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2003 Annual Science Report

University of Colorado, Boulder Reporting  |  JUL 2002 – JUN 2003

Symbiosis and the Origin of Multicellularity in Photosynthetic Organisms

4 Institutions
3 Teams
0 Publications
0 Field Sites
Field Sites

Project Progress

Symbioses, the mutually beneficial relationships between two organisms, have evolved numerous times over the course of the evolutionary history of life on Earth. Different forms of symbiosis have resulted in some of the most profound evolutionary radiations; e.g., the origin of the mitochondrion from a symbiosis of a proteobacterium with early eukaryotes, the origin of the chloroplast from a symbiosis of a cyanobacterium with an originally heterotrophic eukaryote resulting in the evolution of all photosynthetic lines of eukaryotes, and the establishment of multicellular photosynthetic organisms (plants) in terrestrial environments from a symbiosis of a fungus and a green alga.

We are characterizing the fungal symbiotic partners that may have been critical to the colonization of terrestrial environments on Earth by photosynthetic organisms. Using deoxyribonucleic acid (DNA) extraction and amplification techniques, we have begun to identify the fungal lineages that currently play a central role in the widespread symbiosis between plants and fungi (mycorrhizal association). We have chosen to work with phylogenetically basal land plant lineages so that we can reconstruct the evolutionary history of this key symbiosis. During the last year, we have discovered a complex relationship between early lineages of multicellular land plants and their fungal partners. During part of the life cycle of ancient lineages of land plants, the fungal symbiotic partner appears to supply mineral nutrients to the host plant and in return, the fungus receives fixed carbon from the plant. During another component of the plant’s life cycle, the symbiosis involves an entirely different fungal partner and in this symbiosis, the plant is essentially a parasite on the fungus, receiving fixed carbon and mineral nutrients from the fungus. Thus, we are beginning to piece together a complex set of symbiotic relationships between early land plants and their fungal symbionts.

During years four and five of the currently funded NASA University of Colorado Astrobiology Program, we (Ph.D. candidate Jennifer Winther and I) began to identify (in essence, discover) some of the fungal species that grow symbiotically within the bodies of ancient lineages of plants. We have exploited genomic small subunit ribosomal DNA (18S rDNA) and genomic ribosomal internal transcribed spacers (ITS) sequences to identify the biotypes of the fungal symbionts of early land plant lineages. Based on comparisons to databased sequences, all of the sequenced mycorrhizal fungi in ancient lineages of land plants we have studied to date belong to the genus Glomus, the same group of fungi that form symbiotic associations in most other (and recently evolved) lineages of land plants. This is the first time that mycorrhizal symbioses in early lineages of land plants have been documented on the basis of the DNA sequence identity of the fungal symbiont. Our preliminary data provide some of the first concrete molecular evidence that the extremely widespread mycorrhizal symbiosis found in extant plants may have arisen during (and potentially enabled) the earliest phases of the colonization of land by plants.

We now have evidence that approximately 75 million years after the original colonization of land by plants, and concurrent with the first increase in land plant stature from centimeters to meters, part of the life cycle of land plants became entirely subterranean (and strictly heterotrophic). This extreme alteration in the ecology of early plants appears to have been accomplished through an alteration of the symbiotic relationship of plants to their fungal partners. In essence, the flow of organic carbon from the plant to the fungus was reversed, and the plant became a parasite upon the fungus and its carbon (ultimately derived from fungal connections with other plants that are photosynthesizing). This type of subterranean habitat during a major portion of the life cycle of plants still exists today and is widely found in ancient lineages of plants. In these lineages of extant plants, the entirely subterranean heterotrophic phase of the life cycle may be as long as 15 years.

    William Friedman William Friedman
    Unspecified Role
    Jennifer Winther

    Joseph Williams

    Objective 4.2
    Foundations of complex life

    Objective 5.1
    Environment-dependent, molecular evolution in microorganisms

    Objective 5.2
    Co-evolution of microbial communities

    Objective 6.1
    Environmental changes and the cycling of elements by the biota, communities, and ecosystems