|Mycorrhizal symbiosis and plant responses to the environment
by Robert M. Augé
Root systems of crop and native plants are commonly colonized by one or more mycorrhizal fungi, naturally occurring soil fungi that increase nutrient absorption and improve soil structure. The hyphae of arbuscular mycorrhizal fungi penetrate roots and grow extensively between and within living cortical cells, forming a very large and dynamic interface between symbionts. The hyphae also extend from root surfaces into the surrounding soil, binding particles and increasing micro- and macro-aggregation.
We have been studying the influence of arbuscular mycorrhizal symbiosis on the water relations and drought responses of host plants. Mycorrhizal fungi often change the rate at which water moves into, through and out of plants. The symbiosis may improve plant resilience to drought, salinity, and other environmental stresses.
We began by determining that these soil fungi can change the stomatal behavior of their hosts, independently of affecting host phosphorus nutrition and during nonstress conditions (Augé et al. 1986a). We then learned that this symbiosis between rose roots and Glomus intraradices and G. deserticola can allow leaves to maintain a more normal water balance (closer to responses of unstressed controls), and fix more carbon, during drought stress (Augé et al. 1987a). We also noted what others had reported as perhaps the most consistent effect of mycorrhizal symbiosis on host water balance: higher transpiration at similar, low soil water potential (Augé 1989). Mycorrhizal effects appeared to be linked to changes in leaf osmotic (Augé et al. 1986b) and elastic (Augé et al. 1987b) properties.
We learned next that the mycorrhizal influence was not confined to foliage; the water balance of roots, too, was affected. Changed root turgors were apparently not related to osmotic adjustment [even though the fungi altered levels of key root solutes (Augé et al. 1992b)] but to changed apoplastic/symplastic water partitioning ((Augé and Stodola 1990). We also learned that mycorrhizal fungi affect can stomatal response when soil water potential is lowered not only via drought, but osmotically (Augé et al. 1992), suggesting that mycorrhizal root systems either scavenged water of low activity more effectively or influenced so-called nonhydraulic root-to-shoot communication differently (see below) than non-infected root systems. Phosphorus nutrition was probably not involved in the mycorrhizal mechanism of influence (Duan and Augé 1992).
In the late 1980's, plant drought physiologists been reporting in earnest about an exciting new theory claiming "nonhydraulic" or chemical control of stomata and leaf growth. Mycorrhizal symbiosis had previously been shown to modify host hormonal relations, so we began to investigate the possibility that these fungi, which are confined to roots and do not even penetrate the root stele, were affecting distant organs like leaf stomata by changing the chemical or hormonal flow of information from roots to shoots in the transpiration stream. We first determined that rose plants having divided root systems -- one half nonmycorrhizal, one half mycorrhizal -- displayed different stomatal conductances upon partial drying, depending on whether mycorrhizal or nonmycorrhizal roots were dried (Augé and Duan 1991).
We determined that mycorrhizal symbiosis can eliminate or lessen the inhibitory effects of drought-induced nonhydraulic root-to-shoot signaling on leaf growth of sorghum (Ebel et al. 1994) and maize (Augé et al. 1994). We next compared the influence of different fungi on the drought-induced
nonhydraulic signaling process, and compared mycorrhizal influence on the signal with the influence of other host and soil factors commonly associated with mycorrhizal symbiosis (Augé et al. 1995). Sometimes, mycorrhizal fungi cause different effects on the way nonhydraulic signals regulate stomatal conductance and leaf growth during drought (Ebel et al. 1996). We had extended our investigations of mycorrhizal effects on the flow of information from roots to shoots during soil drying to simultaneous measurements of hydraulic signals (e.g. shoot water potential) and chemicals signals (xylem ABA, cytokinins, pH, calcium and phosphorus concentrations) (Duan et al. 1996, Ebel et al. 1997). Recently, we determined that some residual mycorrhizal effect remains in detached leaves of rose plants, but that the mycorrhizal enhancement of stomatal conductance observed in cowpea leaves disappeared when leaves were no longer in physical contact with the mycorrhizae-to-shoot transpiration stream (Green et al. 1998).