Basal Angiosperm Family Research Articles

Chromosome-level genome assembly of watershield (Brasenia schreberi)

Watershield (Brasenia schreberi) is an aquatic plant that belongs to the basal angiosperm family Cabombaceae. This species has been cultivated as an aquatic vegetable for more than 3000 years in East Asia, but the natural populations have greatly declined in recent decades and have become endangered in several countries of East Asia. In this study, by using PacBio long reads, Illumina short reads, and Hi-C sequencing data, we assembled the genome of B. schreberi, which was approximately 1170.4 Mb in size with a contig N50 of 7.1 Mb. Of the total assembled sequences, 93.6% were anchored to 36 pseudochromosomes with a scaffold N50 of 28.9 Mb. A total of 74,699 protein-coding genes were predicted in the B. schreberi genome, and 558 Mb of repetitive elements occupying 47.69% of the genome were identified. BUSCO analysis yielded a completeness score of 95.8%. The assembled high-quality genome of B. schreberi will be a valuable reference for the study of conservation, evolution and molecular breeding in this species.

The complete plastid genome sequence of Chloranthus fortunei (A. Gray) Solms-Laub. in Chloranthaceae

Chloranthus fortunei (A. Gray) Solms-Laub. is a perennial herb in a basal angiosperm family Chloranthaceae. Here, we reported the complete plastid genome of C. fortunei using Illumina short-read data. The total genome size was 157,063 bp in length, containing 79 protein-coding genes, 30 tRNA genes, and four rRNA genes. The gene content and order were consistent with previously reported Chloranthus plastid genomes. The overall GC content of the C. fortunei plastid genome was 39.0%. In the phylogenetic result, genus Chloranthus was monophyletic and divided into two subclades: C. japonicus+C. angustifolius+C. fortunei, and C. henryi+C. spicatus+C. erectus. Our phylogenetic result was consistent with previous phylogenetic studies, and was supported by a previously proposed infrageneric classification of the genus Chloranthus.

Anatomical and histochemical features of Brasenia schreberi (Cabombaceae) shoots

The present research on Brasenia schreberi, a member of the aquatic, basal angiosperm family, Cabombaceae, investigates the anatomy and histochemistry of this critically endangered plant. The shoots of B. schreberi have vertical rhizomes, horizontal rhizomes, and stolons with peduncles and leaves. Most stems typically have polysteles with bicollateral vascular bundles, each with two groups of primary xylem tracheids and primary phloem sieve tube elements, an endodermis with Casparian bands around each vascular bundle, and epidermis with glandular trichomes or “mucilaginous hairs” and discontinuous cuticle. Most stems have a protoxylem lacuna between the two regions of primary xylem and primary phloem in each bicollateral vascular bundle and extensive aerenchyma in ground tissues. Epidermal glandular trichomes are composed of two disk-like stalk cells and enlarged glandular or hair cells with storage space and mucilage, which covers the cells. The structural features of B. schreberi are generally consistent with those of other aquatic basal angiosperms and with its adaptation to an aquatic environment.

The complete chloroplast genome of tulip tree, Liriodendron tulifipera L. (Magnoliaceae): investigation of intra-species chloroplast variations

Liriodendron tulifipera L. belongs to Magnoliaceae which is one of the basal angiosperm families. To understand intra-species variations on chloroplast genome in Liriodendron genus, we presented complete chloroplast genome of L. tulifipera, which is 156,387 bp long and has four subregions: 85,606 bp of large single copy (LSC) and 18,778 bp of small single copy (SSC) regions are separated by 26,002 bp of inverted repeat (IR) regions including 129 genes (84 coding genes, 8 rRNAs, and 37 tRNAs). The overall GC content of the chloroplast genome is 37.0% and those in the LSC, SSC, and IR regions are 34.9%, 30.5%, and 42.8%, respectively. Twelve single nucleotide polymorphisms (SNPs) located in one region and one insertion and deletion are found between two L. tulifipera genomes. INDEL Phylogenetic trees show that two L. tulifipera chloroplasts are clustered together and are sister to Magnolia species.

Hedycaryamacrofossils and associatedPlanarpollenitespollen from the early Miocene of New Zealand

The history of the basal angiosperm family Monimiaceae is based largely on fossil wood and leaf and floral fossils of uncertain affinity. Fossilized leaves with a well-preserved cuticle and Hedycarya-like flowers, including one with in situ pollen tetrads and fruits from an early Miocene lacustrine diatomite deposit in southern New Zealand implies a long record for Hedycarya in New Zealand. The flowers contain pollen grains that are very similar to those of the modern New Zealand species Hedycarya arborea and the Australian H. angustifolia but are considerably smaller. We undertook comparative studies of the leaf, flower and fruit morphology of the newly discovered macrofossils and compared the in situ pollen grains from the flower with dispersed pollen grains from extant species. The leaves are referred to a new, extinct species, Hedycarya pluvisilva Bannister, Conran, Mildenh. & D.E.Lee, (Monimiaceae), and associated with fossilized Hedycarya-like flowers that include in situ pollen and an infructescence of three drupes from the same site. Phylogenetic analysis placed the fossil into Hedycarya, sister to H. angustifolia in a clade with H. arborea and Levieria acuminata. A new name, Planarpollenites fragilis Mildenh., is proposed for dispersed fossil pollen tetrads at the site and those associated with the flower. The fossils are similar to those of modern Australian and New Zealand Hedycarya species, suggesting that the genus and related taxa have been significant components of the rainforests of Australia and the former Zealandian subcontinent for most of the Cenozoic.

Fruits and leaves with cuticle of Laurelia otagoensis sp. nov. (Atherospermataceae) from the early Miocene of Otago (New Zealand)

Conran, J.G., Bannister, J.M. & Lee, D.E., 2013. Fruits and leaves with cuticle of Laurelia otagoensis sp. nov. (Atherospermataceae) from the early Miocene of Otago (New Zealand). Alcheringa 37, 496–509. ISSN 0311-5518.Laurelia otagoensis sp. nov. Conran, Bannister & D.E. Lee (Laurales: Atherospermataceae) is described from the earliest Miocene Foulden Maar diatomite deposit, Otago, New Zealand. The new species is represented by mummified fossil leaves with well-preserved cuticle and associated clusters of achenes bearing persistent, long plumose styles. This basal angiosperm family is of significance because of its classic southern disjunctions and ecological importance in extant Gondwana-type rainforests, but has a very sparse fossil record. The present study describes one of very few convincing leaf fossils for Atherospermataceae and the only definitive fossil fruits. The presence of fossil Laurelia in Oligo–Miocene New Zealand combined with fossil leaf impressions from the late Eocene, Miocene dispersed cuticle and pollen from the Oligocene to Holocene shows that the family has had a long history in Cenozoic New Zealand. These new fossils also support palaeoclimatic data suggesting warmer conditions in the earliest Miocene of New Zealand.John G. Conran [john.conran@adelaide.edu.au], Australian Centre for Evolutionary Biology & Biodiversity and Sprigg Geobiology Centre, School of Earth and Environmental Sciences, Benham Bldg DX 650 312, The University of Adelaide, SA 5005 Australia; Jennifer M. Bannister [jennifer.bannister@xtra.co.nz], Department of Botany, University of Otago, PO Box 56, Dunedin, New Zealand; Daphne E. Lee [daphne.lee@otago.ac.nz], Department of Geology, University of Otago, PO Box 56, Dunedin, New Zealand. Received 17.12.2012; revised 9.4.2013; accepted 15.4.2013.

Fruit structure in Magnoliaceae s.l. and Archaeanthus and their relationships

The family Magnoliaceae s.l. is a basal angiosperm family with two subfamilies-Magnolioideae and Liriodendroideae, which differ by the types and structure of their fruits and seeds. The late Albian genus Archaeanthus shares many features of its reproductive organs with Magnoliaceae s.l., but its pericarp anatomy was never studied in detail. A broad-scale carpological investigation of Archaeanthus and Magnoliaceae s.l. was undertaken to reveal the nature of the similarities in fruit structure and to reconstruct Archaeanthus pericarp anatomy. These data are important to determine the early stages of fruit morphogenesis and thus to clarify relationships of Archaeanthus to the taxa of Magnoliaceae s.l. The pericarp anatomy was studied with light microscopy, SEM, and polarizing microscopy. The dehiscent, polyspermous follicles shed from the receptacle of Archaeanthus share similarities with dehiscent follicles of Magnoliaceae s.s. and shedding nutlets of Liriodendron. The seeds of Archaeanthus are dorsiventrally flattened, ovoid, and encircled with a single circular wing. The pericarps of all the taxa studied are differentiated into exocarp (epidermis), multilayered mesocarp, and endocarp (fiber-like sclereids). The mesocarp consists of parenchyma with scattered secretory cells and sclereid clusters (Magnoliaceae s.s., Archaeanthus) or composed by sclerenchyma (Liriodendron). The specializations of dehiscent multifollicles of unknown Cretaceous ancestors for different modes of seed and fruitlet dispersal formed the basis for the differentiation of two evolutionary lines with their divergence occurring more than 100 million years ago: Magnoliaceae s.s. and the Archaeanthus-Liriodendroidea-Liriodendron line (Liriodendraceae s.l.) within the order Magnoliales.

Characterization of the basal angiosperm Aristolochia fimbriata: a potential experimental system for genetic studies.

BackgroundPrevious 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).ResultsWe 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.ConclusionsAristolochia 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.

Regeneration and plantlet development from somatic tissues of Aristolochia fimbriata

Aristolochia fimbriata is a small herbaceous perennial in the basal angiosperm family Aristolochiaceae. The family contains diverse floral forms ranging from radial to monosymmetric flowers with a wide variety of insect pollinators. Additionally, Aristolochia species contain secondary metabolites that are important natural toxins and traditional medicines, and are critical to the reproduction of swallowtail butterflies. These characteristics, in combination with the small genome size and short life cycle of A. fimbriata, have prompted further development of this species as a model system to study the evolution of basal angiosperms. As a prerequisite for developing a genetic transformation procedure for Aristolochia, we developed protocols for in vitro plant multiplication, shoot organogenesis, rooting, and acclimation of tissue culture-derived plants. Two varieties of Aristolochia were multiplied in vitro and rooted with 100% efficiency. Shoot regeneration was achieved within 1 month of culture initiation from whole leaf, internodal stem, and petiole explants. The highest regeneration success (97%) was recorded for stem explants. Regenerated and rooted shoots were acclimated to greenhouse conditions and developed flowers within 4 weeks of transplanting.

The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): Implications for pollen evolution

Most angiosperms release bicellular pollen. However, in about one-third of extant angiosperms, the second pollen mitosis occurs before anthesis such that pollen is tricellular upon release. The shift from bicellular to tricellular development has occurred several times independently, but its causes are largely unknown. In this work, we observed the coexistence of both kinds of pollen at anther dehiscence in Annona cherimola, a species that belongs to the basal angiosperm family Annonaceae. Examination of pollen cell number during anther development showed that this coexistence was due to a late mitosis starting shortly before pollen shedding. Both types of pollen germinated equally well over the course of development. Because variable proportions of bicellular and tricellular pollen were observed at different sampling times, we tested the role of temperature by performing field and growth chamber experiments, which showed that higher temperatures near anthesis advanced the time of pollen mitosis II. The results show that selection could favor the production of tricellular pollen under certain environmental circumstances that prime rapid pollen germination and provide evidence of a system in which developmental variation persists, but that can be modified by external factors such as temperature.

Perfume‐collecting male euglossine bees as pollinators of a basal angiosperm: the case of Unonopsis stipitata (Annonaceae)

Pollination of Unonopsis stipitata (Annonaceae) by males of two perfume-collecting bees, Euglossa imperialis and Eulaema bombiformis (Euglossini) is described. This is the first detailed account of this pollination mode in a member of a basal angiosperm family. Pollinator behaviour, identification of the odour bouquet and electrophysiological reaction of one of the two pollinators to the odour bouquet were determined. The collected odour is produced by 'osmophores' located adaxially on the petals. Starch and polysaccharides accumulated in petals are metabolized during odour emission. Mainly monoterpenes were detected in the scent samples, among them trans-carvone oxide. This molecule is thought by several authors to be the key attractant for male Eulaema bees and may be pivotal for convergent evolution of the perfume-collecting syndrome among dicotyledonous and monocotyledonous plants. It is speculated that Unonopsis, which on the basis of molecular age dating is considered a relatively recent genus of the Annonaceae (being 15-30 million years old), has diversified in relation to male euglossine bee pollinators.

Early steps of angiosperm–pollinator coevolution

The hypothesis that early flowering plants were insect-pollinated could be tested by an examination of the pollination biology of basal angiosperms and the pollination modes of fossil angiosperms. We provide data to show that early fossil angiosperms were insect-pollinated. Eighty-six percent of 29 extant basal angiosperm families have species that are zoophilous (of which 34% are specialized) and 17% of the families have species that are wind-pollinated, whereas basal eudicot families and basal monocot families more commonly have wind and specialized pollination modes (up to 78%). Character reconstruction based on recent molecular trees of angiosperms suggests that the most parsimonious result is that zoophily is the ancestral state. Combining pollen ornamentation, size, and aperture characteristics and the abundance of single-species pollen clumps of Cenomanian angiosperm-dispersed pollen species from the Dakota Formation demonstrates a dominance of zoophilous pollination (76% versus 24% wind pollination). The zoophilous pollen species have adaptations for pollination by generalist insects (39%), specialized pollen-collecting insects (27%), and other specialized pollinators (10%). These data quantify the presences of more specialized pollination modes during the mid-Cretaceous angiosperm diversification.

Papilio aegeus Donovan (Lepidoptera: Papilionidae) host plant range evaluated experimentally on ancient angiosperms

Abstract Chemical similarities among ancient Angiosperms presumably played a role in the ecological and evolutionary diversification of the swallowtail butterflies (Papilionidae). The abilities of neonate larvae of the Citrus swallowtail, Papilio (=Princeps) aegeus (from Queensland, Australia), to eat, survive and grow on leaves (a choice of young and old) of 34 plant species from families of ancient Angiosperms; 8 Rutaceae, 3 Magnoliaceae, 13 Lauraceae, 3 Monimiaceae, 1 Aristolochiaceae, 2 Apiaceae, 1 Sapotaceae, 1 Winteraceae and 2 Annonaceae were tested. It was apparent that there is genetic variation in populations of Rutaceae‐specialised Australian P. aegeus for acceptance, consumption and larval growth, reflecting differential suitability of some native Australian Lauraceae species as food plants (as well as certain Winteraceae, Monimiaceae and non‐Australian Magnoliaceae, Lauraceae and Annonaceae). No consumption or survival of P. aegeus was seen on Aristolochia elegans (Aristolochiaceae) or Pouteria australis (Sapotaceae) despite literature records alluding to this possibility. The Rutaceae specialist P. aegeus appears to have the fundamental detoxification capabilities for processing many existing species of the basal Angiosperm families, without having direct ancestors that historically had fed on them.

First nuclear DNA C-values for 18 eudicot families.

A key target set at the second Plant Genome Size Workshop, held at the Royal Botanic Gardens, Kew in 2003, was to produce first DNA C-value data for an additional 1 % of angiosperm species, and, within this, to achieve 75 % familial coverage overall (up from approx. 50 %) by 2009. The present study targeted eudicot families for which representation in 2003 (42.5 %) was much lower than monocot (72.8 %) and basal angiosperm (69.0 %) families. Flow cytometry or Feulgen microdensitometry were used to estimate nuclear DNA C-values, and chromosome counts were obtained where possible. First nuclear DNA C-values are reported for 20 angiosperm families, including 18 eudicots. This substantially increases familial representation to 55.2 % for angiosperms and 48.5 % for eudicots. The importance of targeting specific plant families to improve familial nuclear DNA C-value representation is reconfirmed. International collaboration will be increasingly essential to locate and obtain material of unsampled plant families, if the target set by the second Plant Genome Size Workshop is to be met.

Ultrastructure and diversity of recent and fossil zona-aperturate pollen grains

A survey of recent and fossil zona-aperturate pollen grains within the angiosperms was undertaken. Zona-aperturate pollen (with complete ring-like apertures) has been evolved independently in several genera of basal angiosperm families (Nymphaeaceae, Eupomatiaceae, Annonaceae, Monimiaceae, Atherospermataceae) and monocots (Araceae, Iridaceae, Laxmanniaceae, Arecaceae, and Rapateaceae). The special case of the eudicot Limnanthes (Limnanthaceae) is discussed. New examples of recent and fossil fully zonate pollen are presented; a noteworthy new example are Scrophulariaceae, with Pedicularis; our fossil examples show affinities either to Nymphaeaceae, or Araceae, or Iridaceae, or cannot be related to an extant taxon. The zona-aperturate pollen grains differ in ornamentation and stratification mostly in the respect of the aperture areas, but sometimes also outside the aperture. The question of polarity is settled only for some taxa because of the frequent lack of tetrad observations. A ring-like aperture may divide the pollen grains in symmetric halves, or if running asymmetrically, divides the pollen grain in two more or less unequal halves; the presence of clearly unequal halves gives a strong argument to assume an equatorial ring in such cases where tetrad configurations were not available. The zona-aperturate condition may be a functional benefit in wet environments: while in dry pollen the apertural ring is completely closed, in wet or very moist realm it expands greatly, and the pollen tube can be formed quickly and everywhere in this area.

Phylogeny and divergence of basal angiosperms inferred from APETALA3- and PISTILLATA-like MADS-box genes.

The B-class MADS-box genes composed of APETALA3 ( AP3) and PISTILLATA ( PI) lineages play an important role in petal and stamen identity in previously studied flowering plants. We investigated the diversification of the AP3-like and PI-like MADS-box genes of eight species in five basal angiosperm families: Amborella trichopoda (Amborellaceae); Brasenia schreberi and Cabomba caroliniana (Cabombaceae); Euryale ferox, Nuphar japonicum, and Nymphaea tetragona (Nymphaeaceae); Illicium anisatum (Illiciaceae); and Kadsura japonica (Schisandraceae). Sequence analysis showed that a four amino acid deletion in the K domain, which was found in all previously reported angiosperm PI genes, exists in a PI homologue of Schisandraceae, but not in six PI homologues of the Amborellaceae, Cabombaceae, and Nymphaeaceae, suggesting that the Amborellaceae, Cabombaceae, and Nymphaeaceae are basalmost lineages in angiosperms. The results of molecular phylogenetic analyses were not inconsistent with this hypothesis. The AP3 and PI homologues from Amborella share a sequence of five amino acids in the 5' region of exon 7. Using the linearized tree and likelihood methods, the divergence time between the AP3 and PI lineages was estimated as somewhere between immediately after to several tens of millions of years after the split between angiosperms and extant gymnosperms. Estimates of the age of the most recent common ancestor of all extant angiosperms range from approximately 140-210 Ma, depending on the trees used and assumptions made.

Floral Development in the Nymphaeales

Numerous phylogenetic analyses and recent paleobotanical findings continue to support the inclusion of Nymphaeales as basal or near‐basal extant angiosperms. The distinctive differences in floral morphology and habit between non‐Nymphaealian taxa of the ANITA grade compared with water lilies, nevertheless, remain perplexing. In this investigation, scanning electron microscope observations on Brasenia (Cabombaceae), Nuphar, Nymphaea, Ondinea, Victoria, and Euryale (Nymphaeaceae) are added to the observations of earlier investigations to enhance our understanding of early floral evolution and shifts in floral ontogeny and to contribute new data for improved cladistic analyses. The enlargement of flowers and amplification of floral parts distinctive in Nymphaeaceae is based on continuing surface area enlargement of the floral apex, allowing numerous organs to be produced acropetally in distinctive parastichies, compared with the ring meristem found in some primitive eudicots (Nelumbonaceae, Papaveraceae) that increase floral organ number but in dense pulses or clusters without clear order. The smaller flowers of the Cabombaceae and their lower number of floral organs are now regarded as more typical of the ancestral angiosperm flower. One may conclude that changes in the size of the floral apex and its geometric conformation alter flower size, number of parts, and phyllotaxy. The ebracteate condition and herbaceous, aquatic habit of Nymphaeales when compared with Archaefructus, a recently discovered herbaceous aquatic angiosperm from the Upper Jurassic/Lower Cretaceous that is proposed as a new basal angiosperm family, continue to question the relationship of early angiosperms to the aquatic habitat. Is the ebracteate state significant, and how did the shift to aquatic habitats impact floral form of early angiosperms?

DNA C-values in seven families fill phylogenetic gaps in the basal angiosperms

The evolutionary significance of the c. 1000-fold range of DNA C-values in angiosperms (1C = c. 0.1–127.4 pg) has often attracted interest. A recent analysis, which superimposed available C-value data onto the angiosperm phylogeny, that placed Ceratophyllaceae as the most basal angiosperm family led to the conclusion that ancestral angiosperms were characterized by small genomes (defined as 1C £ 3.5 pg). However, with the recent increase in DNA sequence data and large-scale phylogenetic analyses, strong support is now provided for Amborellaceae and/or Nymphaeaceae as the most basal angiosperm families, followed by Austrobaileyales (comprising Schisandraceae, Trimeniaceae and Austrobaileyaceae). Together these five families comprise the ANITA grade. The remaining basal angiosperm families (Ceratophyllaceae, Chloranthaceae and magnoliids), together with monocotyledons and eudicotyledons, form a strongly supported clade. A survey showed that C-value data were scarce in the basal angiosperm families, especially the ANITA grade. The present paper addresses these phylogenetic gaps by providing C-value estimates for each family in ANITA, together with C-values for species in Chloranthaceae, Ceratophyllaceae and a previously unrepresented family in the magnoliids, the Winteraceae. © The Linnean Society of London, Botanical Journal of the Linnean Society, 2002, 140, 175–179.

Archaefructaceae, a new basal angiosperm family.

Archaefructaceae is proposed as a new basal angiosperm family of herbaceous aquatic plants. This family consists of the fossils Archaefructus liaoningensis and A. sinensis sp. nov. Complete plants from roots to fertile shoots are known. Their age is a minimum of 124.6 million years from the Yixian Formation, Liaoning, China. They are a sister clade to all angiosperms when their characters are included in a combined three-gene molecular and morphological analysis. Their reproductive axes lack petals and sepals and bear stamens in pairs below conduplicate carpels.

Evolutionary trends in Winteraceae pollen

The Winteraceae, being considered as one of the most basal angiosperm families, has been extensively studied palynologically. The present study reviews the characters dispersal unit (monad versus tetrad) and size of the lumina in the tectum in the light of recent molecular research. Monads and small-meshed reticula appear to be derived from large-meshed tetrads. The fossil record supports the apomorphic state of a small-meshed tectum. In contrast to earlier reports, genuine monads are unknown as fossils. The fossil monads recorded so far are considered to be detached from permanent tetrad configurations.