Soil memory as a potential mechanism for encouraging sustainable plant health and productivity
Graphical abstract
Introduction
Studies of plant fossils demonstrate a close association between plants and soil microbial symbionts since transitioning onto land, and conservation of the mechanisms modulating these interactions [1]. The microbial metagenome of plants acts as an extra-organismal matrix enabling greater environmental adaptability, resource acquisition, internal and external defense responses, and the communication between plants necessary to ensure the fitness of a species or health of entire ecosystems [2]. This indelible relationship between the plant and the soil microbiome is essential to plant health and productivity [3, 4, 5]. Still, the soil microbial community is diverse, and comprised of species that may be beneficial, commensal, or detrimental to plants. Plants and microbes have therefore co-evolved a tightly regulated defense system for protection that also tolerates formation of beneficial relationships (reviewed by [6, 7]).
Soil bacterial or fungal species that impart some benefit to plants are commonly known as Plant Growth Promoting Microorganisms (PGPM) — many of which have been developed for commercial distribution as soil amendments for implementation in agricultural systems [8]. PGPM that are introduced into soils must be able to colonize the area around (rhizosphere) or directly inside (endophytes) the roots, compete with other microbes for limited resources, and persist in the soil environment [9]. Enhancing soils with the application of beneficial microbes therefore produces inherently variable results, as bacteria can be unpredictable in terms of establishment and degree of plant growth promotion [10]. Sarma et al. compiled a thorough list of the microbial consortia studied for their anti-phytopathogenic activities [11]. Preferentially, the development of suppressive soils, or soils where pathogens are present yet their impact on the host is significantly decreased [12•], offers an alternative to improving crop health and yield.
In this review, we discuss current advances in knowledge of microbial plant growth promotion and defense, suppressive soils, and microbial applications in agroecosystems. Using recent findings on this topic, we propose that soil microbial communities convey attributes of specificity, heterogeneity, and growth promotion in soil that could be inherited by future crop cycles, much like mammalian microbial colonizers are passed to their offspring [13]. The maturation and maintenance of the rhizosphere community is similar to the development of the human microbiota: colonization begins at birth, and as the infant matures, the microbial community increases in population size and complexity [14] — seeded by intimate contacts with caregivers and the environment [15]. Microbes acquired by individuals to successfully adapt to their environment are then passed down to offspring [13]. We document that the current literature displays evidence that a similar phenomenon may occur in plants through a kind of ‘soil memory’, and review practices which we believe can encourage the phenomenon, plus identify intriguing areas for future research.
Section snippets
Choice mechanisms of PGPM activity
In addition to nutrient supplementation by microbes, regulation of plant hormones either by microbial synthesis or degradation, is a simple yet effective way in which symbionts can decrease abiotic stress symptoms caused by drought, salinity, or heat stress to maintain health of host plants [16, 17]. Reduction of abiotic stress symptoms by microbes may also occur via influencing plant genetics as opposed to direct molecular interventions; a myriad of genes related to stress tolerance,
Soil memory as a potential mechanism
Certain plants have the ability to pass on endophytic PGPM acquired from the soil to their offspring; strawberries can pass microbes through their stolons [27], while several forb species pass them directly through their seeds [28]. It is likely, therefore, that plants have also developed similar mechanisms to pass on free-living PGPM, or a specific dynamic soil microbial community to their offspring as a means of imparting the adaptive advantages developed during their life to their
Understanding suppressive soils
An area of interest to sustainable agriculture research is the phenomena of suppressive soils. Suppressive soils are those that decrease or prevent disease occurrence despite the presence of a pathogen, a compatible plant host, and favorable environmental conditions [12•]. We postulate that suppressive soils are formed though the soil memory mechanism, therefore the current understanding of the process is reviewed here. Suppresiveness is categorized as either general or specific. General
Promotion of soil suppression
The development and maintenance of healthy, pathogen-suppressive soils can be a goal for productive and sustainable agriculture. Many problems in agriculture related to soil pests and diseases can be linked to poor management practices. Farming practices which do not protect soil health lead to poor drainage, structure, organic matter, and fertility, and have negative impacts on the soil microbial community [48, 49]. Tilling often requires complete vegetative removal between crops and leads to
Concluding remarks
Despite continuing research on the topic of suppressive soil, there are many gaps in our understanding of the phenomenon. Our understanding of plants as chemical factories responsible for coordinating many underground interactions [54] prompts exploration of spatial relationships, soil environmental variables, and soil chemistry requirements of suppressive soils [44]. Additionally, while many studies have explored the dynamics of suppressive soil microbial communities, few functional
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We acknowledge the journal Current Opinion in Biotechnology for inviting us to write this article. The authors thank Janice M Lapsansky, and Alyssa T Cochran for their crucial revisions of this article.
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- 1
ERL and AMM contributed equally to this paper.
- 2
ERL and AMM conceived, developed the theme, and wrote the paper.
- 3
MJA and JMV provided critical revisions.