Performance of Taxonomically Diverse Native Isolates of Mycorrhizal Fungi in Symbiosis with Young Grapevines

Authors:
R. Paul Schreiner USDA-ARS, Horticultural Crops Research Laboratory, 3420 NW Orchard Avenue, Corvallis, OR 97330

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Tian Tian Department of Horticulture, Agriculture and Life Sciences Building, Oregon State University, Corvallis, OR 97340

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Abstract

Grapevines rely on arbuscular mycorrhizal fungi (AMF) to obtain ample phosphorus (P) from soils with low to moderate P like the Ultisols of western Oregon. Prior research indicated that nine species, or virtual taxa, of AMF colonized the roots of ‘Pinot noir’ at greater than 1% abundance in a single vineyard. However, little is known about how different taxa within a community vary in their capacity to function as symbionts with grapevines. The effectiveness of five native AMF species representing five genera to promote growth and nutrient uptake of ‘Pinot noir’ was examined in a fumigated Ultisol soil under well-watered and periodically dry conditions. Plants were grown with each of the different isolates alone or without AMF. After 8 and 16 weeks, whole vines were destructively harvested and biomass and nutrients were determined. Results showed that four of the isolates colonized roots extensively, increased root and shoot biomass, and predominantly increased P uptake. A Claroideoglomus isolate was superior in promoting shoot growth as compared with Rhizophagus irregularis, even though both isolates increased P uptake to the same extent, suggesting a higher carbon cost for R. irregularis. Scutellospora calospora failed to colonize roots beyond a trace and had no impact on vine performance. The ability to increase P uptake among the four effective fungi was not related to the frequency of arbuscules in roots suggesting that some P exchange occurs via hyphae within the cortex, particularly for Funneliformis mosseae. Water limitation reduced P uptake as a main effect across all mycorrhizal treatments, suggesting that the native isolates studied here have similar functionality under well-watered and periodically dry conditions.

Grapevines (Vitis vinifera L.) are highly reliant on arbuscular mycorrhizal fungi (AMF) to obtain ample phosphorus (P) from the red hill soils used for vineyards in western Oregon (Schreiner, 2007). Grapevines are particularly receptive hosts to AMF given the exceptional density of arbuscules and hyphae present in fine, feeder roots under field and glasshouse conditions (Schreiner and Scagel, 2016). In the field, grapevines are colonized by multiple species of AMF simultaneously, but the specific taxa within a community that deliver the most benefit are unclear. Little is known about the functional roles that may be performed by different fungal taxa within a community or whether the specific fungi that are dominant in roots in the field (often Rhizophagus spp. in Oregon) are good mutualists. If AMF symbiosis relies on a fair exchange between partners (i.e., good P providers are rewarded with more C from hosts and vice versa), one would expect that the dominant fungi within a given host should enhance P uptake more than less common taxa (Fellbaum et al., 2014; Kiers et al., 2011). However, other factors beyond efficient delivery of nutrients (mainly P) may control why some taxa are common in roots. Nonnutritional benefits (e.g., enhanced tolerance to drought or pests) may be important in some environmental contexts (Augé, 2001; Veresoglou and Rillig, 2012). While some fungi might be rewarded for providing a nonnutritive benefit, it is difficult to understand how host plants may recognize and distinguish which fungal taxa provide them. In contrast, C for P exchange in cortical cells containing arbuscules is highly regulated allowing plants to potentially reward specific fungi that provide more P (Baier et al., 2010; Javot et al., 2007; Luginbuehl and Oldroyd, 2017).

Grapevines grown for wine production often experience moderate water stress imposed to control canopy growth and improve red wine quality (Matthews et al., 1990; Roby et al., 2004). The drought tolerance of grapevines was improved by AMF in potted vines (Nikolaou et al., 2003; van Rooyen et al., 2004), and the frequency of arbuscules in roots increased in response to less irrigation in a Cabernet Sauvignon vineyard (Schreiner et al., 2007) or within drier zones of a ‘Pinot noir’ vineyard (Donkó et al., 2014). Given the well-known role that AMF play in mitigating drought stress in annual plants (Augé, 2001), they may play an even greater role in perennials like grapevines that are such receptive hosts (Trouvelot et al., 2015). Even though many western Oregon vineyards have not experienced severe drought stress historically (Reeve et al., 2016; Schreiner et al., 2006), drought stress in vineyards is expected to worsen over time as average temperatures in the region increase and due to increased use of devigorating rootstocks in place of own-rooted vines. The differences between AMF species or isolates in mitigating the impact on vine water stress are not clear for grapevines.

The goal of this study was to compare the effectiveness of AMF isolates that represent taxonomically diverse fungi that are native to the soil used in the study. Five isolates were compared in this study: two that were commonly amplified from ‘Pinot noir’ roots from the vineyard where they were isolated (Rhizophagus irregularis, and Glomus sp. 3E); one that was amplified from roots occasionally (Scutellospora calospora); and two that were not amplified from ‘Pinot noir’ roots, but were isolated as spores from the vineyard soil (Clariodeoglomus sp., Funneliformis mosseae) (Schreiner, 2020; Schreiner and Mihara, 2009). Each of these isolates was compared with a nonmycorrhizal control, and half of all treatments were either exposed to periodic water limitation or were well-watered. We tested the hypothesis that those isolates that were common in the roots of the vines in the field would be better mutualists in this low P soil. In addition, we examined whether periodic water limitation would alter the colonization of roots and differentially alter vine response to the different fungi.

Materials and Methods

Experimental design, treatments, and soil.

The experiment was conducted in fumigated Jory soil [fine, mixed, active, mesic Xeric Palehumult (USDA-Natural Resources Conservation Service, 2011)], collected from the Oregon State University, Woodhall Research Vineyard (WRV) located in Alpine, OR (44°20′ N, 123°24′ W). The AMF used in this study were isolated from the same soil at the WRV. The experiment was a 6 × 2 × 2 factorial design with six AMF treatments (nonmycorrhizal Control (NM), S. calospora, Claroideoglomus sp., F. mosseae, R. irregularis, and Glomus sp. 3E), two irrigation regimes (well watered, wet; and periodic water limitation, dry), and two destructive plant harvests at 8 and 16 weeks. Each unique treatment was replicated five times giving a total of 120 experimental units comprising a single grapevine grown in a 4-L pot. The soil was collected from 0 to 30 cm depth at the WRV, mixed 1:1 with coarse river sand (prestress sand mix, Morse Bros Inc., Corvallis, OR) to improve drainage, and limed at the rate of 35 g dolomite lime per kg of soil mix to bring pH to 6.0. After mixing, the soil was fumigated with methyl bromide:chloropicrin (67:33) at a rate equivalent to 448 kg per hectare to kill resident AMF (Trident Ag Products, Woodland, WA). The P availability in the soil was low, with Bray 1-extractable P concentration of 14 mg/kg. Other available nutrients in soil (mg/kg) were NO3-N, 5.3; K, 121; Ca, 1,158; Mg, 285; SO4-S, 77; Fe, 62; Mn, 70; B, 0.2; Zn, 1.4; Cu, 1.0.

The nonmycorrhizal controls received no AMF inoculum, but the remaining five AMF treatments received 50 g of a whole soil inoculum of a single AMF isolate that included spores, hyphae, and colonized root fragments. Inoculum for each fungus was propagated using Sorghum bicolor and Trifolium incarnatum grown together in the same container in a low P, sandy loam soil. We were confident that this dose of inoculum would provide ample propagules based on prior studies with inoculum produced in the same manner (Schreiner, 2007; Schreiner et al., 2012) and the very receptive nature of grapevines to form mycorrhizas with AMF. Each fungus was isolated from the WRV by selecting uniform spores of each isolate after wet-sieving topsoil collected from the WRV. Initial trap cultures using spores were cultured with S. bicolor in a low P, sandy loam soil that was autoclaved before use. Spores of each isolate were re-picked based on uniformity and re-cultured with S. bicolor in the same soil for at least two more growth cycles. Each isolate was confirmed to be a single species culture by cloning and sequencing 10 random clones of the small subunit ribosomal DNA (ssu-rDNA) amplified from S. bicolor root DNA extracts using primers specific for AMF as per Schreiner and Mihara (2009). All sequences showed >99.5% homology among the 10 sequences amplified. Sequences were blasted against MaarjAM database to identify each isolate to its virtual taxon (Öpik et al., 2010). More information including propagule numbers for each isolate used appears in Supplemental Table S1.

Pre-rooted, two-node cuttings of ‘Pinot noir’ (Pommard clone, FPS4) were transplanted into each experimental unit on 22 Mar. After topping off each pot with sterile soil to within 1.5 cm of the lip, all pots received a microbial extract derived from each of the AMF inocula and live Jory soil to provide similar microflora in the different treatments. This extract was prepared by mixing 100 g of whole soil inoculum from each of the five AMF and 200 g of live Jory soil collected from the WRV with 10 L of water and incubating this slurry for 4 h at room temperature mixing every 30 min. The soil microflora extract was then allowed to settle for 30 min, and sieved three times through a 25-μm screen to remove AMF propagules. The final extract was diluted to ∼30 L total volume and 250 mL was added to each pot. Plants were grown in a greenhouse with temperatures set at 15/30 °C, resulting in actual temperatures of 14 to 20/20 to 35 °C (night/day). Plants also received supplemental lighting using 1000 W Phosphor coated metal-halide lamps (GE, USA) on a 16-h photoperiod that provided ∼500 μmol·m−2·s−1 PAR in addition to sunlight at the pot surface. The PAR levels in the greenhouse on sunny days ranged from 1000 to 1700 μmol·m−2·s−1, and on cloudy days from 400 to 1000 μmol·m−2·s−1. After 1 week, a single shoot was retained per vine and trained upright on a bamboo stake. Micronized sulfur sprays were used to control powdery mildew as needed. Half of the plants in each unique treatment were grown for 8 weeks (22 Mar. to 16 May) before the first destructive harvest and the remaining plants were grown for 16 weeks for the second harvest (22 Mar. to 13 July).

Fertilizer and water management.

Plants were fertilized once per week (every Monday morning) by providing 400 mL of a ½ strength Hoagland’s solution (containing P at ½ strength as well), although micronutrients were boosted about 2-fold from the original recipe to avoid any micronutrient deficiencies (Hoagland and Arnon, 1950; Schreiner et al., 2018). Just before receiving fertilizer, all plants were given enough water to visibly see water draining from the bottom to avoid salt accumulation. Plants were watered every 2–3 d in all treatments for the first 4 weeks (22 Mar. to 19 Apr.) to reduce water limitation due to transplant shock and to foster growth. Between 4 and 8 weeks (19 Apr. to 16 May), the vines in the wet treatment were watered every second day and the vines in the dry treatment were watered every third day (although each Monday all vines were watered and fertilized). Between 8 and 16 weeks, the vines in the wet treatment were watered as soon as the soil surface was dry for each pot, and vines in the dry treatment were watered when the growing tip or tendrils began to wilt. Plants were checked four times daily, and every 2 h when the greenhouse temperature was above 30 °C. On a few occasions, when plants could not be monitored carefully throughout the day, all vines were watered early in the day. No plants in wet treatment wilted throughout the study, but vines in each of the four AMF treatments that promoted plant growth in the dry treatment wilted once or twice a week during the last 8 weeks of the experiment.

Assays.

Shoot lengths were measured periodically (every 6–14 d) with a flexible tape ruler only using those replicates that remained for the entire 16-week period. Leaf area was also measured on the same vines on four occasions by comparing each leaf to a set of concentric circles of known area (Schreiner et al., 2018). Stomatal conductance (gS) to water vapor was measured using the SC-1 porometer (Decagon Devices Inc., Pullman, WA) on 3 sunny days on fully sunlit leaves using the most recently fully expanded leaf, or an older leaf within three nodes. The first 2 d (27 Apr. and 11 May) occurred before the first destructive harvest at 8 weeks, and the wet vines had gone 1 d without water and the dry vines had gone 2 d without water. On the third measurement day (7 June), the wet vines had received water that morning while the dry vines had not been watered for 2–3 d.

Destructive harvests at 8 and 16 weeks were used to determine the dry mass and nutrient concentrations in all plant parts. The new shoots were cut at the basal end of the stem, and stems (including the tendrils), leaf blades, and petioles were separated and weighed after oven drying each part at 65 °C for 3 d. Woody trunks (original cutting) were chopped into ∼1 cm pieces to facilitate drying. The soil and roots from each pot were placed on a large tray where the bulk of roots were quickly separated by shaking off the soil. The soil was thoroughly mixed and subsamples for soil moisture (∼50 g) and for extraradical hyphal lengths (∼20 g) were removed. Soil moisture was determined gravimetrically after oven drying at 105 °C. The samples for hyphae were stored in a sealed bag at −20 °C. The main root ball was washed with cold tap water and blotted dry, and the smaller fragments of roots remaining in the soil were retrieved by vigorously washing with cold tap water and decanting onto a 500-µm sieve. Total fresh weight (FW) of all roots was determined and they were dried as per other plant tissues, after removing subsamples for mycorrhizal colonization. A random assortment (0.4–0.6 g FW) of fine roots (large woody roots excluded) was removed, weighed, and stored in 50% ethanol with 5% acetic acid. The length of roots with any AMF structures (AMF colonization), or with only arbuscules or vesicles was assessed after clearing and staining roots with trypan blue and mounting roots between two microscope slides that were carefully squashed. The length of extra radical AMF hyphae was determined at 16 weeks only, using a grid-line filtration and trypan blue staining method described by Bethlenfalvay et al. (1999).

All dried plant tissues were ground to fine powder in a stainless steel Wiley mill (Digital ED 5; Thomas Scientific, Swedesboro NJ). Nitrogen concentrations in ground samples were determined using combustion and conversion to N2 by the Dumas method in a C-N analyzer, and all other nutrients were measured using inductively coupled plasma-optical emission spectrometry after acid digestion in nitric acid (Jones and Case, 1990). Nutrient contents of different plant parts were calculated from the concentration and dry mass data. In addition, five of the prerooted cuttings were destructively harvested and analyzed per above on the day of transplanting to provide baseline biomass and nutrient data. This data were not used in statistical analyses, but were plotted with the data from two destructive harvests.

Inoculum retest.

Given the extremely poor root colonization by S. calospora in this trial, a follow-up study was undertaken to test larger quantities of inoculum. Doses of 100, 200, and 400 g of S. calospora inoculum per 4 L pot (two to eight times greater inoculum than the main experiment) were compared using three replicate ‘Pinot noir’ plants that were grown for 8 and 16 weeks. Roots were assessed for AMF colonization using the same method as above.

Data analysis.

The shoot length and leaf area data measured on the same vines were analyzed using a repeated measure, two-way analysis of variance (ANOVA) with irrigation and AMF treatment factors in the model. The means for different AMF treatments or for the wet and dry treatment at each time point were compared using Tukey’s honestly significant difference test at 95% confidence (after showing significant interactions between time and AMF treatment, and between time and irrigation treatment). The gS data were analyzed separately at each time point using two-factor ANOVA with irrigation and AMF treatments as factors. The nutrient concentration data in shoots and roots, the dry mass and nutrient contents of roots, shoots, and whole vines, and the mycorrhizal root colonization parameters were analyzed using three-factor ANOVA with time (destructive harvest date), irrigation, and AMF treatments as factors. Both the S. calospora and NM treatments were excluded from the root colonization analysis, since colonization was absent (NM vines) or only a minor trace (S. calospora vines). The length of extra radical hyphae at 16 weeks was analyzed using two-factor ANOVA with irrigation and AMF treatments as factors. Some variables were transformed to satisfy variance assumptions for ANOVA and these are indicated in the tables and figures. The mean and standard error of the mean are shown in all tables and figures for simplicity and consistency in data representation.

The relative biomass and relative nutrient concentrations in whole vines at the final (16 weeks) harvest were calculated in relation to the NM controls by dividing the values for total plant mass or total plant nutrient concentrations for each nutrient in each replicate by the mean value of the NM control vines and multiplying those values by 100. Plotting the relationship between relative biomass change and the relative nutrient concentrations as opposed to actual dry weights and concentrations for each nutrient allows for multiple nutrients to be compared in a single plot. A similar approach was used by Valentine and Allen (1990) to interpret whether nutrients were deficient or sufficient in response to fertilizers, but required a separate plot for each nutrient examined. The relative biomass and relative nutrient concentration data were analyzed using two-factor ANOVA with irrigation and AMF treatments as factors.

Results

Root colonization and soil hyphal lengths.

Four of the five isolates (Claroideoglomus sp., F. mosseae, R. irregularis, Glomus sp. 3E) colonized roots extensively, reaching over 95% of root length colonized by 16 weeks (Fig. 1A). The interaction between AMF treatment and time was significant for these four fungi because small differences among isolates occurred at 8 weeks, but not at 16 weeks. At 8 weeks, R. irregularis vines had slightly greater length of roots colonized than vines with Claroideoglomus sp. or F. mosseae. Only S. calospora did not colonize roots well in this study, and was removed from the ANOVA along with the NM treatment. We observed somewhat numerous infection units in roots in the S. calospora vines, but the internal development of hyphae was always sparse and only rarely were arbuscules observed (Supplemental Fig. S1). Colonization by S. calospora averaged about 2% of root length at both harvests, but even this value overestimates colonization by this fungus compared with the other fungi because the density of fungal structures in the roots was so low. Vines in the NM treatment were not colonized by AMF. Irrigation treatment did not alter root length colonized by AMF as a main effect (P = 0.058), nor did it interact with AMF treatment or time. The four isolates that colonized roots extensively, differed substantially in the extent of arbuscules in roots (Fig. 1B). Arbuscular colonization among the four effective fungi was also altered by the interaction between AMF treatment and time (P = 0.049) because F. mosseae and Glomus sp. 3E showed a declining trend for arbuscules between 8 and 16 weeks but R. irregularis tended to increase. However, arbuscular colonization did not differ between the two times for any single fungus. Claroideoglomus sp. and Glomus sp. 3E had the highest frequency of arbuscules in roots with about 50% of root length containing arbuscules, followed next by R. irregularis with about 35%, which was greater than F. mosseae with only about 10% of roots with arbuscules. In addition, the intercellular hyphae of F. mosseae in roots were often of larger diameter than the other isolates, colonizing the intercellular spaces between cortical cells more intensely than the other fungi (Supplemental Fig. S1). Irrigation treatment did not alter arbuscules in roots (P = 0.450). Rhizophagus irregularis produced the most spores or vesicles in roots. The length of extra radical hyphae at 16 weeks was altered by AMF treatment (P < 0.001), but not by irrigation treatment (P = 0.461). The NM vines had 4.2 ± 0.3 m/g dry soil of hyphae having a morphology consistent with AMF, and this did not differ from S. calospora with 5.2 ± 0.5 m/g (data not shown). The four AMF that colonized roots well produced greater hyphal lengths than the NM and S. calospora treatments (Clariodeoglomus sp. had 15.8 ± 1.0, F. mosseae had 12.9 ± 0.7, R. irregularis had 14.6 ± 0.9, and Glomus sp. 3E had 13.6 ± 1.0 m/g dry soil of extra radical hyphae).

Fig. 1.
Fig. 1.

Effects of fungal isolate and sampling date on root length colonized by mycorrhizal fungal structures (A), root length colonized by arbuscules (B), plant shoot length (C), leaf area (D), shoot biomass (E), and root biomass (F) in ‘Pinot noir’ grapevines grown in fumigated Jory soil (n = 10). Data for (A, B, E, and F) were analyzed using three-factor analysis of variance (ANOVA) [time × irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment], and letters indicate significant groups based on the interaction between time and AMF treatment based on Tukey’s honestly significant difference (HSD) test at 95% confidence. Data for (C) and (D) were analyzed by repeated measures ANOVA, and letters indicate significant groups at each sampling time based on Tukey’s HSD test at 95% confidence. The nonmycorrhizal and Scutellospora calospora treatments were excluded from analysis of root colonization data in (A) and (B). Data for (B, E, and F) were square root transformed to satisfy variance assumptions. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

Citation: HortScience 57, 9; 10.21273/HORTSCI16648-22

The additional S. calospora inoculum dose experiment using up to eight times more inoculum than was used in the main experiment did not result in good levels of root colonization by this fungus. The highest rate of inoculum of 400 g per pot increased root length colonized by S. calospora slightly (3.5%) over the 100 g dose (2.1%), but the density of fungal structures in roots was still sparse as observed in the main experiment (Supplemental Fig. S1).

Vine growth.

Vines in all treatments initially grew well, but those vines with one of the four AMF that colonized roots well began to grow faster than the NM and S. calospora vines at about 6 weeks (Fig. 1C). Thereafter, shoot growth in the NM and S. calospora vines was arrested. By the first harvest at 8 weeks, vines inoculated with Claroideoglomus sp., F. mosseae, and R. irregularis were taller than NM and S. calospora vines, and vines colonized by Glomus sp. 3E were intermediate between those two groups. By 16 weeks, the Claroideoglomus sp. vines outperformed all other treatments attaining a height of about 150 cm. Vines colonized by F. mosseae, R. irregularis, and Glomus sp. 3E reached a similar final height of about 100 cm, while the NM and S. calospora vines reached only about 40 cm. The same pattern was observed for leaf area per vine, showing Claroideoglomus sp. leading the pack, with the three other effective isolates intermediate between it and the NM and S. calospora vines, although the Glomus sp. 3E vines initially lagged behind (Fig. 1D). The main effect of AMF treatment from the repeated measures ANOVA was significant for both shoot length and leaf area as well as the time × AMF treatment interaction.

The irrigation treatment did not alter shoot length or leaf area nearly as much as the different AMF treatments, and the main effect of drought was not significant for either shoot length or leaf area in the repeated measures model. However, the drought treatment interacted with time to alter shoot length on the last four dates it was measured (27 May to 11 July) and to affect leaf area on the last two measures taken (data not shown). By 16 weeks, the wet vines were on average about 10 cm taller than the dry vines and their leaf area was about 130 cm2 greater.

The irrigation treatment significantly altered gS to water vapor on each of three sunny days when it was assessed (Table 1). In addition, on the first two dates, which occurred before the first destructive harvest (27 Apr. and 11 May), an interaction between AMF and irrigation treatments occurred because the four growth-promoting isolates (Claroideoglomus sp., F. mosseae, R. irregularis, Glomus sp. 3E) showed larger differences in gS between wet and dry treatments than what occurred in NM and S. calospora vines. Although the means of the wet and dry treatments differed only for Claroideoglomus sp. and R. irregularis vines based on Tukey’s post hoc test. The dry vines on both of these days had not been watered for 2 d, while the wet vines were watered the previous day. On 7 June, when only the main effect of irrigation treatment altered gS, vines in the wet treatment were watered that morning while the dry vines had gone without water for 2–3 d, depending on the specific AMF treatment.

Table 1.

Stomatal conductance of ‘Pinot noir’ grapevines on 3 d in Pinot noir grapevines grown in fumigated Jory soil obtained using the SC-1 porometer. Measurements were conducted between 10:00 am and 2:00 pm on sunny days on fully expanded leaves located near the top of the shoot.

Table 1.

Shoot biomass and root biomass were both altered predominantly by AMF treatment and time (harvest) and the interaction between these factors was significant (Fig. 1E and F). At 8 weeks, there were small differences between the various AMF treatments for both shoot and roots (for example, shoot mass was higher than the NM vines for two AMF isolates), but differences due to AMF became quite large by 16 weeks. Shoot mass was about 2-fold greater in the Claroideoglomus sp. vines than in vines with one of the other three effective isolates (F. mosseae, R. irregularis, and Glomus sp. 3E), which were about two times larger than the NM and S. calospora vines. For root biomass, there was no difference between the four effective isolates at the final harvest, which were all nearly three times heavier than the NM or S. calospora vines. Root mass had nearly doubled in the small NM and S. calospora vines between 8 and 16 weeks but shoot mass did not increase after 8 weeks.

The irrigation treatment also altered the biomass of shoots, as a main effect in the ANOVA model (Table 2), but did not alter root mass or whole vine mass. The shoots in the wet treatment were on average about 1 g heavier (10% increase) than the dry vines when data were pooled across all AMF treatments and both harvests. When data for shoot biomass were analyzed separately at each harvest, irrigation treatment was not significant. Roots were not altered by irrigation (P = 0.577) and neither was whole vine mass (P = 0.293).

Table 2.

Tissue nutrient concentration, plant biomass, and nutrient content variables that were altered by irrigation treatment (main effect) in ‘Pinot noir’ grapevines grown in fumigated Jory soil and harvested after 8 or 16 weeks. Data are pooled means (SEM) from all AMF treatments at both sampling dates (destructive harvests, n = 60).

Table 2.

Nutrient concentrations and contents.

Nutrient concentrations for every nutrient examined here in shoots and roots were strongly altered by AMF treatment, time, and their interaction (Supplemental Tables S2 and S3). To briefly summarize these data, the largest change in both shoots and roots had occurred for P concentrations, increasing dramatically in vines inoculated with each of the four effective AMF isolates (Claroideoglomus sp., F. mosseae, R. irregularis, and Glomus sp. 3E), as compared with the NM and S. calospora vines which did not differ. For example, at 8 weeks, shoot P was only about 0.6 g/kg DW in the NM and S. calospora vines, and this concentration had doubled or tripled in shoots of the remaining AMF treatments (Supplemental Table S2). Roots in NM and S. calospora vines only had about 0.3 g P/kg DW at both harvests and P was two to three times higher in roots with each of the four effective isolates (Supplemental Table S3). The concentration of K also increased in both shoots and roots of the Claroideoglomus sp., R. irregularis, and Glomus sp. 3E vines compared with the NM and S. calospora vines. Nitrogen concentrations in shoots and roots at the second harvest were always lower in vines colonized by each of four effective isolates than in NM and S. calospora vines. Although the concentration of N in shoots was greater in Claroideoglomus sp. vines than Glomus sp. 3E vines at 8 weeks, and these were greater than the NM vines. Root N concentrations at 8 weeks were lower in the R. irregularis and Glomus sp. 3E vines than in the NM vines. Other minor differences among the AMF treatments had occurred for other nutrients in roots or shoots, but these effects were generally small in magnitude and were not consistently expressed in both tissues and at both times. Although Mn concentrations were consistently the highest in the R. irregularis vines in both shoots and roots at both harvests.

The irrigation treatment also altered nutrient concentrations in vine tissues, but these effects were mostly confined to roots (Table 2). Concentrations of P, K, Ca, and Zn were greater in the roots of the well-watered vines, but root N showed the opposite change with higher concentrations in the dry treatment. Shoot N concentrations were also higher in dry vines as compared with wet vines, along with shoot S concentrations.

Whole vine nutrient contents (indicative of uptake, given the small quantities of all nutrients in the transplanted cuttings) are summarized together with the changes in whole vine biomass in Fig. 2. Total vine biomass closely reflected what occurred in shoots, except for minor differences among some AMF treatments at 8 weeks. By 16 weeks, Claroideoglomus sp. vines had greater biomass than all other treatments being 2.6 times larger than the NM and S. calospora vines (Fig. 2A). The three remaining effective isolates (F. mosseae, R. irregularis, and Glomus sp. 3E) were 2.0 times larger than the NM and S. calospora vines (Fig. 2A). Clearly, the biggest impact of AMF on nutrient uptake was for P, having increased P contents by 4.8 (F. mosseae, Glomus sp. 3E) to 8.0 times (Claroideoglomus sp.) more than the NM and S. calospora vines at 16 weeks (Fig. 2B). Total vine P content in R. irregularis vines did not differ from Claroideoglomus sp. vines at 16 weeks. No other nutrient had increased nearly as much as P in response to colonization by the four effective isolates. Only the NM and S. calospora vines did not improve their P contents between 8 and 16 weeks (Fig. 2B). Vine N, K, B, and Cu showed a similar pattern of how different AMF treatments altered their uptake from soil (N shown in Fig. 2C). The increase in total vine N ranged from 1.6 to 2.0 times more N in vines colonized by each of the four effective isolates compared with the N content of the NM vines. Total vine contents of N, K, B, and Cu at 16 weeks fit the pattern of Claroideoglomus sp. > F. mosseae, R. irregularis, Glomus sp. 3E > NM and S. calospora vines. Whole vine Ca, Mg, and S behaved in a similar fashion, in that all four effective isolates had similar contents of these elements at 16 weeks, although minor differences occurred among these isolates at either harvest (Ca shown in Fig. 2D). Uptake of Mn was unique in that R. irregularis vines had greater contents of Mn than any other treatment (Fig. 2E), as was reflected by the higher concentrations of Mn observed for shoots and roots at both harvests (Supplemental Tables S2 and S3). Finally, Zn had a unique pattern among AMF treatments with lower contents occurring in the F. mosseae vines at 16 weeks than in Claroideoglomus sp. and R. irregularis vines (Fig. 2F).

Fig. 2.
Fig. 2.

Interactive effect of fungal isolate and sampling date on total vine biomass (A), total vine phosphorus (B), total vine nitrogen (C), total vine calcium (D), total vine manganese (E), and total vine zinc (F) in ‘Pinot noir’ grapevines grown in fumigated Jory soil (n = 10). Data were analyzed using three-factor analysis of variance (ANOVA) [time × irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment], and letters indicate significant groups based on the interaction between date and AMF treatment using Tukey’s honestly significant difference test at 95% confidence. Data for (A, B, C, and E) were square-root-transformed to satisfy variance assumptions. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

Citation: HortScience 57, 9; 10.21273/HORTSCI16648-22

The irrigation treatment altered the shoot contents of P, K, Ca, Mg, and B, but only P content was altered by irrigation on a whole vine basis (Table 2). In all cases where nutrient contents differed between irrigation treatments, the wet treatment vines had higher contents. The increase in total vine P content in wet over dry vines was about 6%. The interaction between AMF treatment and irrigation treatment was not significant for P contents (or any other nutrient), indicating that all AMF treatments responded similarly to irrigation.

Comparing how each of the AMF isolates altered whole vine biomass and whole vine macronutrient concentrations relative to the NM vines revealed that each of the four effective isolates (Claroideoglomus sp., F. mosseae, R. irregularis, and Glomus sp. 3E) had achieved total vine biomass levels with total vine P concentrations that were more than 200% of the respective values in NM vines (Fig. 3). However, the relationship between the increase in P and increase in biomass was unique for R. irregularis vines. The increase in P concentration in R. irregularis vines was more than 300% of the P concentration in NM vines, while biomass was just over 200% of the biomass in NM vines. The other three fungi had similar relative increases in both biomass and P concentration (closer to 1:1). Potassium was the only other macronutrient that showed a relative increase in concentration in the mycorrhizal vines to about 140% of the NM vine K levels. The concentration of Mg was diluted in Claroideoglomus sp. vines, but not in other AMF treatments. Vine N concentrations were diluted more than all other macronutrients to a similar extent in all the AMF vines relative to NM vines. The S. calospora vines never differed from the NM controls (data not shown). Irrigation treatment also influenced N as a main effect, with total vine N concentrations higher in the dry vines than in wet vines (data not shown). No interactions occurred between AMF and irrigation treatments for relative biomass or relative nutrient concentrations.

Fig. 3.
Fig. 3.

Relationship between relative biomass and relative whole vine nutrient concentrations of macroelements as altered by fungal isolate in ‘Pinot noir’ grapevines grown in fumigated Jory soil for 16 weeks (n = 10). Data were analyzed using two-factor analysis of variance (ANOVA) [irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment]. Data for Scutellospora calospora are not shown as no measure differed from nonmycorrhizal vines. Data for P were log-transformed to satisfy variance assumptions for ANOVA. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. Different AMF treatments are indicated by the shape of symbols and different nutrients are indicated by color. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

Citation: HortScience 57, 9; 10.21273/HORTSCI16648-22

Discussion

The first hypothesis tested in this comparison of native fungal isolates, namely that isolates that are more commonly amplified from vine roots in the field would provide more P and increase growth better than those species that were not present in roots in the field, was rejected. The Claroideoglomus isolate tested here was superior to all other isolates in promoting shoot growth and P uptake in this soil and this fungus was not found in the roots of ‘Pinot noir’ in the field (Schreiner, 2020). However, R. irregularis, which was the most common fungus found in roots of ‘Pinot noir’ at the WRV, was just as effective as Claroideoglomus sp. in promoting P uptake. It was just not as effective in stimulating shoot growth. In addition, F. mosseae and Glomus sp. 3E both promoted P uptake and vine growth to a similar extent, but Glomus sp. 3E was common in ‘Pinot noir’ roots in the vineyard while F. mosseae was not amplified from field roots (Schreiner, 2020). These four fungi that promoted vine P uptake and growth had all colonized roots extensively, reaching over 80% of root length colonized at 8 weeks and over 95% at 16 weeks. Comparing the effectiveness of these four isolates appears to be valid based on the degree of root colonization, but S. calospora was excluded from this comparison given the very poor colonization by this isolate. Our findings do not support the idea that the most common root colonizing fungi in the field provide the greatest plant benefit when tested under greenhouse conditions in their native soil. Obviously, the use of fumigated soil and examination of each fungus individually represents a different set of conditions than what occurs in the vineyard where mature vines are interacting with a community of AMF. The situation in the field where a community of fungi is competing for root occupancy is far more complicated. However, one cannot compare the effectiveness of different AMF taxa without separating them to examine their unique impact on the plants, nor removing the AMF already present in the soil. Our goal was not to examine competition among different fungi here (also an interesting question), but rather to test for effectiveness in P uptake in this low P soil. Such differences between controlled studies with AMF and how these results equate to AMF effects in the field have been a limiting factor in the interpretation of most studies with AMF (Lekberg and Koide, 2013).

Another caveat to consider in interpreting findings here was our use of young vines that differ in their nutrient physiology relative to mature vines. The initial content of nutrients in the rooted cuttings was low, so the vast majority of the nutrients in the vines at end of this experiment were taken up during the 16-week growth period. Of the total nutrient content in vines at the end of this experiment, 87–90% of total N, 97–98% of total P, and 95–96% of total K were taken up after transplanting the vines for those vines colonized by any of the four effective isolates. Even in the NM and S. calospora vines that produced very little biomass more than 80% of the total N, P, and K accrued after transplanting. Older vines in the field rely heavily on stored reserves, particularly for N and P, supplying about 50% of canopy needs by the time of fruit maturity (Schreiner et al., 2006). In addition, the root system of young vines is being built from scratch relying on C fixed by the newly developing shoots, and a high proportion of the root system are fine feeder roots in young vines. However, the vast majority of roots of mature vines in the field are woody roots and fine feeder roots active in nutrient and water uptake represent less than 6% of total root mass (Schreiner et al., 2006; Pradubsuk and Davenport, 2010). These differences between young and old vines would alter the source-sink relations for C and nutrients within different vine tissues, which may have influenced the amount of C directed to fine roots to support AMF.

The primary driver of vine response to AMF in this study was due to increased P uptake and release of the host plant from P deficiency. This is no surprise given the very low available P in the soil. The differences between isolates were largely due to their differing capacity to improve P uptake, which translated into improved shoot growth. However, Claroideoglomus sp. increased shoot growth more than the other fungi even though R. irregularis had increased P uptake to the same extent. Vines colonized by R. irregularis had similar dry matter as those colonized by F. mosseae or Glomus sp. 3E, which did not take up as much P as the Claroideoglomus sp. and R. irregularis vines (Fig. 2). A possible explanation for why Claroideoglomus sp. improved shoot growth better than R. irregularis is because Claroideoglomus sp. had also improved N uptake. A similar result showing greater increases in shoot biomass and both N and P uptake among Claroideoglomus isolates as compared with isolates of three other species of AMF was observed for one of two woody AMF host plants (Schinus terebinthifolia) evaluated simultaneously (Schoen et al., 2021). In this study, Claroideoglomus sp. vines had taken up more N than R. irregularis vines at both harvests, while both fungi stimulated similar P uptake. This suggests that the release from P deficiency by both fungi may have led to N limitation, and that N was more efficiently taken up by vines with Claroideoglomus sp. (either directly or indirectly). This interpretation is supported by the observation that Claroideoglomus sp. vines had higher N concentrations as well as N contents in both shoots and roots at 8 weeks than the R. irregularis vines. However, by comparing the relative changes of macro-nutrient concentrations in whole vines with the relative biomass changes as shown in Fig. 3, a different interpretation of these results can be reached. Based on that analysis, whole vine relative P concentrations were boosted by both Claroideoglomus sp. and R. irregularis to the same extent (which was greater than for F. mosseae and Glomus sp. 3E), but total vine N concentrations were diluted to the same extent by all four AMF. The similar dilution of N concentrations coupled with large biomass increases by all four fungi indicates that N was still at a sufficient level in the vines, but was simply diluted due to increased biomass (Valentine and Allen, 1990). Indeed, R. irregularis clearly stands out as unique among the four effective isolates in Fig. 3, having the smallest biomass gain relative to P concentration gain. This indicates that R. irregularis may incur a greater C cost to obtain P compared with the other three fungi that had roughly equal gains in biomass vs. P concentrations. Even though Clariodeoglomus sp. was superior to F. mosseae and Glomus sp. 3E in terms of P uptake and vine growth, these three fungi were closer to the 1:1 correspondence line in Fig. 3. These findings indicate that Clariodeoglomus sp. would be a good fungus to use as inoculum for planting grapevines in this soil (even if it is eventually outcompeted by other fungi over time, which appears to be the case at WRV), since it promoted the quickest gains in both P and biomass.

A higher C cost in the R. irregularis vines to gain a similar increase in P is consistent with its ecological role as ruderal and cosmopolitan species of AMF (Nielsen et al., 2016; Öpik et al., 2006). Among the fungi examined here, it produced copious numbers of spores and/or vesicles in roots. Ensuring the production of numerous propagules is consistent with its cosmopolitan nature and capacity to rapidly colonize disturbed sites and new environments (Mathimaran et al., 2005; Nielsen et al., 2016). However, R. irregularis is also known to have wide intraspecific variation in its ability to provide P and increase plant growth (Angelard et al., 2010; Koch et al., 2006). How well the specific isolate of R. irregularis examined here represents the overall range in traits that influence P uptake by grapevines and its own reproductive output within the population of this fungus at the WRV is not known.

Rhizophagus irregularis also differentiated itself here in promoting the greatest uptake of Mn among the fungi tested. While this would be advantageous in low Mn soils (such as alkaline soils in arid regions), this trait offers no obvious benefit to plants grown in acidic soils like the Jory soil used here with high available Mn. Increased uptake of Mn by R. irregularis was noted in other woody perennials (olive and poplar), although it was not increased to a greater extent than was biomass or other nutrients as observed here with grapevines (Tekaya et al., 2017; Wu et al., 2018). Whether such effects on Mn uptake are typical for R. irregularis in symbiosis with grapevines or whether it is unique to the isolate used here is not clear. The level of trait variation that may occur for Mn uptake within different isolates of R. irregularis is not known, but this information would be helpful in developing inocula of this fungus for use in acid vs. basic soils (Savary et al., 2018).

The observed differences among the fungi examined here in effectiveness to obtain P and promote shoot growth was not related to the production of extraradical hyphae in soil. The four effective isolates produced similar quantities of hyphae in soil even though Claroideoglomus sp. and R. irregularis had outperformed the others in P uptake. However, other properties of extraradical hyphae might contribute to the observed differences in P uptake and potential host plant cost among the fungi studied here. This could be due to differences in their morphology, frequency of anastomoses, metabolism and activity of P transporters, or even interactions with different mycelium-associated bacteria (Avio et al., 2006; Emmett et al., 2021; Kameoka et al., 2019; Thonar et al., 2011). Alternatively, the growth rate of the extraradical mycelium may differ among the fungi which may have allowed quicker access to soil P (Jakobsen et al., 1992). Faster growth of mycelium in soil and quicker access to soil P could explain why Claroideoglomus sp. had outperformed the other fungi in this study.

The effectiveness among the fungi examined here was not related to the frequency of arbuscules in roots, as one might expect. Arbuscules occupied about 50% of the root length in both Claroideoglomus sp. and Glomus sp. 3E vines, but Claroideoglomus sp. vines took up significantly more P. Perhaps more striking is that F. mosseae and Glomus sp. 3E vines had obtained the same amount of P, yet F. mosseae vines only had arbuscules in 10–15% of vine root length. These results indicate that not all P exchange is under such tight control across the arbuscular interface by both partners. The very low incidence of arbuscules in F. mosseae indicates that at least in this isolate that some P exchange likely occurs across hyphal interfaces in roots as well as arbuscules. Indeed, arbuscules were not necessary for P transfer to the host as shown for S. calospora in the rmc (reduced mycorrhizal colonization) tomato mutant that did form arbuscules (Manjarrez et al., 2010). It is ironic that this was observed for S. calospora in tomato, which was the only fungus studied here that failed to substantially colonize grapevine roots. The reason that S. calospora performed so poorly with ‘Pinot noir’ in this study is not known, and does not agree with its often aggressive capacity to colonize roots in annual plants, sometimes to the point of suppressing plant growth (Bennett and Bever, 2007; Dickson et al., 1999). The low frequency of arbuscules in ‘Pinot noir’ roots observed for F. mosseae here does corroborate prior work in the grapevine rootstock, SO4, where F. mosseae also had lower levels of arbuscules in roots as compared with R. irregularis (Cangahuala-Inocente et al., 2011). In SO4, F. mosseae, but not R. irregularis increased root mass, while both fungi increased shoot mass and shoot P concentrations.

Variation in P uptake and growth among the fungi examined here was expected, as responses to different AMF taxa are known to vary in numerous host plants including grapevines. However, our findings are generally not consistent with prior studies on grapevines where some of the same fungal taxa or their close relatives were studied. For example, Karagiannidis et al. (1995) compared the effects of Rhizophagus fasciculatus, F. mosseae, and Funneliformis geosporus (formerly known as Glomus geosporum) on four grapevine genotypes including three rootstocks and a table grape cultivar. They found that on average F. mosseae and F. geosporus promoted shoot growth and increased shoot P concentrations better than R. fasciculatus opposite of our findings here comparing F. mosseae and R irregularis. Similarly, Schubert et al. (1988) also found a Funneliformis monosporus (formerly known as Glomus monosporum) to colonize roots faster and, in general, promote the growth of 420A rootstock in three different soils better than R. fasciculatus. Ozdemir et al. (2010) compared F. mosseae to R. irregularis in a soil mix with a moderate level of P on four grape genotypes and found that shoot weight was increased by F. mosseae in three of four genotypes, while R. irregularis had increased shoot weight in two of the genotypes. Both fungi increased leaf P concentrations to a similar extent in that study, but the nonmycorrhizal controls were not as limited by P as the vines studied here in Jory soil. The leaf P concentrations ranged from 1.50 to 2.50 g P/kg DW among the four genotypes in the prior work, while shoot P was only 0.47 g P/kg DW at 16 weeks in the ‘Pinot noir’ vines studied here. Prior work with ‘Pinot noir’ in this soil and another soil with moderate P, showed that AMF improved P uptake in both soils, but growth was only increased by AMF in the Jory soil as shown here (Schreiner, 2007).

The second hypothesis that periodic water limitation would alter root colonization and vine responses to the different fungal isolates tested here was also rejected. The lower irrigation regime applied here did not alter root colonization by any fungus, and no interaction between irrigation and AMF treatments had occurred. However, the dry treatment reduced shoot growth of vines as a main effect across all AMF treatments. Irrigation regime also influenced the concentrations of some nutrients (primarily in roots), and vine P uptake as a main effect. The dry vines acquired less P than the wet vines, although the uptake of no other nutrient was altered by irrigation treatment. These findings indicate that the species tested here have similar performance under well-watered and periodically dry conditions. However, the level of drought stress imposed here, by replenishing soil moisture when plants began to wilt, may not have been the best test of this hypothesis. Perhaps, a more severe dry period, especially if it could have been imposed gradually before shoots wilted, would have produced different results. In prior work with ‘Chenin blanc’ grapevines, a drought period of 4 weeks reduced root colonization by F. mosseae by about 50% compared with well-watered vines (Valentine et al., 2006). Although in field conditions, others have observed the opposite response, as root colonization by arbuscules increased under drier conditions (Donkó et al., 2014; Schreiner et al., 2007). The fact that the dry treatment applied here did not alter root colonization by any AMF isolates suggests that the difference between wet and dry treatments applied here was not severe enough to differentiate potential differences among these fungi in response to drought. Further work evaluating the role of different isolates in alleviating grapevine water stress is needed, as water deficits are commonly used in wine grapes (Keller, 2005; Matthews et al., 1990).

The fact the dry treatment applied to ‘Pinot noir’ in this study resulted in lower P uptake, but did not alter other nutrients is a testament to how P deficient this Jory soil is. Indeed, the NM and S. calospora vines were clearly deficient in P (as noted earlier) and the vines in these two treatments responded accordingly. For example, root mass had doubled between 8 and 16 weeks in the NM and S. calospora vines and P concentrations in roots remained the same, but shoots had not gained any mass and shoot P concentrations actually had decreased between 8 and 16 weeks. These findings show that vines in these two treatments were allocating resources to roots to obtain P.

The lower P uptake in the dry treatment vines supports prior findings from a whole-vine nutrient budget experiment that was conducted at the WRV in the same soil type. In that study, vine P uptake was reduced in a dry year vs. a wet year, yet other macronutrients had the same or slightly higher uptake rates from the soil in the dry year (Schreiner et al., 2006). Typically, K is thought to be the nutrient most affected by low soil moisture or reduced irrigation inputs in grapevines (Hepner and Bravdo, 1985; Mpelasoka et al., 2003). Here, root K concentrations and shoot K contents were lower in the dry vines, but total vine K uptake was not. This is likely because we used young vines that had carried no fruit crop, which is a large sink for K in grapevines (Mpelasoka et al., 2003).

The uptake of K was improved by AMF in those vines colonized by each of the four effective isolates more so than vine biomass was improved. Indeed, K was the only macronutrient other than P that had increased more than biomass had increased. Total K content in vines colonized by the four effective fungi was three to four times greater than the NM plants, while biomass increased about 2-fold. In comparison, P uptake was five to eight times greater than the NM vines. No other macronutrient was increased by AMF more so than biomass, except for Mn uptake in vines colonized only by R. irregularis. Greater K uptake due to AMF in this soil supports a few prior studies (Karagiannidis et al., 2007; Nikolaou et al., 2002). However, in those studies, K had not increased more than biomass in mycorrhizal vines, indicating that the additional uptake of K was driven mostly by a biomass increase after release from P deficiency. The role of AMF in K uptake and transport to plants is less clear than what is known for ectomycorrhizal fungi (Garcia and Zimmermann, 2014), but recent studies indicate that specific plant K channels appear to operate in roots colonized by AMF to obtain K taken up by the mycorrhizal pathway (Liu et al., 2019; Zhang et al., 2017). The greater uptake of all other nutrients, including N, by the vines here was due to the biomass increase after releasing P limitation.

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Supplemental Fig. 1.
Supplemental Fig. 1.

Roots of ‘Pinot noir’ cleared and stained with trypan blue revealing fungal structures in roots typical of those colonized by Scutello-spora calospora (A) showing only a trace of internal hyphae; Claroideoglomus sp. (B) showing arbuscules and intercellular hyphae; Funneliformis mos-seae (C) showing extensive and coarse intercellular hyphae; Rhizophagus irregularis ( D) showing vesicles/spores, arbuscules, and hyphae; and Glomus sp. 3E (E) showing vesicles, arbuscules, and hyphae after 8 weeks of growth in Jory soil mixed with sand and fumigated prior to inoculation. a = arbuscules; v = vesicles/spores.

Citation: HortScience 57, 9; 10.21273/HORTSCI16648-22

Supplemental Table S1.

Summary of five native arbuscular mycorrhizal fungi isolated from Jory soil at the Oregon State University-WRV used in this study.

Supplemental Table S1.
Supplemental Table S2.

Interactive effect of sampling date and AMF treatment on shoot nutrient concentrations 8 and 16 weeks after transplanting ‘Pinot noir’ grapevines in fumigated Jory soil. Data are pooled means (SEM) from both irrigation treatments (n = 10).

Supplemental Table S2.
Supplemental Table S3.

Interactive effect of sampling date and mycorrhizal treatment on root nutrient concentrations 8 and 16 weeks after transplanting ‘Pinot noir’ grapevines in fumigated Jory soil. Data are pooled means (SEM) from both irrigation treatments (n = 10).

Supplemental Table S3.
  • Fig. 1.

    Effects of fungal isolate and sampling date on root length colonized by mycorrhizal fungal structures (A), root length colonized by arbuscules (B), plant shoot length (C), leaf area (D), shoot biomass (E), and root biomass (F) in ‘Pinot noir’ grapevines grown in fumigated Jory soil (n = 10). Data for (A, B, E, and F) were analyzed using three-factor analysis of variance (ANOVA) [time × irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment], and letters indicate significant groups based on the interaction between time and AMF treatment based on Tukey’s honestly significant difference (HSD) test at 95% confidence. Data for (C) and (D) were analyzed by repeated measures ANOVA, and letters indicate significant groups at each sampling time based on Tukey’s HSD test at 95% confidence. The nonmycorrhizal and Scutellospora calospora treatments were excluded from analysis of root colonization data in (A) and (B). Data for (B, E, and F) were square root transformed to satisfy variance assumptions. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

  • Fig. 2.

    Interactive effect of fungal isolate and sampling date on total vine biomass (A), total vine phosphorus (B), total vine nitrogen (C), total vine calcium (D), total vine manganese (E), and total vine zinc (F) in ‘Pinot noir’ grapevines grown in fumigated Jory soil (n = 10). Data were analyzed using three-factor analysis of variance (ANOVA) [time × irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment], and letters indicate significant groups based on the interaction between date and AMF treatment using Tukey’s honestly significant difference test at 95% confidence. Data for (A, B, C, and E) were square-root-transformed to satisfy variance assumptions. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

  • Fig. 3.

    Relationship between relative biomass and relative whole vine nutrient concentrations of macroelements as altered by fungal isolate in ‘Pinot noir’ grapevines grown in fumigated Jory soil for 16 weeks (n = 10). Data were analyzed using two-factor analysis of variance (ANOVA) [irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment]. Data for Scutellospora calospora are not shown as no measure differed from nonmycorrhizal vines. Data for P were log-transformed to satisfy variance assumptions for ANOVA. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. Different AMF treatments are indicated by the shape of symbols and different nutrients are indicated by color. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

  • Supplemental Fig. 1.

    Roots of ‘Pinot noir’ cleared and stained with trypan blue revealing fungal structures in roots typical of those colonized by Scutello-spora calospora (A) showing only a trace of internal hyphae; Claroideoglomus sp. (B) showing arbuscules and intercellular hyphae; Funneliformis mos-seae (C) showing extensive and coarse intercellular hyphae; Rhizophagus irregularis ( D) showing vesicles/spores, arbuscules, and hyphae; and Glomus sp. 3E (E) showing vesicles, arbuscules, and hyphae after 8 weeks of growth in Jory soil mixed with sand and fumigated prior to inoculation. a = arbuscules; v = vesicles/spores.

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  • Schreiner, R.P 2007 Effects of native and nonnative arbuscular mycorrhizal fungi on growth and nutrient uptake of “Pinot noir” (Vitis vinifera L.) in two soils with contrasting levels of phosphorus Appl. Soil Ecol. 36 205 215 https://doi.org/10.1016/j.apsoil.2007.03.002

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R. Paul Schreiner USDA-ARS, Horticultural Crops Research Laboratory, 3420 NW Orchard Avenue, Corvallis, OR 97330

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Tian Tian Department of Horticulture, Agriculture and Life Sciences Building, Oregon State University, Corvallis, OR 97340

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Contributor Notes

This work was funded by USDA-ARS CRIS Project 2072-21000-055-00D.

We thank Matthew Scott, Suean Ott, and David Janos for the technical assistance. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Current address for T.T.: University of California Cooperative Extension, Kern County, 1031 South Mount Vernon Avenue, Bakersfield, CA 93307

R.P.S. is the corresponding author. E-mail: paul.schreiner@usda.gov.

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  • Fig. 1.

    Effects of fungal isolate and sampling date on root length colonized by mycorrhizal fungal structures (A), root length colonized by arbuscules (B), plant shoot length (C), leaf area (D), shoot biomass (E), and root biomass (F) in ‘Pinot noir’ grapevines grown in fumigated Jory soil (n = 10). Data for (A, B, E, and F) were analyzed using three-factor analysis of variance (ANOVA) [time × irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment], and letters indicate significant groups based on the interaction between time and AMF treatment based on Tukey’s honestly significant difference (HSD) test at 95% confidence. Data for (C) and (D) were analyzed by repeated measures ANOVA, and letters indicate significant groups at each sampling time based on Tukey’s HSD test at 95% confidence. The nonmycorrhizal and Scutellospora calospora treatments were excluded from analysis of root colonization data in (A) and (B). Data for (B, E, and F) were square root transformed to satisfy variance assumptions. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

  • Fig. 2.

    Interactive effect of fungal isolate and sampling date on total vine biomass (A), total vine phosphorus (B), total vine nitrogen (C), total vine calcium (D), total vine manganese (E), and total vine zinc (F) in ‘Pinot noir’ grapevines grown in fumigated Jory soil (n = 10). Data were analyzed using three-factor analysis of variance (ANOVA) [time × irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment], and letters indicate significant groups based on the interaction between date and AMF treatment using Tukey’s honestly significant difference test at 95% confidence. Data for (A, B, C, and E) were square-root-transformed to satisfy variance assumptions. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

  • Fig. 3.

    Relationship between relative biomass and relative whole vine nutrient concentrations of macroelements as altered by fungal isolate in ‘Pinot noir’ grapevines grown in fumigated Jory soil for 16 weeks (n = 10). Data were analyzed using two-factor analysis of variance (ANOVA) [irrigation treatment × arbuscular mycorrhizal fungi (AMF) treatment]. Data for Scutellospora calospora are not shown as no measure differed from nonmycorrhizal vines. Data for P were log-transformed to satisfy variance assumptions for ANOVA. Symbols are pooled means (± SEM) from the wet and dry treatments within each AMF treatment. Different AMF treatments are indicated by the shape of symbols and different nutrients are indicated by color. NM = nonmycorrhizal control; S. cal. = S. calospora; Cl. sp. = Claroideoglomus sp.; F. mos. = F. mosseae; Rh. irr. = R. irregularis; Gl. 3E = Glomus sp. 3E.

  • Supplemental Fig. 1.

    Roots of ‘Pinot noir’ cleared and stained with trypan blue revealing fungal structures in roots typical of those colonized by Scutello-spora calospora (A) showing only a trace of internal hyphae; Claroideoglomus sp. (B) showing arbuscules and intercellular hyphae; Funneliformis mos-seae (C) showing extensive and coarse intercellular hyphae; Rhizophagus irregularis ( D) showing vesicles/spores, arbuscules, and hyphae; and Glomus sp. 3E (E) showing vesicles, arbuscules, and hyphae after 8 weeks of growth in Jory soil mixed with sand and fumigated prior to inoculation. a = arbuscules; v = vesicles/spores.

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