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1.  Patterns of morphological integration in marine modular organisms: supra-module organization in branching octocoral colonies. 
Despite the relative simplicity of their modular growth, marine invertebrates such as arborescent gorgonian octocorals (Octocorallia: Cnidaria) generate complex colonial forms. Colony form in these taxa is a consequence of modular (polyp) replication, and if there is a tight integration among modular and supramodular traits (e.g. polyp aperture, inter-polyp spacing, branch thickness, internode and branch length), then changes at the module level may lead to changes in colony architecture. Alternatively, different groups of traits may evolve semi-independently (or conditionally independent). To examine the patterns of integration among morphological traits in Caribbean octocorals, we compared five morphological traits across 21 species, correcting for the effects of phylogenetic relationships among the taxa. Graphical modelling and phylogenetic independence contrasts among the five morphological characters indicate two groups of integrated traits based on whether they were polyp- or colony-level traits. Although all characters exhibited bivariate associations, multivariate analyses (partial correlation coefficients) showed the strongest integration among the colony-level characters (internode distance and branch length). It is a quantitative demonstration that branching characters within the octocorals studied are independent of characters of the polyps. Despite the universally recognized modularity of octocorals at the level of polyps, branching during colony development may represent an emergent level of integration and modularity.
doi:10.1098/rspb.2003.2471
PMCID: PMC1691470  PMID: 14561292
2.  Evolution of Growth Habit, Inflorescence Architecture, Flower Size, and Fruit Type in Rubiaceae: Its Ecological and Evolutionary Implications 
PLoS ONE  2012;7(7):e40851.
During angiosperm evolution, innovations in vegetative and reproductive organs have resulted in tremendous morphological diversity, which has played a crucial role in the ecological success of flowering plants. Morindeae (Rubiaceae) display considerable diversity in growth form, inflorescence architecture, flower size, and fruit type. Lianescent habit, head inflorescence, small flower, and multiple fruit are the predominant states, but arborescent habit, non-headed inflorescence, large flower, and simple fruit states occur in various genera. This makes Morindeae an ideal model for exploring the evolutionary appearances and transitions between the states of these characters. We reconstructed ancestral states for these four traits using a Bayesian approach and combined nuclear/chloroplast data for 61 Morindeae species. The aim was to test three hypotheses: 1) self-supporting habit is generally ancestral in clades comprising both lianescent and arborescent species; 2) changes from lianescent to arborescent habit are uncommon due to “a high degree of specialization and developmental burden”; 3) head inflorescences and multiple fruits in Morindeae evolved from non-headed inflorescences and simple fruits, respectively. Lianescent habit, head inflorescence, large flower, and multiple fruit are inferred for Morindeae, making arborescent habit, non-headed inflorescence, small flower, and simple fruit derived within the tribe. The rate of change from lianescent to arborescent habit is much higher than the reverse change. Therefore, evolutionary changes between lianescent and arborescent forms can be reversible, and their frequency and trends vary between groups. Moreover, these changes are partly attributed to a scarcity of host trees for climbing plants in more open habitats. Changes from large to small flowers might have been driven by shifts to pollinators with progressively shorter proboscis, which are associated with shifts in breeding systems towards dioecy. A single origin of dioecy from hermaphroditism is supported. Finally, we report evolutionary changes from headed to non-headed inflorescences and multiple to simple fruits.
doi:10.1371/journal.pone.0040851
PMCID: PMC3397938  PMID: 22815842
3.  How early ferns became trees. 
A new anatomically preserved fern, discovered from the basalmost Carboniferous of Australia, shows a unique combination of very primitive anatomical characters (solid centrarch cauline protostele) with the elaboration of an original model of the arborescent habit. This plant possessed a false trunk composed of a repetitive branching system of very small stems, which established it as the oldest tree-fern known to date. The potential of this primitive zygopterid fern to produce such an unusual growth form-without real equivalent among living plants-is related to the possession of two kinds of roots that have complementary functional roles: (i) large roots produced by stems with immediate positive geotropism, strongly adapted to mechanical support and water uptake from the soil; and (ii) small roots borne either on large roots or on petiole bases for absorbing humidity inside the false trunk.
doi:10.1098/rspb.2001.1785
PMCID: PMC1088834  PMID: 11564354
4.  The function of the aerenchyma in arborescent lycopsids: evidence of an unfamiliar metabolic strategy 
Most species of the modern family Isoëtaceae (Quillworts) some other modern hydrophytes, use a metabolic pathway for carbon fixation that involves uptake of sedimentary carbon and enrichment of CO2 in internal gas spaces as a carbon-concentrating mechanism. This metabolism, which is related to ‘aquatic CAM’, is characterized by morphological, physiological and biochemical adaptations for decreasing photorespirative loss, aerating roots and maintaining high growth rates in anoxic, oligotrophic, stressed environments. Some of the closest relatives of the Isoëtaceae were the ‘arborescent lycopsids’, which were among the dominant taxa in the coal swamps found in lowland ecosystems during the Carboniferous and Permian periods (approx. 300 Ma). Morphological, ecological and geochemical evidence supports the hypothesis that the arborescent lycopsids had an unusual metabolism similar to that of modern Isoëtaceae and processed a biogeochemically significant proportion of organically fixed carbon over a period of about 100 million years in the late Palaeozoic. The temporal coincidence between the dominance of plants with this metabolism and an anomalous global atmosphere (high O2; low CO2) supports the idea that biosphere feedbacks are important in regulating global climatic homeostasis. The potential influence of this metabolism on the global carbon cycle and its specific adaptive function suggest that it should perhaps be considered a fourth major photosynthetic pathway.
doi:10.1098/rspb.2010.0224
PMCID: PMC2894907  PMID: 20356894
aerenchyma; aquatic CAM; arborescent lycopsids; metabolic pathways; parichnos
5.  Shape Self-Regulation in Early Lung Morphogenesis 
PLoS ONE  2012;7(5):e36925.
The arborescent architecture of mammalian conductive airways results from the repeated branching of lung endoderm into surrounding mesoderm. Subsequent lung’s striking geometrical features have long raised the question of developmental mechanisms involved in morphogenesis. Many molecular actors have been identified, and several studies demonstrated the central role of Fgf10 and Shh in growth and branching. However, the actual branching mechanism and the way branching events are organized at the organ scale to achieve a self-avoiding tree remain to be understood through a model compatible with evidenced signaling. In this paper we show that the mere diffusion of FGF10 from distal mesenchyme involves differential epithelial proliferation that spontaneously leads to branching. Modeling FGF10 diffusion from sub-mesothelial mesenchyme where Fgf10 is known to be expressed and computing epithelial and mesenchymal growth in a coupled manner, we found that the resulting laplacian dynamics precisely accounts for the patterning of FGF10-induced genes, and that it spontaneously involves differential proliferation leading to a self-avoiding and space-filling tree, through mechanisms that we detail. The tree’s fine morphological features depend on the epithelial growth response to FGF10, underlain by the lung’s complex regulatory network. Notably, our results suggest that no branching information has to be encoded and that no master routine is required to organize branching events at the organ scale. Despite its simplicity, this model identifies key mechanisms of lung development, from branching to organ-scale organization, and could prove relevant to the development of other branched organs relying on similar pathways.
doi:10.1371/journal.pone.0036925
PMCID: PMC3353953  PMID: 22615846
6.  A study on the extracts of Cuscuta reflexa Roxb. in treatment of cyclophosphamide induced alopecia 
Background
Alopecia is a dermatological disorder with psychosocial implications on patients with hair loss. Hair loss is one of the most feared side effects of chemotherapy. Plants have been widely used for hair growth promotion since ancient times in Ayurveda, Chinese and Unani systems of medicine. The effect of extracts of Cuscuta reflexa Roxb. in testosterone induced alopecia was reported.
Objective
In the present study, the efficacies of the extracts of Cuscuta reflexa in promoting hair growth in cyclophosphamide-induced hair loss have been determined.
Materials and methods
The study was performed by treated with petroleum ether and ethanolic extract of Cuscuta reflexa at the dose 250 mg/kg in male swiss albino rats. Cyclophosphamide (125 mg/kg) was used to induce alopecia.
Results
Groups treated with extracts of plant showed hair regrowth. Histopathology and gross morphologic observations for hair regrowth at shaved sites revealed active follicular proliferation.
Conclusions
It concluded that extracts of Cuscuta reflexa shown to be capable of promoting follicular proliferation or preventing hair loss in cyclophosphamide-induced hair fall.
doi:10.1186/2008-2231-22-7
PMCID: PMC3922840  PMID: 24393240
Cuscuta reflexa; Chemotherapy; Alopecia; Cyclophosphamide; Hair loss
7.  Diel time-courses of leaf growth in monocot and dicot species: endogenous rhythms and temperature effects 
Journal of Experimental Botany  2010;61(6):1751-1759.
Diel (24 h) leaf growth patterns were differently affected by temperature variations and the circadian clock in several plant species. In the monocotyledon Zea mays, leaf elongation rate closely followed changes in temperature. In the dicotyledons Nicotiana tabacum, Ricinus communis, and Flaveria bidentis, the effect of temperature regimes was less obvious and leaf growth exhibited a clear circadian oscillation.These differences were related neither to primary metabolism nor to altered carbohydrate availability for growth. The effect of endogenous rhythms on leaf growth was analysed under continuous light in Arabidopsis thaliana, Ricinus communis, Zea mays, and Oryza sativa. No rythmic growth was observed under continuous light in the two monocotyledons, while growth rhythmicity persisted in the two dicotyledons. Based on model simulations it is concluded that diel leaf growth patterns in mono- and dicotyledons result from the additive effects of both circadian-clock-controlled processes and responses to environmental changes such as temperature and evaporative demand. Apparently very distinct diel leaf growth behaviour of monocotyledons and dicotyledons can thus be explained by the different degrees to which diel temperature variations affect leaf growth in the two groups of species which, in turn, depends on the extent of the leaf growth control by internal clocks.
doi:10.1093/jxb/erq049
PMCID: PMC2852670  PMID: 20299442
Circadian clock; elongation; expansion; image analysis; photosynthesis; starch; sucrose
8.  Plexin A3 and Turnout Regulate Motor Axonal Branch Morphogenesis in Zebrafish 
PLoS ONE  2013;8(1):e54071.
During embryogenesis motor axons navigate to their target muscles, where individual motor axons develop complex branch morphologies. The mechanisms that control axonal branching morphogenesis have been studied intensively, yet it still remains unclear when branches begin to form or how branch locations are determined. Live cell imaging of individual zebrafish motor axons reveals that the first axonal branches are generated at the ventral extent of the myotome via bifurcation of the growth cone. Subsequent branches are generated by collateral branching restricted to their synaptic target field along the distal portion of the axon. This precisely timed and spatially restricted branching process is disrupted in turnout mutants we identified in a forward genetic screen. Molecular genetic mapping positioned the turnout mutation within a 300 kb region encompassing eight annotated genes, however sequence analysis of all eight open reading frames failed to unambiguously identify the turnout mutation. Chimeric analysis and single cell labeling reveal that turnout function is required cell non-autonomously for intraspinal motor axon guidance and peripheral branch formation. turnout mutant motor axons form the first branch on time via growth cone bifurcation, but unlike wild-type they form collateral branches precociously, when the growth cone is still navigating towards the ventral myotome. These precocious collateral branches emerge along the proximal region of the axon shaft typically devoid of branches, and they develop into stable, permanent branches. Furthermore, we find that null mutants of the guidance receptor plexin A3 display identical motor axon branching defects, and time lapse analysis reveals that precocious branch formation in turnout and plexin A3 mutants is due to increased stability of otherwise short-lived axonal protrusions. Thus, plexin A3 dependent intrinsic and turnout dependent extrinsic mechanisms suppress collateral branch morphogenesis by destabilizing membrane protrusions before the growth cone completes navigation into the synaptic target field.
doi:10.1371/journal.pone.0054071
PMCID: PMC3549987  PMID: 23349787
9.  Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii 
BMC Plant Biology  2007;7:45.
Background
The holoparasitic plant genus Cuscuta comprises species with photosynthetic capacity and functional chloroplasts as well as achlorophyllous and intermediate forms with restricted photosynthetic activity and degenerated chloroplasts. Previous data indicated significant differences with respect to the plastid genome coding capacity in different Cuscuta species that could correlate with their photosynthetic activity. In order to shed light on the molecular changes accompanying the parasitic lifestyle, we sequenced the plastid chromosomes of the two species Cuscuta reflexa and Cuscuta gronovii. Both species are capable of performing photosynthesis, albeit with varying efficiencies. Together with the plastid genome of Epifagus virginiana, an achlorophyllous parasitic plant whose plastid genome has been sequenced, these species represent a series of progression towards total dependency on the host plant, ranging from reduced levels of photosynthesis in C. reflexa to a restricted photosynthetic activity and degenerated chloroplasts in C. gronovii to an achlorophyllous state in E. virginiana.
Results
The newly sequenced plastid genomes of C. reflexa and C. gronovii reveal that the chromosome structures are generally very similar to that of non-parasitic plants, although a number of species-specific insertions, deletions (indels) and sequence inversions were identified. However, we observed a gradual adaptation of the plastid genome to the different degrees of parasitism. The changes are particularly evident in C. gronovii and include (a) the parallel losses of genes for the subunits of the plastid-encoded RNA polymerase and the corresponding promoters from the plastid genome, (b) the first documented loss of the gene for a putative splicing factor, MatK, from the plastid genome and (c) a significant reduction of RNA editing.
Conclusion
Overall, the comparative genomic analysis of plastid DNA from parasitic plants indicates a bias towards a simplification of the plastid gene expression machinery as a consequence of an increasing dependency on the host plant. A tentative assignment of the successive events in the adaptation of the plastid genomes to parasitism can be inferred from the current data set. This includes (1) a loss of non-coding regions in photosynthetic Cuscuta species that has resulted in a condensation of the plastid genome, (2) the simplification of plastid gene expression in species with largely impaired photosynthetic capacity and (3) the deletion of a significant part of the genetic information, including the information for the photosynthetic apparatus, in non-photosynthetic parasitic plants.
doi:10.1186/1471-2229-7-45
PMCID: PMC2089061  PMID: 17714582
10.  On the Origin of Branches in Escherichia coli 
Journal of Bacteriology  1999;181(21):6607-6614.
Some Escherichia coli strains with impaired cell division form branched cells at high frequencies during certain growth conditions. Here, we show that neither FtsI nor FtsZ activity is required for the development of branches. Buds did not form at specific positions along the cell surface during high-branching conditions. Antibiotics affecting cell wall synthesis had a positive effect on branch formation in the case of ampicillin, cephalexin, and penicillin G, whereas mecillinam and d-cycloserine had no substantial effect. Altering the cell morphology by nutritional shifts showed that changes in morphology preceded branching, indicating that the cell’s physiological state rather than specific medium components induced branching. Finally, there was no increased probability for bud formation in the daughters of a cell with a bud or branch, showing that bud formation is a random event. We suggest that branch formation is caused by abnormalities in cell wall elongation rather than by aberrant cell division events.
PMCID: PMC94123  PMID: 10542160
11.  Replacement of the Endogenous Starch Debranching Enzymes ISA1 and ISA2 of Arabidopsis with the Rice Orthologs Reveals a Degree of Functional Conservation during Starch Synthesis 
PLoS ONE  2014;9(3):e92174.
This study tested the interchangeability of enzymes in starch metabolism between dicotyledonous and monocotyledonous plant species. Amylopectin - a branched glucose polymer - is the major component of starch and is responsible for its semi-crystalline property. Plants synthesize starch with distinct amylopectin structures, varying between species and tissues. The structure determines starch properties, an important characteristic for cooking and nutrition, and for the industrial uses of starch. Amylopectin synthesis involves at least three enzyme classes: starch synthases, branching enzymes and debranching enzymes. For all three classes, several enzyme isoforms have been identified. However, it is not clear which enzyme(s) are responsible for the large diversity of amylopectin structures. Here, we tested whether the specificities of the debranching enzymes (ISA1 and ISA2) are major determinants of species-dependent differences in amylopectin structure by replacing the dicotyledonous Arabidopsis isoamylases (AtISA1 and AtISA2) with the monocotyledonous rice (Oryza sativa) isoforms. We demonstrate that the ISA1 and ISA2 are sufficiently well conserved between these species to form heteromultimeric chimeric Arabidopsis/rice isoamylase enzymes. Furthermore, we were able to reconstitute the endosperm-specific rice OsISA1 homomultimeric complex in Arabidopsis isa1isa2 mutants. This homomultimer was able to facilitate normal rates of starch synthesis. The resulting amylopectin structure had small but significant differences in comparison to wild-type Arabidopsis amylopectin. This suggests that ISA1 and ISA2 have a conserved function between plant species with a major role in facilitating the crystallization of pre-amylopectin synthesized by starch synthases and branching enzymes, but also influencing the final structure of amylopectin.
doi:10.1371/journal.pone.0092174
PMCID: PMC3958451  PMID: 24642810
12.  Growth and posture control strategies in Fagus sylvatica and Acer pseudoplatanus saplings in response to canopy disturbance 
Annals of Botany  2011;107(8):1345-1353.
Background and Aims
Forest tree saplings that grow in the understorey undergo frequent changes in their light environment to which they must adapt to ensure their survival and growth. Crown architecture, which plays a critical role in light capture and mechanical stability, is a major component of sapling adaptation to canopy disturbance. Shade-adapted saplings typically have plagiotropic stems and branches. After canopy opening, they need to develop more erect shoots in order to exploit the new light conditions. The objective of this study was to test whether changes in sapling stem inclination occur after canopy opening, and to analyse the morphological changes associated with stem reorientation.
Methods
A 4-year canopy-opening field experiment with naturally regenerated Fagus sylvatica and Acer pseudoplatanus saplings was conducted. The appearance of new stem axes, stem basal diameter and inclination along the stem were recorded every year after canopy opening.
Key Results
Both species showed considerable stem reorientation resulting primarily from uprighting (more erect) shoot movements in Fagus, and from uprighting movements, shoot elongation and formation of relay shoots in Acer. In both species, the magnitude of shoot uprighting movements was primarily related to initial stem inclination. Both the basal part and the apical part of the stem contributed to uprighting movements. Stem movements did not appear to be limited by stem size or by stem growth.
Conclusions
Stem uprighting movements in shade-adapted Fagus and Acer saplings following canopy disturbance were considerable and rapid, suggesting that stem reorientation processes play a significant role in the growth strategy of the species.
doi:10.1093/aob/mcr058
PMCID: PMC3101137  PMID: 21444338
Advance regeneration; canopy gap; biomechanics; gravitropism; shade tolerance; Fagus sylvatica; Acer pseudoplatanus
13.  Synopsis of Martinella Baill. (Bignonieae, Bignoniaceae), with the description of a new species from the Atlantic Forest of Brazil 
PhytoKeys  2014;15-24.
Martinella has traditionally included two species, Martinella iquitoensis and Martinella obovata, that are characterized by the presence of interpetiolar ridges surrounding the stems and minute prophylls of the axillary buds. A third species, Martinella insignis, is here described as new, illustrated and compared to other species in the genus. Martinella insignis is the first record of the genus in the Atlantic Forest of Brazil, and differs from other species of Martinella by the yellow corolla (vs. red to dark purple) and 5-lobed calices (vs. 2–4-lobed).
doi:10.3897/phytokeys.37.6940
PMCID: PMC4023332  PMID: 24843296
Martinella; Bignonieae; Bignoniaceae; Neotropics; Brazilian Atlantic Forest
14.  Mitochondria as integrators of information in an early-evolving animal: insights from a triterpenoid metabolite 
Mitochondria have the capacity to integrate environmental signals and, in animals with active stem cell populations, trigger responses in terms of growth and growth form. Colonial hydroids, which consist of feeding polyps connected by tube-like stolons, were treated with avicins, triterpenoid electrophiles whose anti-cancer properties in human cells are mediated in part by mitochondria. In treated hydroids, both oxygen uptake and mitochondrial reactive oxygen species were diminished relative to controls, similar to that observed in human cells exposed to avicins. While untreated colonies exhibit more stolon branches and connections in the centre of the colony than at the periphery, treated colonies exhibit the opposite: fewer stolon branches in the centre of the colony than at the periphery. The resulting growth form suggests an inversion of the normal pattern of colony development mediated by mitochondrial and redox-related perturbations. An as-yet-uncharacterized gradient within the colony may determine the ultimate phenotypic effect of avicin perturbation.
doi:10.1098/rspb.2004.2981
PMCID: PMC1578710  PMID: 15799949
avicins; cancer; hydroids; Podocoryna; reactive oxygen species; redox state
15.  Accelerated evolution and coevolution drove the evolutionary history of AGPase sub-units during angiosperm radiation 
Annals of Botany  2012;109(4):693-708.
Background and Aims
ADP-glucose pyrophosphorylase (AGPase) is a key enzyme of starch biosynthesis. In the green plant lineage, it is composed of two large (LSU) and two small (SSU) sub-units encoded by paralogous genes, as a consequence of several rounds of duplication. First, our aim was to detect specific patterns of molecular evolution following duplication events and the divergence between monocotyledons and dicotyledons. Secondly, we investigated coevolution between amino acids both within and between sub-units.
Methods
A phylogeny of each AGPase sub-unit was built using all gymnosperm and angiosperm sequences available in databases. Accelerated evolution along specific branches was tested using the ratio of the non-synonymous to the synonymous substitution rate. Coevolution between amino acids was investigated taking into account compensatory changes between co-substitutions.
Key Results
We showed that SSU paralogues evolved under high functional constraints during angiosperm radiation, with a significant level of coevolution between amino acids that participate in SSU major functions. In contrast, in the LSU paralogues, we identified residues under positive selection (1) following the first LSU duplication that gave rise to two paralogues mainly expressed in angiosperm source and sink tissues, respectively; and (2) following the emergence of grass-specific paralogues expressed in the endosperm. Finally, we found coevolution between residues that belong to the interaction domains of both sub-units.
Conclusions
Our results support the view that coevolution among amino acid residues, especially those lying in the interaction domain of each sub-unit, played an important role in AGPase evolution. First, within SSU, coevolution allowed compensating mutations in a highly constrained context. Secondly, the LSU paralogues probably acquired tissue-specific expression and regulatory properties via the coevolution between sub-unit interacting domains. Finally, the pattern we observed during LSU evolution is consistent with repeated sub-functionalization under ‘Escape from Adaptive Conflict’, a model rarely illustrated in the literature.
doi:10.1093/aob/mcr303
PMCID: PMC3286274  PMID: 22307567
Angiosperms; monocotyledons; dicotyledons; paralogue genes; molecular evolution; coevolution; neofunctionalization; subfunctionalization; starch synthesis; AGPase
16.  Early reproductive developmental anatomy in Decaisnea (Lardizabalaceae) and its systematic implications 
Annals of Botany  2009;104(6):1243-1253.
Background and Aims
Decaisnea insignis, known as ‘dead man's fingers’ (Lardizabalaceae), is widely distributed in China and the Himalayan foothill countries. This economically important plant, which is the only species in the genus, has not been the subject of any embryological studies aside from one brief, older paper that lacks micrographs. Data on Decaisnea are also important because its systematic position has been unstable since the genus was established in 1855. Therefore, the objectives of this study were: (a) to use modern microscopy to document early reproductive anatomical development in Decaisnea; and (b) to compare qualitatively these early embryological characters with allied taxa in a systematic context.
Methods
Decaisnea insignis floral buds and inflorescences were regularly collected from Shaanxi Province, China and prepared for light microscopy. The embryological characters studied were qualitatively compared with those of allied taxa via a thorough examination of the existing literature.
Key Results
Early reproductive anatomy in Decaisnea was documented and novel revelations made. It was discovered that the pollen is shed when three-celled (not two-celled, as previously reported), and that endosperm formation is nuclear (not cellular or helobial, as previously reported). These two newly revealed embryological characters are not found in any other members of Lardizabalaceae. Furthermore, neither are persistent antipodal cells, which we confirmed to be present in Decaisnea.
Conclusions
Decaisnea and other Lardizabalaceae characteristically have tetrasporangiate anthers, a secretory tapetum, simultaneous microsporocyte cytokinesis, primarily bitegmic, crassinucellate ovules, and a Polygonum type embryo sac. However, in the family, persistent antipodals, nuclear endosperm, and pollen shed at the three-celled stage are only found in Decaisnea. These embryological data prompted the suggestion that Decaisnea needs elevation above the level of genus.
doi:10.1093/aob/mcp232
PMCID: PMC2766214  PMID: 19759039
Decaisnea insignis; embryology; endosperm; Lardizabalaceae; microscopy; pollen; reproductive anatomy; systematics
17.  Morphogenesis of the branching reef coral Madracis mirabilis 
Understanding external deciding factors in growth and morphology of reef corals is essential to elucidate the role of corals in marine ecosystems, and to explain their susceptibility to pollution and global climate change. Here, we extend on a previously presented model for simulating the growth and form of a branching coral and we compare the simulated morphologies to three-dimensional (3D) images of the coral species Madracis mirabilis. Simulation experiments and isotope analyses of M. mirabilis skeletons indicate that external gradients of dissolved inorganic carbon (DIC) determine the morphogenesis of branching, phototrophic corals. In the simulations we use a first principle model of accretive growth based on local interactions between the polyps. The only species-specific information in the model is the average size of a polyp. From flow tank and simulation studies it is known that a relatively large stagnant and diffusion dominated region develops within a branching colony. We have used this information by assuming in our model that growth is entirely driven by a diffusion-limited process, where DIC supply represents the limiting factor. With such model constraints it is possible to generate morphologies that are virtually indistinguishable from the 3D images of the actual colonies.
doi:10.1098/rspb.2004.2934
PMCID: PMC1634949  PMID: 15695202
morphogenesis; scleractinian corals; diffusion-limited growth; morphological plasticity; computed tomography scanning; stable isotope analysis
18.  A membrane-bound matrix-metalloproteinase from Nicotiana tabacum cv. BY-2 is induced by bacterial pathogens 
BMC Plant Biology  2009;9:83.
Background
Plant matrix metalloproteinases (MMP) are conserved proteolytic enzymes found in a wide range of monocotyledonous and dicotyledonous plant species. Acting on the plant extracellular matrix, they play crucial roles in many aspects of plant physiology including growth, development and the response to stresses such as pathogen attack.
Results
We have identified the first tobacco MMP, designated NtMMP1, and have isolated the corresponding cDNA sequence from the tobacco suspension cell line BY-2. The overall domain structure of NtMMP1 is similar to known MMP sequences, although certain features suggest it may be constitutively active rather than dependent on proteolytic processing. The protein appears to be expressed in two forms with different molecular masses, both of which are enzymatically active as determined by casein zymography. Exchanging the catalytic domain of NtMMP1 with green fluorescent protein (GFP) facilitated subcellular localization by confocal laser scanning microscopy, showing the protein is normally inserted into the plasma membrane. The NtMMP1 gene is expressed constitutively at a low level but can be induced by exposure to bacterial pathogens.
Conclusion
Our biochemical analysis of NtMMP1 together with bioinformatic data on the primary sequence indicate that NtMMP1 is a constitutively-active protease. Given its induction in response to bacterial pathogens and its localization in the plasma membrane, we propose a role in pathogen defense at the cell periphery.
doi:10.1186/1471-2229-9-83
PMCID: PMC2715019  PMID: 19563670
19.  The hierarchical structure and mechanics of plant materials 
The cell walls in plants are made up of just four basic building blocks: cellulose (the main structural fibre of the plant kingdom) hemicellulose, lignin and pectin. Although the microstructure of plant cell walls varies in different types of plants, broadly speaking, cellulose fibres reinforce a matrix of hemicellulose and either pectin or lignin. The cellular structure of plants varies too, from the largely honeycomb-like cells of wood to the closed-cell, liquid-filled foam-like parenchyma cells of apples and potatoes and to composites of these two cellular structures, as in arborescent palm stems. The arrangement of the four basic building blocks in plant cell walls and the variations in cellular structure give rise to a remarkably wide range of mechanical properties: Young's modulus varies from 0.3 MPa in parenchyma to 30 GPa in the densest palm, while the compressive strength varies from 0.3 MPa in parenchyma to over 300 MPa in dense palm. The moduli and compressive strength of plant materials span this entire range. This study reviews the composition and microstructure of the cell wall as well as the cellular structure in three plant materials (wood, parenchyma and arborescent palm stems) to explain the wide range in mechanical properties in plants as well as their remarkable mechanical efficiency.
doi:10.1098/rsif.2012.0341
PMCID: PMC3479918  PMID: 22874093
plant materials; mechanics; wood; parenchyma; palm stems
20.  Cyclone Tolerance in New World Arecaceae: Biogeographic Variation and Abiotic Natural Selection 
Annals of Botany  2008;102(4):591-598.
Background and Aims
Consistent abiotic factors can affect directional selection; cyclones are abiotic phenomena with near-discrete geographic limits. The current study investigates selective pressure of cyclones on plants at the species level, testing for possible natural selection.
Methods
New World Arecaceae (palms) are used as a model system, as plants with monopodial, unbranched arborescent form are most directly affected by the selective pressure of wind load. Living specimens of known provenance grown at a common site were affected by the same cyclone. Data on percentage mortality were compiled and analysed in biogeographic and phylogenetic contexts.
Key Results
Palms of cyclone-prone provenance exhibited a much lower (one order of magnitude) range in cyclone tolerance, and significantly lower (P < 0·001) mean percentage mortality than collections from cyclone-free areas. Palms of cyclone-free provenance had much greater variation in tolerance, and significantly greater mean percentage mortality. A test for serial independence recovered no significant phylogenetic autocorrelation of percentage mortality.
Conclusions
Variation in cyclone tolerance in New World Arecaceae correlates with biogeography, and is not confounded with phylogeny. These results suggest natural selection of cyclone tolerance in cyclone-prone areas.
doi:10.1093/aob/mcn132
PMCID: PMC2701779  PMID: 18669575
Abiotic selection; Arecaceae; biogeography; cyclone; hurricane; phylogenetic independence
21.  Blow me down: A new perspective on Aloe dichotoma mortality from windthrow 
BMC Ecology  2014;14:7.
Background
Windthrow, the uprooting of trees during storms associated with strong winds, is a well-established cause of mortality in temperate regions of the world, often with large ecological consequences. However, this phenomenon has received little attention within arid regions and is not well documented in southern Africa. Slow rates of post-disturbance recovery and projected increases in extreme weather events in arid areas mean that windthrow could be more common and have bigger impacts on these ecosystems in the future. This is of concern due to slow rates of post-disturbance recovery in arid systems and projected increases in extreme weather events in these areas. This study investigated the spatial pattern, magnitude and likely causes of windthrown mortality in relation to other forms of mortality in Aloe dichotoma, an iconic arid-adapted arborescent succulent and southern Africa climate change indicator species.
Results
We found that windthrown mortality was greatest within the equatorward summer rainfall zone (SRZ) of its distribution (mean = 31%, n = 11), and was derived almost exclusively from the larger adult age class. A logistic modelling exercise indicated that windthrown mortality was strongly associated with greater amounts of warm season (summer) rainfall in the SRZ, higher wind speeds, and leptosols. A statistically significant interaction term between higher summer rainfall and wind speeds further increased the odds of being windthrown. While these results would benefit from improvements in the resolution of wind and substrate data, they do support the hypothesised mechanism for windthrow in A. dichotoma. This involves powerful storm gusts associated with either the current or subsequent rainfall event, heavy convective rainfall, and an associated increase in soil malleability. Shallow rooting depths in gravel-rich soils and an inflexible, top-heavy canopy structure make individuals especially prone to windthrown mortality during storms.
Conclusions
Results highlight the importance of this previously unrecognised form of mortality in A. dichotoma, especially since it seems to disproportionately affect reproductively mature adult individuals in an infrequently recruiting species. Smaller, more geographically isolated and adult dominated populations in the summer rainfall zone are likely to be more vulnerable to localised extinction due to windthrow events.
doi:10.1186/1472-6785-14-7
PMCID: PMC3995187  PMID: 24641794
Aloe dichotoma; Arid environment; Convective rainfall; Indicator species; Mortality; Southern Africa; Wind speed; Windthrow
22.  The Electron Microscopy of the Left Colleterial Gland of the Cockroach 
A study has been made of the cells of the left colleterial gland of the cockroach, Periplaneta americana (L.), using the electron microscope, and the results compared with previous histological and histochemical studies. The colleterial gland consists of an arborescent bunch of long tubules composed mainly of the cells which secrete the structural protein of the egg case ("type 4 cells"). Other types of cells: chitinogenic cells and "type 2 and 3 cells" each with a different cytology are described. The type 4 cells, which form the structural protein, reveal a cytological pattern very similar to that described for mammalian cells in a state of active protein synthesis. There is an elaborate development of particle-studded membranes in the cytoplasm. Smaller, rounded agranular vesicles also occur. The free secretory surface of the secreting cells forms the "end-apparatus" of the light microscopists. The invaginated surface is cast into numerous long narrow processes usually radially arranged and directed into a funnel-like formation derived from the thin intima lining the lumen of the gland (Text-fig. 2). The secretion in the form of small balls may be seen in the cavity of the end-apparatus and sometimes in the narrow processes. The small chitinogenic cells, lying between the protein-forming cells and the thin intima which they secrete, have a different cytology perhaps related to the fact that they form a polysaccharide rather than a protein. There is a very poor development of the particle-studded membranes of the type found in protein-forming cells. The type 2 cells, supposed to form an oxidase, have an end-apparatus that is similar to, but more complex than, those of the type 4 cells and their cytoplasm is almost completely filled with mitochondria. There is some evidence that mitochondria play a part in forming the oxidase and pass into the tubules of the end-apparatus. Type 3 cells resemble both types 2 and 4 and are probably a transient intermediate form.
PMCID: PMC2224657  PMID: 13654446
23.  Aboveground Allometric Models for Freeze-Affected Black Mangroves (Avicennia germinans): Equations for a Climate Sensitive Mangrove-Marsh Ecotone 
PLoS ONE  2014;9(6):e99604.
Across the globe, species distributions are changing in response to climate change and land use change. In parts of the southeastern United States, climate change is expected to result in the poleward range expansion of black mangroves (Avicennia germinans) at the expense of some salt marsh vegetation. The morphology of A. germinans at its northern range limit is more shrub-like than in tropical climes in part due to the aboveground structural damage and vigorous multi-stem regrowth triggered by extreme winter temperatures. In this study, we developed aboveground allometric equations for freeze-affected black mangroves which can be used to quantify: (1) total aboveground biomass; (2) leaf biomass; (3) stem plus branch biomass; and (4) leaf area. Plant volume (i.e., a combination of crown area and plant height) was selected as the optimal predictor of the four response variables. We expect that our simple measurements and equations can be adapted for use in other mangrove ecosystems located in abiotic settings that result in mangrove individuals with dwarf or shrub-like morphologies including oligotrophic and arid environments. Many important ecological functions and services are affected by changes in coastal wetland plant community structure and productivity including carbon storage, nutrient cycling, coastal protection, recreation, fish and avian habitat, and ecosystem response to sea level rise and extreme climatic events. Coastal scientists in the southeastern United States can use the identified allometric equations, in combination with easily obtained and non-destructive plant volume measurements, to better quantify and monitor ecological change within the dynamic, climate sensitive, and highly-productive mangrove-marsh ecotone.
doi:10.1371/journal.pone.0099604
PMCID: PMC4074035  PMID: 24971938
24.  Characterization of the Floral Transcriptome of Moso Bamboo (Phyllostachys edulis) at Different Flowering Developmental Stages by Transcriptome Sequencing and RNA-Seq Analysis 
PLoS ONE  2014;9(6):e98910.
Background
As an arborescent and perennial plant, Moso bamboo (Phyllostachys edulis (Carrière) J. Houzeau, synonym Phyllostachys heterocycla Carrière) is characterized by its infrequent sexual reproduction with flowering intervals ranging from several to more than a hundred years. However, little bamboo genomic research has been conducted on this due to a variety of reasons. Here, for the first time, we investigated the transcriptome of developing flowers in Moso bamboo by using high-throughput Illumina GAII sequencing and mapping short reads to the Moso bamboo genome and reference genes. We performed RNA-seq analysis on four important stages of flower development, and obtained extensive gene and transcript abundance data for the floral transcriptome of this key bamboo species.
Results
We constructed a cDNA library using equal amounts of RNA from Moso bamboo leaf samples from non-flowering plants (CK) and mixed flower samples (F) of four flower development stages. We generated more than 67 million reads from each of the CK and F samples. About 70% of the reads could be uniquely mapped to the Moso bamboo genome and the reference genes. Genes detected at each stage were categorized to putative functional categories based on their expression patterns. The analysis of RNA-seq data of bamboo flowering tissues at different developmental stages reveals key gene expression properties during the flower development of bamboo.
Conclusion
We showed that a combination of transcriptome sequencing and RNA-seq analysis was a powerful approach to identifying candidate genes related to floral transition and flower development in bamboo species. The results give a better insight into the mechanisms of Moso bamboo flowering and ageing. This transcriptomic data also provides an important gene resource for improving breeding for Moso bamboo.
doi:10.1371/journal.pone.0098910
PMCID: PMC4051636  PMID: 24915141
25.  Responses of Crown Development to Canopy Openings by Saplings of Eight Tropical Submontane Forest Tree Species in Indonesia: A Comparison with Cool-temperate Trees 
Annals of Botany  2006;97(4):559-569.
• Background and Aims Growth in trunk height in canopy openings is important for saplings. How saplings increase height growth in canopy openings may relate to crown architectural constraints. Responses of crown development to canopy openings in relation to trunk height growth were studied for saplings (0·2–2·5 m tall) of eight tropical submontane forest tree species in Indonesia. The results of this study were also compared with those of temperate trees in northern Japan.
• Methods The crown architecture differed among the eight tropical species, i.e. they had sparsely to highly developed branching structures. Crown allometry was compared among the eight species in each canopy condition (closed canopy or canopy openings), and between closed canopy and canopy openings within a species. A general linear regression model was used to analyse how each species increases height growth rate in canopy openings. Crown allometry and its plasticity were compared between tropical and temperate trees by a nested analysis of covariance.
• Key Results Tropical submontane trees had responses similar to cool-temperate trees, showing an increase in height in canopy openings, i.e. taller saplings of sparsely branched species increase height growth rates by increasing the sapling leaf area. Cool-temperate trees have a wider crown projection area and a smaller leaf area per crown projection area to avoid self-shading within a crown compared with tropical submontane trees. Plasticity of the crown projection area is greater in cool-temperate trees than in tropical submontane trees, probably because of the difference in leaf longevity.
• Conclusions This study concluded that interspecific variation in the responses of crown development to canopy openings in regard to increasing height related to the species' branching structure, and that different life-forms, such as evergreen and deciduous trees, had different crown allometry and plasticity.
doi:10.1093/aob/mcl003
PMCID: PMC2803653  PMID: 16399792
Cool-temperate trees; crown allometry; crown architecture; height growth; Indonesia; saplings; plasticity; tropical trees

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