently in approximately 10 lineages of flowering plants [41,42]. Carnivorous plants such as N. miranda, which was used in this study, possess specialized traps derived from leaves that are able to attract and catch small animals such as insects and retain them in these pitchers. ...
The carnivorous pitcher plants of the genus Nepenthes exhibit many ethnobotanical uses, including treatments of stomachache and fever. In this study, we prepared different extracts from the pitcher, stem, and leaf extracts of Nepenthes miranda obtained using 100% methanol and analyzed their inhibitory effects on recombinant single-stranded DNA-binding protein (SSB) from Klebsiella pneumoniae (KpSSB). SSB is essential for DNA replication and cell survival and thus an attractive target for potential antipathogen chemotherapy. Different extracts prepared from Sinningia bullata, a tuberous member of the flowering plant family Gesneriaceae, were also used to investigate anti-KpSSB properties. Among these extracts, the stem extract of N. miranda exhibited the highest anti-KpSSB activity with an IC50 value of 15.0 ± 1.8 μg/mL. The cytotoxic effects of the stem extract of N. miranda on the survival and apoptosis of the cancer cell lines Ca9-22 gingival carcinoma, CAL27 oral adenosquamous carcinoma, PC-9 pulmonary adenocarcinoma, B16F10 melanoma, and 4T1 mammary carcinoma cells were also demonstrated and compared. Based on collective data, the cytotoxic activities of the stem extract at a concentration of 20 μg/mL followed the order Ca9-22 > CAL27 > PC9 > 4T1 > B16F10 cells. The stem extract of N. miranda at a concentration of 40 μg/mL completely inhibited Ca9-22 cell migration and proliferation. In addition, incubation with this extract at a concentration of 20 μg/mL boosted the distribution of the G2 phase from 7.9% to 29.2% in the Ca9-22 cells; in other words, the stem extract might suppress Ca9-22 cell proliferation by inducing G2 cell cycle arrest. Through gas chromatography–mass spectrometry, the 16 most abundant compounds in the stem extract of N. miranda were tentatively identified. The 10 most abundant compounds in the stem extract of N. miranda were used for docking analysis, and their docking scores were compared. The binding capacity of these compounds was in the order sitosterol > hexadecanoic acid > oleic acid > plumbagin > 2-ethyl-3-methylnaphtho[2,3-b]thiophene-4,9-dione > methyl α-d-galactopyranoside > 3-methoxycatechol > catechol > pyrogallol > hydroxyhydroquinone; thus, sitosterol might exhibit the greatest inhibitory capacity against KpSSB among the selected compounds. Overall, these results may indicate the pharmacological potential of N. miranda for further therapeutic applications.
We present the counterpart to Chap. 4 in Chap. 5, where we focus on the role of “permanent” exceptions and their importance in scientific knowledge and biology. These exceptions can be analyzed at any scale and are often not appreciated beyond anecdotal mentions. They can be aberrant or teratological groups, taxonomic groups unique for some features of their biology, “intermediate exceptions” with minorities of species or clades with certain characteristics compared to the majority, or organisms with exceptional distributions in space or time. In this chapter, we reviewed groups that have been difficult to classify because of their rarity, rarities that can be used for human benefit, exceptional groups that make us rethink phylogenetic relationships, rare and incredible biological phenomena, and evolutionary and ecological aspects of rare species. Our goal is to vindicate rarities and minorities, to highlight their importance for the understanding of evolution, and to begin to make these cases visible and treasured in the teaching of biology.
Subgenome dominance after whole-genome duplication generates distinction in gene number and expression at the level of chromosome sets, but it remains unclear how this process may be involved in evolutionary novelty. Here we generated a chromosome-scale genome assembly of the Asian pitcher plant Nepenthes gracilis to analyse how its novel traits (dioecy and carnivorous pitcher leaves) are linked to genomic evolution. We found a decaploid karyotype and a clear indication of subgenome dominance. A male-linked and pericentromerically located region on the putative sex chromosome was identified in a recessive subgenome and was found to harbour three transcription factors involved in flower and pollen development, including a likely neofunctionalized LEAFY duplicate. Transcriptomic and syntenic analyses of carnivory-related genes suggested that the paleopolyploidization events seeded genes that subsequently formed tandem clusters in recessive subgenomes with specific expression in the digestive zone of the pitcher, where specialized cells digest prey and absorb derived nutrients. A genome-scale analysis suggested that subgenome dominance likely contributed to evolutionary innovation by permitting recessive subgenomes to diversify functions of novel tissue-specific duplicates. Our results provide insight into how polyploidy can give rise to novel traits in divergent and successful high-ploidy lineages.
Resumen
Diferentes análisis filogenéticos moleculares muestran que la familia Crassulaceae es monofilética y se encuentra dentro del clado de los Superrosidos Orden Saxifragales. Sin embargo, las relaciones filogenéticas y el establecimiento de grupos monofiléticos dentro de la familia se han vuelto inciertos y difíciles de delimitar a nivel de subfamilia y género. El clado Acre, incluye los taxones más variables y confusos, entre estos taxones están, Graptopetalum, Echeveria, Lenophyllum, Sedum y Pachyphytum. Moran subdividió a este último con base en caracteres anatómicos de la flor en sección Pachyphytum, sección Ixiocaulon y sección Diotostemon; mismas secciones reconocidas por Meyrán y Chávez; sin embargo, Thiede solo reconoce la sección Pachyphytum y la sección Diotostemon, e incluye a la sección Ixiocaulon dentro de la sección Pachyphytum. El género Pachyphytum es un grupo monofilético y grupo hermano del “grupo Echeveria”, dentro del clado Acre. Este género está constituido en la actualidad por aproximadamente ± 21 especies, por otro lado, Pachyphytum representa endemismo para México y su distribución está restringida al centro
del país. Se espera encontrar evidencias significativas de la anatomía interna que apoyen la subdivisión del género Pachyphytum propuesta por Moran. Se realizó un estudio de las características anatómicas mediante cortes transversales de tallos y hojas, así como, un análisis de secciones de epidermis de siete especies del género Pachyphytum. El 98% de los rasgos anatómicos son homogéneos. Los caracteres que mostraron variación fue el número de células adyacentes al complejo estomático y la presencia de crecimiento secundario en P. caesium y P. glutinicaule. El análisis comparativo de la anatomía interna no permitió establecer posibles
diferencias en estructura y organización interna de las especies utilizadas, para lograr una separación entre secciones, sin embargo, la información aporta conocimiento sobre la anatomía interna del género Pachyphytum.
Palabras clave: Pachyphytum, Crassulaceae, anatomía interna, intrusiones cuticulares, índice estomático, hoja anfiestomática
Central American and Mexican Pinguicula species are characterized by enormous divergence in size and color of flowers and are pollinated by butterflies, flies, bees, and hummingbirds. It is known that floral trichomes are key characters in plant-pollinator interaction. The main aim of our study was to verify our hypothesis that the distribution and diversity of non-glandular and glandular trichomes are related to the pollinator syndromes rather than the phylogenetic relationships. The studied sample consisted of Central American and Mexican species. In our study, we relied on light microscopy and scanning electron microscopy with a phylogenetic perspective based on ITS DNA sequences. The flower morphology of species pollinated by butterflies and hummingbirds was similar in contrast to species pollinated by flies and bees. Species pollinated by butterflies and hummingbirds contained low diversity of non-glandular trichomes, which occurred mostly in the tube and basal part of the spur. Surprisingly, in P. esseriana and P. mesophytica, non-glandular trichomes also occurred at the base of lower lip petals. In the case of species pollinated by flies/bees, we observed a high variety of non-glandular trichomes, which occurred on the surface of corolla petals, in the tube, and at the entrance to the spur. Furthermore, we did not identify any non-glandular trichomes in the spur. The capitate glandular trichomes were of similar morphology in all examined species. There were minor differences in the shape of the trichome head, as well as the length and the number of stalk cells. The distribution and the diversity of non-glandular and glandular trichomes and pollinator syndromes were mapped onto a phylogenetic reconstruction of the genus. Most micromorphological characters appear to be associated more with floral adaptation to pollinators and less with phylogeny.
According to a broad definition, homeosis is the assumption by one part of an organism of likeness to another part. In developmental terms this means that at the site of one part another part or features of another part are expressed. Whereas homeosis continues to be actively investigated in animals, especially at the genetic level, it has been almost completely ignored or overlooked in plants. One purpose of this article is to draw attention to the fact that homeosis is widespread in plants from the cellular to the organismal level. Another purpose is to examine some of the consequences of this phenomenon for developmental and evolutionary plant biology, particularly homology, punctuated equilibra, and macroevolution.
Certain leaves of Triphyophyllum peltatum (Hutch. & Dalz.) Airy Shaw (Dioncophyllaceae) have an extended, erect midrib covered with stalked and sessile glands exhibiting insect-trapping ability. The stalked glands secrete a sticky, acid mucilage to which numerous insects in various stages of decay were observed adhering. The morphology and anatomy of the glandular leaves were investigated with light and scanning electron microscopy. The midrib and the lamina in the lowermost part of the leaf bear stomata. Those of the midrib are transitional between actinocytic and cyclocytic in type. Parenchyma cells in mature and immature portions of the midrib and in the glands contain numerous crystals and amyloplasts. The anatomy of the stalked and sessile glands is remarkably similar to that of Drosophyllum lusitanicum (L.) Link. (Droseraceae). A distinct cuticle covers the gland head, but no pores are visible. Three distinct layers underlie the cuticle: a definite epidermal layer with irregularly thickened cell walls, and two layers of more loosely arranged cells. A fourth layer, endodermoid in nature with radially thickened cell walls, connects the head and stalk of the stalked glands and the head and midrib parenchyma of the sessile glands. Vascular elements (including helical and scalariform tracheary elements) reach the endodermoid layer. According to recent studies, Triphyophyllum and Drosophyllum have different phylogenetic origins; the morphological and anatomical similarities in the insect-trapping glandular leaves show more support for their convergent evolution rather than for an alliance of the Dioncophyllaceae with the Droseraceae.
The way some plants function as carnivores gives insights into plant form, function, and evolution not otherwise readily available. They exhibit features which are common to many other non-carnivorous plants. The extent to which these features have developed, however, and the combination of different features in small organs is unique. The main sections of the book are: the syndrome and the habitat; attraction and trapping; nutrition and digestion; phytochemical aspects; exploitation and mutualism; evolution. -from Publisher
The "tendency" for homoplasy to appear in closely related taxa has been widely discussed but rarely quantified. This paper proposes statistical tests that examine the topological distribution of homoplasy within characters in phylogenies. They test whether character changes are localized (confined to some subtree), or clustered (occur in proximity to each other), relative to two null models of character evolution. Null Model I assumes that the observed number of character changes are dispersed randomly among the internodes of the tree, whereas Model II weights the probability that an internode contains a change by the length of that internode-estimated by the total number of character changes along that internode. Localization is measured by the largest furthest-neighbor distance between changes, clustering by the mean nearest neighbor distance. Distances are measured either by the number of intervening branches or the number of intervening character changes. Analyses of four cladistic data sets from the literature reveal very few characters that exhibit significant levels of clustering or localization-no more than would be expected by chance. In every data set a majority of characters exhibited at least weak tendencies, but in only one data set was there a significant excess of such characters. The present findings do not provide compelling evidence for the existence of "tendencies" in homoplasy, at least among characters used to reconstruct phylogenies. They should be sought elsewhere, in cladistic analyses of larger scope, probably among a class of characters defined a priori on a structural or functional basis.
Previous studies have shown that in several angiosperms and the liverwort Marchantia the chloroplast gene rpl2, encoding ribosomal protein L2, is interrupted by an intron, but that in spinach (Spinacia oleracea, Caryophyllales) this intron has been lost. We have determined the distribution of the rpl2 intron for 390 species representing 116 angiosperm families. Filter hybridizations reveal that the intron is absent from the chloroplast genomes of all examined families of the Caryophyllales, suggesting that the intron was lost in the common ancestor of the order. Sequencing of the rpl2 gene in five genera of the Caryophyllales and in Rumex (Polygonales) not only confirms the filter hybridization results, but also shows that for all taxa lacking the intron, the rpl2 gene has undergone a precise deletion of the intron. In all cases, it is the original rpl2 gene that has sustained loss of its intron. This implies that in chloroplast DNA, integration of exogenous genes (e.g., a reverse transcript of a spliced mRNA) occurs mainly by homologous, replacement recombination, rather than by illegitimate recombination elsewhere in the genome. Filter hybridizations also reveal that the rpl2 intron was lost independently in the common ancestors of at least five other lineages of dicotyledons: Saxifragaceae (s.s.), Convolvulaceae (including Cuscuta), Menyanthaceae, two genera of Geraniaceae, and one genus of Droseraceae. The molecular and phylogenetic implications of these independent intron losses are discussed.
Studies of character evolution have frequently relied on ahistorical correlations rather than on phylogenies. However, correlations do not estimate the number of times that a trait evolved, and they are insensitive to the direction or the temporal sequence of character transformation. In contrast, cladograms can provide this information. A cladistic test of the hypothesis that the evolution of dioecy is favored in animal-dispersed plants indicates that dioecy may have originated somewhat more often in such lineages. Nevertheless, differences in rates of speciation or extinction must largely account for the observed species-level correlation between dispersal and breeding system. In considering the evolution of individual traits, cladograms help identify the context in which a feature evolved and specify which organisms should be compared in evaluating the causes of character change. Determining whether a feature and a performance advantage were strictly historically correlated or followed one another in sequence helps to distinguish whether the trait is an adaptation or an exaptation for the function. For example, cladograms of seed plants suggest that double fertilization arose incidentally prior to the origin of angiosperms and that the resulting product was later co-opted and elaborated as a nutritive tissue for the developing embryo. The order of character assembly in a lineage also bears on the evolution of functional and developmental interdependencies. In particular, it may be possible to trace the evolution of a character's "burden" from an initial period, during which change is more likely, through later stages, wherein successful modification is less likely owing to the evolution of dependent characters. The evolution of vessels and of floral phyllotaxis in angiosperms may exemplify this pattern. Recognition that the likelihood of character transformation may change during the evolution of a group warns against character weighting in phylogenetic analysis.
Studies of ontogenetic processes are fundamentally dependent on hypotheses of phylogeny. The model of Alberch et al. (1979) is reformulated in terms of phylogenetics and used to describe how heterochronic ontogenetic processes can be detected in nature. Heterochronic processes producing paedomorphosis can result in morphologies which resemble primitive (retained ancestral) traits; the conditions under which paedomorphic and primitive features can and cannot be distinguished are described. The utility of ontogeny for determination of evolutionary character transformations and character polarity and for detection of convergence and parallelism are considered. The ontogenetic criterion for assessing polarity is independent of hypotheses of phylogeny and may be as effective as outgroup comparison. Ontogenetic analysis may aid in the detection of convergence but not in the detection of parallelism.
Phylogenetic systematics discovers pattern; ontogenetic systematics uncovers processes behind pattern. Plant diversity, as recognized in the field, herbarium, or library, stems from the diversity of plant form. How an organism develops determines its phenotype, and therefore differences among ontogenies are what generate diversity. The molecular basis for these differences is of fundamental importance to plant systematics, yet the topic remains poorly understood.