Towards an Integrated Mycorrhizal Technology: Harnessing Mycorrhiza for Sustainable Intensification in Agriculture

摘要

Background Sustainability in agriculture In order to meet future needs of a growing human population and to achieve food security in the context of climate change, food production will likely need to increase—among other measures—while at the same time minimizing negative environmental impact (Foley et al., 2011 ). Sustainable intensification of agriculture (Garnett et al., 2013 ; Pretty and Bharucha, 2014 ; Andres and Bhullar, 2016 ; Gunton et al., 2016 ), sometimes also called ecological intensification, is likely to include key aspects of conservation agriculture (e.g., Hobbs et al., 2008 ; Giller et al., 2015 ). Pillars of conservation agriculture (FAO, 2015 ) are no-till practices (Pittelkow et al., 2015 ), continuous crop cover (by various means, for example cover crops) and diversification practices (multi-cropping and crop rotations; Ponisio et al., 2015 ). The potential role of mycorrhiza in sustainable agriculture There is a steadily growing appreciation of the integral importance of soil life in agricultural sustainability (e.g., M?der et al., 2002 ; Wagg et al., 2014 ; Bender et al., 2016 ), including plant-symbiotic associations. Among these symbioses a prominent player is mycorrhiza, the widespread symbiotic association of fungi with plant roots (Smith and Read, 2008 ). Much has been written about the role of mycorrhiza in agroecosystems, in particular about arbuscular mycorrhiza (AM), formed by fungi in the phylum Glomeromycota, to which this paper mostly refers. AM fungi are obligate symbionts (they need a living host during their entire life cycle) with tight regulation of carbon-for-nutrients exchange between the host and the fungus. During their evolution, AM fungi have lost the enzymatic ability to degrade carbon compounds (Tisserant et al., 2013 ), which prevents them from becoming necrotrophic pathogens (the most common type of root-fungal pathogens). The AM symbiosis has been much discussed in the context of agriculture, (i) because AM is the dominant mycorrhiza formed by most crops (an exception being for example crops in the Brassicaceae); (ii) because of the potentially positive, multifunctional role of AM in plant nutrition, pathogen protection, stress tolerance and soil structure provision (Hamel, 1996 ; Smith and Read, 2008 ; Gianinazzi et al., 2010 ; Leifheit et al., 2014 ); (iii) because many agricultural practices (e.g., tillage, fertilization, non-host crops) tend to negatively affect AM fungal abundance and diversity, thus potentially affecting functioning; and (iv) because AM fungi can be managed. Defining mycorrhizal technology The focus in applied research on mycorrhiza in sustainable agriculture could be circumscribed as developing mycorrhizal technology. Clearly most easily recognized as a mycorrhizal technology is the production and application of mycorrhizal fungal inoculum (Gianinazzi et al., 2002 ; Vosatka et al., 2012 ; Solaiman et al., 2014 ), directly addressing the decline in mycorrhizal abundance in agricultural fields. Inoculation can have demonstrable yield benefits, powerfully documented by the recent, very in-depth study by Hijri ( 2016 ) analyzing 231 potato field trials. Nevertheless, we argue here that this should not be the exclusive focus of next-generation mycorrhizal technology. A recent analysis concluded that one of the most striking aspects of sustainable agricultural intensification is an “increase in knowledge per hectare” (Buckwell et al., 2014 ), i.e., a better understanding of how to achieve resource-efficient agroecosystems with minimal environmental impacts in any given location. This is a very useful conceptualization that helps frame what mycorrhizal technology could or should increasingly mean.We here propose a definition of “mycorrhizal technology” as the set of measures to optimize local mycorrhizal abundance and diversity in terms of functioning for attaining sustainability of agroecosystems. Optimization here means increasing mycorrhizal benefits (in terms of yield and sustainability of other ecosystems processes) within given socioeconomic constraints, i.e., there will always be practical limits at the farm level to achieving the full theoretical potential (e.g., Lamarque et al., 2014 ). This definition includes sustainability as a clear goal and it is inclusive of many approaches discussed in the following. Mycorrhizal technology: components and research needs Components of an inclusive mycorrhizal technology We propose some key elements of an inclusive mycorrhizal technology (Figure 1 ): monitoring, agricultural management, database tools, plant breeding and ecological engineering of communities of mycorrhizal fungi (“myco-engineering”) and their associated microbiota. Monitoring refers to assessment of the abundance (in roots and soil) and diversity of mycorrhizal fungal abundance in the field. Management represents a complex set of tools that can impact abundance and diversity of mycorrhiza, including agronomic practices with