Abstract

Mutualistic plant–microbial functioning relies on co-adapted symbiotic partners as well as conducive environmental conditions. Choosing particular plant genotypes for domestication and subsequent cultivar selection can narrow the gene pools of crop plants to a degree that they are no longer able to benefit from microbial mutualists. Elevated mineral nutrient levels in cultivated soils also reduce the dependence of crops on nutritional support by mutualists such as mycorrhizal fungi and rhizobia. Thus, current ways of crop production are predestined to compromise the propagation and function of microbial symbionts, limiting their long-term benefits for plant yield stability. The influence of mutualists on non-native plant establishment and spread, i.e. biological invasions, provides an unexplored analogue to contemporary crop production that accounts for mutualistic services from symbionts like rhizobia and mycorrhizae. The historical exposure of organisms to biotic interactions over evolutionary timescales, or so-called eco-evolutionary experience (EEE), has been used to explain the success of such invasions. In this paper, we stress that consideration of the EEE concept can shed light on how to overcome the loss of microbial mutualist functions following crop domestication and breeding. We propose specific experimental approaches to utilize the wild ancestors of crops to determine whether crop domestication compromised the benefits derived from root microbial symbioses or not. This can predict the potential for success of mutualistic symbiosis manipulation in modern crops and the maintenance of effective microbial mutualisms over the long term.

Highlights

  • Rapid climate change and the need to utilize resources more efficiently call for crops that are able to cope with perturbation and stress while supporting stable yields

  • Microbial symbionts may adapt to newly encountered abiotic conditions which, in turn, influence the performance and benefits received by host plants (Bennett and Klironomos 2019)

  • An approach to experimentally determine the existence and importance of ecoevolutionary experience of modern crop cultivars to microbial symbionts

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Summary

Introduction

Rapid climate change and the need to utilize resources more efficiently call for crops that are able to cope with perturbation and stress while supporting stable yields. Based on the experimental setup outlined in Box 1, the degree and strength of the effects of EEE can be estimated based on (i) the ability of modern cultivars to establish symbioses with ancestral mutualists and (ii) the ability of modern cultivars to benefit more from these associations than from those present in arable soils This allows determining whether crop domestication and breeding have (i) compromised the genetic basis for beneficial plant–microbe interactions (i.e. symbiotic capacity), or whether (ii) the practices and conditions of cultivation impaired microbial symbiont survival and propagation (i.e. symbiont availability). Knowing whether a crop still relies on symbiotic services at all and whether these are derived from ancestral or novel associations can inform the development of inocula and of agronomic measures to promote crop-beneficial symbionts (i.e. symbiont management) (Fig. 2) Both reciprocal symbiosis partner and symbiont-environment adaptations promoted by EEE are expected to increase the benefits plants reap from microbial symbionts. Examples suggesting the utility of such interventions are the joint introduction of European forage legumes and their root nodule symbiosis partners in Australia and New Zealand (Weir et al 2004), or cultivation of pine trees in the southern hemisphere owing to co-introduction of compatible EM fungal symbiosis partners (Vellinga et al 2009; Dickie et al 2010)

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