VA Mycorrhizae in Water

"Terrestrial plants are so much a part of the human experience that aquatic photosynthetic organisms are often overlooked."
-- Aquatic Photosynthesis, Falkowski and Raven 1997

       We have a fairly good understanding of VA mycorrhizae in terrestrial plants, although there are still countless questions to investigate in terrestrial systems.  Why, then, can't we apply that knowledge to aquatic plants?  In a few cases, we can.  Terrestrial and aquatic plants share some benefits of mycorrhizal infection, such as increased water uptake.  Even hydrophytes must deal with drought on occasion, and as in terrestrial plants, aquatic plants with mycorrhizal infection are thought to be considerably more drought resistant (but see Jurgensen et al. 1997 for how little we actually know about the ecological impacts of VA mycorrhizae in hydrophytes).  Hydrophytes most likely benefit from VA mycorrhizae's effect on soil structure, since soils with periodic flooding can become compacted, and mycorrhizal hyphae tend to hold soil particles in place (Nadian et al. 1996 in Smith and Read 1997). Mycorrhizae may also help anchor plants.  Hydrophytes with mycorrhizal infection may have increased rates of nutrient uptake as well (see Rickerl et al. 1994).  But this is where the considerable differences between mycorrhizal plants in terrestrial and aquatic soils begin.  Hydrophytes are not just wet terrestrial plants, and in order to understand them we must first understand their physiology.

 Leek root with aerenchymous air spaces, photo by Mark Brundrett     Most plants cannot survive periodic flooding.  Those that can survive react with growth responses that essentially separate them from areas of flooded soil and water.  Plants that cannot grow up out of the water, change their roots, or otherwise return themselves to an environment in which they are not surrounded by water, generally die.  As water level in soil rises, the amount of oxygen available for plant roots and for organisms living in the soil decreases (Laan et al. 1989b in Blom et al. 1996).  Hypoxia tends to develop as soil microorganisms consume what little oxygen is left in the soil, and oxygen diffusion from the surface slows.  Nitrification rate is inhibited, and toxic compounds are often formed as anaerobic bacteria use nitrate, manganese, and sulfate as alternative electron acceptors (Patrick and Mahapatra, 1968, Reddy et al. 1989).  In areas with periods of flooding and drydown, soil particles can settle between floods, increasing the mechanical resistance of the soil to growing roots (Blom et al. 1996).

 Willow root with stars indicating aerenchymous air spaces, photo by Mark Brundrett     In response to these changes in soil chemistry and structure, hydrophytes alter their root systems when in submerged soils. Plant cells need oxygen, whether they are photosynthetic or not, and root cells require oxygen in order to divide and grow. To ensure transport of oxygen to roots, flood-resistant plant species partially replace their root systems with aerenchymous tissue when flooded.  These new roots are characterized by aerenchyma formed by cell differentiation and collapse (lysigenous aerenchyma) or by cell separation without collapse (schizogenous aerenchyma) (Justin and Armstrong 1987, Blom et al. 1996).  This forms large continuous air spaces that allow diffusion of oxygen from shoot to root.  Of course, this system works best in plants that are also able to elongate their shoots during flooding, in order to raise leaves above the water level.  A build-up of ethylene is thought to contribute to this shoot elongation (Blom et al. 1996).  Plants such as Rumex spp. can replace more than 20% of their old roots with aerenchymous root after just two weeks of flooding. There appears to be a genetic component to flood resistance, since in this same study Rumex plants from low-lying areas had longer aerenchymous roots than Rumex from drier habitats (Blom et al. 1996).

Oxidized rhizosphere, taken from Reddy et al. (1989)     Some of the oxygen transported through the aerenchyma to plant root tips leaks out of pores in the root (pores result from aerenchyma formation) and into the surrounding soil.  This can result in a small zone of oxygenated soil around individual roots, called the oxidized rhizosphere (Armstrong and Armstrong 1988 in Blom et al. 1996).  Oxygen-depleted soils can reach almost original oxygen concentrations around plant roots (Blom et al. 1996). This oxidized rhizosphere allows normal root metabolism to occur, even in flooded soils (Engelaar et al. 1991, 1993a in Blom et al. 1996).  The absorption of toxic manganese and sulfur compounds which build up in anaerobic sediments is partially blocked by the oxidized rhizosphere, which provides a zone around roots in which toxic compounds can be oxidized into less harmful forms. The oxidized rhizosphere also has a major effect on the two nutrients that most often limit hydrophyte growth, phosphorus (P) and nitrogen (N) (Barko et al. 1991)..  Hydrophytes have a second potential source for phosphorus and nitrogen uptake, the surrounding water, but take up the majority of their P and N from aquatic sediments (Barko et al. 1991). Nutrient uptake in aquatic sediments is often limited by the slow rate of N and P diffusion over low-density organic sediments as opposed to terrestrial soils (Drew and Lynch 1980 in Barko et al. 1991, Patrick and Mahapatra, 1968). In normal aquatic sediments, this slow rate of diffusion is counteracted by the higher amounts of soluble N and P compounds in the soil, but this is not the case in the oxidized rhizosphere. Aerenchymous roots provide root cells with much-needed oxygen, but can rob them of nutrients by forming insoluble phosphorus and nitrogen compounds when excess oxygen leaks from the roots (Tessenow 1978, Baynes 1978 in Barko et al. 1991). The hydrophyte Hydrilla verticillata, for example, was found to reduce sediment nitrogen concentrations by more than 90%, and phosphorus concentrations by more than 30%, over a matter of weeks (Barko et al. 1988 in Barko et al. 1991). Transport of nutrients to shoots and leaves of hydrophytes also contributes to sediment nutrient depletion, at least until the plants later decompose. Since nutrient levels can play a major role in determining the extent of VA mycorrhizal infection in terrestrial plants, and under some conditions can even result in parasitic rather than mutualist infection , it seems likely that nutrient levels play a similarly important role in determining infection in hydrophytes (Johnson 1993). 

     Nutrient levels, however, do not most severely limit the distribution and spread of VA mycorrhizae in hydrophytes. Oxygen concentration is thought to play a larger role in determining VA mycorrhizal distribution in aquatic sediments. VA mycorrhizae are assumed to be obligate aerobes, although as Andre Cantelmos and Joan Ehrenfeld most recently pointed out, this assumption has never been tested (1999).  Read and Armstrong (1972) came closest to explicitly testing this hypothesis, but their conclusions about ectomycorrhizae may not apply to VA mycorrhizae.  If VA mycorrhizae can only survive in oxygenated environments, it was thought, they cannot grow in completely flooded soils.  Several researchers have shown that this is not the case, that hydrophytes in submerged soils can develop substantial mycorrhizal infection (Keeley 1980, Cooke and Lefor 1998, Fennessy and Marx unpublished data 1999).  Yet mycorrhizal infection varies vertically in submerged soils (Cooke et al. 1993). If mycorrhizae do not need oxygen to survive, why are they limited to certain areas of submerged hydrophyte roots?  The few studies that have addressed these questions suggest that VA mycorrhizae may be dependent on the presence of an oxidized rhizosphere, but not necessarily confined by its area (Keeley 1980, Cantelmos and Ehrenfeld 1999). The range of oxygen concentrations in which VA mycorrhizae can survive, and whether or not such a range limits their distribution, is unknown. Knowing whether or not VA mycorrhizae are constrained by the oxidized rhizosphere will help answer important questions about the role of VA mycorrhizae in hydrophyte community dynamics. For a description of some of the research examining these questions, see Where do we go from here?