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1.  Detecting and Characterizing the Highly Divergent Plastid Genome of the Nonphotosynthetic Parasitic Plant Hydnora visseri (Hydnoraceae) 
Genome Biology and Evolution  2016;8(2):345-363.
Plastid genomes of photosynthetic flowering plants are usually highly conserved in both structure and gene content. However, the plastomes of parasitic and mycoheterotrophic plants may be released from selective constraint due to the reduction or loss of photosynthetic ability. Here we present the greatly reduced and highly divergent, yet functional, plastome of the nonphotosynthetic holoparasite Hydnora visseri (Hydnoraceae, Piperales). The plastome is 27 kb in length, with 24 genes encoding ribosomal proteins, ribosomal RNAs, tRNAs, and a few nonbioenergetic genes, but no genes related to photosynthesis. The inverted repeat and the small single copy region are only approximately 1.5 kb, and intergenic regions have been drastically reduced. Despite extreme reduction, gene order and orientation are highly similar to the plastome of Piper cenocladum, a related photosynthetic plant in Piperales. Gene sequences in Hydnora are highly divergent and several complementary approaches using the highest possible sensitivity were required for identification and annotation of this plastome. Active transcription is detected for all of the protein-coding genes in the plastid genome, and one of two introns is appropriately spliced out of rps12 transcripts. The whole-genome shotgun read depth is 1,400× coverage for the plastome, whereas the mitochondrial genome is covered at 40× and the nuclear genome at 2×. Despite the extreme reduction of the genome and high sequence divergence, the presence of syntenic, long transcriptionally active open-reading frames with distant similarity to other plastid genomes and a high plastome stoichiometry relative to the mitochondrial and nuclear genomes suggests that the plastome remains functional in H. visseri. A four-stage model of gene reduction, including the potential for complete plastome loss, is proposed to account for the range of plastid genomes in nonphotosynthetic plants.
doi:10.1093/gbe/evv256
PMCID: PMC4779604  PMID: 26739167
parasitic plants; holoparasite; nonphotosynthetic; Hydnoraceae; plastome; plastid genome
2.  Biomechanics and functional morphology of a climbing monocot 
AoB Plants  2016;8:plw005.
Climbing monocots can develop into large bodied plants despite being confined by primary growth. In our study on Flagellaria indica we measured surprisingly high stem biomechanical properties (in bending and torsion) and we show that the lack of secondary growth is overcome by a combination of tissue maturation processes and attachment mode. This leads to higher densities of mechanically relevant tissues in the periphery of the stem and to the transition from self-supporting to climbing growth. The development of specialised attachment structures has probably underpinned the evolution of numerous other large bodied climbing monocot taxa.
Plants with a climbing growth habit possess unique biomechanical properties arising from adaptations to changing loading conditions connected with close attachment to mechanical supports. In monocot climbers, mechanical adaptation is restricted by the absence of a bifacial vascular cambium. Flagellaria indica was used to investigate the mechanical properties and adaptations of a monocot climber that, uniquely, attaches to the surrounding vegetation via leaf tendrils. Biomechanical methods such as three-point bending and torsion tests were used together with anatomical studies on tissue development, modification and distribution. In general, the torsional modulus was lower than the bending modulus; hence, torsional stiffness was less than flexural stiffness. Basal parts of mature stems showed the greatest stiffness while that of more apical stem segments levelled off. Mechanical properties were modulated via tissue maturation processes mainly affecting the peripheral region of the stem. Peripheral vascular bundles showed a reduction in the amount of conducting tissue while the proportion and density of the bundle sheath increased. Furthermore, adjacent bundle sheaths merged resulting in a dense ring of fibrous tissue. Although F. indica lacks secondary cambial growth, the climbing habit is facilitated by a complex interaction of tissue maturation and attachment.
doi:10.1093/aobpla/plw005
PMCID: PMC4789545  PMID: 26819259
Biomechanics; climbing plants; Flagellaria indica; functional morphology; monocotyledons; structural bending modulus; structural modulus of torsion; three-point bending; twist-to-bend ratio
3.  The multi-layered protective cuticle of Collembola: a chemical analysis 
Collembola, also known as springtails, are soil-dwelling arthropods that typically respire through the cuticle. To avoid suffocating in wet conditions, Collembola have evolved a complex, hierarchically nanostructured, cuticle surface that repels water with remarkable efficiency. In order to gain a more profound understanding of the cuticle characteristics, the chemical composition and architecture of the cuticle of Tetrodontophora bielanensis was studied. A stepwise removal of the different cuticle layers enabled controlled access to each layer that could be analysed separately by chemical spectrometry methods and electron microscopy. We found a cuticle composition that consisted of three characteristic layers, namely, a chitin-rich lamellar base structure overlaid by protein-rich nanostructures, and a lipid-rich envelope. The specific functions, composition and biological characteristics of each cuticle layer are discussed with respect to adaptations of Collembola to their soil habitat. It was found that the non-wetting characteristics base on a rather typical arthropod cuticle surface chemistry which confirms the decisive role of the cuticle topography.
doi:10.1098/rsif.2014.0619
PMCID: PMC4233743  PMID: 25100321
Collembola; cuticle; lipid; protein; chitin
4.  Major trends in stem anatomy and growth forms in the perianth-bearing Piperales, with special focus on Aristolochia 
Annals of Botany  2014;113(7):1139-1154.
Background and Aims
The order Piperales has the highest diversity of growth forms among the earliest angiosperm lineages, including trees, shrubs, climbers and herbs. However, within the perianth-bearing Piperales (Asarum, Saruma, Lactoris, Hydnora, Prosopanche, Thottea and Aristolochia), climbing species only occur in the most species-rich genus Aristolochia. This study traces anatomical and morphological traits among these lineages, to detect trends in growth form evolution and developmental processes.
Methods
Transverse stem sections of different developmental stages of representatives of Asarum, Saruma, Lactoris, Hydnora, Thottea and Aristolochia were compared and anatomical traits were linked to growth form evolution. Biomechanical properties of representative climbers were determined in three-point bending tests and are discussed based on the anatomical observations. Growth form evolution of the perianth-bearing Piperales was reconstructed by ancestral character state reconstruction using Mesquite.
Key Results
While species of Asarum and Saruma are exclusively herbaceous, species of the remaining genera show a higher diversity of growth habit and anatomy. This growth form diversity is accompanied by a more complex stem anatomy and appropriate biomechanical properties. The ancestral growth form of the perianth-bearing Piperales is reconstructed with either a shrub-like or herbaceous character state, while the following three backbone nodes in the reconstruction show a shrub-like character state. Accordingly, the climbing habit most probably evolved in the ancestor of Aristolochia.
Conclusions
Since the ancestor of the perianth-bearing Piperales has been reconstructed with a herb- or shrub-like habit, it is proposed that the climbing habit is a derived growth form, which evolved with the diversification of Aristolochia, and might have been a key feature for its diversification. Observed anatomical synapomorphies, such as the perivascular fibres in Lactoris, Thottea and Aristolochia, support the phylogenetic relationship of several lineages within the perianth-bearing Piperales. In addition, the hypothesis that the vegetative organs of the holoparasitic Hydnoraceae are most probably rhizomes is confirmed.
doi:10.1093/aob/mcu044
PMCID: PMC4030810  PMID: 24694829
Aristolochia; Thottea; Lactoris; Hydnora; Asarum; Saruma; growth form; anatomy; biomechanics; secondary woodiness; heterochrony; perianth-bearing Piperales
5.  The betrayed thief – the extraordinary strategy of Aristolochia rotunda to deceive its pollinators 
The New Phytologist  2014;206(1):342-351.
Pollination of several angiosperms is based on deceit. In such systems, the flowers advertise a reward that ultimately is not provided. We report on a previously unknown pollination/mimicry system discovered in deceptive Aristolochia rotunda (Aristolochiaceae).Pollinators were collected in the natural habitat and identified. Flower scent and the volatiles of insects (models) potentially mimicked were analyzed by chemical analytical techniques. Electrophysiological and behavioral tests on the pollinators identified the components that mediate the plant–pollinator interaction and revealed the model of the mimicry system.The main pollinators of A. rotunda were female Chloropidae. They are food thieves that feed on secretions of true bugs (Miridae) while these are eaten by arthropod predators. Freshly killed mirids and Aristolochia flowers released the same scent components that chloropids use to find their food sources. Aristolochia exploits these components to deceive their chloropid pollinators.Aristolochia and other trap flowers were believed to lure saprophilous flies and mimic brood sites of pollinators. We demonstrate for A. rotunda, and hypothesize for other deceptive angiosperms, the evolution of a different, kleptomyiophilous pollination strategy. It involves scent mimicry and the exploitation of kleptoparasitic flies as pollinators. Our findings suggest a reconsideration of plants assumed to show sapromyiophilous pollination.
doi:10.1111/nph.13210
PMCID: PMC4357391  PMID: 25488155
Aristolochia; chemical mimicry; Chloropidae; Croatia; deception; kleptoparasites; pollination system
6.  Ontogenetic tissue modification in Malus fruit peduncles: the role of sclereids 
Annals of Botany  2013;113(1):105-118.
Background and Aims
Apple (Malus) fruit peduncles are highly modified stems with limited secondary growth because fruit ripening lasts only one season. They must reliably connect rather heavy fruits to the branch and cope with increasing fruit weight, which induces dynamic stresses under oscillating wind loads. This study focuses on tissue modification of these small, exposed structures during fruit development.
Methods
A combination of microscopic, static and dynamic mechanical tests, as well as Raman spectroscopy, was used to study structure–function relationships in peduncles of one cultivar and 12 wild species, representatively chosen from all sections of the genus Malus. Tissue differentiation and ontogenetic changes in mechanical properties of Malus peduncles were observed throughout one growing season and after successive removal of tissues.
Key Results
Unlike in regular stems, the vascular cambium produces mainly phloem during secondary growth. Hence, in addition to a reduced xylem, all species developed a centrally arranged sclerenchyma ring composed of fibres and brachysclereids. Based on differences in cell-wall thickness, and proportions and arrangement of sclereids, two types of peduncle construction could be distinguished. Fibres provide an increased maximum tensile strength and contribute most to the overall axial rigidity of the peduncles. Sclereids contribute insignificantly to peduncle strength; however, despite being shown to have a lower elastic modulus than fibres, they are the most effective tissue in stiffening peduncles against bending.
Conclusions
The experimental data revealed that sclereids originating from cortical parenchyma act as ‘accessory’ cells to enhance proportions of sclerenchyma during secondary growth in peduncles. The mechanism can be interpreted as an adaptation to continuously increasing fruit loads. Under oscillating longitudinal stresses, sclereids may be regarded as regulating elements between maintenance of stiffness and viscous damping, the latter property being attributed to the cortical parenchyma.
doi:10.1093/aob/mct262
PMCID: PMC3864733  PMID: 24287811
Apple; biomechanics; fibres; fruit peduncle; fruit load; functional anatomy; Malus; sclereids; viscous damping
7.  Functional morphology and biomechanics of branch–stem junctions in columnar cacti 
Branching in columnar cacti features morphological and anatomical characteristics specific to the subfamily Cactoideae. The most conspicuous features are the pronounced constrictions at the branch–stem junctions, which are also present in the lignified vascular structures within the succulent cortex. Based on finite-element analyses of ramification models, we demonstrate that these indentations in the region of high flexural and torsional stresses are not regions of structural weakness (e.g. allowing vegetative propagation). On the contrary, they can be regarded as anatomical adaptations to increase the stability by fine-tuning the stress state and stress directions in the junction along prevalent fibre directions. Biomimetic adaptations improving the functionality of ramifications in technical components, inspired, in particular, by the fine-tuned geometrical shape and arrangement of lignified strengthening tissues of biological role models, might contribute to the development of alternative concepts for branched fibre-reinforced composite structures within a limited design space.
doi:10.1098/rspb.2013.2244
PMCID: PMC3813340  PMID: 24132310
columnar cacti; functional anatomy; branching; finite-element analysis; biomimetics
8.  Aristolochia quangbinhensis (Aristolochiaceae), a new species from Central Vietnam  
PhytoKeys  2014;51-59.
Aristolochia quangbinhensis T.V. Do, a new species from Central Vietnam, is described and illustrated. According to morphology, the species belongs to Aristolochia subgenus Isotrema. A detailed description, along with line drawings, photographs, ecology, distribution, conservation status as well as a comparison to morphologically similar species is provided.
doi:10.3897/phytokeys.33.6094
PMCID: PMC3921559  PMID: 24526848
Aristolochia; Aristolochia quangbinhensis; Aristolochiaceae; Isotrema; new species; Vietnam
9.  Single-Copy Nuclear Genes Place Haustorial Hydnoraceae within Piperales and Reveal a Cretaceous Origin of Multiple Parasitic Angiosperm Lineages 
PLoS ONE  2013;8(11):e79204.
Extreme haustorial parasites have long captured the interest of naturalists and scientists with their greatly reduced and highly specialized morphology. Along with the reduction or loss of photosynthesis, the plastid genome often decays as photosynthetic genes are released from selective constraint. This makes it challenging to use traditional plastid genes for parasitic plant phylogenetics, and has driven the search for alternative phylogenetic and molecular evolutionary markers. Thus, evolutionary studies, such as molecular clock-based age estimates, are not yet available for all parasitic lineages. In the present study, we extracted 14 nuclear single copy genes (nSCG) from Illumina transcriptome data from one of the “strangest plants in the world”, Hydnora visseri (Hydnoraceae). A ∼15,000 character molecular dataset, based on all three genomic compartments, shows the utility of nSCG for reconstructing phylogenetic relationships in parasitic lineages. A relaxed molecular clock approach with the same multi-locus dataset, revealed an ancient age of ∼91 MYA for Hydnoraceae. We then estimated the stem ages of all independently originated parasitic angiosperm lineages using a published dataset, which also revealed a Cretaceous origin for Balanophoraceae, Cynomoriaceae and Apodanthaceae. With the exception of Santalales, older parasite lineages tend to be more specialized with respect to trophic level and have lower species diversity. We thus propose the “temporal specialization hypothesis” (TSH) implementing multiple independent specialization processes over time during parasitic angiosperm evolution.
doi:10.1371/journal.pone.0079204
PMCID: PMC3827129  PMID: 24265760
10.  Characterization of the basal angiosperm Aristolochia fimbriata: a potential experimental system for genetic studies 
BMC Plant Biology  2013;13:13.
Background
Previous studies in basal angiosperms have provided insight into the diversity within the angiosperm lineage and helped to polarize analyses of flowering plant evolution. However, there is still not an experimental system for genetic studies among basal angiosperms to facilitate comparative studies and functional investigation. It would be desirable to identify a basal angiosperm experimental system that possesses many of the features found in existing plant model systems (e.g., Arabidopsis and Oryza).
Results
We have considered all basal angiosperm families for general characteristics important for experimental systems, including availability to the scientific community, growth habit, and membership in a large basal angiosperm group that displays a wide spectrum of phenotypic diversity. Most basal angiosperms are woody or aquatic, thus are not well-suited for large scale cultivation, and were excluded. We further investigated members of Aristolochiaceae for ease of culture, life cycle, genome size, and chromosome number. We demonstrated self-compatibility for Aristolochia elegans and A. fimbriata, and transformation with a GFP reporter construct for Saruma henryi and A. fimbriata. Furthermore, A. fimbriata was easily cultivated with a life cycle of just three months, could be regenerated in a tissue culture system, and had one of the smallest genomes among basal angiosperms. An extensive multi-tissue EST dataset was produced for A. fimbriata that includes over 3.8 million 454 sequence reads.
Conclusions
Aristolochia fimbriata has numerous features that facilitate genetic studies and is suggested as a potential model system for use with a wide variety of technologies. Emerging genetic and genomic tools for A. fimbriata and closely related species can aid the investigation of floral biology, developmental genetics, biochemical pathways important in plant-insect interactions as well as human health, and various other features present in early angiosperms.
doi:10.1186/1471-2229-13-13
PMCID: PMC3621149  PMID: 23347749
11.  Chasing the hare - Evaluating the phylogenetic utility of a nuclear single copy gene region at and below species level within the species rich group Peperomia (Piperaceae) 
Background
The rapidly increasing number of available plant genomes opens up almost unlimited prospects for biology in general and molecular phylogenetics in particular. A recent study took advantage of this data and identified a set of nuclear genes that occur in single copy in multiple sequenced angiosperms. The present study is the first to apply genomic sequence of one of these low copy genes, agt1, as a phylogenetic marker for species-level phylogenetics. Its utility is compared to the performance of several coding and non-coding chloroplast loci that have been suggested as most applicable for this taxonomic level. As a model group, we chose Tildenia, a subgenus of Peperomia (Piperaceae), one of the largest plant genera. Relationships are particularly difficult to resolve within these species rich groups due to low levels of polymorphisms and fast or recent radiation. Therefore, Tildenia is a perfect test case for applying new phylogenetic tools.
Results
We show that the nuclear marker agt1, and in particular the agt1 introns, provide a significantly increased phylogenetic signal compared to chloroplast markers commonly used for low level phylogenetics. 25% of aligned characters from agt1 intron sequence are parsimony informative. In comparison, the introns and spacer of several common chloroplast markers (trnK intron, trnK-psbA spacer, ndhF-rpl32 spacer, rpl32-trnL spacer, psbA-trnH spacer) provide less than 10% parsimony informative characters. The agt1 dataset provides a deeper resolution than the chloroplast markers in Tildenia.
Conclusions
Single (or very low) copy nuclear genes are of immense value in plant phylogenetics. Compared to other nuclear genes that are members of gene families of all sizes, lab effort, such as cloning, can be kept to a minimum. They also provide regions with different phylogenetic content deriving from coding and non-coding parts of different length. Thus, they can be applied to a wide range of taxonomic levels from family down to population level. As more plant genomes are sequenced, we will obtain increasingly precise information about which genes return to single copy most rapidly following gene duplication and may be most useful across a wide range of plant groups.
doi:10.1186/1471-2148-11-357
PMCID: PMC3252395  PMID: 22151585
12.  Smart Skin Patterns Protect Springtails 
PLoS ONE  2011;6(9):e25105.
Springtails, arthropods who live in soil, in decaying material, and on plants, have adapted to demanding conditions by evolving extremely effective and robust anti-adhesive skin patterns. However, details of these unique properties and their structural basis are still unknown. Here we demonstrate that collembolan skin can resist wetting by many organic liquids and at elevated pressures. We show that the combination of bristles and a comb-like hexagonal or rhombic mesh of interconnected nanoscopic granules distinguish the skin of springtails from anti-adhesive plant surfaces. Furthermore, the negative overhang in the profile of the ridges and granules were revealed to be a highly effective, but as yet neglected, design principle of collembolan skin. We suggest an explanation for the non-wetting characteristics of surfaces consisting of such profiles irrespective of the chemical composition. Many valuable opportunities arise from the translation of the described comb-like patterns and overhanging profiles of collembolan skin into man-made surfaces that combine stability against wear and friction with superior non-wetting and anti-adhesive characteristics.
doi:10.1371/journal.pone.0025105
PMCID: PMC3184130  PMID: 21980383
13.  Verhuellia is a segregate lineage in Piperaceae: more evidence from flower, fruit and pollen morphology, anatomy and development 
Annals of Botany  2010;105(5):677-688.
Background and Aims
The perianthless Piperales, i.e. Saururaceae and Piperaceae, have simple reduced flowers strikingly different from the other families of the order (e.g. Aristolochiaceae). Recent molecular phylogenies proved Verhuellia to be the first branch in Piperaceae, making it a promising subject to study the detailed structure and development of the flowers. Based on recently collected material, the first detailed study since 1872 was conducted with respect to morphology, anatomy and development of the inflorescence, pollen ultrastructure and fruit anatomy.
Methods
Original scanning electron microscopy (SEM), transmission electron microscopy (TEM) and light microscopy (LM) observations on Verhuellia lunaria were compared with those of Piperaceae, Saururaceae and fossils.
Key Results
The inflorescence is an indeterminate spike with sessile flowers, each in the axil of a bract, developing in acropetal, helical succession. Flowers consist of two (occasionally three) stamens with basifixed tetrasporangiate anthers and latrorse dehiscence by a longitudinal slit. The gynoecium lacks a style but has 3–4 stigma branches and a single, basal orthotropous and unitegmic ovule. The fruit is a drupe with large multicellular epidermal protuberances. The pollen is very small, inaperturate and areolate, with hemispherical microechinate exine elements.
Conclusions
Despite the superficial similarities with different genera of Piperaceae and Saururaceae, the segregate position of Verhuellia revealed by molecular phylogenetics is supported by morphological, developmental and anatomical data presented here. Unitegmic ovules and inaperturate pollen, which are synapomorphies for the genus Peperomia, are also present in Verhuellia.
doi:10.1093/aob/mcq031
PMCID: PMC2859909  PMID: 20237114
Verhuellia lunaria; Piperales; Peperomia; Appomattoxia ancistrophora; floral development; floral anatomy; fruit morphology; pollen morphology; unitegmic ovule; inaperturate pollen
14.  Superhydrophobicity in perfection: the outstanding properties of the lotus leaf 
Summary
Lotus leaves have become an icon for superhydrophobicity and self-cleaning surfaces, and have led to the concept of the ‘Lotus effect’. Although many other plants have superhydrophobic surfaces with almost similar contact angles, the lotus shows better stability and perfection of its water repellency. Here, we compare the relevant properties such as the micro- and nano-structure, the chemical composition of the waxes and the mechanical properties of lotus with its competitors. It soon becomes obvious that the upper epidermis of the lotus leaf has developed some unrivaled optimizations. The extraordinary shape and the density of the papillae are the basis for the extremely reduced contact area between surface and water drops. The exceptional dense layer of very small epicuticular wax tubules is a result of their unique chemical composition. The mechanical robustness of the papillae and the wax tubules reduce damage and are the basis for the perfection and durability of the water repellency. A reason for the optimization, particularly of the upper side of the lotus leaf, can be deduced from the fact that the stomata are located in the upper epidermis. Here, the impact of rain and contamination is higher than on the lower epidermis. The lotus plant has successfully developed an excellent protection for this delicate epistomatic surface of its leaves.
doi:10.3762/bjnano.2.19
PMCID: PMC3148040  PMID: 21977427
epicuticular wax; leaf surface; Lotus effect; papillae; water repellency

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