Heather D. Toler

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.

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.

Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect

Terpenoids serve as an important form of chemical defense for plants. A greenhouse study was conducted to investigate the effects of two types of beneficial fungi on the accumulation of terpenoids in tomato plants and on defense against herbivorous insects. Control tomato plants without any fungal inoculation constitutively made monoterpenes and sesquiterpenes. Inoculation by Rhizophagus intraradices (N.C. Schenck & G.S. Sm.) C. Walker & A. Schüßler, an arbuscular mycorrhizal fungus, and Beauveria bassiana (Bals.-Criv.) Vuill., an endophytic entomopathogenic fungus, individually or in combination, led to enhanced levels of monoterpenes and sesquiterpenes, which included new monoterpenes not found in the control plants. Herbivore feeding assays using beet armyworm (Spodoptera exigua Hübner) were performed to compare the levels of defense in tomato plants with or without fungal inoculation. Beet armyworm larvae fed on tomato plants inoculated by either or both types of fungi were found to gain significantly less weight than those fed on control non-inoculated plants. This suggests that fungus-inoculated tomato plants had a stronger defense response against beet armyworm than control plants, which may be partly attributed to the difference in the levels of terpenoids.

Fungal mutualists enhance growth and phytochemical content in Echinacea purpurea

An emerging paradigm in sustainable biotechnique is the use of mutualists to enhance plant growth and secondary metabolism. Our objective was to determine impact of two groups of fungal mutualists on growth and phytochemistry of Echinacea purpurea. Growth, development, and phytochemical concentration were measured in greenhouse-grown 12-week-old plants colonized by arbuscular mycorrhizal fungi (AMF) (Rhizophagus intraradices and Gigaspora margarita) or the endophytic entomopathogen, Beauveria bassiana. In one experiment, all measured growth parameters were increased in mycorrhizal plants. Biomass of AMF-colonized plants was over 13-fold greater than non-mycorrhizal controls receiving the same levels of phosphorous, and over 4-fold greater than non-mycorrhizal controls given additional phosphorous. Endophytic colonization by B. bassiana had minor effects on growth. Colonization by AMF and B. bassiana alone or in combination altered concentrations of phytochemicals (pigments, polyphenolics, alkylamides, and terpenes). Mycorrhizal plants produced up to 4.6-fold higher concentration of polyphenolics. Specific alkylamides increased 1.7 fold in plants colonized only with B. bassiana and up to a 2.4-fold increase in plants colonized by both mutualists. Changes in other phytochemical classes were related to differences in plant size induced by AMF. Phytochemical content (concentration × biomass) was increased up to 30-fold in mycorrhizal plants. Phytochemical relationships to plant biomass were confirmed in a second experiment in which non-mycorrhizal plants were fertilized to produce biomass equivalent to that of mycorrhizal plants. Based on this study, mycorrhizal colonization of E. purpurea enhances phytochemical content; this has major implications for the natural product industries and growers of E. purpurea.

Mycorrhizal Stimulation of Leaf Gas Exchange in Relation to Root Colonization, Shoot Size, Leaf Phosphorus and Nitrogen: A Quantitative Analysis of the Literature Using Meta-Regression

Arbuscular mycorrhizal (AM) symbiosis often stimulates gas exchange rates of the host plant. This may relate to mycorrhizal effects on host nutrition and growth rate, or the influence may occur independently of these. Using meta-regression, we tested the strength of the relationship between AM-induced increases in gas exchange, and AM size and leaf mineral effects across the literature. With only a few exceptions, AM stimulation of carbon exchange rate (CER), stomatal conductance (gs), and transpiration rate (E) has been significantly associated with mycorrhizal stimulation of shoot dry weight, leaf phosphorus, leaf nitrogen:phosphorus ratio, and percent root colonization. The sizeable mycorrhizal stimulation of CER, by 49% over all studies, has been about twice as large as the mycorrhizal stimulation of gs and E (28 and 26%, respectively). CER has been over twice as sensitive as gs and four times as sensitive as E to mycorrhizal colonization rates. The AM-induced stimulation of CER increased by 19% with each AM-induced doubling of shoot size; the AM effect was about half as large for gs and E. The ratio of leaf N to leaf P has been more closely associated with mycorrhizal influence on leaf gas exchange than leaf P alone. The mycorrhizal influence on CER has declined markedly over the 35 years of published investigations.

Global meta-analysis reveals agro-grassland productivity varies based on species diversity over time

Ecological research suggests increased diversity may improve ecosystem services, as well as yield stability; however, such theories are sometimes disproven by agronomic research, particularly at higher diversity levels. We conducted a meta-analysis on 2,753 studies in 48 articles published over the last 53 years to test: if biological N2 fixation (BNF) supplies adequate nitrogen (N) for plant growth relative to synthetic fertilizers; how crop physiological traits affect legume-grass symbiosis; and, how cultural practices affect BNF over a range of soils and climates overtime (in polycultures versus sole grasslands). Globally, net primary productivity (NPP; total aboveground production response of grass and legume in higher-diversity treatments) increased 44% via legume associations relative to sole grass controls (including both with and without N fertilizer). Several moderating variables affected NPP including: (i) plant photosynthetic pathway (mixtures of C3 grasses resulted in a 57% increase in NPP, whereas mixtures of C4 grasses resulted in a 31% increase; similarly cool-season legumes increased NPP 52% compared to a 27% increase for warm-season legumes relative to grasslands without diversity); (ii) legume life cycle [NPP response for perennial legume mixtures was 50% greater than sole grass controls, followed by a 28% increase for biennial, and a 0% increase for annual legumes)]; and, (iii) species richness (one leguminous species in a grassland agroecosystem resulted in 52% increase in NPP, whereas >2 legumes resulted in only 6% increases). Temporal and spatial effect sizes also influenced facilitation, considering facilitation was greatest (114% change) in Mediterranean climates followed by oceanic (84%), and tropical savanna (65%) environments; conversely, semiarid and subarctic systems had lowest Rhizobium-induced changes (5 and 0% change, respectively). Facilitation of grass production by legumes was also affected by soil texture. For example, a 122% NPP increase was observed in silt clay soils compared to 14% for silt loam soils. Niche complementarity effects were greatest prior to 1971 (61% change), compared to recent studies (2011–2016; -7% change), likely owing to reduced global sulfur deposition and increased ambient temperatures overtime. These historical trends suggest potential for legume intercrops to displace inorganic-N fertilizer and sustainably intensify global NPP. Results herein provide a framework for ecologists and agronomists to improve crop diversification systems, refine research goals, and heighten BNF capacities in agro-grasslands.