Patrick T. Martone

Red and Green Algal Monophyly and Extensive Gene Sharing Found in a Rich Repertoire of Red Algal Genes

The Plantae comprising red, green (including land plants), and glaucophyte algae are postulated to have a single common ancestor that is the founding lineage of photosynthetic eukaryotes. However, recent multiprotein phylogenies provide little or no support for this hypothesis. This may reflect limited complete genome data available for red algae, currently only the highly reduced genome of Cyanidioschyzon merolae, a reticulate gene ancestry, or variable gene divergence rates that mislead phylogenetic inference. Here, using novel genome data from the mesophilic Porphyridium cruentum and Calliarthron tuberculosum, we analyze 60,000 novel red algal genes to test the monophyly of red + green (RG) algae and their extent of gene sharing with other lineages. Using a gene-by-gene approach, we find an emerging signal of RG monophyly (supported by ∼50% of the examined protein phylogenies) that increases with the number of distinct phyla and terminal taxa in the analysis. A total of 1,808 phylogenies show evidence of gene sharing between Plantae and other lineages. We demonstrate that a rich mesophilic red algal gene repertoire is crucial for testing controversial issues in eukaryote evolution and for understanding the complex patterns of gene inheritance in protists.

Evolution of Red Algal Plastid Genomes: Ancient Architectures, Introns, Horizontal Gene Transfer, and Taxonomic Utility of Plastid Markers

Red algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal plastid genomes we show they all share a highly compact and slowly-evolving architecture and uniquely rich gene complements. Both chromosome structure and gene content have changed very little during red algal diversification, and suggest that plastid-to nucleus gene transfers have been rare. Despite their ancient character, however, the red algal plastids also contain several unprecedented features, including a group II intron in a tRNA-Met gene that encodes the first example of red algal plastid intron maturase – a feature uniquely shared among florideophytes. We also identify a rare case of a horizontally-acquired proteobacterial operon, and propose this operon may have been recruited for plastid function and potentially replaced a nucleus-encoded plastid-targeted paralogue. Plastid genome phylogenies yield a fully resolved tree and suggest that plastid DNA is a useful tool for resolving red algal relationships. Lastly, we estimate the evolutionary rates among more than 200 plastid genes, and assess their usefulness for species and subspecies taxonomy by comparison to well-established barcoding markers such as cox1 and rbcL. Overall, these data demonstrates that red algal plastid genomes are easily obtainable using high-throughput sequencing of total genomic DNA, interesting from evolutionary perspectives, and promising in resolving red algal relationships at evolutionarily-deep and species/subspecies levels.

Mechanics without Muscle: Biomechanical Inspiration from the Plant World

Plant and animal biomechanists have much in common. Although their frame of reference differs, they think about the natural world in similar ways. While researchers studying animals might explore airflow around flapping wings, the actuation of muscles in arms and legs, or the material properties of spider silk, researchers studying plants might explore the flow of water around fluttering seaweeds, the grasping ability of climbing vines, or the material properties of wood. Here we summarize recent studies of plant biomechanics highlighting several current research themes in the field: expulsion of high-speed reproductive projectiles, generation of slow movements by shrinking and swelling cell walls, effects of ontogenetic shifts in mechanical properties of stems, flexible reconfiguration and material properties of seaweeds under crashing waves, and the development of botanically-inspired commercial products. Our hope is that this synopsis will resonate with both plant and animal biologists, encourage cross-pollination across disciplines, and promote fruitful interdisciplinary collaborations in the future.

New, resurrected and redefined species of Mastocarpus (Phyllophoraceae, Rhodophyta) from the northeast Pacific

Lindstrom S.C., Hughey J.R. and Martone P.T. 2011. New, resurrected and redefined species of Mastocarpus (Phyllophoraceae, Rhodophyta). Phycologia 50: 661–683. DOI: 10.2216/10-38.1 Recent molecular phylogenetic investigations of the red algal genus Mastocarpus from the northeast Pacific resolved numerous cryptic species. Although species were clearly defined through genetic analyses, the correct names to apply to the species remained unclear due to both morphological variability within species and morphological similarity between species. To determine the appropriate name for each entity, we analyzed DNA from type material of taxa previously ascribed to Mastocarpus. In combination with this analysis, an updated phylogeny based on a broad range of geographical and morphological collections is presented that includes data from nuclear (ribosomal internal transcribed spacers [ITS]), chloroplast (rbcL) and mitochondrial [cytochrome oxidase I (COI)] genomes. By analyzing partial ITS region sequences of type specimens, we are able to match currently accepted names (Mastocarpus papillatus, M. pacificus and M. jardinii) to modern collections. We resurrect the following specific epithets and propose the new combinations Mastocarpus cristatus, Mastocarpus latissimus and Mastocarpus agardhii, and we create new species for which we were unable to verify an existing name: Mastocarpus alaskensis, Mastocarpus intermedius, Mastocarpus vancouveriensis, Mastocarpus californianus and Mastocarpus rigidus. The species formerly included in M. papillatus are now identified as Mastocarpus alaskensis, M. papillatus, Mastocarpus intermedius, Mastocarpus cristatus, Mastocarpus vancouveriensis and Mastocarpus latissimus. The name M. jardinii applies to a species thus far collected only from Moss Beach in San Mateo County and the Monterey Peninsula, both in California. Specimens other than the type previously assigned to M. jardinii are now separated into three species: Mastocarpus rigidus, Mastocarpus californianus and Mastocarpus agardhii. Mastocarpus cristatus represents a species closely allied to Clade 3 (Mastocarpus intermedius), and M. pacificus represents Clade 7. Morphological and anatomical diagnoses, along with vertical distributions and geographic ranges, are provided for each species.

Morphometric and molecular analyses confirm two distinct species of Calliarthron (Corallinales, Rhodophyta), a genus endemic to the northeast Pacific

Gabrielson P.W., Miller K.A. and Martone P.T. 2011. Morphometric and molecular analyses confirm two distinct species of Calliarthron (Corallinales, Rhodophyta), a genus endemic to the northeast Pacific. Phycologia 50: 298–316. DOI: 10.2216/10-42.1 Phylogenetic analyses of rbcL sequences demonstrate that Calliarthron as currently constituted is paraphyletic. Calliarthron yessoense and C. latissimum from the northwest Pacific belong in Alatocladia and are conspecific. After the transfer of C. yessoense and C. latissimum, Calliarthron is monophyletic, known only from the northeast Pacific and comprises two species, C. cheilosporioides and C. tuberculosum, which are distinct morphologically, biogeographically and by molecular sequence. Sequence data for the types of C. regenerans and C. setchelliae confirm that they are heterotypic synonyms of C. tuberculosum. Lectotypes are designated for C. cheilosporioides, C. regenerans and C. setchelliae. A morphometric analysis shows that three measured characters reliably distinguish C. cheilosporioides from C. tuberculosum. Alatocladia is monophyletic, known only from the northwest Pacific and comprises two species, A. modesta and A. yessoensis, which are distinct morphologically, biogeographically and by molecular sequence. rbcL sequence data of the type species of Alatocladia, Bossiella, Calliarthron and Chiharaea confidently differentiate these genera with strong bootstrap support.

Adapted for invasion? Comparing attachment, drag and dislodgment of native and nonindigenous hull fouling species

Invasive species possess unique traits that allow them to navigate the invasion process in order to establish and spread in new habitats. Successful hull fouling invaders must resist both physical and physiological stressors associated with their voyage. We characterised attachment strength and drag coefficient of common fouling species in order to estimate the velocity required to dislodge them from boat hulls. We hypothesized nonindigenous fouling species would possess biomechanical properties that enable them to remain attached to hulls more successfully than similar native species. Indeed, the well-known invasive ascidian Styela clava had both high attachment strength and low drag coefficient and its dislodgment velocity was well above that of fast moving vessels. In contrast, the native congener Styela gibbsii had low attachment strength and higher drag coefficient. Colonial invasive species employed a different hitchhiking strategy; despite their low attachment strengths, Botrylloides violaceus and Didemnum vexillum had low drag coefficients allowing them to be transported on slower-moving vessels, such as sailboats and barges. The biomechanical adaptations of invasive species show promise in predicting future invaders and informing vector management strategies at the first node in the invasion process: transport by the vector.

Kelp versus coralline: cellular basis for mechanical strength in the wave-swept seaweed Calliarthron (Corallinaceae, Rhodophyta)1

Previous biomechanical studies of wave‐swept macroalgae have revealed a trade‐off in growth strategies to resist breakage in the intertidal zone: growing in girth versus growing strong tissues. Brown macroalgae, such as kelps, grow thick stipes but have weak tissues, while red macroalgae grow slender thalli but have much stronger tissues. For example, genicular tissue in the articulated coralline Calliarthron cheilosporioides Manza is more than an order of magnitude stronger than some kelp tissues, but genicula rarely exceed 1 mm in diameter. The great tissue strength of Calliarthron genicula results, at least in part, from a lifelong strengthening process. Here, a histological analysis is presented to explore the cellular basis for mechanical strengthening in Calliarthron genicula. Genicula are composed of thousands of fiber‐like cells, whose cell walls thicken over time. Thickening of constitutive cell walls likely explains why older genicula have stronger tissues: a mature geniculum may be >50% cell wall. However, the material strength of genicular cell wall is similar to the strength of cell wall from a freshwater green alga, suggesting that it may be the quantity—not the quality—of cell wall material that gives genicular tissue its strength. Apparent differences in tissue strength across algal taxa may be a consequence of tissue construction rather than material composition.

Misleading morphologies and the importance of sequencing type specimens for resolving coralline taxonomy (Corallinales, Rhodophyta): Pachyarthron cretaceum is Corallina officinalis.

Coralline red algae play a key role in the ecology of near shore marine ecosystems and are increasingly being used to study the effects of climate change in the marine environment. Corallines are very difficult to identify to species, and even to genus, using morpho‐anatomy, likely complicating studies of their ecology, physiology, and biodiversity. We sequenced a 296 base pair fragment of chloroplast DNA from a 187‐year‐old isolectotype specimen of Pachyarthron cretaceum, a morphologically distinct geniculate species, to demonstrate that coralline morphology is often misleading and that species names can only be applied unequivocally by comparing DNA sequences from type material with sequences from field‐collected specimens. Our results indicate that Pachyarthron cretaceum is synonymous with Corallina officinalis.

CHIHARAEA AND YAMADAIA (CORALLINALES, RHODOPHYTA) REPRESENT REDUCED AND RECENTLY DERIVED ARTICULATED CORALLINE MORPHOLOGIES 1

Phycologists have hypothesized that the diminutive fronds produced by species in the genera Chiharaea and Yamadaia, which are composed of comparatively few genicula and intergenicula, represent morphological intermediates in the evolution of articulated corallines from crustose ancestors. We test this “intermediate frond hypothesis” by comparing rbcL sequences from the generitype species Chiharaea bodegensis and Yamadaia melobesioides to sequences from other coralline genera. We demonstrate that Chiharaea includes two other NE Pacific species, Arthrocardia silvae and Yamadaia americana. Chiharaea species are characterized morphologically by inflated intergenicula and axial conceptacles with apical or acentric pores. Although relationships among the three species are unresolved, Chiharaea bodegensis, C. americana comb. nov., and C. silvae comb. nov. are distinguished from one another by DNA sequences, morphology, habitat, and biogeography. Chiharaea occurs together with Alatocladia, Bossiella, Calliarthron, and Serraticardia macmillanii in a strongly supported clade of nearly endemic north Pacific articulated coralline genera and species that have evolved relatively recently compared to other articulated corallines. In contrast, NW Pacific Yamadaia melobesioides belongs in a clade with Corallina officinalis, the generitype species of Corallina, and therefore we reduce Yamadia to a synonym of Corallina and propose Corallina melobesioides comb. nov. We reject the ‘intermediate frond hypothesis’ and conclude that Chiharaea and Yamadaia are recently derived taxa that evolved from articulated coralline ancestors and represent a reduction in the number of genicula and intergenicula.

Ancient origin of the biosynthesis of lignin precursors.

BackgroundLignin plays an important role in plant structural support and water transport, and is considered one of the hallmarks of land plants. The recent discovery of lignin or its precursors in various algae has raised questions on the evolution of its biosynthetic pathway, which could be much more ancient than previously thought. To determine the taxonomic distribution of the lignin biosynthesis genes, we screened all publicly available genomes of algae and their closest non-photosynthetic relatives, as well as representative land plants. We also performed phylogenetic analysis of these genes to decipher the evolution and origin(s) of lignin biosynthesis.ResultsEnzymes involved in making p-coumaryl alcohol, the simplest lignin monomer, are found in a variety of photosynthetic eukaryotes, including diatoms, dinoflagellates, haptophytes, cryptophytes as well as green and red algae. Phylogenetic analysis of these enzymes suggests that they are ancient and spread to some secondarily photosynthetic lineages when they acquired red and/or green algal endosymbionts. In some cases, one or more of these enzymes was likely acquired through lateral gene transfer (LGT) from bacteria.ConclusionsGenes associated with p-coumaryl alcohol biosynthesis are likely to have evolved long before the transition of photosynthetic eukaryotes to land. The original function of this lignin precursor is therefore unlikely to have been related to water transport. We suggest that it participates in the biological defense of some unicellular and multicellular algae.ReviewersThis article was reviewed by Mark Ragan, Uri Gophna, Philippe Deschamps.