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Glomus deserticola on rose root


Our work deals with protecting plants and soils from environmental stresses: understanding how things like drought, too much shade, and saline irrigation water injure plants and reduce health and vigor. We also study how plants cope with stress, and in particular how one beneficial, naturally-occurring soil organism helps protect both plants and soils.

Mycorrhizal symbiosis and plant responses to the environment  

Root systems of crop and native plants (including nursery trees) are commonly colonized by one or more mycorrhizal fungi, naturally occurring soil fungi that increase nutrient absorption and that may provide a measure of stress resistance to the host. 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.

Mycorrhizal fungi and agricultural sustainability
Mycorrhizal Literature Exchange

Water relations and drought resistance

We have been studying the influence of arbuscular mycorrhizal symbiosis on the water relations of host plants. At the time we began, some good work with soybean, onion and citrus had led scientists to suspect that mycorrhizal effects on foliar water relations parameters such as gas exchange and leaf water potential were simply an indirect result of mycorrhizal improvement of phosphorus nutrition.

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; Kubikova et al. 2001) 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). Colonization of roots by Glomus intraradices does not appear to affect the lethal foliar dehydration tolerance of host plants (Augé et al. 2001).

We have determined that mycorrhizal effects on host stomatal behavior appear to vary with temperature and irradiance (Augé et al. 2004).

We have also learned that the often higher stomatal conductance of mycorrhizal leaves is tied to slightly higher water potential gradients across leaves, consistent with the higher rates of gas exchange necessary to supply the carbon needs of the fungal symbiont (Augé et al. 2008).

Using meta-analysis to get a quantitative overview across the literature of mycorrhizal influences on stomatal conductance shows that dicotyledonous hosts, especially legumes, have been slightly more responsive to AM symbiosis than monocotyledonous hosts, and C3 plants have shown over twice the AM-induced promotion of stomatal opening as that seen in C4 plants. The extent of root colonization is important, with heavily colonized plants showing ×10 the promotion of stomatal conductance as lightly colonized plants. AM promotion has been larger in growth chambers and in the field than in greenhouse studies, almost ×3 as large when plants were grown under high light than low light, and ×2.5 as large in purely mineral soils than in soils having an organic component (Augé et al. 2014).

Root to shoot signaling

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). We have 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).

Salt stress

AM plants are often more resistance to salt stress than nonAM plants, and we tested the idea that part of the reason the symbiosis confers drought resistance to host plants is related to increased resistance to the salt stress that occurs as solutes concentrate in drying soils (Cho et al. 2006). Looking at mycorrhizal influence on osmotic adjustment across the literature, a meta-analysis determined that AM symbioses have had marked effects on plant K+, increasing root and shoot K+ concentrations by an average of 47 and 42%, respectively, and root and shoot K+/Na+ ratios by 47 and 58%, respectively. Among organic solutes, soluble carbohydrates have been most impacted, with average AM-induced increases of 28 and 19% in shoots and roots. The symbiosis has had no consistent effect on several characteristics, including root glycine betaine concentration, root or shoot Cl− concentrations, leaf Ψπ, or shoot proline or polyamine concentrations (Augé et al. 2014).

Soil effects

We have determined that mycorrhizal symbiosis can also modify the water relations of soils (Augé et al. 2001). Some findings support the assertion that colonization of soil may play as important a role as colonization of roots regarding how AM symbiosis affects the water relations of host plants (Augé et al. 2004, Augé 2004). Hyphal development in soil has been better correlated with mycorrhiza-induced effects on plant drought resistance (Augé et al. 2003) and stomatal conductance (Augé et al. 2007) than hyphal development in roots.

Reviews: Augé 2000, Augé 2001, Augé 2004, Augé and Moore 2005.

Dogwood stomate

Nonhydraulic root-to-shoot signaling of soil drying

We first became interested in root-sourced, chemical regulation of stomatal behavior during drought as a way of explaining mycorrhizal effects on host plant water relations (Augé and Duan 1991). In subsequent investigations, we confirmed that stomatal opening and leaf growth can be inhibited during drying in the absence of perturbations in leaf water status, in several herbaceous and woody species.

We learned that the comparative sensitivity of stomata and leaf growth to nonhydraulic signals is species-specific, possibly linked to the ecophysiological tendencies for species to resist drought by tolerance or avoidance (Ebel et al. 1994, Augé et al. 1994, Ebel et al. 1996). We have related the magnitude of the signal's influence to the product of days roots dried x mass of roots drying (Ebel et al. 1994), and we have compared the relative influences of several plant and environmental characteristics on the magnitude of the nonhydraulic signal's inhibition of growth during drought (Augé et al. 1995). We have compared hydraulic and nonhydraulic factors implicated in control of stomata during soil drying (Duan et al. 1996).

We have also attempted to characterize the ecophysiological significance of nonhydraulic root-to-shoot signaling of soil drying by correlating the relative sensitivity of several tree species to the nonhydraulic signal (Croker et al. 1998; Augé and Moore 2002) with species tendencies toward drought avoidance vs. tolerance (Augé et al. 1998). We have investigated the relative roles of hydraulic and hormonal signals in regulation of stomata in temperate forest trees (Augé et al. 2000, Augé 2003) and urban trees (Johnson et al. 2001)

Lethal leaf water potential experiment: native trees

Dehydration tolerance

Because of our interest in the ecophysiological implications of species sensitivity to so-called nonhydraulic root-to-shoot signals of soil drying (Croker et al. 1998), we have characterized the relative drought avoidance/tolerance of several native, ornamental and agronomic plant species (Chapman and Augé 1994; Kubikova et al. 2001; Augé et al. 1998; Augé et al. 2001; Augé et al. 2003). We suspect that species that tend to resist drought by avoiding it rather than tolerating it are species that have strong relative sensitivity to the nonhydraulic signal: stomatal closure at relatively high soil water content, and ultimately relatively large degrees of stomatal inhibition (Augé and Moore 2002).

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