Plant Biology Blog

Endophytes in Grapevine: Potential for Sustainable Viticulture?

By Matevz Likar

December 6, 2017

Viticulture is an important agronomic sector that has the potential to greatly benefit by improvements in our understanding of grapevine cultivation. Although conventional viticulture relies to a great extent on pesticide and fertilizer application, more sustainable approaches involve management practices that favor plant–fungus interactions that have positive effects on the nutritional quality of the grapes and reduce production costs (i.e., of pesticides and fertilizers) and thus reduce the negative effects on the environment. Fungal endophytes in grapevine belong to different taxa, with the majority of reports focusing on fungi that form arbuscular mycorrhizal associations. These fungal endophytes have been demonstrated to confer beneficial growth and nutrition effects to their plant hosts via improved exploitation of the substrate and improved tolerance of the grapevine to abiotic and biotic stresses.

Arbuscular mycorrhizal fungi

The arbuscular mycorrhizal fungi (AMF) are among the most important beneficial fungal root endophytes, and they are known to colonise the roots of the majority of land plants, including grapevines (Karagiannidis and Nikolaou 1999; Schreiner and Mihara 2009; Likar et al. 2013). The AMF comprise of some 270 species of fungi from phylum Glomeromycota (Schüßler et al. 2001; Schüßler 2017), which associate with 80% of vascular plant species (mostly herbaceous plants, but also various woody plant families). AMF are obligate biotrophs, relying on living root tissue for carbohydrate supply. AMF colonize short roots and replace the function of root hairs. They supply water and nutrients, particularly phosphate but also nitrogen and other minerals including zinc, to the host plant. Inside the roots they form arbuscules and coils that improve the exchange between the symbionts through increased area of contact (Smith and Read 2008).

arbuscules
Detached root cells with arbuscules formed inside. Fungal hyphae and arbuscules were stained using Trypan Blue.

Jacott et al. (2017) DOI:10.3390/agronomy7040075 provide a good review on the importance of AMF in agro-ecosystems.

Dark septate endophytes

In addition to AMF, fungi that form septate hyphae with melanized cell walls are common colonizers of plant roots in natural environments. These fungi are referred to as dark septate endophytes (DSEs), and they represent a heterogeneous group of ascomycetes that occur across a wide range of terrestrial ecosystems, although they are most numerous in extreme habitats (for a review see Mandyam and Jumpponen 2005, DOI:10.3114/sim.53.1.173). Among the DSEs, members of the order Helotiales are commonly observed, although frequently these isolates are not fully identified or they are grouped with the anamorphic genera Phialocephala, Rhynchosporium, and Phialophora.

Dark septate endophytes
Septated and melanised hyphae of dark septate endophytes in roots of a willow.

The knowledge on involvement of DSEs in plant nutrition is still very limited. The first reports on DSEs showed that they can promote the uptake of nitrogen and phosphorus into plants, although their effects on the overall plant biomass appeared to be dependent on host–symbiont combinations and soil conditions. With further studies, a wider range of effects on host physiology have been reported, from negative or negligible to positive (Newsham 2011).

Fungal endophytes in grapevine

Vineyard soils also support fungal endophytes like AMF and DSEs, including endophytes in grapevine (Likar et al. 2013; Oehl et al. 2005; Radić et al. 2014).  AMF can have positive effects on grapevine performance (Biricolti et al. 1997; Linderman and Davis 2001). Furthermore, low root density and coarse root texture of grapevines suggest that they are highly dependent on symbiotic fungi, making these an important factor for grapevine’s growth and development. This is especially true in organic vineyards with low-input practices, as these support higher abundance and diversity of AMF (Oehl et al. 2004).

Fungal endophytes on grapevine
Positive effects of arbuscular mycorrhizal (AM) colonization. The hyphal network of arbuscular mycorrhizal fungi (AMF) extends beyond the depletion zone (grey), accessing a greater area of soil for phosphate uptake. A mycorrhizal-phosphate depletion zone will also eventually form around AM hyphae (purple). Other nutrients that have enhanced assimilation in AM-roots include nitrogen (ammonium) and zinc. Benefits from colonization include tolerances to many abiotic and biotic stresses through induction of systemic acquired resistance (SAR). From: Jacott et al. (2017) DOI:10.3390/agronomy7040075.

The presence of DSEs on grapevine is still not fully confirmed.  The bulk of our knowledge on DSE fungi is restricted to the colder and temperate zones. Although DSEs are found throughout the world, studies performed in Mediterranean have failed to observe DSE taxa that dominate the colder regions (Girlanda et al. 2006). Therefore DSE communities in vineyards, which are by nature based in warmer climates, might be formed by completely different fungi. Consequently their absence in grapevine could be due to the fact that DSE species from warmer climates are not yet known.
For a review on fungal endophytes in grapevine see Likar and Regvar (2017) DOI: 10.1007/978-3-319-53064-2_13 that reviews current knowledge on the importance and potential of these diverse fungal groups for grapevine production and expose the gaps in our understanding of possible functions of fungal groups that are currently little studied.

References

  • Biricolti S, Ferrini F, Rinaldeli E et al (1997) VAM fungi and soil lime content influence rootstock growth and nutrient content. Am J Enol Vitic 48:93–99
  • Girlanda M, Perotto S, Luppi AM (2006) Molecular diversity and ecological roles of mycorrhiza- associated sterile fungal endophytes in mediterranean ecosystems. In: Schulz B, Boyle C, Sieber T (eds) Soil biology. Springer, Berlin, pp 207–226
  • Jacott CN, Murray, JD, Ridout CJ (2017) Trade-Offs in Arbuscular Mycorrhizal Symbiosis: Disease Resistance, Growth Responses and Perspectives for Crop Breeding. Agronomy 7:75
  • Karagiannidis N, Velemis D, Stavropoulos N (1997) Root colonization and spore population by VA-mycorrhizal fungi in four grapevine rootstocks. Vitis 36:57–60
  • Likar M, Regvar M (2017) Arbuscular Mycorrhizal Fungi and Dark Septate Endophytes in Grapevine: The Potential for Sustainable Viticulture?In: Varma A et al. (eds) Mycorrhiza – Function, Diversity, State of the Art. Springer, pp 275-289. doi: 10.1007/978-3-319-53064-2_13
  • Likar M, Hančević K, Radić T, Regvar M (2013) Distribution and diversity of arbuscular mycorrhizal fungi in grapevines from production vineyards along the eastern Adriatic coast. Mycorrhiza 23:209–219. doi:10.1007/s00572-012-0463-x
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  • Schüßler A (2017) Glomeromycota (version Jan 2016). In: Roskov Y, Abucay L, Orrell T, Nicolson D, Bailly N, Kirk PM, Bourgoin T, DeWalt RE, Decock W, De Wever A, Nieukerken E van, Zarucchi J, Penev L (eds) Species 2000 and ITIS Catalogue of Life, 29th May 2017. Digital resource at www.catalogueoflife.org/col. Species 2000: Naturalis, Leiden, the Netherlands. ISSN 2405-8858.
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