Next Article in Journal
The Coexistence of Local and Global Food Supply Chains: The Lombardy Region Case Study
Next Article in Special Issue
Climate Change Impacts Assessment on Wine-Growing Bioclimatic Transition Areas
Previous Article in Journal
Machine Learning Model for Nutrient Release from Biopolymers Coated Controlled-Release Fertilizer
Previous Article in Special Issue
Effect of Vineyard Floor Management on Seasonal Changes of Cultivable Fungal Diversity in the Rhizosphere
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 10
Issue 11
10.3390/agriculture10110539
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Performance and Establishment of a Commercial Mycorrhizal Inoculant in Viticulture

by
Daniel Rosa
1,*,
Antreas Pogiatzis
1,
Pat Bowen
2,
Vasilis Kokkoris
3,
Andrew Richards
1,*,
Taylor Holland
1 and
Miranda Hart
1
1
Department of Biology, University of British Columbia—Okanagan, 3187 University Way, Kelowna, BC V1V 1V7, Canada
2
Summerland Research and Development Centre, Agriculture and Agri-food Canada, 4200 Highway, 97 South, Summerland, BC V0H 1Z0, Canada
3
Department of Biology, University of Ottawa, 75 Laurier Ave. E., Ottawa, ON K1N 6N5, Canada
*
Authors to whom correspondence should be addressed.
Agriculture 2020, 10(11), 539; https://doi.org/10.3390/agriculture10110539
Submission received: 6 October 2020 / Revised: 5 November 2020 / Accepted: 6 November 2020 / Published: 10 November 2020
(This article belongs to the Special Issue Sustainable Agriculture and Viticulture)
Browse Figures
Versions Notes

Abstract

:
(1) Background: Arbuscular mycorrhizal (AM) fungi are symbiotic organisms that help plants acquire nutrients from the soil in exchange for photosynthetic carbon. Commercial AM fungal inoculants are widely available and are used extensively in agriculture including wine grape production. However, positive growth responses from inoculants are more consistent in the greenhouse compared to the field. (2) Methods: We grew three grapevine rootstocks with and without an AM fungal inoculant in the greenhouse for one year, then they were transplanted to the field for two years. To quantify the establishment of the inoculant, we analyzed root samples with a digital PCR assay. (3) Results: We show that AM fungal inoculation increased biomass production only in the greenhouse. After two growing seasons in the field, the commercial inoculant colonized roots but did not increase biomass production compared to uninoculated rootstocks. (4) Conclusions: This study highlights that AM fungal inoculants do not always promote growth of grapevines in the field. Future research should focus on inoculant strains designed for viticulture applications and take rootstock into consideration to maximize their efficacy.

1. Introduction

Arbuscular mycorrhizal (AM) fungi are obligate root symbionts that associate with most plants, including grapevines. They provide many benefits to their host, such as nutrient uptake and stress tolerance, in exchange for carbon [1,2]. Over the years, viticulture research has shown that grapevines are highly responsive to AM fungi [3,4,5,6,7] which elucidated the potential of AM fungal inoculation as a management strategy [8].
While there is evidence that inoculation of AM fungi in the greenhouse results in positive plant growth responses [3,9,10,11,12,13,14], the benefits of AM fungal inoculants in field studies are not as consistent [4,15,16]. Compared to resident AM fungi, commercial inoculants may be more successful in the greenhouse if they sporulate and grow quickly in disturbed soil [17]. AM fungal inoculation of grapevines in the field does not always result in increased shoot production [13], overall biomass [18] or yield [19]. Although inoculation may improve growth during the first few years, uninoculated plants may eventually become colonized by resident AM fungi [20] and perform as good or better than inoculated plants [21].
While commercial inoculants are beneficial in broadacre farming [22,23], there is reason to believe that perennial systems may benefit less because they have relatively intact soil ecosystems which experience low levels of disturbance after initial soil preparation [24]. Thus, they may already possess effective resident mycorrhizal populations making inoculation redundant, or even unsuccessful if priority effects are important for inoculant establishment [25].
Inoculation with commercial AM fungi may not be effective due to variation in host response to a particular fungus [26,27]. In addition, soil type and mineral profiles can heavily influence host–symbiont interactions [28]. Finally, interactions between host, symbiont, and soil source can determine the direction and intensity of the plant response to the mycorrhizal inoculant [29]. These factors make it difficult to determine if inoculation will be successful in an agroecosystem.
Despite variation in host–symbiont responses, some growers augment resident populations with commercial AM fungal inoculants to maximize the benefits of AM fungi [30]. In viticulture, grapevine rootstocks are grown in nurseries for the first season, where AM fungal inoculants are often applied aiming to increase the survival and growth rates [31]. Under controlled conditions, rootstock genotypes show differences in root colonization and shoot growth in response to AM inoculation [32]. Similarly, the composition of AM fungal communities in a vineyard could be driven primarily by host identity [33]. Variation in AM fungal response among rootstocks may affect their response to commercial inoculants and thus, the efficacy of commercial inoculants in vineyards.
This study aimed to evaluate the host response of three grapevine rootstocks to a commercial AM fungal inoculant. We hypothesized that inoculation would improve growth of grapevine rootstocks in the greenhouse but not in the field after transplantation.

2. Materials and Methods

In order to examine the effect of AM fungal inoculation on rootstock identity we conducted a three-year experiment. The first year of the experiment (nursery) took place in a greenhouse and then transitioned to the field for the next two years. The greenhouse and the experimental field were located at the Summerland Research and Development Centre (SuRDC) in Summerland, BC Canada, (49°33′49.2″ N–119°38′19.0″ W) and the experiment took place from September 2015 to March 2018. Additional site details including soil physiochemical properties are listed in Table A1.
The experiment consisted of a factorial combination of two AM fungi treatments (with and without AM fungal inoculation) and three rootstocks. Each treatment had eight replications (n = 48) in a complete randomized design.

2.1. Rootstock Treatments

We selected Riparia Gloire (Vitis riparia), Schwarzmann (Vitis riparia × Vitis rupestris), and Salt Creek (Vitis champinii), three rootstocks commonly used in North America [34,35]. To generate the rootstocks, dormant cuttings containing two buds each were placed in auxin solution (1500 mg L-1 of indol-3-butyric acid) for 30 s then transferred to moist perlite filled flats in a growth chamber at 28 °C until callus formation. We selected 16 cuttings from each rootstock cultivar based on callus development and rooted them in moist Turface-filled flats until appearance of roots. Finally, rooted cuttings were transplanted into 7.6-L pots containing expanded clay (Turface; Profile products LCC) and placed in a greenhouse at SuRDC. Plants were supplied with approximately 60 mL (3 × 20 mL) of water every day, using an 8-emitter circular line within each pot to provide water uniformly onto the medium surface.

2.2. AM Fungal Inoculant

We used the commercial inoculant MYKE® PRO GR (Premier Tech, Inc) that contained Rhizoglomus irregulare (DAOM 197198) Schenck & Smith (synonym Rhizophagus irregularis, Glomus intraradices) (Sieverding et al., 2015). Approximately 15 g (~2130 spores) were added to each pot, following manufacturer’s instructions. We used vermiculite as a spore carrier and expanded clay as a growth medium (Turface, Profile products LCC).
During the nursery period, plants were hand watered every day with approximately 60 mL (3 × 20 mL). Plants were manually fertilized every two weeks with 60 mL of (1) solution of 0.42 g L-1 of 12-2-14 (50 ppm N) during the first two months, and (2) 1.5 g L-1 of 20-20-20 (300 ppm N) for the next two months. During foilar establishment, plants were sprayed once with sulphur (S) (Kumulus DF, BASF) to prevent mildew.
Rooted cuttings grew for four months in the greenhouse. After this growth period, each vine was trimmed with a set of pruners and the material was weighed. Leaf number was also recorded before transplantation to the field. The field trial took place over two growing seasons (2016–2017) and consisted of eight blocks spanned across one row. A block was defined as the space between two trellis posts about five metres apart. Treatments were randomly placed within each block and inoculated blocks were separated from uninoculated control blocks by a guard plant.
In 2018 after the two-year growth period, vines were removed from the soil and 10 samples of roots (~5 g each) were randomly collected from each plant for DNA extraction. Roots and shoots were separated for biomass quantification.

2.3. Biomass Production

At the end of each growing season, the shoots were collected and dried at 65 °C to constant mass and then the dry matter was determined using a precision scale. In the last growing season, when the plants were pulled out from the soil, the root dry matter was determined by following the same protocol used for shoots.

2.4. Quantification of Inoculant Establishment Via Digital PCR Assay

2.4.1. DNA Extraction

At the time of harvest each season, ten root samples of 0.25 g were randomly collected from each plant root system for the following rootstocks: Riparia Gloire (Vitis riparia), Salt Creek (Vitis champinii), and Schwarzmann (Vitis riparia × Vitis rupestris). Root samples were stored at −20 °C and surface sterilized with 5% sodium hypochlorite before DNA extraction. DNA extractions were performed using the FastDNA SPIN kit for Soil (MP Biomedicals-USA).

2.4.2. Digital PCR Assay

We used droplet digital PCR (ddPCR) to determine the establishment of the commercial mycorrhizal inoculant as well as quantify its presence in the rootstocks. Using a ddPCR probe assay, we tested rootstocks for the presence of R. irregulare DAOM 197198 with the Bio-Rad QX100 Droplet Digital PCR system (Bio-Rad Laboratories, Inc., Hercules, California). Droplets were generated according to manufacturer’s instructions. We amplified a region of the cox3-rnl intergenic mtDNA using a primer pair and probe specific to R. irregulare DAOM 197198, forward 5′-AGCAAATCTAAGTTCCTCAGAG-3′, reverse 5′-ACTTCTATGGCTTTGTACAGG -3′, and probe 5′-FAM/CCCACCAGG/ZEN/GCAGATTAATCTTCCTT/3IABKFQ-3′ [36].
Twenty μL of total reaction volume was used which contained 10 μL of ddPCR Supermix for probes (Bio-Rad Inc.), 1 μL of primer-probe mix (diluted 20×, 500 nM primers and 250 nM probe in final reaction) (Integrated DNA Technologies), 2 μL of root DNA and 7 μL of DNase free water. After droplet generation, the final reaction volume per sample was 40 μL. DNA was amplified using the Bio-Rad C1000 Thermal Cycler (Bio-Rad) using the following settings: initial heating at 95 °C for 10 min, 40 cycles with denaturation at 94 °C for 30 s and annealing at 59 °C for 30 s, and a final step at 98 °C for 10 min. A ramp rate of 2 °C/s was used for every step. Each plate contained three non-template controls (NTC) to detect contamination and three environmental negative controls (ENC) to set an accurate fluorescence threshold. ENCs consisted of a control with environmental DNA but without DNA from the inoculant used in this study. Droplets were analyzed with the BioRad QX100 Droplet Reader and amplification data was collected using Quantalife software ver. 1.7.4. (Bio-Rad).
In order to obtain abundance data per gram of root tissue, the raw Quantalife software data (copies per μL of reaction) were back-calculated with the following formula [36]:
Cpgr = (Quantalife value ∗ (RV/SQ) ∗ EQ)/QR
where Cpgr represents target copies per gram of root, Quantalife value is copies per μL of reaction, RV is volume of the reaction, SQ is sample DNA quantity used in the reaction, EQ is quantity of DNA extraction, and QR is quantity of root tissue used for the extraction.

2.5. Statistical Analyses

2.5.1. Establishment

In order to assess establishment of the AM fungi, we used a linear mixed model lmer [37] to compare between control and inoculated rootstocks, with “block” as a random factor and “inoculation” as a fixed factor. Data was assessed for normality by plotting a histogram of the model residuals using the hist function in graphics (3.6.2). Log transformations were applied to all analyses to satisfy model assumptions. Pairwise comparisons were made using the emmeans package (1.4.3.01). We asked whether the abundance of the AM fungal inoculant was due to each rootstock.

2.5.2. Software

All statistical analyses were performed using the RStudio version 1.2.5033 (R Core Team 2019).

3. Results

3.1. Growth Response

The inoculation of AM fungi in the greenhouse-grown cultivation increased the shoot dry matter production in two of the three rootstocks tested, Riparia Gl. (p = 0.043) and Salt Creek (p = 0.012) (Figure 1). AM fungal inoculation did not increase shoot dry mass production in Schwarzmann.
The number of leaves on the vines grown in the greenhouse differed among the rootstocks (Figure A1). Among inoculated rootstocks, the highest number of leaves was found on Salt Creek grapevines (p < 0.001), while the lowest number of leaves was found on Riparia Gl. vines.
After rootstocks grew in the field for two years, we observed that the inoculation of AM fungi did not increase shoot dry matter production, instead it decreased the dry matter production for Schwarzmann (p = 0.06) (Figure 2). The rootstocks, Riparia Gl. and Salt creek, neither increased or decreased shoot dry mass production by AM fungal inoculation.
Contrary to the growth responses in the greenhouse, the shoot dry matter obtained after one year of field cultivation was highest in Riparia Gl. vines (p < 0.001). Salt Creek produced the lowest amount of shoot biomass although not statistically different from Schwarzmann (Figure A2).
We also observed that the root dry matter production from rootstocks grown in the field for two years, increased by the inoculation of AM fungi for Salt Creek (p < 0.001) (Figure 3). Riparia Gl. and Schwarzmann neither increased nor decreased in shoot dry mass production by AM fungal inoculation.
Similar to the first growing season, the shoot dry matter yield obtained after two years of field cultivation was highest in Riparia Gl. vines (p < 0.001). Salt Creek produced the lowest amount of shoot biomass although not statistically different from Schwarzmann (Figure A3). The root dry matter of the vines obtained at two years of field cultivation showed no difference between the rootstocks (p = 0.278) (Figure A4).

3.2. Establishment of Commercial Inoculant

Overall, we found that the inoculant established and persisted in the field over all growing seasons (Figure 4). All of the three rootstocks, Riparia Gl., Salt Creek, and Schwarzmann, tested positive for Rhizoglomus irregulare (DAOM 197198) which could not be detected in high numbers in control vines.

4. Discussion

In this study, we observed limited success of AM fungal inoculation on the performance of grapevine rootstocks. Only two rootstock cultivars in the greenhouse showed increased dry biomass, Riparia Gl. and Salt Creek, but this success was not maintained when the vines were transplanted to the field.
Several studies have found positive results on plant performance using AM fungi-containing inoculants [38,39,40,41]. However, in other cases inoculation was not effective [42,43,44]. Greenhouse studies that evaluate AM inoculants on plant performance do not always capture the complexities of field conditions [45]. This makes it clear that positive growth responses observed from inoculation in the greenhouses are not a great predictor of success under field conditions.
In many cases greenhouse studies are performed using autoclaved soil which means there is no comparison between the AM inoculant and resident AM fungi. [46,47]. In addition, the range of environmental conditions that the isolate has contact with in the field is much larger than under greenhouse conditions, which are tightly controlled and generally favourable to AM fungi. These conditions may compromise the inoculant performance in the field [48].
Failure to adapt to local field conditions can also impair the AM fungal inoculant. Agricultural fields typically harbour a lower rate of mycorrhizal fungi compared to natural environments [49,50]. This suggests that the unique agricultural conditions, including high disturbance via tillage and high fertilization, may select AM fungi strains that are better adapted to the local agricultural conditions than the introduced isolates contained in the inoculant. In their majority, mycorrhizal inoculants are mass produced under in-vitro conditions that represent a highly artificial environment which is extremely different from any natural environment [51] It is possible that studies conducted in greenhouses may overestimate the success of mycorrhizal fungal inoculant performance, since field studies often result in poorer grapevine performance compared to the greenhouse. As a result, field studies often result in poorer grapevine performance compared to the greenhouse [52].
After two years in the field, the lack of performance increase in inoculated vines may be due to the fact that the foreign isolate was not adapted to the local environmental conditions and/or did not engage in an efficient mutualism with the rootstock. Here, we showed that the inoculant successfully colonised roots in the field but did not increase vine performance. Mycorrhizal associations act on a continuum from mutualism to parasitism [38,53] and previous studies show that suboptimal environmental conditions (light, minerals) can impact the interaction [54]. Likewise, AM fungi, although a generalist species, will benefit some plants more than others [55]. It should be emphasized that AM fungi-containing inoculants are intended for general use and are not designed for a specific host species [56] although some companies do advertise use with certain crops.
To increase the efficiency of inoculants, some authors suggest using a product that contains multiple AM fungi isolates, thereby increasing the chances that one or more isolates may better adapt. Another possibility is to select locally occurring isolates that are more likely to perform well in the local environment [48]. Future studies that test specific strains for specific applications are needed.
The fact that the commercial inoculant persisted in rootstocks during the two field years poses a risk of invasion [57,58] and alteration of resident AM fungal communities in roots [59]. If the commercial inoculant can expand its hyphal network from the rootstocks and/or sporulate rapidly, it may colonise vineyard weeds, cover crops, and other nearby plants [60,61]. This may change the priority effects of AM fungi [62], meaning that the commercial inoculant could rapidly colonize and occupy a large proportion of diverse neighboring roots which inevitably affects the colonization, growth ability, and survival of other fungal and bacterial species that naturally occur around roots and hyphae [63,64,65]. Such changes in fungal and bacterial communities could shift ecosystem functioning and further research is required to determine if this impacts crop performance.

5. Conclusions

Inoculation of the grapevines with Rhizoglomus irregulare (DAOM 197198) subtly favoured the performance of Riparia Gl. and Salt Creek grapevine rootstocks in the greenhouse. After transplantation to the field, inoculation with AM fungi did not provide any benefit to grapevine growth and decreased the performance of Schwarzmann. The inoculated fungal strain successfully established and maintained the symbiosis with grapevines detected after three years of inoculation, but without benefits. Future research should focus on the development of different strains for applications in viticulture and other perennial agroecosystems as well as elucidate the risk of invasion and potential microbial shifts if a commercial inoculant is to persist in soil.

Author Contributions

Conceptualization, D.R., P.B., V.K., T.H. and M.H.; methodology, D.R., A.P. and T.H.; validation, V.K., P.B. and M.H.; formal analysis, A.R.; data curation, D.R.; Writing—Original draft preparation, D.R.; Writing—Review and editing, A.R. and M.H.; supervision, P.B.; funding acquisition, P.B. and M.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Agriculture and Agri-Food Canada, Going Forward.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Table
Table A1. Site information and soil physiochemical properties during the 2016 growing season.
Table A1. Site information and soil physiochemical properties during the 2016 growing season.
Site Information
Soil textureLoamy sand
pH6.68
Organic matter (%)2.27
Nitrogen (Kjeldahl)0.03
Phosphorous (Mehlich 3)57.86
Irrigation typeDrip
Agriculture 10 00539 g0a1 550
Figure A1. Total number of leaves on rootstocks inoculated with AM fungi and grown in the greenhouse. Letters above treatments represent significant differences at p < 0.05.
Figure A1. Total number of leaves on rootstocks inoculated with AM fungi and grown in the greenhouse. Letters above treatments represent significant differences at p < 0.05.
Agriculture 10 00539 g0a1
Agriculture 10 00539 g0a2 550
Figure A2. Shoot dry matter (g) in grapevine rootstocks inoculated with AM fungi at one year of field cultivation. Letters above treatments represent significant differences at p < 0.05.
Figure A2. Shoot dry matter (g) in grapevine rootstocks inoculated with AM fungi at one year of field cultivation. Letters above treatments represent significant differences at p < 0.05.
Agriculture 10 00539 g0a2
Agriculture 10 00539 g0a3 550
Figure A3. Shoot dry matter (g) in grapevine rootstocks inoculated with AM fungi at two years of field cultivation. Letters above boxes indicate significant differences at p < 0.05.
Figure A3. Shoot dry matter (g) in grapevine rootstocks inoculated with AM fungi at two years of field cultivation. Letters above boxes indicate significant differences at p < 0.05.
Agriculture 10 00539 g0a3
Agriculture 10 00539 g0a4 550
Figure A4. Root dry matter (g) in grapevine rootstocks inoculated with AM fungi after two years of field cultivation.
Figure A4. Root dry matter (g) in grapevine rootstocks inoculated with AM fungi after two years of field cultivation.
Agriculture 10 00539 g0a4

References

  1. Cabral, L.; Soares, C.R.F.S.; Giachini, A.J.; Siqueira, J.O. Arbuscular mycorrhizal fungi in phytoremediation of contaminated areas by trace elements: Mechanisms and major benefits of their applications. World J. Microbiol. Biotechnol. 2015, 31, 1655–1664. [Google Scholar] [CrossRef] [PubMed]
  2. Delavaux, C.S.; Smith-Ramesh, L.M.; Kuebbing, S.E. Beyond nutrients: A meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 2017, 98, 2111–2119. [Google Scholar] [CrossRef] [PubMed]
  3. Brunetto, G.; Rosa, D.J.; Ambrosini, V.G.; Heinzen, J.; Ferreira, P.A.A.; Ceretta, C.A.; Soares, C.R.F.S.; Melo, G.W.B.; Soriani, H.H.; Nicoloso, F.T.; et al. Use of phosphorus fertilization and mycorrhization as strategies for reducing copper toxicity in young grapevines. Sci. Hortic. 2019, 248, 176–183. [Google Scholar] [CrossRef]
  4. Holland, T.; Bowen, P.; Kokkoris, V.; Urbez-Torres, J.R.; Hart, M. Does Inoculation with Arbuscular Mycorrhizal Fungi Reduce Trunk Disease in Grapevine Rootstocks? Horticulturae 2019, 5, 61. [Google Scholar] [CrossRef] [Green Version]
  5. Bruisson, S.; Maillot, P.; Schellenbaum, P.; Walter, B.; Gindro, K.; Deglène-Benbrahim, L. Arbuscular mycorrhizal symbiosis stimulates key genes of the phenylpropanoid biosynthesis and stilbenoid production in grapevine leaves in response to downy mildew and grey mould infection. Phytochemistry 2016, 131, 92–99. [Google Scholar] [CrossRef]
  6. Ferrer, R.L.; Přikryl, Z.; Gryndler, M.; Vančaar;cura, V. Natural Occurrence of Vesicular-Arbuscular Fungi in Grape Vine and Apple Trees. Dev. Soil Sci. 1989, 18, 141–147. [Google Scholar] [CrossRef]
  7. Biricolti, S.; Ferrini, F.; Rinaldelli, E.; Tamantini, I.; Vignozzi, N. VAM Fungi and Soil Lime Content Influence Rootstock Growth and Nutrient Content. Am. J. Enol. Vitic. 1997, 48, 93–99. [Google Scholar]
  8. Trouvelot, S.; Bonneau, L.; Redecker, D.; van Tuinen, D.; Adrian, M.; Wipf, D. Arbuscular mycorrhiza symbiosis in viticulture: A review. Agron. Sustain. Dev. 2015, 35, 1449–1467. [Google Scholar] [CrossRef] [Green Version]
  9. Azcón, R.; Medina, A.; Roldán, A.; Biró, B.; Vivas, A. Significance of treated agrowaste residue and autochthonous inoculates (Arbuscular mycorrhizal fungi and Bacillus cereus) on bacterial community structure and phytoextraction to remediate soils contaminated with heavy metals. Chemosphere 2009, 75, 327–334. [Google Scholar] [CrossRef]
  10. Ames, R.N.; Reid, C.P.P.; Ingham, E.R. Rhizosphere bacterial population responses to root colonization by a vesicular-arbuscular mycorrh1zal fungus. New Phytol. 1984, 96, 555–563. [Google Scholar] [CrossRef]
  11. Zhang, W.; Cao, J.; Zhang, S.; Wang, C. Effect of earthworms and arbuscular mycorrhizal fungi on the microbial community and maize growth under salt stress. Appl. Soil Ecol. 2016, 107, 214–223. [Google Scholar] [CrossRef]
  12. Torres, N.; Goicoechea, N.; Antolín, M.C. Antioxidant properties of leaves from different accessions of grapevine (Vitis vinifera L.) cv. Tempranillo after applying biotic and/or environmental modulator factors. Ind. Crops Prod. 2015, 76, 77–85. [Google Scholar] [CrossRef]
  13. Camprubí, A.; Estaún, V.; Nogales, A.; García-Figueres, F.; Pitet, M.; Calvet, C. Response of the grapevine rootstock Richter 110 to inoculation with native and selected arbuscular mycorrhizal fungi and growth performance in a replant vineyard. Mycorrhiza 2008, 18, 211–216. [Google Scholar] [CrossRef] [PubMed]
  14. Lovato, P.; Guillemin, J.; Gianinazzi, S. Application of commercial arbuscular endomycorrhizal fungal inoculants to the establishment of micropropagated grapevine rootstock and pineapple plants. Agronomie 1992, 12, 873–880. [Google Scholar] [CrossRef] [Green Version]
  15. Holland, T.C.; Hart, M.M.; Bogdanoff, C.; Bowen, P. Response of grapevine rootstocks to soil inocula from different sources. Am. J. Enol. Vitic. 2018, 69, 94–100. [Google Scholar] [CrossRef]
  16. Antolín, M.C.; Izurdiaga, D.; Urmeneta, L.; Pascual, I.; Irigoyen, J.J.; Goicoechea, N. Dissimilar responses of ancient grapevines recovered in Navarra (Spain) to arbuscular mycorrhizal symbiosis in terms of berry quality. Agronomy 2020, 10, 473. [Google Scholar] [CrossRef] [Green Version]
  17. Antunes, P.M.; Koch, A.M.; Dunfield, K.E.; Hart, M.M.; Downing, A.; Rillig, M.C.; Klironomos, J.N. Influence of commercial inoculation with Glomus intraradices on the structure and functioning of an AM fungal community from an agricultural site. Plant Soil 2009, 317, 257–266. [Google Scholar] [CrossRef]
  18. Nogales, A.; Luque, J.; Estaún, V.; Camprubí, A.; Garcia-Figueres, F.; Calvet, C. Differential Growth of Mycorrhizal Field-Inoculated Grapevine Rootstocks in Two Replant Soils. Am. J. Enol. Vitic. 2009, 60, 484–489. [Google Scholar]
  19. Berdeni, D.; Cotton, T.E.A.; Daniell, T.J.; Bidartondo, M.I.; Cameron, D.D.; Evans, K.L. The effects of arbuscular mycorrhizal fungal colonisation on nutrient status, growth, productivity, and canker resistance of apple (Malus pumila). Front. Microbiol. 2018, 9, 1461. [Google Scholar] [CrossRef]
  20. Estaún, V.; Camprubí, A.; Calvet, C.; Pinochet, J. Nursery and field response of olive trees inoculated with two arbuscular mycorrhizal fungi, Glomus intraradices and Glomus mosseae. J. Am. Soc. Hortic. Sci. 2003, 128, 767–775. [Google Scholar] [CrossRef] [Green Version]
  21. Middleton, E.L.; Richardson, S.; Koziol, L.; Palmer, C.E.; Yermakov, Z.; Henning, J.A.; Schultz, P.A.; Bever, J.D. Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 2015, 6, art276. [Google Scholar] [CrossRef]
  22. Bona, E.; Cantamessa, S.; Massa, N.; Manassero, P.; Marsano, F.; Copetta, A.; Lingua, G.; D’Agostino, G.; Gamalero, E.; Berta, G. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: A field study. Mycorrhiza 2017, 27, 1–11. [Google Scholar] [CrossRef] [PubMed]
  23. Köhl, L.; Lukasiewicz, C.E.; van der Heijden, M.G.A. Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant Cell Environ. 2016, 39, 136–146. [Google Scholar] [CrossRef] [PubMed]
  24. Bruggisser, O.T.; Schmidt-Entling, M.H.; Bacher, S. Effects of vineyard management on biodiversity at three trophic levels. Biol. Conserv. 2010, 143, 1521–1528. [Google Scholar] [CrossRef] [Green Version]
  25. Ryan, M.H.; Kirkegaard, J.A. The agronomic relevance of arbuscular mycorrhizas in the fertility of Australian extensive cropping systems. Agric. Ecosyst. Environ. 2012, 163, 37–53. [Google Scholar] [CrossRef]
  26. Klironomos, J.N.J. Host-specificity and functional diversity among arbuscular mycorrhizal fungi. Microb. Biosyst. New Front. 2000, 1, 845–851. [Google Scholar]
  27. Klironomos, J.N. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 2003, 84, 2292–2301. [Google Scholar] [CrossRef]
  28. Herrera-Peraza, R.A.; Hamel, C.; Fernández, F.; Ferrer, R.L.; Furrazola, E. Soil-strain compatibility: The key to effective use of arbuscular mycorrhizal inoculants? Mycorrhiza 2011, 21, 183–193. [Google Scholar] [CrossRef] [Green Version]
  29. Rúa, M.A.; Antoninka, A.; Antunes, P.M.; Chaudhary, V.B.; Gehring, C.; Lamit, L.J.; Piculell, B.J.; Bever, J.D.; Zabinski, C.; Meadow, J.F.; et al. Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol. Biol. 2016, 16, 122. [Google Scholar] [CrossRef] [Green Version]
  30. Gianinazzi, S.; Vosátka, M. Inoculum of arbuscular mycorrhizal fungi for production systems: Science meets business. Can. J. Bot. 2004, 82, 1264–1271. [Google Scholar] [CrossRef]
  31. Holland, T.; Bowen, P.; Kokkoris, V.; Richards, A.; Rosa, D.; Hart, M. The effect of root pruning on the arbuscular mycorrhizal symbiosis in grapevine rootstocks. Chem. Biol. Technol. Agric. 2019, 6, 21. [Google Scholar] [CrossRef] [Green Version]
  32. Pogiatzis, A. Comparative Responses of Six Grapevine Rootstocks to Inoculation with Arbuscular Mycorrhizal Fungi Based on Root Traits. Master’s Thesis, University of British Columbia, Kelowna, BC, Canada, 2017. Available online: https://open.library.ubc.ca/cIRcle/collections/ubctheses/24/items/1.0347985 (accessed on 2 November 2020).
  33. Holland, T.C.; Bowen, P.; Bogdanoff, C.; Hart, M.M. How distinct are arbuscular mycorrhizal fungal communities associating with grapevines? Biol. Fertil. Soils 2014, 50, 667–674. [Google Scholar] [CrossRef]
  34. BC Wine Grape Council. 2010 Best Practices Guide for Grapes; British Columbia Ministry of Agriculture and Lands: Peachland, BC, Canada, 2010.
  35. Lowe, K.M.; Walker, M.A. Genetic linkage map of the interspecific grape rootstock cross Ramsey (Vitis champinii) × Riparia Gloire (Vitis riparia). Theor. Appl. Genet. 2006, 112, 1582–1592. [Google Scholar] [CrossRef] [PubMed]
  36. Kokkoris, V.; Li, Y.; Hamel, C.; Hanson, K.; Hart, M. Site specificity in establishment of a commercial arbuscular mycorrhizal fungal inoculant. Sci. Total Environ. 2019, 660, 1135–1143. [Google Scholar] [CrossRef] [PubMed]
  37. Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 2015, 67, 1–48. [Google Scholar] [CrossRef]
  38. Hoeksema, J.D.; Chaudhary, V.B.; Gehring, C.A.; Johnson, N.C.; Karst, J.; Koide, R.T.; Pringle, A.; Zabinski, C.; Bever, J.D.; Moore, J.C.; et al. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol. Lett. 2010, 13, 394–407. [Google Scholar] [CrossRef]
  39. Pellegrino, E.; Bedini, S.; Avio, L.; Bonari, E.; Giovannetti, M. Field inoculation effectiveness of native and exotic arbuscular mycorrhizal fungi in a Mediterranean agricultural soil. Soil Biol. Biochem. 2011, 43, 367–376. [Google Scholar] [CrossRef]
  40. Pellegrino, E.; Öpik, M.; Bonari, E.; Ercoli, L. Responses of wheat to arbuscular mycorrhizal fungi: A meta-analysis of field studies from 1975 to 2013. Soil Biol. Biochem. 2015, 84, 210–217. [Google Scholar] [CrossRef]
  41. Hernádi, I.; Sasvári, Z.; Albrechtová, J.; Vosátka, M.; Posta, K. Arbuscular Mycorrhizal Inoculant Increases Yield of Spice Pepper and Affects the Indigenous Fungal Community in the Field. HortScience 2012, 47, 603–606. [Google Scholar] [CrossRef] [Green Version]
  42. Ortas, I.; Sari, N.; Akpinar, Ç.; Yetisir, H. Screening mycorrhiza species for plant growth, P and Zn uptake in pepper seedling grown under greenhouse conditions. Sci. Hortic. 2011, 128, 92–98. [Google Scholar] [CrossRef]
  43. Janoušková, M.; Krak, K.; Wagg, C.; Štorchová, H.; Caklová, P.; Vosátka, M. Effects of Inoculum Additions in the Presence of a Preestablished Arbuscular Mycorrhizal Fungal Community. Appl. Environ. Microbiol. 2013, 79, 6507–6515. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Emam, T. Local soil, but not commercial AMF inoculum, increases native and non-native grass growth at a mine restoration site. Restor. Ecol. 2016, 24, 35–44. [Google Scholar] [CrossRef]
  45. Berruti, A.; Lumini, E.; Balestrini, R.; Bianciotto, V. Arbuscular Mycorrhizal Fungi as Natural Biofertilizers: Let’s Benefit from Past Successes. Front. Microbiol. 2016, 6, 1559. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Wang, J.; Zhong, H.; Zhu, L.; Yuan, Y.; Xu, L.; Wang, G.G.; Zhai, L.; Yang, L.; Zhang, J. Arbuscular mycorrhizal fungi effectively enhances the growth of Gleditsia sinensis Lam. Seedlings under greenhouse conditions. Forests 2019, 10, 567. [Google Scholar] [CrossRef] [Green Version]
  47. Urcelay, C.; Vaieretti, M.V.; Pérez, M.; Díaz, S. Effects of arbuscular mycorrhizal colonisation on shoot and root decomposition of different plant species and species mixtures. Soil Biol. Biochem. 2011, 43, 466–468. [Google Scholar] [CrossRef]
  48. Verbruggen, E.; van der Heijden, M.G.A.; Rillig, M.C.; Kiers, E.T. Mycorrhizal fungal establishment in agricultural soils: Factors determining inoculation success. New Phytol. 2013, 197, 1104–1109. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Oehl, F.; Laczko, E.; Bogenrieder, A.; Stahr, K.; Bösch, R.; van der Heijden, M.; Sieverding, E. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol. Biochem. 2010, 42, 724–738. [Google Scholar] [CrossRef]
  50. Schnoor, T.K.; Mårtensson, L.-M.; Olsson, P.A. Soil disturbance alters plant community composition and decreases mycorrhizal carbon allocation in a sandy grassland. Oecologia 2011, 167, 809–819. [Google Scholar] [CrossRef]
  51. Kokkoris, V.; Hart, M.M. In vitro propagation of arbuscular mycorrhizal fungi may drive fungal evolution. Front. Microbiol. 2019, 10, 22. [Google Scholar] [CrossRef]
  52. Lekberg, Y.; Koide, R.T. Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003. New Phytol. 2005, 168, 189–204. [Google Scholar] [CrossRef]
  53. Johnson, N.C.; Graham, J.H.; Smith, F.A. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 1997, 135, 575–585. [Google Scholar] [CrossRef]
  54. Johnson, N.C. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol. 2010, 185, 631–647. [Google Scholar] [CrossRef] [PubMed]
  55. Wilson, G.W.; Hartnett, D.C. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am. J. Bot. 1998, 85, 1732–1738. [Google Scholar] [CrossRef] [PubMed]
  56. Faye, A.; Dalpé, Y.; Ndung’u-Magiroi, K.; Jefwa, J.; Ndoye, I.; Diouf, M.; Lesueur, D. Evaluation of commercial arbuscular mycorrhizal inoculants. Can. J. Plant Sci. 2013, 93, 1201–1208. [Google Scholar] [CrossRef]
  57. Hart, M.M.; Antunes, P.M.; Abbott, L.K. Unknown risks to soil biodiversity from commercial fungal inoculants. Nat. Ecol. Evol. 2017, 1, 0115. [Google Scholar] [CrossRef]
  58. Ricciardi, A.; Blackburn, T.M.; Carlton, J.T.; Dick, J.T.A.; Hulme, P.E.; Iacarella, J.C.; Jeschke, J.M.; Liebhold, A.M.; Lockwood, J.L.; MacIsaac, H.J.; et al. Invasion Science: A Horizon Scan of Emerging Challenges and Opportunities. Trends Ecol. Evol. 2017, 32, 464–474. [Google Scholar] [CrossRef] [Green Version]
  59. Mummey, D.L.; Antunes, P.M.; Rillig, M.C. Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol. Biochem. 2009, 41, 1173–1179. [Google Scholar] [CrossRef]
  60. Thomsen, C.N.; Hart, M.M. Using invasion theory to predict the fate of arbuscular mycorrhizal fungal inoculants. Biol. Invasions 2018, 20, 2695–2706. [Google Scholar] [CrossRef]
  61. Camargo-Ricalde, S.L. Dispersal, distribution and establishment of arbuscular mycorrhizal fungi: A review. Bot. Sci. 2017, 33. [Google Scholar] [CrossRef] [Green Version]
  62. Werner, G.D.A.; Kiers, E.T. Order of arrival structures arbuscular mycorrhizal colonization of plants. New Phytol. 2015, 205, 1515–1524. [Google Scholar] [CrossRef]
  63. Toljander, J.F.; Artursson, V.; Paul, L.R.; Jansson, J.K.; Finlay, R.D. Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol. Lett. 2006, 254, 34–40. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Andrade, G.; Mihara, K.L.; Linderman, R.G.; Bethlenfalvay, G.J. Bacteria from rhizosphere and hyphosphere soils of different arbuscular-mycorrhizal fungi. Plant Soil 1997, 192, 71–79. [Google Scholar] [CrossRef]
  65. Giovannini, L.; Palla, M.; Agnolucci, M.; Avio, L.; Sbrana, C.; Turrini, A.; Giovannetti, M. Arbuscular Mycorrhizal Fungi and Associated Microbiota as Plant Biostimulants: Research Strategies for the Selection of the Best Performing Inocula. Agronomy 2020, 10, 106. [Google Scholar] [CrossRef] [Green Version]
Agriculture 10 00539 g001 550
Figure 1. Above ground biomass (grams) of greenhouse-grown rootstocks during the first year. Blue plots represent uninoculated while red plots represent inoculated rootstocks. Red stars above inoculated plots depict significant positive AM fungal response compared to uninoculated control. Statistical analysis was performed on the log scale.
Figure 1. Above ground biomass (grams) of greenhouse-grown rootstocks during the first year. Blue plots represent uninoculated while red plots represent inoculated rootstocks. Red stars above inoculated plots depict significant positive AM fungal response compared to uninoculated control. Statistical analysis was performed on the log scale.
Agriculture 10 00539 g001
Agriculture 10 00539 g002 550
Figure 2. Above ground biomass (grams) of grapevine rootstocks after two years of field cultivation. Blue plots represent uninoculated (control) while red plots represent inoculated rootstocks. Statistical analysis was performed on the log scale.
Figure 2. Above ground biomass (grams) of grapevine rootstocks after two years of field cultivation. Blue plots represent uninoculated (control) while red plots represent inoculated rootstocks. Statistical analysis was performed on the log scale.
Agriculture 10 00539 g002
Agriculture 10 00539 g003 550
Figure 3. Below ground biomass (grams) of grapevine rootstocks after two years of field cultivation. Blue plots represent uninoculated while red plots represent inoculated rootstocks. Red stars above inoculated plots depict significant positive AM fungal response compared to uninoculated control. Statistical analysis was performed on the log scale.
Figure 3. Below ground biomass (grams) of grapevine rootstocks after two years of field cultivation. Blue plots represent uninoculated while red plots represent inoculated rootstocks. Red stars above inoculated plots depict significant positive AM fungal response compared to uninoculated control. Statistical analysis was performed on the log scale.
Agriculture 10 00539 g003
Agriculture 10 00539 g004 550
Figure 4. DNA copies per gram of roots (log(x)) of Rhizoglomus irregulare (DAOM 197198), found in the roots of grapevine rootstocks in the second year of the field study. Red boxes represent control vines and, the blue boxes represent AM fungi inoculated vines. Letters above boxes indicate significant differences within the rootstock (control and inoculated) by t-test (p < 0.001).
Figure 4. DNA copies per gram of roots (log(x)) of Rhizoglomus irregulare (DAOM 197198), found in the roots of grapevine rootstocks in the second year of the field study. Red boxes represent control vines and, the blue boxes represent AM fungi inoculated vines. Letters above boxes indicate significant differences within the rootstock (control and inoculated) by t-test (p < 0.001).
Agriculture 10 00539 g004
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Rosa, D.; Pogiatzis, A.; Bowen, P.; Kokkoris, V.; Richards, A.; Holland, T.; Hart, M. Performance and Establishment of a Commercial Mycorrhizal Inoculant in Viticulture. Agriculture 2020, 10, 539. https://doi.org/10.3390/agriculture10110539

AMA Style

Rosa D, Pogiatzis A, Bowen P, Kokkoris V, Richards A, Holland T, Hart M. Performance and Establishment of a Commercial Mycorrhizal Inoculant in Viticulture. Agriculture. 2020; 10(11):539. https://doi.org/10.3390/agriculture10110539

Chicago/Turabian Style

Rosa, Daniel, Antreas Pogiatzis, Pat Bowen, Vasilis Kokkoris, Andrew Richards, Taylor Holland, and Miranda Hart. 2020. "Performance and Establishment of a Commercial Mycorrhizal Inoculant in Viticulture" Agriculture 10, no. 11: 539. https://doi.org/10.3390/agriculture10110539

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop