Arbuscular Mycorrhizal Fungi in Viticulture: Should We Use Biofertilizers?

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1 REVIEW Arbuscular Mycorrhizal Fungi in Viticulture: Should We Use Biofertilizers? Taylor Holland, 1 Eric Vukicevich, 1 Corrina Thomsen, 1 Antreas Pogiatzis, 1 Miranda Hart, 1 and Pat Bowen 2 * Cite this article: Arbuscular mycorrhizal fungi in viticulture: Should we use biofertilizers? Holland T, Vukicevich E, Thomsen C, Pogiatzis A, Hart M and Bowen P. Catalyst 2: Summary Aim: Arbuscular mycorrhizal (AM) fungi are a group of symbiotic soil fungi known for their role in promoting host-plant growth by improving nutrient uptake, providing pathogen protection, and increasing tolerance to common vineyard soil abiotic stressors such as salinity, extreme ph, and low water availability. Use of commercially produced AM fungal inoculants, known as fungal biofertilizers, is growing in viticulture, but remains untested under field conditions. Here we discuss factors that affect the performance of fungal biofertilizers and scenarios where they may be more, and less, advantageous. Key Themes: Fungal biofertilizer use is increasing globally, but does their use translate to improved grapevine performance under vineyard conditions? What are the key considerations for incorporating AM fungi into vineyard management? Impact and Significance: While the importance of AM fungi for plant performance is well known, inoculation with fungal biofertilizers does not increase plant growth or yield consistently. This may be due to context dependency of the AM symbiosis, which can be affected by vineyard management practices like fertilizer use and tillage. Where AM fungi are not limiting, as in most vineyard soils, adding inoculants when compatible fungi are abundant may be redundant. However, in situations where soil fungi may be limiting, such as in greenhouse propagation nurseries using near-sterile media, or in fields with a history of heavy fertilizer use, AM fungal additions may be warranted. Key words: biofertilizer, inoculation, mycorrhizal fungi, soil, vineyard management 1 University of British Columbia, Kelowna, BC, V1V 1V7; and 2 Summerland Research and Development Centre, Agriculture and Agri-Food Canada, 4200 Highway 97, Summerland, BC, V0H 1Z0. *Corresponding author (pat.bowen@ agr.gc.ca, tel: ) Acknowledgments: The authors acknowledge funding provided by NSERC CGSD (TH), NSERC CGSM (CT), ASEV Student Scholarships (TH, EV, AP), Agriculture and Agri-Food Canada and Organic Cluster (MMH), and BC Wine Grape Council (PB). Manuscript submitted Dec 2017, revised June 2018, Sept 2018, accepted Sept 2018 doi: /catalyst Overview Arbuscular mycorrhizal (AM) fungi associate naturally with grapevines in a symbiosis whose importance for vineyard performance is becoming increasingly clear. Decades of research attest to the role of AM fungi in increasing nutrient supply for host plants 1,2 and in providing protection from soil-borne pathogens. 3 Fungal biofertilizers are marketed to capitalize on these services. Whether these products are consistently beneficial or cost-effective for growers is unclear. 4,5 The benefits of AM fungal inoculations to plant performance are observed regularly under sterile conditions; however, the effects of fungal biofertilizers on the performance of perennial crops like grapevine under field conditions are virtually unexamined. Key Themes The global trend in AM fungal biofertilizers. AM fungi are a quickly growing class of biofertilizers. These fungi act as an extension of the host roots, increasing nutrient uptake 2,6 and providing other benefits such as pathogen protection 3 and improved stress tolerance. 6,7 The AM symbiosis often leads to increased growth and fitness for the host plant, which is termed the mycorrhizal effect. 8 page 59

2 60 Holland et al. Because AM fungi form a symbiosis with 74% of angiosperm species, 8 including many important crops, they are marketed to producers of most agronomic and horticultural crops, 9,10 including grapevine. Although the production and use of AM fungal biofertilizers has increased as part of the sustainability movement, 10 there is limited field-based evidence that their use results in improved host performance, and few application techniques and rates have been established. 11 While some studies show AM fungal biofertilizers can provide modest increases in performance of grains, 12 legumes, 13 lettuce and zucchini, 14 potato, 15 and tomato, 16 there are numerous studies that show no benefit 17,18 or declining perfomance. 18,19 Because there is such a wide range of mycorrhizal outcomes, some likely arising from different inocula applied, the efficacy of a fungal biofertilizer cannot be predicted from prior testing, which should be considered before large scale applications. Are AM fungal biofertilizers suitable for perennials? Perennials may respond differently to biofertilizers than annual crops, due to fundamental differences in biology. The long-term development of perennial plants and exposure to natural AM fungal communities make it difficult to fully understand the impact AM additions can have, while with annuals, the effect is more apparent. If perennial plants are grown in environments with limited AM fungi, then there may be long-term advantages associated with AM fungal biofertilizer use. Unfortunately, studies have not been conducted to address this question. What we know about perennials and AM fungal biofertilizers comes from a small number of studies. AM fungal biofertilizers were beneficial in the production of perennial tubers such as cassava, 4 but results are less consistent for grapevines. 20,21 Given that perennial systems are relatively undisturbed, compared with annual cropping systems, the value of commercial fungal additions to grapevines is still unknown. Biofertilizer effects on vineyard performance may be difficult to evaluate, because studies must span the long period between planting and crop production (typically three years in grapevine), and effects of inoculation may not be apparent immediately. Knowledge about AM symbiosis (natural or biofertilizer) in grapevine roots is far from complete, making it difficult to predict long term effects. AM fungal biofertilizers and grapevines. In theory, grapevines should benefit from fungal biofertilizers. They are highly mycorrhizal-dependent: their growth increases in the presence of AM fungi 20,21 and is stunted when grown without AM fungi in sterile soil. 22,23 Such dependency may stem from the range of stressful growing conditions that prevail in the native ranges of grape rootstock species, such as rocky stream banks and droughty, calcareous soils. 24,25 It is possible that the mycorrhizal associations allowed these ancestral rootstocks to better tolerate their native landscapes, allowing them to access otherwise unavailable nutrients or water sources during stressful periods. These stressors also exist in vineyards to some degree (i.e., salinity, 26,27 extreme ph, 28,29 or low water availability 30 ). While the importance of AM fungal symbiosis for grapevine growth is clear, 31 there is no research yet supporting (or discouraging) the use of AM fungal biofertilizers in viticulture. Whether existing resident vineyard AM fungi are sufficient to fully realize the benefits associated with AM symbiosis has not yet been tested, but may depend on factors specific to each vineyard. Below, we discuss factors that affect the outcome of the AM symbiosis. These factors apply equally to biofertilizers and naturally occurring AM fungi. It is important to remember that biofertilizers are simply fungi, subject to the same constraints as naturally occurring fungi. Such constraints may be overlooked by growers hoping to capitalize on a green alternative to fertilizer. 1) The AM symbiosis is context dependent. Host identity, 18 rootstock, 32,33 soil conditions, 6,34 and climate 35 in concert determine whether an AM fungal isolate will have a positive, neutral, or even negative effect on host performance. The context dependency of the grapevine- AM symbiosis makes it unlikely, if not impossible, for a single fungal inoculant to be beneficial across growing conditions. 2) Soil fertility determines host response to AM fungi. The AM symbiosis is most beneficial in soils that are deficient in nutrients, especially phosphorus. 1,34,36,37 Fertilizer use negatively impacts both the abundance 1,38 and functioning 19 of AM. Plants growing in nutrient rich-soils are unlikely to develop robust AM symbioses, natural or otherwise. Thus, when fertilizer is used, the addition of fungal biofertilizers may be ineffective. Further, when fungal biofertilizers are applied in systems with adequate phosphorus, but limited nitrogen, the fungi can act as parasites, reducing plant growth. 39 3) Tillage destroys fungal networks. There is a long history of research clearly showing the negative effects of tillage on AM fungal abundance, 40 community structure, 41 and functioning. 42 If tillage is required to control weeds or improve soil drainage, then the use of biofertilizer post-tillage may mitigate the effects by

3 Arbuscular Mycorrhizal Fungi as Biofertilizers 61 increasing the inoculum potential of the soil, leading to quicker recovery and a better mycorrhizal response. 20,43 However, if the goal is to maintain and enhance local fungi, or to promote the establishment of an inoculant, then it is important to look for alternatives to tillage. Tillage is incompatible with long-term, sustainable AM fungal populations. 4) Ground covers change AM fungi in soil. An important component of viticulture is management of groundcovers, both inter- and in-row vegetation. 44 Landscapes with diverse groundcover species may also have more abundant and diverse AM fungal communities. 45,46 Since AM fungi can associate with different hosts, this may negate the need for additional inoculation, or even impede inoculant establishment. 47,48 Abundant and diverse groundcovers may enhance AM fungal abundance and diversity naturally. When are AM fungal biofertilizers a good idea? In well-managed vineyards, there is good reason for growers to assume that their crop is already colonized by AM fungi. Field-grown grapevines usually sustain healthy AM fungal communities naturally, so AM fungal biofertilizers may be redundant. Similarly, biofertilizers may also be ineffective in highly fertile production systems where nutrient levels may suppress mycorrhizal functioning. Under some circumstances, however, AM fungal biofertilizers may be a good investment. Soils with low inoculum potential may arise following non-mycorrhizal crops (i.e., brassicas), 49 pre-planting fumigation, 50 or removal of the surface soil. 51 In such soils, AM fungi may be in low numbers or absent. A biofertilizer may give vines a competitive advantage over non-mycorrhizal weeds. 52 This also holds in artificial growing systems that lack soil biota, like hydroponics, tissue culture, sterile greenhouse soils, or peat. Marginal vineyards with a history of high pathogen load or poor soil conditions may require rehabilitation, including microbial additions. 20,27 Similarly, agriculture with high inputs of fertilizer, herbicides, fungicides, and/ or tillage will result in less diverse AM fungal communities. 47 In addition to providing direct benefits to host plants, biofertilizers may help crops compete against non-mycorrhizal weeds. 52,53 Significance Clearly, AM fungal biofertilizers are not useful in all situations. A situation highly likely to benefit from biofertilizers is when the natural abundance of AM fungi is low. Determining the diversity and abundance of AM fungi within soil requires specialized laboratory analysis, such as inoculum potential growth assays, root staining, molecular quantification, and DNA community profiling, but may be a worthwhile investment for sites suspected of having poor soil conditions for plant growth. In addition, before a fungal biofertilizer is applied on a large scale, it is worthwhile to conduct tests to determine spore viability of the product and the ability of the AM fungi to colonize a particular rootstock under the soil conditions of the vineyard. AM fungi are an integral contributor to the health of perennial crops. Growers hoping to use this symbiosis in their cropping system may do well to ask: How can I best promote AM fungi in my vineyard? For instance, the presence of weeds can increase inoculum potential and AM fungal species richness if the weeds are hosts of mycorrhizal fungi. 54 In more resource-limited soils, native species may have the greatest positive impact on AM fungal communities, as they preferentially associate with locally-adapted, robust AM fungal genotypes. 37 An exotic AM fungus may not be as beneficial as locallyadapted isolates, and may reduce plant performance 18 and decrease AM fungal diversity. 55,56 Managing the soil as an ecosystem, rather than a resource, may provide the most beneficial long-term growing conditions. References and Footnotes 1. Gosling P, Hodge A, Goodlass G and Bending GD Arbuscular mycorrhizal fungi and organic farming. Agr Ecosyst Environ 113: Marschner H and Dell B Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159: Borowicz VA Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82: Ceballos I, Ruiz M, Fernández C, Peña R, Rodríguez A and Sanders IR The in vitro mass-produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS ONE 8:e Ryan MH and Graham JH Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244: Entry JA, Rygiewicz PT, Waturd LS and Donnelly PK Influence of adverse soil conditions on the formation and function of arbuscular mycorrhizas. Adv Environ Res 7: Augé RM Water relations, drought and vesiculararbuscular mycorrhizal symbiosis. Mycorrhiza 11: Smith SE and Read DJ Mycorrhizal Symbiosis. 3rd ed. Academic Press, London. 9. Berutti A, Lumini E, Balestrini R and Bianciotto V Arbuscular mycorrhizal fungi as natural biofertilizers: Let s benefit from past successes. Front Microbiol 6: Gianinazzi S and Vosátka M Inoculum of arbuscular mycorrhizal fungi for production systems: Science meets business. Can J Bot 82:

4 62 Holland et al. 11. Hart MM, Antunes PM, Chaudhary VB and Abbott LK Fungal inoculants in the field: Is the reward greater than the risk? Funct Ecol 32: Mohammad MJ, Pan WL and Kennedy AC Seasonal mycorrhizal colonization of winter wheat and its effect on wheat growth under dryland field conditions. Mycorrhiza 8: González Cañizares PJ, Ramírez Pedroso JF, Rivera Espinosa R, Hernández Jimenez A and Crespo Flores G Effectiveness of inoculation of two forage legumes grown on two soil types with arbuscular mycorrhizal fungi. Trop Grasslands 4: Colla G, Rouphael Y, Di Matta E, El-Nakhel C and Cardarelli M Co-inoculation of Glomus intraradices and Trichoderma atroviride acts as a biostimulant to promote growth, yield and nutrient uptake of vegetable crops. J Sci Food Agric 95: Hijri M Analysis of a large dataset of mycorrhizal inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26: Douds Jr DD, Lee J, McKeever L, Ziegler-Ulsh C and Ganser S Utilization of inoculum of AM fungi produced on-farm increases the yield of Solanum lycopersicum: A summary of 7 years of field trials on a conventional vegetable farm with high soil phosphorus. Sci Hortic 207: Cordiki L, Allen EB, Merhaut D, Allen MF, Downer J, Bohn J and Evans M Assessing the infectivity of commercial mycorrhizal inoculants in plant nursery conditions. J Environ Hortic 22: Klironomos JN Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84: Graham JH and Eissenstat DM Field evidence for carbon cost of citrus mycorrhizas. New Phytol 140: Nogales A, Luque J, Estúan V, Camprubí A, García-Figueres F and Calvet C Differential growth of mycorrhizal field-inoculated grapevine rootstocks in two replant soils. Am J Enol Vitic 60: Camprubí A, Estúan V, Nogales A, García-Figueres F, Pitet M and 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 18: Menge JA, Raski DJ, Lider LA, Johnson ELV, Jones NO, Kissler JJ and Hemstreet CL Interactions between mycorrhizal fungi, soil fumigation and growth of grapes in California. Am J Enol Vitic 34: Linderman RG and Davis AE Comparative response of selected grapevine rootstocks and cultivars to inoculation with different mycorrhizal fungi. Am J Enol Vitic 52: Morano LD and Walker MA Soils and plant communities associated with three Vitis species. Am Midl Nat 134: Ocete R, Armendáriz I, Cantos M, Álvarez D and Azcón R Ecological characterization of wild grapevine habitats focused on arbuscular mycorrhizal symbiosis. Vitis 54: Walker RR, Blackmore DH, Clingeleffer PR and Emanuelli D Rootstock type determines tolerance of Chardonnay and Shiraz to long-term saline irrigation. Aust J Grape Wine Res 20: Belew D, Astatkie T, Mokashi MN, Getachew Y and Patil CP Effects of salinity and mycorrhizal inoculation (Glomus fasciculatum) on growth responses of grape rootstocks (Vitis spp.). S Afr J Enol Vitic 31: Bavaresco L and Poni S Effect of calcareous soil on photosynthesis rate, mineral nutrition, and source-sink ratio of table grape. J Plant Nutr 26: Reyes JM, del Campillo MC and Torrent J Soil properties influencing iron chlorosis in grapevines grown in the Montilla-Moriles area, southern Spain. Commun Soil Sci Plan 37: Chaves MM, Zarrouk O, Francisco R, Costa JM, Santos T, Regalado AP, Rodrigues ML and Lopes CM Grapevine under deficit irrigation: Hints from physiological and molecular data. Ann Bot 105: Trouvelot S, Bonneau L, Redecker D, van Tuinen D, Adrian M and Wipf D Arbuscular mycorrhizal symbiosis in viticulture: A review. Agron Sustain Dev 35: Schreiner PR Mycorrhizal colonization of grapevine rootstocks under field conditions. Am J Enol Vitic 54: Aguín O, Mansilla JP, Vilariño A and Sainz MJ Effects of mycorrhizal inoculation on root morphology and nursery production of three grapevine rootstocks. Am J Enol Vitic 55: Hetrick BAD, Wilson GWT and Todd TC Relationships of mycorrhizal symbiosis, rooting strategy, and phenology among tallgrass prairie forbs. Can J Bot 70: Hayman DS Plant growth responses to vesiculararbuscular mycorrhiza. VI. Effect of light and temperature. New Phytol 73: Schreiner RP 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: Johnson NC, Wilson GWT, Bowker MA, Wilson JA and Miller MR Resource limitation is a driver of local adaptation in mycorrhizal symbioses. PNAS 107: Treseder KK A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO 2 in field studies. New Phytol 164: Johnson NC, Wilson GWT, Wilson JA, Miller RM and Bowker MA Mycorrhizal phenotypes and the law of the minimum. New Phtyol. 205: Lekberg Y and Koide RT Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A metaanalysis of studies published between 1988 and New Phtyol 168: Mirás-Avalos JM, Antunes PM, Koch A, Khosla K, Klironomos JN and Dunfield KE The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiologia 54: McGonigle TP and Miller MH Mycorrhizal development and phosphorus absorption in maize under conventional and reduced tillage. Soil Sci Soc Am J 57:

5 Arbuscular Mycorrhizal Fungi as Biofertilizers Schalamuk S, Cabello MN, Chidichimo H and Golik S Effects of inoculation with Glomus mosseae in conventionally tilled and nontilled soils with different levels of nitrogen fertilization on wheat growth, arbuscular mycorrhizal colonization, and nitrogen nutrition. Commun Soil Sci Plan 42: Guerra B and Steenwerth K Influence of floor management technique on grapevine growth, disease pressure, and juice and wine composition: A review. Am J Enol Vitic 63: Holland TC, Bowen PA, Bogdanoff CP, Lowery TD, Shaposhnikova O, Smith S and Hart MM Evaluating the diversity of soil microbial communities in vineyards relative to adjacent native ecosystems. Appl Soil Ecol 100: Bever JD, Schultz PA, Pringle A and Morton JB Arbuscular mycorrhizal fungi: More diverse than meets the eye, and the ecological tale of why: The high diversity of ecologically distinct species of arbuscular mycorrhizal fungi within a single community has broad implications for plant ecology. Bioscience 51: Verbruggen E, Roling WFM, Gamper HA, Kowalchuk GA, Verhoef HA and van der Heijden MGA Positive effects of organic farming on below-ground mutualists: Large-scale comparison of mycorrhizal fungal communities in agricultural soils. New Phytol 186: Köhl L, Lukasiewicz CE and van der Heijden MGA Establishment and effectiveness of inoculated arbuscular mycorrhizal fungi in agricultural soils. Plant Cell Environ 39: Schreiner RP and Koide RT Mustards, mustard oils and mycorrhizas. New Phytol 123: Menge JA Effect of soil fumigants and fungicides on vesicular-arbuscular fungi. Phytopathology 72: Oehl F, Sieverding E, Ineichen K, Ris EA, Boller T and Wiemken A Community structure of arbuscular mycorrhizal fungi at different soil depths in extensively and intensively managed agroecosystems. New Phtyol 165: Rinaudo V, Bàrberi P, Giovanneti M and van der Heijden MGA Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil 333: Viega RSL, Jansa J, Frossard E and van der Heijden MGA Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS ONE 6:e Ramos-Zapata JA, Marrufo-Zapata D, Guadarrama P, Carrillo- Sánchez L, Hernández-Cuevas L and Caamal-Maldonado A Impact of weed control on arbuscular mycorrhizal fungi in a tropical agroecosystem: A long-term experiment. Mycorrhiza. 22: Koch AM, Antunes PM, Barto EK, Cipollini D, Mummey DL and Klironomos JN The effects of arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol Invasions 13: Pellegrino E, Turrini A, Gamper HA, Cafà G, Bonari E, Young JPW and Giovannetti M Establishment, persistence and effectiveness of arbuscular mycorrhizal fungal inoculants in the field revealed using molecular genetic tracing and measurement of yield components. New Phytol 194:

Mycorrhizal inoculation of grapevine rootstocks suitable for mediterranean soils: evaluation of their growth response

Mycorrhizal inoculation of grapevines in replant soils: improved field application and plant performance Nogales A., Camprubí A., Estaún V., Calvet C. IRTA, Recerca i Tecnologia Agroalimentàries, Ctra.