Sarah T. Wagner

Detecting and Characterizing the Highly Divergent Plastid Genome of the Nonphotosynthetic Parasitic Plant Hydnora visseri (Hydnoraceae)

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.

Escaping the lianoid habit: evolution of shrub-like growth forms in Aristolochia subgenus Isotrema (Aristolochiaceae)

UNLABELLED PREMISE OF THE STUDY A large range of growth forms is a notable aspect of angiosperm diversity and arguably a key element of their success. However, few studies within a phylogenetic context have explored how anatomical, developmental, and biomechanical traits are linked with growth form evolution. Aristolochia (∼500 species) consists predominantly of climbers, but a handful of shrub-like species are known from Aristolochia subgenus Isotrema (hereafter, shortened to Isotrema). We test hypotheses proposing that the establishment of functional traits linked to lianescence might limit the ability to evolve structurally diverse growth forms, particularly self-supporting forms. • METHODS We focus on the origin of the shrub habit in Isotrema, from which we sampled representatives from climbing to self-supporting forms. Morphological, anatomical, and biomechanical characters are optimized on a chloroplast- and nuclear-derived phylogeny. • KEY RESULTS Character-state reconstructions revealed that the climbing habit is plesiomorphic in Isotrema and shrub-like forms are derived from climbers. However, shrubs do not constitute a monophyletic group. Both shrubs and climbers show large multiseriate rays, but differ in terms of vessel size and proportion of fibers and soft tissues. • CONCLUSION We suggest that while shrub-like species might have partly escaped from the constraints of life as lianas; their height size and stability are not typical of self-supporting shrubs and trees. Shrubs retained lianoid stem characters that are known to promote flexibility such as ray parenchyma. The transitions to a shrub-like form likely involved relatively simple, developmental changes that may be attributed to heterochronic processes.

Growth Form Evolution in Piperales and Its Relevance for Understanding Angiosperm Diversification: An Integrative Approach Combining Plant Architecture, Anatomy, and Biomechanics

A striking feature of early angiosperm lineages is the variety of life forms and growth forms, which ranges from herbs, aquatic herbs, climbers, and epiphytes to woody shrubs and trees. This morphological and anatomical diversity is arguably one of the factors explaining how angiosperms dominate many ecosystems worldwide. However, just how such a wide spectrum of growth forms has evolved in angiosperms remains unclear. In this review, we investigate patterns of growth form diversification in Piperales, an early-diverging lineage (with stem age estimated at 201–128 Myr ago) and the most morphologically diverse clade among magnoliids. We outline patterns of growth form diversity and architecture as well as the biomechanical significance of developmental characters, such the organization, loss, and gain of woodiness. Asaroideae and Saururaceae are terrestrial as well as semiaquatic to aquatic herbaceous perennials bearing rhizomes. The Aristolochioideae and Piperaceae show higher levels of growth form diversity and biomechanical organization, with complex patterns of increasing or decreasing woodiness and architectural organization. The climbing habit has probably evolved independently in the Aristolochiaceae and Piperaceae, while mechanically unstable shrubs and, less frequently, treelets have evolved several times within these two most species-rich clades. A key developmental character underlying diversity in most Piperales—with the exception of the herbaceous Saruma (Asaroideae)—is the conserved development of the wood cylinder, in which fusiform initials are limited to fascicular cambial initials. The resulting large fraction of raylike tissue in the stem—a highly characteristic feature of woody species in the Piperales—potentially introduced mechanical constraints on the diversification of self-supporting architectures. This was possibly circumvented by the architectural development of repeated, large-diameter meristems in some shrublike habits via sympodial growth. Patterns of growth form evolution within Piperales potentially mirror some of the overall trends observed among early-diverging angiosperms as a whole as well as angiosperms in general. These include profound changes in life form and growth form linked to large-scale transitions in woodiness, diversity of mechanical organization, and shifts in architectural development.

Biological Archetypes for Self-Healing Materials

Damage and fatigue are ever-present facts of life. Given enough time, even the most robust material, whether man-made or natural, succumbs to the deleterious effects of cracks, fissures, and defects during normal use. Traditionally, materials engineers have approached this problem by creating damage-tolerant structures, intensive quality control before use, vigilant inspection during use, and designing materials to function well below their theoretical limit. Living organisms, on the other hand, routinely produce materials that function close to their theoretical limit as a result of their remarkable ability to self-heal a range of non-catastrophic damage events. For this reason, many researchers in the last 15 years have turned to nature for inspiration for the design and development of self-healing composites and polymeric materials. However, these efforts have so far only scratched the surface of the richness of natural self-repair processes. In the present review, we provide an overview of some paradigmatic and well-studied examples of self-repair in living systems. The core of this overview takes the form of a number of case studies that provide a detailed description of the structure–function relationships defining the healing mechanism. Case studies include a number of examples dependent on cellular action in both animals (e.g., limb regeneration, antler growth, bone healing, and wound healing) and plants (e.g., latex-based healing, plant grafting, and wound closure in woody vines and succulent plants). Additionally, we examine several examples of acellular self-repair in biopolymeric materials (e.g., mussel byssus, caddisfly silks, and whelk egg capsules) that are already inspiring the development of a number of self-healing polymers.

Major trends in stem anatomy and growth forms in the perianth-bearing Piperales, with special focus on Aristolochia

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.

Biomechanics and functional morphology of a climbing monocot

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.

Stem anatomy and the evolution of woodiness in Piperales

Premise of research. Piperales displays a wide diversity of growth forms that appears to be linked with differences in cambial activity and subsequent derived wood production. To date, no overall synthesis of the evolution of woodiness in Piperales has been done and few studies have proposed an ancestral habit (woody/herbaceous). We provide anatomical data of all lineages within Piperales and reconstruct ancestral character states, focusing on the origin of woodiness within the order and on the ecological significance of key anatomical features. Methodology. Stem anatomical observations with special emphasis on wood anatomical features were performed on 28 species of the Piperales; by combining previously published studies with original data, we conducted phylogenetic reconstructions of cambial activity and vessel element perforation plates to assess the origin of woodiness and vessel evolution in Piperales. Pivotal results. Different patterns of cambial activity are observed in Piperales, from active secondary growth in both intra- and interfascicular areas in Aristolochia, Thottea (Aristolochiaceae), Saruma (Asaraceae), Manekia, and Piper (Piperaceae) to cambial activity mainly restricted to fascicular areas in Saururaceae and a complete lack of secondary growth in Verhuellia. Vessels in Piperaceae, Aristolochiaceae, and Asaraceae present simple perforation plates, while those of Saururaceae are mostly scalariform. A stem endodermis bearing a Casparian band—an atypical feature in aerial stems—is reported for all genera within the Piperaceae and for Saururus and Houttuynia in the Saururaceae. Conclusions. The common ancestor of the order likely had an active cambium and woody habit, including vessel elements with simple perforation plates. All woody species share several wood features, including wide and tall rays, suggesting a single origin of wood in the order. The high diversity of growth forms observed in Piperales is linked to frequent shifts in cambial activity and changes in habit-related features within the different lineages.

Four New Species of Aristolochia Subsection Pentandrae from Western Mexico

Abstract Four new Aristolochia species from the Mexican states of Colima, Jalisco, and Nayarit are described and illustrated. The four new species, Aristolochia nahua, A. pacifica, A. savannoidea, and A. tuitensis, belong to Aristolochia subsection Pentandrae, and are morphologically similar to A. buntingii and A. tresmariae. All of these species grow in the biogeographic province of the Mexican Pacific Coast, an important area of diversity and species richness of Aristolochia subsection Pentandrae.