Green algae—the nexus of plant/animal ancestry

Genes of a tiny, single-celled green alga called Chlamydomonas reinhardtii may contain scores more data about the common ancestry of plants and animals than the richest paleontological dig. This work is described in an article in the October 12, 2007, issue of Science.

A group of researchers*, including Arthur Grossman of the Carnegie Institution, report on the results of a major effort to obtain the full library of genes, or the genome sequence, of Chlamydomonas and to compare its ~15,000 genes to those of plants and animals, including humans. The research shows that this alga has maintained many genes that were lost during the evolution of land plants, has others that are associated with functions in humans, and has numerous genes of unknown function, but which are associated with critical metabolic processes.

“Although Chlamydomonas is certainly more plant than animal, there are clear similarities between this photosynthetic organism and animals that would surprise the average person on the street,” comments Grossman. “Just twenty years ago no one would have guessed that an alga would have retained many of the functions we associate with humans and would be useful for developing a basic understanding of certain human diseases.”

Chlamydomonas, affectionately called Chlamy, is an alga of 10 micrometres in size that is present in soil and freshwater environments. It performs photosynthesis like plants, but it diverged evolutionarily from flowering land plants about 1 billion years ago. It is even more distantly related to animals (the split between animals and plants was ~1.6 billion years ago). Chlamy moves using two anterior, hair-like flagella that were lost by its cousins, the flowering land plants, after the evolutionary split of the two lineages. The flagella are equivalent to the cilia and centrioles in animal cells. Centrioles are structures involved in cell division; they form a spindle apparatus, which helps separate genetic material into two new cells during mitosis. Cilia are important to many animal functions.

The study identified many new proteins that are likely associated with the flagella, and has distinguished those proteins of the flagella that are critical for movement and those that are associated with sensory functions (feeling the conditions in the environment). The analysis has also generated new insights about human diseases associated with ciliary dysfunction in humans, including those of the kidney and the eye.

The researchers also performed a comparative gene analysis across species to explore the evolutionary history of Chlamy, and the relationship of this alga to other organisms. Of the 6,968 protein families that have so-called homologs —proteins that have similar amino acid sequences, often reflecting a similar or related function among the species — they found that Chlamy shared 35% (2,489/6,968) with both flowering plants and humans, and an additional 10% (706/6,968) with humans but not with flowering plants.

In addition, there are numerous proteins in Chlamy that make it suited to live in soil environments, including large families of specific transporters—proteins that help move material across cell membranes— that enable it to scavenge nutrients from the soil. While some of these transporters have an affiliation with transporters in plants, others are more closely related to those in animals. Moreover, the Chlamy genome encodes many families of regulatory elements, including one that contains over 50 guanylyl/adenylyl cyclases-- enzymes probably involved in distinct developmental processes including mating and sexual signaling. There are also numerous genes and gene families that relate to making sugars and polysaccharides, to use the sugars and polysaccharides to produce energy and to build a highly structured and efficient chloroplast, the factory where the cell harnesses the energy of sunlight.

Indeed, many great insights from the genome analysis have come in the area of photosynthesis, the process of the chloroplast by which plants convert carbon dioxide, water and the energy of sunlight into oxygen and sugars. In a comparative genomic analysis, the scientists identified protein families that are shared by Chlamy, flowering plants, other algae, but are not present in nonphotosynthetic organisms. This exercise led them to identify photosynthesis-related proteins conserved across the plant kingdom, with many even conserved in the ancient cyanobacteria. (Cyanobacteria have been on the planet for ~3 billion years.) The majority of the identified proteins have unknown functions, but are probably critical since they have been exclusively maintained in photosynthetic organisms over nearly the entire period that life has inhabited the Earth.

As Grossman states, “The work has generated a clear roadmap for exploring the roles of numerous genes in photosynthetic function, for defining the structure and dynamic aspects of flagellar function and for understanding how the soil environment, with its large fluctuations in nutrients, has molded the functionality of organisms through evolutionary time.”

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Acknowledgements: While most of the sequence analysis was supported by DOE and the Joint Genome Institute, some aspects of the work were supported by The Chlamydomonas Genome Grant, NSF Grant MCB 0235878 awarded to ARG.

* Authors on the paper are Sabeeha Merchant, UCLA; Simon Prochnik USDOE, Joint Genome Institute; Olivier Vallon, CNRS, Université Paris 6; Elizabeth Harris, Duke University; Steven Karpowicz, UCLA; George Witman, University of Massachusetts Medical School; Astrid Terry, USDOE Joint Genome Institute; Asaf Salamov, USDOE Joint Genome Institute; Lillian Fritz-Laylin, UC Berkeley; Laurence Marechal-Drouard, Institut de Bioloigie Moléculaire des Plantes; Wallace Marshall, UC San Francisco; Liang-Hu Qu, Zhongshan University, Guangzhou, China; David Nelson, University of Tennessee; Anton Sanderfoot, University of Minnesota; Martin Spalding, Iowa State University; Vladimir Kapitonov, Genetic Information Research Institute; Qinghu Ren, Institute for Genome Research; Patrick Ferris, Salk Institute; Erika Lindquist, USDOE Joint Genome Institute; Harris Shapiro, USDOE Joint Genome Institute; Susan Lucas, USDOE Joint Genome Institute; Jane Grimwood, Stanford University School of Medicine; Jeremy Schmutz, Stanford University School of Medicine; Chlamydomonas Annotation Team, JGI Annotation Team; Igor Grigoriev, USDOE, Joint Genome Institute; Daniel Rokhsar, USDOE, Joint Genome Institute and UC Berkeley; Arthur Grossman, Carnegie Institution Department of Plant Biology.