Soil memory as a potential mechanism for encouraging sustainable plant health and productivity

https://doi.org/10.1016/j.copbio.2016.01.014Get rights and content

Highlights

  • Interactions between roots and the soil microbiome have a co-evolutionary component.

  • The development of suppressive soils is related to soil microbiome associations.

  • Development of a framework to understand suppressive soil associations.

The unspecified components of plant–microbe and plant–microbiome associations in the rhizosphere are complex, but recent research is simplifying our understanding of these relationships. We propose that the strong association between hosts, symbionts, and pathogens could be simplified by the concept of soil memory, which explains how a plant could promote their fecundity and protect their offspring through tightly associated relationships with the soil. Although there are many questions surrounding the mechanisms of this phenomenon, recent research has exposed evidence of its existence. Along with evidence from observations and mechanisms related to soil memory, we report means to utilize our understanding as sustainable protection for agricultural crops and propose future research questions.

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.

References (55)

  • J.M. Chaparro et al.

    Manipulating the soil microbiome to increase soil health and plant fertility

    Bio Fert Soils

    (2012)
  • T.R. Turner et al.

    The plant microbiome

    Genome Biol

    (2013)
  • V. Lakshmanan et al.

    Functional soil microbiome: belowground solutions to an aboveground problem

    Plant Physiol

    (2014)
  • J.P. Anderson et al.

    Plants versus pathogens: an evolutionary arms race

    Funct Plant Biol

    (2010)
  • L. Trda et al.

    Perception of pathogenic or beneficial bacteria and their evasion of host immunity: pattern recognition receptors in the frontline

    Front Plant Sci

    (2015)
  • K. Hjort et al.

    Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics

    Appl Microbiol Biotechnol

    (2014)
  • N. El-Mougy et al.

    Evaluating survival and antagonistic activity of introduced bio-agents to the soil under greenhouse conditions

    JASR

    (2012)
  • M. Mazzola

    Manipulation of rhizosphere bacterial communities to induce suppressive soils

    J Nematol

    (2007)
  • C.R. Penton et al.

    Fungal community structure in disease suppressive soils assessed by 28S LSU gene sequencing

    PLoS One

    (2014)
  • J.E. Koenig et al.

    Succession of microbial consortia in the developing infant gut microbiome

    Proc Natl Acad Sci U S A

    (2011)
  • G.E. Kaiko et al.

    Host–microbe interactions shaping the gastrointestinal environment

    Trends Immunol

    (2014)
  • F. Liu et al.

    Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings

    Appl Microbiol Biotechnol

    (2013)
  • A.L. Khan et al.

    Resilience of Penicillium resedanum LK6 and exogenous gibberellin in improving Capsicum annuum growth under abiotic stresses

    J Plant Res

    (2015)
  • S.-M. Choi et al.

    Transcriptome analysis of induced systemic drought tolerance elicited by Pseudomonas chlororaphis O6 in Arabidopsis thaliana

    Plant Pathol

    (2013)
  • J.-H. Lim et al.

    Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper

    Plant Pathol

    (2013)
  • M.A. Salas-Marina et al.

    The Epl1 and Sm1 proteins from Trichoderma atroyiride and Trichoderma virens differentially modulate systemic disease resistance against different life style pathogens in Solanum lycopersicum

    Front Plant Sci

    (2015)
  • Z. Babikova et al.

    Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack

    Ecol Lett

    (2013)
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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.

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