August 28, 2006

Role of fungi in the establishement of land plants

The paramount role of fungi in the establishement of plants on land

Nourou S. Yorou

Depart Biologie I and Geo-Bio Center, Biodiversity Research group: Section Mycology. Menzinger Str. 67, 80638, Munich, Germany. email: yorou2001@yahoo.fr

Recent studies of the best-known early fossil land ecosystem, the so called Rhynie-Chert of Scotlands, gave evidence of the early-stage mycorrhizal relationship between the first land plant and the members of the fungal group Glomeromycota. Life started in water as stated by various publications but when the first vascular plants started colonizing lands at least in late Silurian (ca 440 Million ago), they were already on Land many others organisms such as bacteria, cyanobacteria, algae, non-vascular plants, all class of fungi without Basidiomycota, lichen-like plants and several animals (mites, spiders, collembola, crustaceae and nematodes). Aquatic plants that were living in water used to take all nutrients, O2 and CO2 from surrounding medium via diffusion, no special organs like roots or stomata were necessary. Neither stabilisation system nor cuticles were required and the floating aquatic plants were not so strong enough to become best candidates for land colonisation. How did the early lands plants succeed in establishing themselves on land? Did they have assistance and which organisms provided them with assistantship?

The Rhynie-Chert: The earliest Land Ecosystems

The well-known earliest fossilised land ecosystem is the so called Rhynie-Chert, near the small village Rhynie in the Gramping Region of Scotland. Recent radiometric dating give an age of ca 400 millions years that corresponds with the Lower Devonian age. The Rhynie-Chert was a hot spring ecosystem, consisting of hot lakes of SiO2 water surrounded by low marshy vegetations of early land plants. The perfect conditions provided a whole ecosystem fossilised in-situ. The importance of the Rhynie-Chert lead not only because it's the oldest fossilised land floras, but also that it holds remarkable diversity of palaeozoic organisms that are well preserved anatomically and in life position showing all organism interactions. More early and less importantly fossilised land floras include those of Gaspé in New Bronswick in Canada and the Devon des Siegerlands of the Rheinische Schiefergebirge in Germany.

Early land plants and fungi

When did the first plants leave water and how did they do it remain open questions? However, leaving water to live on lands suppose great anatomical modifications including evolvement of roots and roots-like organs (like Rhizoids) and water transport vessels, stronger membranes plus cuticles but also wood for stabilisation and special pores and stomata for transpiration and photosynthesis. The earliest Land plant had indeed creeping rhizomes and upright, dichotomous branched stems. The earliest fossil of this primitive land was called Cooksonia. It looks similar to today's Psilotum or Tmesipteris-fern and was not a vascular plant at all. 7 vascular plants are however known from the Lower Devonian among them Rhynie gwynne and Aglaophyton major, both with creeping structure cluster to the rhizoid. Microslides of rhizomes and even stems showed a clear mycorrhizal layers and an outer cortical layer and gives then evidence of the fungal colonisation since this state. At which time do the colonisation occur, whether already in aquatic condition or once on land, remains unknown. The fungus, which was called Glomites (ancien Glomus), did not grow intracellularic, it forms arbuscular-like structures and as the colonisation patterns of this fungi is similar to the recent arbuscular endomycorhizae, it is assumed to have mycorrhizal symbiosis with Rhinia and Aglaophyton. The fungal type-specie is called Glomites rhyniensis (Taylor et al., 1995).

Fungi are assumed to colonise land about 100 million years earlier than plants did, however no fossil evidence is given. Rhynie-Chert provides excellent preserved fungal fossils that were living in the early land ecosystems of the Lower Devonian. The mycorrhizal morphology and the colonisation pattern of the early fungi with the early land plants is identical to modern arbuscular endomycorrhizae of Glomeromycota. Further, the oldest knowm Ascomycota are found in Rhynie-Chert, too (Taylor et al., 1999) and seems to be 100 million years older.

In summary, the all modern division of fungal kingdom (perhaps except only the Basidiomycota whose existence in Devonian is still questionable) were already present in the earlier terrestrial ecosystems like the Rhinie-Chert and they all kept interactions in a way or another with other organisms. This is also evidence of the oldness of symbiosis relationship that appear to be settle since first life forms. If we admit that fungi were also present on Land ecosystems maybe long time before plants, what could be their relevance for plants establishment on lands. Otherwise, what is the significance and effectiveness of colonisation of early land plants by fungi?

Symbiotic relationships

Remembering that the Lower Devonian land plants had no real roots but only small, filamentous rhizoids of only few cm, there is no doubt that their fungal partners (Glomites) enlarged the plant's expansion capacity into soils, since the fungus hyphal network covers greater areas, spreads in the soils and reaches even into very fine caves of bare rocks. From these fine rock layers, the glomeran fungi should have been able to acquire N and P and provides them to their plant partners, and then the plant should have offer them with assimilated products. It has been shown that Arbuscular mycorrhizae improve plant nutrition, enhance productivity, contribute to soil aggregation and soils structures. It is much likely that the glomeran fungi played such role for early land plants. More importantly, they should have protect those plants from roots pathogen when remembering that before plant colonised the lands, many microbes were already present. The mycorrhizal structures of the glomeran fungi did certainly act as roots for early land plants, both should have co-involved in the evolution of roots (Brundrett, 2002)

Influence of parasitic fungi

Pathogenic fungi and other microbes were already present on land before plant started their colonisation. Pathogenic fungi should have played an important role for the adaptation of aquatic plants to terrestrial conditions. Collinge et al (1997) proved that the presence of phytopathogens lead to strong reactions of the plants, resulting in stronger membranes and thicker cuticles and that they promote the lignification of plant cells. The morphological adaptation were then necessary to enable life on lands and there is no doubt that early plants need this adaptation strategies. But it raises up then the question, which relationship, symbiontic or parasitical one occurs firstly? as previously stated, first land plants were weak, had thin membrane and were highly water permeable, they must have undoubtedly been high attractive substrates for living pathogens fungi of soils. Indeed, land plant fossils are heavily infected by endophytic fungi. The first association may have been parasitic one, but then from this the symbiontic relationship were supposed to have evolved. Anyway the most important role devoted to pathogen fungi of the Lower Devonian is the enhancement of the lignifications of early land plants. Further, soil saprotrophic and parasitic fungi are assumed to be involved in the soil formation. By recycling dead organic materials, accumulating organic substances and by dissolving minerals from the bare rocks through various enzymes. Soils fungi were assumed to play an important role in the early soil and humus formation of the Rhynie-Chert ecosystems.

In summary, higher plants life on lands would have not been possible without the aid of fungi, indirectly by forming the soil for plants to grow and directly through the obligate mycorrhizal relationship. On the nutrient-poorly bar soil of the so far non-colonised Land, it would have been quiet impossible for a plant with small rhizoid to get all required nutrients. Whether the relationship was established since aquatic state of the plants or once on land remains questionable. Anyway, there is no more doubt that symbiotic relation between plants and fungi date back to early land plants and both groups of living organisms are co-involved in an evolution process. This wonderful way of life survive up to know and did not change at all. More than 90% of higher plants still trust and depend on this symbiotic relation. Indeed, most plants don't have roots, they do have rather mycorrhizae.

References

Brundrett M. C. 2002. Coevolution of roots and mycorrhizas of land plants. New Phytolgist 154 (2): 275-304

Collinge D. B., Bryngelsson, T., Gergersen, P. L., Smedegaard-Petersen V. & Thordal-Christensen H., 1997. Resistance against frungal pathogns: its nature and regulation. In Basra A. S., Basra R.K.: Mechanisms of environmental Stress Resistance in Plants. Harwood Academic Publishers, London: 335-372

Taylor T. N., Remy W., Haas H. & Kerp H., 1995. Fossil arbuscular mycorrhizae from the early Devonian. Mycologia 87 (4): 560-573

Taylor T.N., Hass H. & Kerp H. 1999. The oldest fossil ascomycetes. Nature 399, 648

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