Keywords

7.1 Introduction

Take-all disease is caused by the soil-borne pathogenic fungus Gaeumannomyces graminis. This pathogen causes the most important root disease of wheat (Triticum aestivum L.) worldwide (Hornby 1983; Cook 2003). However, Ggt can affect another cereal plants as rye (Secale cereale L.) and triticale (×Triticosecale, hybrid of wheat and rye). This fact affects significantly the cultural control of the pathogen, due to agronomic rotation is a better alternative that consists of the culture with non-susceptible crop hosts for 1–2 years (Cook 2003).

The discovery of suppressive soils limiting the proliferation or damage of the pathogen opened new alternatives for environmentally friendly techniques for soil-borne disease biocontrol. This is very important due to the soil-borne pathogen could increase their incidence as a consequence of climate change (Delgado-Baquerizo et al. 2020).

Soil suppression is defined as the ability of a natural soil to reduce or suppress the activity of plant pathogens, mostly due to the presence and activity of soil microorganisms. Their presence increases the ecosystem resilience by creating redundancy in ecosystem services, making soil less vulnerable to short-term changes in the environment (Wall et al. 2012). The suppressiveness could be achieved indirectly by creating a physical environment that limits the survival, spread, or infectivity of the pathogen, or favors the plant over the pathogen; or directly by supporting the proliferation of antagonistic microorganisms (Löbmann et al. 2016). For example, several studies showed the relation of Pseudomonas spp. and Ggt suppression due to the production of 2,4-diacetylphloroglucinol (DAPG) (Weller et al. 2002; Garbeva et al. 2004; Mavrodi et al. 2007; Yang et al. 2014).

Aspects of suppressiveness are still debated, as the relation between pathogen density and disease incidence. In the case of Fusarium sp. suppression, early studies reported no relation between these parameters (Amir and Alabouvette 1993). Mazzola (2002) defined suppressive soils as those in which disease development is minimal even in the presence of a virulent pathogen and a susceptible plant host. On the other hand, authors showed that the magnitude of suppression of take-all is largely dependent on the amount of the pathogen present in the soil relative to the natural antagonists, the cropping history, and the soil types, likely resulting in differing capability to suppress take-all (Cook 2003; Chng et al. 2015). In Gaeumannomyces graminis, recent studies revealed that no differences in fungal concentration between suppressive and conducive soils were found, confirming that suppressive soils had low disease incidence despite Ggt DNA concentration (Duran et al. 2018). Similarly, Chng et al. (2015) evidenced low disease severity coupled with high Ggt DNA concentrations in roots. Thus, despite that suppressive soils have been studied for over 100 years (Chandrashekara et al. 2012) and have been demonstrated for a wide range of soil-borne plant pathogens including bacteria, nematodes, oomycetes, and fungi (Table 7.1). Techniques to take advantage the important niche of suppressive soils have not developed.

Table 7.1 Soil-borne pathogen suppression
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Actuality, considering that recombinant DNA techniques have provided a solution to obstacles associated with the use of culture-dependent techniques generating independence on cultivating those organisms in the laboratory (Foo et al. 2017). Additionally, with the sequencing of RNA that includes full-length cDNA analyses, serial analysis of gene expression (SAGE)-based methods, and noncoding RNA improvement, the next-generation sequencing as “meta-omics’ tools have been improved widely the progress in research that involved the study of microbiomes, defined as microbiota, metagenome, and surrounding environment of a microbial community (Sheth et al. 2016).

Here, we review new research horizon in agriculture to improve plant health by engineering microbiome from conducive to suppressive soil considering Gaeumannomyces graminis as a model to propose the next generation to soil-borne disease biocontrol.

7.2 The Pathogen Causing of Take-All Disease

Take-all is caused by the fungus Gaeumannomyces graminis (Sacc.) Arx et Olivier var. tritici (Walker) or Ggt. This fungus is an ascomycete belonging to the family Magnaporthaceae and also affects barley, rye, and related grasses as triticale, but is best known and is most important for the disease it causes on wheat (Cook 2003).

G. graminis can survive saprophytic on infected or dead root and crown debris from previous crops through parasitism causing primary infection (Fig. 7.1a, b), where the pathogen uses these substrata as source of food to infect the next wheat crop (Hornby 1983). Roots come into contact with the ascospores and dark runner hyphae of Ggt colonize the roots superficially and then penetrate directly by hyaline hyphae beneath the hyphopodia into the roots cortex and across the endodermis into the stele obtaining nutrients, carbon, and energy becoming to the secondary infection (Fig. 7.1c, d) (Gilligan et al. 1994; Fang 2009; Weller 2015).

Fig. 7.1
figure 1

Cycle of life of Gaeumannomyces graminis var. tritici (a) that present two stages: primary infection (saprophytic stage) where apothecium and residues of infected plants residing in the soil, (b) secondary infection where plants are infected by ascospores (c, d)

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The infection starts as a root rot, causing stunting and deficiency of nutrient in the shoots due to that the mycelia invading causes disrupting water transport and assimilates translocation due to the colonization of vascular tissues causing characteristic black lesions and runner hyphae continue to grow over the root surface, to other roots, and upward to the crown and stem bases (Cook 2003; Weller 2015). The rapid progress of the infection from root to stem basis causes yellowing of lower leaves, stunting, and premature death of plants (Cook 2003; Weller 2015). In fields symptoms appear as chlorotic spot due to the presence of symptomatic plants (Fig. 7.1c).

7.2.1 Control Methods

Strategies based on chemical control of take-all have been inefficient due to that the control of soil-borne pathogen is depending on the use of soil fumigants of broad-spectrum gaseous as methyl bromide, chloropicrin, metam sodium which are unacceptable in agriculture (Weller 2015), whereas systemic fungicides as triadimefon moves very inefficiently or not at all downward into the roots where the early protection is needed (Cook 2003). On the other hand, the complexity of the fungal cycle due to the existence of the primary and secondary infection is related with the root structure. Thus, Bailey et al. (2004) showed that the seed treatments are restricted to reduce the infection to the seminal roots by particulate soil inoculum but secondary infection affects seminal and adventitious root systems and consequently not affects the ability of adventitious roots to pass on the disease. For this reason, main cultural practice to take-all control is crop rotation with no susceptible host due to the pathogen is able to survive in crop residue saprophytically as explained above. Contrary, take-all is also controlled by take-all decline (TAD), which occurs naturally with wheat monoculture wheat or barley after a severe outbreak of the disease (Hornby et al. 1998; Weller et al. 2002; Kwak et al. 2012). This phenomenon has been recently called as host-mediated microbiota engineering (Rodriguez and Durán 2020).

7.2.2 Biological Control

Biological control of take-all has been poorly studied and the most of studies has been realized under in vitro conditions. In the last years, studies related with Ggt biocontrol has been restricted to Pseudomonas fluorescens producers of 2,4-diacetylphloroglucinol (2,4-DAPG) (Mazzola 2002; La Fuente et al. 2004; Validov et al. 2005; Jamali et al. 2009; Kwak et al. 2009, 2012). However, in natural soil system Pseudomonas rhizosphere microorganisms comprise only 1–10% of the total culturable bacteria (Mavrodi et al. 2007) and culturable bacteria represent only a small portion (1–10%) of total bacteria in the rhizosphere (Nannipieri et al. 2003). In addition, Pseudomonas strains are highly sensible to desiccation and other adverse factors, thus the dominance and permanence in soil are a limiting aspect (Normander et al. 1999; Liu et al. 2009).

Considering that endophytic bacteria have ecological advantage over rhizobacteria due to plant tissues offer protection against environmental conditions and they have a stronger association with plants than rhizobacteria (Sturz et al. 1999; Reiter et al. 2002; Pathak and Keharia 2013). Several reports have been included endophytic microorganism to be used in agriculture (e.g., soil-borne pathogen control) (Strobel et al. 1996; Zhang et al. 1999; Strobel and Daisy 2003; Babu et al. 2013). In this context, Liu et al. (2009) showed that endophytic Bacillus subtilis can successfully inhibit the development of G. graminis and other phytopathogens under in vitro and field conditions similar to the treatment with the fungicide triadimefon. In addition, was able to promote the plant growth of wheat seedlings. Similarly, Durán et al. (2014) showed that endophytic strains Acinetobacter sp., Bacillus sp., and Klebsiella sp. inhibited the Ggt mycelia growth in vitro conditions (from 30 to 100%).

Due to cereal plants are able to form symbiotic association with arbuscular mycorrhizal fungi (AMF), Castellanos-Morales et al. (2012) tested the influence of Glomus mosseae, Glomus intraradices, and Gigaspora rosea against Gaeumannomyces graminis, demonstrating the influence of AMF on take-all incidence despite different colonization rates among Glomus species. In contrast, Duran et al. (2018) reported no effect of Claroideoglomus claroideum in terms of root infection on wheat plants inoculated with Ggt. However, mycorrhizal plants resulted in an increase in plant biomass. Authors attributed this role to endophytic bacteria (Acinetobacter sp. E6.2 and Bacillus sp. E5) was able to diminish efficiently the pathogen incidence, confirming the role of these microorganism in order to promote the plant growth and protect against take-all under greenhouse conditions.

7.3 Soil Suppression Against Take-All Disease

Suppression is termed general suppression when it is based in a general antagonist effect of the total soil microbial biomass (Mazzola 2002; Weller 2007). In the general suppression no-specific microorganism or a selected group of microorganisms is solely responsible for the effect (Cook 2003). These specific microbes are recently called key species or core microbiome, driving the microbiome composition and function (Dong et al. 2020). Thus, general suppression is non-transferrable between soils (Andrade et al. 2011; Kwak and Weller 2013). In contrast, the so-called specific suppression, which is specific to a particular pathogenic microorganism and is mediated by specific microorganisms although using mechanisms similar to those operating in general suppression (Cook 2003; Andrade et al. 2011). It has been shown that the addition of 1% (w/w) of natural suppressive soil into sterile suppressive soil inoculated with Ggt is sufficient to transfer the suppression against take-all disease (Andrade et al. 2011; Chng et al. 2015; Durán et al. 2017).

7.3.1 Factors Required for Take-All Suppression

According to Weller et al. (2002) three factors are needed to produce take-all suppression: (1) monoculture of susceptible host, (2) presence of Ggt, and (3) outbreak of take-all (Fig. 7.2). Thus, studies showed that conductive soil where has been developed the disease and wheat monoculture produces a diminution of disease although the pathogen is present in soil “suppression” (Garbeva et al. 2004; Andrade et al. 2011). This phenomenon of take-all decline could be developed during the traditional agronomic practice of wheat monoculture, where the same crop is cultivated in the same soil continuously. Regarding the timing, take-all suppression appeared after 4–6 years of wheat monoculture (Gardener 2004), and even after and showed that soils with 3–4 years of monoculture under relatively high pathogen inoculum concentrations (Chng et al. 2015). In fact, early studies by Baker and Cook (1974) showed that 3 years of successive wheat cropping could be sufficient for the development of specific suppression.

Fig. 7.2
figure 2

Factors involved in take-all suppression

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7.3.2 Abiotic Factors Involved in Take-All Suppression

Abiotic factors as chemical and physical parameters of soil as pH, organic matter, and clay content can influence the soil-borne suppression directly affecting the pathogen, or indirectly through the impact on the soil microbial activity (Mazzola 2002).

7.3.2.1 Soil Chemical Parameters

Physicochemical characteristics such as pH, temperature, chemical composition, texture, and humidity of a soil can influence Gaeumannomyces graminis suppression (Whipps 1997). For example, studies shown that G. graminis prefers soil with pH from 5.5 to 8.5 (Cook 2003; Freeman and Ward 2004). Thus, the pathogen is less present in soils or rhizosphere soils with less pH, which also can be attributable to the trace nutrients also can be more available in acid than in alkaline soils (Cook 2003). This fact was reported previously by Sarniguet et al. (1992), where showed that N (nitrogen) source is a determinant factor to Gaeumannomyces graminis inhibition. Thus, NH4 treated soils were more suppressive to take-all disease than NH3 one, causing more acidic on the rhizosphere and favoring the diseases suppression by soil microorganisms. Similarly, Durán et al. (2017) showed that rhizosphere microorganism from suppressive Andisol was directly correlated with soil chemistry mainly P, pH, and Al saturation. However, low knowledge about the influence of physicochemical soil characteristics on the suppression of take-all disease of wheat (Andrade et al. 2011).

7.3.2.2 Rainfall

Take-all is most severe when wheat is grown under high rainfall or irrigation generating a moist ambient, called “Wetland take-all” (Roget and Rovira 1991; Cook 2003). However, take-all can occur in zones with less than 45 cm of annual precipitation called “dryland take-all” (Paulitz et al. 2002).

However, it is important to consider other abiotic factors that could coexist in soils. Therefore, criterion is difficult to apply to suppression mediated by abiotic factors. In fact, studies showed that suppression is more related with soil microbiome (biotic factors) than abiotic factors due to when soils is sterilized (discarding the effects of soil microorganisms) (Durán et al. 2017). Thus, soil suppression could result from biotic and abiotic factors through a diverse and complex set of mechanisms, the biotic aspects, mainly related to the soil microbiota activity.

7.4 Plant–Microbe–Soil Interactions Involved in Take-All Suppression

7.4.1 Microbial Rhizosphere Effect on Soil Suppression

The mechanisms implicated in disease suppression by microbial antagonists include competition for nutrients and colonization sites, antibiosis, synthesis of hydrogen cyanide (HCN), siderophores production, secretion of cell-wall degrading enzymes, production of volatile compounds, lowering ethylene, bacteriophages, interference with the pathogen quorum sensing (quorum quenching), and induction of plant systemic resistance (ISR) (Bakker et al. 2013; Glick 2015). Thus, microbial rhizosphere may act directly or indirectly through parasitism or antibiosis, amensalism or competition for resources (Fig. 7.3).

Fig. 7.3
figure 3

Types of suppression: specific suppression that inhibits the infection of a particular soil-borne pathogen and general suppression or no-specific that inhibits the infection of two or more soil-borne pathogens

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A study realized by Latz et al. (2016) showed that Rhizoctonia solani suppression in potato plants was mediated by rhizosphere bacteria belong to Actinomyces, Bacillus, and Pseudomonas genera (Latz et al. 2016). Trivedi et al. (2017) showed that Fusarium oxysporum suppression could be attributed to multiple soil microbial genera where Actinobacteria phyla act as biological indicator of soil suppression against F. oxysporum due to inhibit 25% of pathogen growth when the relative abundance of Actinobacteria was above 8%, suggesting this microbial phyla as biological indicator of soil suppression against F. oxysporum. Thus, plants could repel or attract (recruit) microbes by using exudates exerting a significant effect on the general health or by managing agronomic practices (Duran et al. 2018; Harkes et al. 2020). Highlighting that microbial selection should consider the origin of the microbes, obtaining and culturing of functional core microorganisms and to optimize the microbial interactions according to their compatibility (Arif et al. 2020).

7.4.2 Antibiosis Influence on Soil Suppression

Antibiosis are commonly the most studied of the mechanisms involved in disease suppression from microbial rhizosphere species. An antibiotic is a secondary metabolite with biocide activity produced by microorganisms to maintain their niche and territory and to enhance survival prospects in competitive environment (Troppens et al. 2013). Their production is a normal part of the self-protective arsenals of multiple microbial species, and consequently these organisms have a great potential for soil conditioning (Pereg and McMillan 2015). Among soil microorganisms, bacteria belonging to genera Streptomyces, Bacillus, and Pseudomonas are particularly prolific producers of secondary metabolites (Troppens et al. 2013). For example, it is well known that several groups of antibiotics are involved in the suppression of fungal phytopathogens by fluorescent Pseudomonas spp. like phenazines, pyoluteorin, pyrrolnitrin, and the polyketide 2,4-diacetylphloroglucinol (DAPG) (Yang et al. 2014).

DAPG has been reported as an efficient inhibitor of bacteria, fungi, oomycetes, and nematodes (Troppens et al. 2013). Indeed, this antibiotic is highly capable to inhibit efficiently Ggt and other soil-borne pathogens as Rhizoctonia solani (Garbeva et al. 2004; Yang et al. 2014). Early studies carry out by Baker and Cook (1974) showed that repeated monoculture of take-all susceptible host favored the presence of dominant microbial species in the rhizosphere. Later research revealed that microbial activities in the soil were likely responsible for the onset of take-all decline (TAD) (Cook 2003; Weller et al. 2002), as it is the case of populations of 2,4- diacetylphloroglucinol (2,4-DAPG)-producing (Phlþ) Pseudomonas fluorescens. Ggt is highly susceptible to the antibiotic 2,4-DAPG, which accumulates in the rhizosphere in sufficient amounts for disease control when the bacteria reach a (above a threshold density of 105 CFU g−1 root, Weller et al. 2002; Weller 2007). Despite 2,4-DAPG is known to induce systemic resistance (Weller et al. 2012) and the pathogen do not develop tolerance in TAD fields even after decades of wheat monoculture (Kwak et al. 2009). Furthermore, 2,4-DAPG is clearly stable and persistent in the rhizosphere (Kwak et al. 2012), studies realized by Brazelton et al. (2008) reported that 2,4-DAPG altered tomato root morphology and physiology, causing brown roots and inhibition of primary root growth and stimulation of root branching. Later, Kwak et al. (2012) showed similar alterations in wheat roots at final concentration of 10 μg mL−1. Recently, Durán et al. (2017) tested the influence of 2,4-DAPG-producing bacteria by phlD gene occurrence in suppressive soils from Chile, but the presence of these microorganism was only detected in one out of the six suppressive soils.

7.4.3 Plant Defense Against Take-All Disease

Disease occurs when a susceptible plant is infected by a infective pathogen under environmental conditions that favor disease (Surico 2013). However, plants are able to induce defense mechanisms against infectious diseases (basal resistance). These mechanisms can be grouped into pre-existing barriers and post-existing. In the case of pre-existing mechanism against pathogens is well known the structural defense mechanisms (i.e., the wax layer and cuticle, epidermal layer, cytoskeleton) and pre-existing biochemical defense are well known (i.e., phytohormones, phytoanticipins, anti-microbial compounds (i.e., terpenoids, pyrethrins, diterpenoids, saponins) (Doughari 2015).

Saponins are glycosylated triterpenoids (triterpenoids with attached sugar groups) that are present in the cell membranes of many plant species which have deter properties and act by disrupting the cell membranes of invading fungal pathogens (González-Lamothe et al. 2009). In general, cereals and grasses are deficient in saponins. However oat had been widely described as saponin producer and has been early implicated in the resistance of oats to Gaeumannomyces graminis var. avenae (Osbourn et al. 1994). The antifungal activity of avenacin is associated with complexes formation with sterols present in fungal membrane leading to pore formation and loss of membrane integrity (Morrissey and Osbourn 1999). The localization of avenacin is in the epidermal cell layer of oat root tips and in the emerging lateral root initials, suggesting a role as a chemical barrier (González-Lamothe et al. 2009). Moreover, roots of plant also may interact via plants by priming plant defense reactions and rhizodeposits that in turn may select microbial populations in the rhizosphere and soils can influence the interaction among microorganisms themselves (Glick 2015). Thus, microbial through several mechanisms including the suppression of infectious diseases, for example, inducing systemic resistance in plants (ISR) which has been recognized as the mechanism that at least partly explains disease suppression (Bakker et al. 2013).

7.4.4 Induced Systemic Resistance (ISR) as the Mechanism of Disease Suppression

Induced resistance could be triggered by abiotic and biotic (including avirulent strains). In general, induced resistance is of the systemic type due to defensive capacity may be produce in non-infected tissues (Van Loon et al. 1998). Induced systemic resistance (ISR) is a state of enhanced defensive capacity developed by a plant when appropriately stimulated and induced by a PGPB (Van Loon et al. 1998; Glick 2015). However, plants also may develop systemic resistance induced by the pathogen itself is called systemic acquired resistance (SAR). However, induced resistance is not always expressed systemically and only is located in tissues primarily involved (Localized acquired resistance, LAR) (Van Loon et al. 1998). SAR and LAR are similar in terms that could be effective against various types of pathogens. However, SAR is characterized by an accumulation of salicylic acid (SA) that also can be stimulated by exogens application of SA, whereas ISR has been involved with the accumulation of jasmonic acid and ethylene (Glick 2015). Therefore, SA and JA are major hormonal regulators of the plant immune signaling network, where SA is typically effective against infection by biotrophic pathogens, whereas JA is essential for the immune response against necrotrophic pathogens and herbivorous insects (Pieterse et al. 2012).

During the last decades ISR has been recognized as an effective mode of action for a range of microbial that acts as biological control agents. Thus, disease suppression has been evolved with competition for nutrients, antibiosis, and ISR (Bakker et al. 2013). In this context, several studies showed that Pseudomonas can activate a plant defense system by ISR in wheat plants affected by Gaeumannomyces graminis by the production of 2,4-DAPG antibiotic (Kwak and Weller 2013). However, the effectivity of Pseudomonas strains as bioinoculant is limited due to their low capacity of survival on soil.

7.5 Conclusions

Studies related with soil disease suppression are numerous, mainly considering biotic factors associated with the disease incidence diminution as microbial composition; however, the mechanisms involved are multiple and complexly interconnected. In fact, studies of plant–microbe–soil interactions guaranty a better understanding of these processes to facilitate their successful applications in biotechnology. Mainly, based in the important niche that offer suppressive soil in terms of microbial effect against to Gaeumannomyces graminis, considering that this soil could be lost in the short term due to industrialization and intensive agriculture. The next-generation sequencing opens new alternatives to plant biocontrol, considering, for example, the engineering plant microbiome in order to improve the plant health and food security.