Robert M. Augé

Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis

Abstract Vesicular-arbuscular mycorrhizal fungi can affect the water balance of both amply watered and droughted host plants. This review summarizes these effects and possible causal mechanisms. Also discussed are host drought resistance and the influence of soil drying on the fungi.

Moisture retention properties of a mycorrhizal soil

The water relations of arbuscular mycorrhizal plants have been compared often, but virtually nothing is known about the comparative water relations of mycorrhizal and nonmycorrhizal soils. Mycorrhizal symbiosis typically affects soil structure, and soil structure affects water retention properties; therefore, it seems likely that mycorrhizal symbiosis may affect soil water relations. We examined the water retention properties of a Sequatchie fine sandy loam subjected to three treatments: seven months of root growth by (1) nonmycorrhizal Vigna unguiculata given low phosphorus fertilization, (2) nonmycorrhizal Vigna unguiculata given high phosphorus fertilization, (3) Vigna unguiculata colonized by Glomus intraradices and given low phosphorus fertilization. Mycorrhization of soil had a slight but significant effect on the soil moisture characteristic curve. Once soil matric potential (Ψm) began to decline, changes in Ψm per unit change in soil water content were smaller in mycorrhizal than in the two nonmycorrhizal soils. Within the range of about −1 to −5 MPa, the mycorrhizal soil had to dry more than the nonmycorrhizal soils to reach the same Ψm. Soil characteristic curves of nonmycorrhizal soils were similar, whether they contained roots of plants fed high or low phosphorus. The mycorrhizal soil had significantly more water stable aggregates and substantially higher extraradical hyphal densities than the nonmycorrhizal soils. Importantly, we were able to factor out the possibly confounding influence of differential root growth among mycorrhizal and nonmycorrhizal soils. Mycorrhizal symbiosis affected the soil moisture characteristic and soil structure, even though root mass, root length, root surface area and root volume densities were similar in mycorrhizal and nonmycorrhizal soils.

Hydraulic conductance and water potential gradients in squash leaves showing mycorrhiza-induced increases in stomatal conductance.

Stomatal conductance (gs) and transpiration rates vary widely across plant species. Leaf hydraulic conductance (kleaf) tends to change with gs, to maintain hydraulic homeostasis and prevent wide and potentially harmful fluctuations in transpiration-induced water potential gradients across the leaf (ΔΨleaf). Because arbuscular mycorrhizal (AM) symbiosis often increases gs in the plant host, we tested whether the symbiosis affects leaf hydraulic homeostasis. Specifically, we tested whether kleaf changes with gs to maintain ΔΨleaf or whether ΔΨleaf differs when gs differs in AM and non-AM plants. Colonization of squash plants with Glomus intraradices resulted in increased gs relative to non-AM controls, by an average of 27% under amply watered, unstressed conditions. Stomatal conductance was similar in AM and non-AM plants with exposure to NaCl stress. Across all AM and NaCl treatments, kleaf did change in synchrony with gs (positive correlation of gs and kleaf), corroborating leaf tendency toward hydraulic homeostasis under varying rates of transpirational water loss. However, kleaf did not increase in AM plants to compensate for the higher gs of unstressed AM plants relative to non-AM plants. Consequently, ΔΨleaf did tend to be higher in AM leaves. A trend toward slightly higher ΔΨleaf has been observed recently in more highly evolved plant taxa having higher productivity. Higher ΔΨleaf in leaves of mycorrhizal plants would therefore be consistent with the higher rates of gas exchange that often accompany mycorrhizal symbiosis and that are presumed to be necessary to supply the carbon needs of the fungal symbiont.

Relating foliar dehydration tolerance of mycorrhizal Phaseolus vulgaris to soil and root colonization by hyphae

Mycorrhizal symbiosis can modify plant response to drying soil, but little is known about the relative contribution of soil vs. root hyphal colonization to drought resistance of mycorrhizal plants. Foliar dehydration tolerance, characterized as leaf and soil water potential at the end of a lethal drying episode, was measured in bean plants (Phaseolus vulgaris) colonized by Glomus intraradices or by a mix of arbuscular mycorrhizal fungi collected from a semi-arid grassland. Path analysis modeling was used to evaluate how colonization rates and other variables affected these lethal values. Of several plant and soil characteristics tested, variation in dehydration tolerance was best explained by soil hyphal density. Soil hyphal colonization had larger direct and total effects on both lethal leaf water potential and soil water potential than did root hyphal colonization, root density, soil aggregation, soil glomalin concentration, leaf phosphorus concentration or leaf osmotic potential. Plants colonized by the semi-arid mix of mycorrhizal fungi had lower lethal leaf water potential and soil water potential than plants colonized by G. intraradices. Our findings support the assertion that external, soil hyphae may play an important role in mycorrhizal influence on the water relations of host plants.

Nonhydraulic signalling of soil drying in mycorrhizal maize

Our objectives were to (1) verify that nonhydraulic signalling of soil drying can reduce leaf growth of maize, (2) determine if a mycorrhizal influence on such signalling can occur independently of a mycorrhizal effect on leaf phosphorus concentration, plant size or soil drying rate, and (3) determine if leaf phosphorus concentration can affect response to the signalling process. Maize (Zea mays L. ‘Pioneer 3147’) seedlings were grown in a glasshouse with root systems split between two pots. The 2 x 3 x 2 experimental design included two levels of mycorrhizal colonization (presence or absence of Glomus intraradices Schenck & Smith), three levels of phosphorus fertilization within each mycorrhizal treatment and two levels of water (both pots watered or one pot watered, one pot allowed to dry). Fully watered mycorrhizal and nonmycorrhizal control plants had similar total leaf lengths throughout the experiment, and similar final shoot dry weights, root dry weights and leaf length/root dry weight ratios. Leaf growth of mycorrhizal plants was not affected by partial soil drying, but final plant leaf length and shoot dry weight were reduced in half-dried nonmycorrhizal plants. At low P fertilization, effects of nonhydraulic signalling were not evident. At medium and high P fertilization, final total plant leaf length of nonmycorrhizal plants was reduced by 9% and 10%, respectively. These growth reductions preceded restriction of stomatal conductance by 7 d. This and the fact that leaf water potentials were unaffected by partial soil drying suggested that leaf growth reductions were nonhydraulically induced. Stomatal conductance of plants given low phosphorus was less influenced by nonhydraulic signalling of soil drying than plants given higher phosphorus. Soil drying was not affected by mycorrhizal colonization, and reductions in leaf growth were not related to soil drying rate (characterized by time required for soil matric potential to drop below control levels and by time roots were exposed to soil matric potential below typical leaf water potential). We conclude that mycorrhizal symbiosis acted independently of phosphorus nutrition, plant size or soil drying rate in eliminating leaf growth response to nonhydraulic root-to-shoot communication of soil drying.

Stomatal response to nonhydraulic root-to-shoot communication of partial soil drying in relation to foliar dehydration tolerance

Abstract This paper culminates a series of works to: (1) compare stomatal response of several temperate, deciduous tree species to nonhydraulic root-to-shoot signals of soil drying; and (2) test whether sensitivity to nonhydraulic signaling is allied with drought avoidance/tolerance tendencies of species. Saplings were grown with roots divided between two pots. Three treatments were compared: half of the root system watered and half droughted (WD); half of the root system watered and half-severed (WS); and both halves watered (WW). Drying about half of the root system caused marked nonhydraulically induced declines in stomatal conductance (gs) in Nyssa sylvatica and Acer saccharum but only slight declines in Quercus alba, Q. rubra, Q prinus and Q. acutissima. Declines in gs were significantly correlated with declining soil matric potential (Ψm) in three species. Soil Ψm when gs of WD plants was 80% of WS controls varied from a high of −0.03 MPa in A. saccharum to a low of −0.18 MPa in Q. alba. Neither lethal leaf water potential nor osmotic adjustment was significantly correlated across all species with any measure of stomatal sensitivity to the nonhydraulic root-to-shoot signal. However, species showing considerable osmotic adjustment also tended to show little inhibition of gs. Additionally, species showing little or no foliar osmotic adjustment also showed high stomatal sensitivity to nonhydraulic drought signaling, as indicated by relatively large changes in gs per unit change in soil Ψm. Stomatal sensitivity to nonhydraulic drought signaling appears mechanistically linked to a limited extent with characteristics that define relative species drought tolerance.

Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis

Arbuscular mycorrhizal (AM) symbiosis can enhance plant resistance to NaCl stress in several ways. Two fundamental roles involve osmotic and ionic adjustment. By stimulating accumulation of solutes, the symbiosis can help plants sustain optimal water balance and diminish Na+ toxicity. The size of the AM effect on osmolytes has varied widely and is unpredictable. We conducted a meta-analysis to determine the size of the AM effect on 22 plant solute characteristics after exposure to NaCl and to examine how experimental conditions have influenced the AM effect. Viewed across studies, 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 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. The AM effect has been very small for shoot Ca++ concentration and root concentrations of Na+, Mg++ and proline. Interpretations about AM-conferred benefits regarding these compounds may be best gauged within the context of the individual studies. Shoot and root K+/Na+ ratios and root proline concentration showed significant between-study heterogeneity, and we examined nine moderator variables to explore what might explain the differences in mycorrhizal effects on these parameters. Moderators with significant impacts included AM taxa, host type, presence or absence of AM growth promotion, stress severity, and whether NaCl constituted part or all of the experimental saline stress treatment. Meta-regression of shoot K+/Na+ ratio showed a positive response to root colonization, and root K+/Na+ ratio a negative response to time of exposure to NaCl.

Mycorrhizal promotion of host stomatal conductance in relation to irradiance and temperature

Colonization of roots and soil by arbuscular mycorrhizal (AM) fungi sometimes promotes stomatal conductance (gs) of the host plant, but scientists have had difficulty predicting or manipulating the response. Our objective was to test whether the magnitude of AM influence on gs is related to environmental conditions: irradiance, air temperature or leaf temperature. Stomatal conductances of two groups of uncolonized sorghum plants were compared to gs of plants colonized by Glomus intraradices (Gi) or Gigaspora margarita (Gm) in 31 morning and afternoon periods under naturally varying greenhouse conditions. Stomatal conductance of Gi and Gm plants was often markedly higher than gs of similarly sized nonAM plants. AM promotion of gs was minimal at the lowest irradiances and lowest air and leaf temperatures, but was substantial at intermediate irradiance and temperatures. AM promotion was again low or absent at the highest irradiances and temperatures. Magnitude of AM promotion of gs was not a function of absolute gs. Promotion of gs by Gi and Gm was remarkably similar. Differing phosphorus fertilization did not affect gs.

Description and field performance of the Walker Branch throughfall displacement experiment: 1993--1996

The authors are conducting a large-scale manipulative field experiment in an upland oak forest on the Walker Branch Watershed in eastern Tennessee to identify important ecosystem responses that might result from future precipitation changes. The manipulation of soil water content is being implemented by a gravity-driven transfer of throughfall from one 6400-m{sup 2} treatment plot to another. Throughfall is intercepted in {approx}1850 subcanopy troughs suspended above the forest floor of the dry plot and transferred by gravity flow across an ambient plot for subsequent distribution onto the wet treatment plot. Soil water content is being monitored at two depths with time domain reflectometers at 310 sampling locations across the site. The experimental system is able to produce statistically significant differences in soil water content in years having both dry and wet conditions. Maximum soil water content differentials between wet and dry plots in the 0- to 0.35-m horizon were 8 to 10% during summers with abundant precipitation and 3 to 5% during drought periods. Treatment impacts on soil water potential were restricted to the surface soil layer. Comparisons of pre- and post-installation soil and litter temperature measurements showed the ability of the experimental design to produce changes in soil water content and water potential without creating large artifacts in the forest understory environment.

Comparative dehydration tolerance of foliage of several ornamental crops

Cultivars of Dahlia, Pentas, Salvia and two Impatiens were subjected to severe soil drying, and their foliar water relations were measured when fewer than eight live leaves remained (defined as the lethal point). Salvia was the most dehydration tolerant of the four genera, as characterized by lethal leaf water potential, and showed the highest osmotic adjustment. Dahlia and the two Impatiens cultivars had similar water relations at the lethal point. Length of the drying period, which was varied by growing plants in three pot sizes, did not affect any leaf water relations parameter. The paper also provides a ranking of the foliar dehydration tolerance of 25 other ornamental plants, measured in additional experiments. Foliage of woody species tended to be more tolerant of dehydration than foliage of herbaceous species. # 2003 Elsevier Science B.V. All rights reserved.