Bio / Environment

Tatsuhiro Ezawa

Microbial symbiosis triggered colonization of land by plants

Tatsuhiro Ezawa , Associate Professor

Research Faculty of Agriculture / Graduate School of Agriculture (Department of Bioscience and Chemistry, School of Agriculture)

High school : Saitama Kawagoe High School

Academic background : Graduate School of Agriculture, Hokkaido University

Research areas
plant physiology,microbiology
Research keywords
plant,microorganism,symbiosis,mycorrhiza,gene,degraded land

Microbial symbiosis boosted plant landing

Fig. 1. Soybean root colonized with Glomeromycotan fungi (upper). Plants take up inorganic phosphate (Pi) directly from the root (white letters) and from the mycorrhizal pathway (green letters) (lower).

In the Silurian period (about 400 million years ago), the plants living in the ocean began to colonize the land. Primitive land plants evolved from algae did not have robust roots like modern plants and thus were not good at taking up nutrients and water from the soil. Prior to plant colonization, filamentous fungi had already adapted to land; they took up nutrients and water through fine, long hyphae that allowed them to access soil solution and were tolerant of draught stress by developing thick cell wall and maintaining high-cellular osmotic pressure. The primitive land plants incorporated Glomeromycotan fungi that were well-adapted to the land environment into their roots (or root-like tissues) and obtained nutrients and water through them. This symbiosis between roots and fungi is referred to as mycorrhiza, and those that successfully associated with the fungi are considered to be the ancestors of modern land plants. Even now, most land plants still maintain this symbiosis and largely depend on their fungal symbionts for obtaining nutrients and water. When a root comes close, spores of Glomeromycotan fungi germinate and colonize the root. Then they construct hyphal networks in the soil, take up nutrients (mainly phosphate) and deliver these to the plants, and in turn the host plant supplies carbohydrates to the fungi as energy source (Fig. 1).


Molecular mechanism underlying mycorrhizal symbiosis: ultimate egoism

Fig. 2. Structural formula of polyphosphate (upper) and massive accumulation in hypha (green fluorescence).

Glomeromycotan fungi are obligate biotrophs that cannot complete their life cycle without a living host. In the roots, there is no competition with other microorganisms for the nutrients, and the fungi can exclusively occupy the niche. This comfortable environment might have allowed the fungi to lose the genes essential for free-living. The plants are capable of supporting the symbiotic fungi with their overwhelming productivity 'photosynthesis, while they depend on the fungi for nutrient acquisition, which seems to be more efficient than doing by themselves. This functional trade-off would be the reason why mycorrhizal symbiosis has been maintained for more than 400 million years.

Mycorrhizal plants have two pathways for phosphate uptake: the mycorrhizal pathway via the symbiotic fungi and the direct pathway from the root surface (Fig. 1). Once the symbiotic associations are established, genes involved in the mycorrhizal pathway are activated, while those involved in the direct pathway are inactivated, switching on the mycorrhizal pathway. Apparently, the symbiotic fungi are capable of accumulating a massive amount of phosphate that exceeds the amount they require, and this is achieved by polyphosphate. Polyphosphate is a linear chain of phosphate linked by high-energy bonds, which provides a large storage for phosphate in the cell (Fig. 2). Recent physiological and molecular studies have revealed that the fungi activate various genes involved in cation uptake during phosphate uptake. This is because phosphate is an anion, and the accumulation of anion causes accumulation of negative charge in the cell, which should be neutralized by cations, otherwise cellular homeostasis would be disturbed by negative charge.

Recent progress in the technologies for analyzing all genes in an organism has given us a comprehensive understanding of various cellular events in which expression of thousands of genes are dynamically and systematically changed. Thus modern biologists should have expertise in bioinformatics, that is, a mathematics-based analytical approach for elucidation of gene networks. It is expected that these technical breakthroughs will unveil the mysteries of the “selfish symbiosis” between plants and the fungi.


Mycorrhizal symbiosis as a hidden driver of terrestrial ecosystems: plays a significant role in restoration of degraded land

Fig. 3. Inhibition of Miscanthus sinensis root growth at pH3.2.

Glomeromycotan fungi are ubiquitously distributed in terrestrial ecosystems where plants are present. Accordingly, it is quite difficult to recognize their role in ecosystems. For example, Glomeromycotan fungi have already been playing a significant role in the nutrient uptake of crops in agricultural ecosystems, but farmers are rarely aware of it.

Fig. 4. Miscanthus sinensis grown near the creator of Sakurajima forms mycorrhiza.

Whereas once sulfur-rich rock is exposed by anthropogenic disturbance or natural disasters, a large amount of sulfuric acid is produced via oxidation of sulfur, generating strongly acidic soil. Mycorrhizal fungi are usually absent in such soils with no history of vegetation in which plant establishment (the restoration of vegetation) may be significantly delayed due to the absence of the fungi as well as the inhibition of root growth by a toxic level of aluminum ions in the soil (Fig. 3). Mycorrhizal formation, however, can rescue the plants; the fungi take over the damaged roots and provide an alternative pathway, the mycorrhizal pathway, for phosphate uptake. Recently, we isolated a highly acid-tolerant fungus that was found to be applicable to revegetation of strongly acidic soils on a commercial scale (see our website). The application of mycorrhizal fungi is likely to be a promising solution not only for the revegetation of acidic soils but also for that of soils contaminated with heavy metals or the slopes of active volcanoes (Fig. 4).