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The multicellular green alga Volvox carteri and its morphologically diverse close relatives (the volvocine algae) are well suited for the investigation of the evolution of multicellularity and development. We sequenced the 138-mega-base pair genome of V. carteri and compared its approximately 14,500 predicted proteins to those of its unicellular relative Chlamydomonas reinhardtii. Despite fundamental differences in organismal complexity and life history, the two species have similar protein-coding potentials and few species-specific protein-coding gene predictions. Volvox is enriched in volvocine-algal-specific proteins, including those associated with an expanded and highly compartmentalized extracellular matrix. Our analysis shows that increases in organismal complexity can be associated with modifications of lineage-specific proteins rather than large-scale invention of protein-coding capacity.

This paper represents an attempt to unify data from various lines of Volvox research: developmental biology, biogeography, and evolution. Several species (such as Volvox carteri and Volvox spermatosphaera) are characterized by rapid divisions of asexual reproductive cells, which may proceed in darkness. By contrast, several other species (such as Volvox aureus, Volvox globator, and Volvox tertius) exhibit slow and light/dependent divisions. The transition from the former pattern of asexual life cycle to the latter one has occurred in three lineages of the genus Volvox. Since V. aureus (unlike V. carteri) is able to complete the life cycle at a short photoperiod (8 h light/16 h dark regime), it is reasonable to suggest that the abovementioned evolutionary transitions might have occurred as adaptations to short winter days in high latitudes under warm climate conditions in the deep past. In the case of the lineage leading to V. tertius + Volvox dissipatrix, the crucial reorganizations of asexual life cycle might have occurred between about 45 and 60 million years ago in relatively high latitudes of Southern Hemisphere.

The prevalence of multicellular organisms is due in part to their ability to form complex structures. How cells pack in these structures is a fundamental biophysical issue, underlying their functional properties. However, much remains unknown about how cell packing geometries arise, and how they are affected by random noise during growth - especially absent developmental programs. Here, we quantify the statistics of cellular neighborhoods of two different multicellular eukaryotes: lab-evolved ‘snowflake’ yeast and the green alga Volvox carteri . We find that despite large differences in cellular organization, the free space associated with individual cells in both organisms closely fits a modified gamma distribution, consistent with maximum entropy predictions originally developed for granular materials. This ‘entropic’ cellular packing ensures a degree of predictability despite noise, facilitating parent-offspring fidelity even in the absence of developmental regulation. Together with simulations of diverse growth morphologies, these results suggest that gamma-distributed cell neighborhood sizes are a general feature of multicellularity, arising from conserved statistics of cellular packing.

Volvox sect. Volvox is a group of green algae with unique morphological features (thick cytoplasmic bridges between somatic cells and spiny zygote walls) and a worldwide distribution. Despite research interest in the diversity of organisms in ancient lakes, Volvox sect. Volvox from ancient lakes worldwide has not been identified to the species level. Here, we established clonal cultures of two species of this group originating from Lake Biwa, an ancient lake in Japan, and performed identification based on morphological and molecular data. One was identified as Volvox kirkiorum based on the nuclear ribosomal DNA internal spacer region (ITS) sequence, bisexual (monoicous or monoecious) spheroids, and zygote morphology. The other showed genetic separation from related species based on the secondary structure of the ITS and results of phylogenetic analysis of a combined data set from the nuclear actin gene, ITS, and two plastid genes (large subunit of RuBisCO and photosystem II CP43 apoprotein gene); it represented a new phylogenetic lineage within Volvox sect. Volvox , suggesting possible endemism in Lake Biwa. This species produced bisexual spheroids with different zygote morphology and zygote number from other species with bisexual spheroids in Volvox sect. Volvox . Therefore, Volvox biwakoensis Nozaki et H. Yamaguchi sp. nov. is described herein. This is the first endemic species of the genus Volvox described from an ancient lake.

Individuality is a complex trait, yet a series of stages each advantageous in itself can be shown to exist allowing evolution to get from unicellular individuals to multicellular individuals. We consider several of the key stages involved in this transition: the initial advantage of group formation, the origin of reproductive altruism within the group, and the further specialization of cell types as groups increase in size. How do groups become individuals? This is the central question we address. Our hypothesis is that fitness tradeoffs drive the transition of a cell group into a multicellular individual through the evolution of cells specialized at reproductive and vegetative functions of the group. We have modeled this hypothesis and have tested our models in two ways. We have studied the origin of the genetic basis for reproductive altruism (somatic cells specialized at vegetative functions) in the multicellular Volvox carteri by showing how an altruistic gene may have originated through cooption of a life-history tradeoff gene present in a unicellular ancestor. Second, we ask why reproductive altruism and individuality arise only in the larger members of the volvocine group (recognizing that high levels of kinship are present in all volvocine algae groups). Our answer is that the selective pressures leading to reproductive altruism stem from the increasing cost of reproduction with increasing group size. Concepts from population genetics and evolutionary biology appear to be sufficient to explain complexity, at least as it relates to the problem of the major transitions between the different kinds of evolutionary individuals.

Flows generated by ensembles of flagella are crucial to development, motility and sensing, but the mechanisms behind this striking coordination remain unclear. We present novel experiments in which two micropipette-held somatic cells of Volvox carteri, with distinct intrinsic beating frequencies, are studied by high-speed imaging as a function of their separation and orientation. Analysis of time series shows that the interflagellar coupling, constrained by lack of connections between cells to be hydrodynamical, exhibits a spatial dependence consistent with theory. At close spacings it produces robust synchrony for thousands of beats, while at increasing separations synchrony is degraded by stochastic processes. Manipulation of the relative flagellar orientation reveals in-phase and antiphase states, consistent with dynamical theories. Flagellar tracking with exquisite precision reveals waveform changes that result from hydrodynamic coupling. This study proves unequivocally that flagella coupled solely through a fluid can achieve robust synchrony despite differences in their intrinsic properties. Sperm cells, as well as many bacteria and algae, propel themselves using whip-like appendages called flagella. Similar, shorter structures called cilia are also found on the surface of many cells, where they perform roles such as moving liquids over the cell. Each cilium or flagellum beats at its own characteristic rhythm, but there are many situations where cilia or flagella must synchronize their beating with other nearby cells. For example, an egg cell is swept along the Fallopian tube by the coordinated beating of the cilia lining the tube. Bull sperm cells are also known to synchronize the beating of their flagella when swimming close to each other. It has been suggested that the movement of the fluid surrounding the beating flagella could be the source of this synchronization. Experiments have produced results that match up with mathematical models describing this fluid movement. However, these experiments have often been designed in ways that didn’t fully exclude other possible sources of synchronization, such as chemical signalling, or—for flagella located on the same cell—a physical connection between the flagella. To overcome this shortcoming, Brumley et al. used high-speed imaging to watch the flagella of cells of Volvox carteri—a species of green alga—that were separated so that they could only communicate through the movement of the fluid around them. The flagella were still able to synchronize their beating, even when the two flagella naturally beat at substantially different rates. The distance between the flagella affects how well the beating synchronizes. When close together, the flagella can lock into the same rhythm for thousands of beats. However, as they move further apart, random biochemical fluctuations within the cells reduce the extent to which the flagella can synchronize. The flagella can also synchronize so that they move in the same direction at the same time, or in opposite directions, depending on how they are oriented relative to each other. Moreover, the results confirm that the fluid flow produced by a beating flagellum is sufficient to synchronize the beating of other nearby flagella.

In recent years, there has been a significant increase in the number of completely sequenced plant genomes. The comparison of fully sequenced genomes allows for identification of new gene family members, as well as comprehensive analysis of gene family evolution. The aldehyde dehydrogenase (ALDH) gene superfamily comprises a group of enzymes involved in the NAD+- or NADP+-dependent conversion of various aldehydes to their corresponding carboxylic acids. ALDH enzymes are involved in processing many aldehydes that serve as biogenic intermediates in a wide range of metabolic pathways. In addition, many of these enzymes function as 'aldehyde scavengers' by removing reactive aldehydes generated during the oxidative degradation of lipid membranes, also known as lipid peroxidation. Plants and animals share many ALDH families, and many genes are highly conserved between these two evolutionarily distinct groups. Conversely, both plants and animals also contain unique ALDH genes and families. Herein we carried out genome-wide identification of ALDH genes in a number of plant species—including Arabidopsis thaliana (thale crest), Chlamydomonas reinhardtii (unicellular algae), Oryza sativa (rice), Physcomitrella patens (moss), Vitis vinifera (grapevine) and Zea mays (maize). These data were then combined with previous analysis of Populus trichocarpa (poplar tree), Selaginella moellindorffii (gemmiferous spikemoss), Sorghum bicolor (sorghum) and Volvox carteri (colonial algae) for a comprehensive evolutionary comparison of the plant ALDH superfamily. As a result, newly identified genes can be more easily analyzed and gene names can be assigned according to current nomenclature guidelines; our goal is to clarify previously confusing and conflicting names and classifications that might confound results and prevent accurate comparisons between studies.

Volvox rousseletii is a dioecious species belonging to Volvox sect. Volvox that has previously only been found in Africa. During field surveys in a large dam lake (Lake Sagami) in Kanagawa Prefecture, central Japan, we encountered a Volvox sect. Volvox species that produces dioecious sexual spheroids in the water column. Although sexual induction of this species in culture did not produce adequately well-developed sexual spheroids for species identification, molecular data directly obtained from field-collected sexual spheroids verified the identity of field-collected male and female sexual spheroids as well as cultured materials. Based on molecular and morphological data, the species was identified as V. rousseletii. This is the first record of a dioecious species of Volvox sect. Volvox in Japan.

Background ATP-binding cassette proteins have been recognized as playing a crucial role in the regulation of growth and resistance processes in all kingdoms of life. They have been deeply studied in vertebrates because of their role in drug resistance, but much less is known about ABC superfamily functions in plants. Results Recently released plant genome sequences allowed us to identify 803 ABC transporters in four vascular plants ( Oryza. sativa, Solanum lycopersicum, Solanum tuberosum and Vitis vinifera ) and 76 transporters in the green alga Volvox carteri , by comparing them with those reannotated in Arabidopsis thaliana and the yeast Saccharomyces cerevisiae . Retrieved proteins have been phylogenetically analysed to infer orthologous relationships. Most orthologous relationships in the A, D, E and F subfamilies were found, and interesting expansions within the ABCG subfamily were observed and discussed. A high level of purifying selection is acting in the five ABC subfamilies A, B, C, D and E. However, evolutionary rates of recent duplicate genes could influence vascular plant genome diversification. The transcription profiles of ABC genes within tomato organs revealed a broad functional role for some transporters and a more specific activity for others, suggesting the presence of key ABC regulators in tomato. Conclusions The findings achieved in this work could contribute to address several biological questions concerning the evolution of the relationship between genomes of different species. Plant ABC protein inventories obtained could be a valuable tool both for basic and applied studies. Indeed, interpolation of the putative role of gene functions can accelerate the discovering of new ABC superfamily members.

Evolutionary transitions in individuality (ETIs) underlie the watershed events in the history of life on Earth, including the origins of cells, eukaryotes, plants, animals, and fungi. Each of these events constitutes an increase in the level of complexity, as groups of individuals become individuals in their own right. Among the best-studied ETIs is the origin of multicellularity in the green alga Volvox, a model system for the evolution of multicellularity and cellular differentiation. Since its divergence from unicellular ancestors, Volvox has evolved into a highly integrated multicellular organism with cellular specialization, a complex developmental program, and a high degree of coordination among cells. Remarkably, all of these changes were previously thought to have occurred in the last 50-75 million years. Here we estimate divergence times using a multigene data set with multiple fossil calibrations and use these estimates to infer the times of developmental changes relevant to the evolution of multicellularity. Our results show that Volvox diverged from unicellular ancestors at least 200 million years ago. Two key innovations resulting from an early cycle of cooperation, conflict and conflict mediation led to a rapid integration and radiation of multicellular forms in this group. This is the only ETI for which a detailed timeline has been established, but multilevel selection theory predicts that similar changes must have occurred during other ETIs.