Edited by: David Turra, Università degli Studi di Napoli Federico II, Italy
Reviewed by: Anwar Hussain, Abdul Wali Khan University Mardan, Pakistan; Muhammad Hamayun, Abdul Wali Khan University Mardan, Pakistan
This article was submitted to Plant Pathogen Interactions, a section of the journal Frontiers in Plant Science
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Plants exist in close association with uncountable numbers of microorganisms around, on, and within them. Some of these endophytically colonize plant roots. The colonization of roots by certain symbiotic strains of plant-associated bacteria and fungi results in these plants performing better than plants whose roots are colonized by only the wild populations of microbes. We consider here crop plants whose roots are inhabited by introduced organisms, referring to them as Enhanced Plant Holobionts (EPHs). EPHs frequently exhibit resistance to specific plant diseases and pests (biotic stresses); resistance to abiotic stresses such as drought, cold, salinity, and flooding; enhanced nutrient acquisition and nutrient use efficiency; increased photosynthetic capability; and enhanced ability to maintain efficient internal cellular functioning. The microbes described here generate effects in part through their production of Symbiont-Associated Molecular Patterns (SAMPs) that interact with receptors in plant cell membranes. Such interaction results in the transduction of systemic signals that cause plant-wide changes in the plants’ gene expression and physiology. EPH effects arise not only from plant-microbe interactions, but also from microbe-microbe interactions like competition, mycoparasitism, and antibiotic production. When root and shoot growth are enhanced as a consequence of these root endophytes, this increases the yield from EPH plants. An additional benefit from growing larger root systems and having greater photosynthetic capability is greater sequestration of atmospheric CO2. This is transferred to roots where sequestered C, through exudation or root decomposition, becomes part of the total soil carbon, which reduces global warming potential in the atmosphere. Forming EPHs requires selection and introduction of appropriate strains of microorganisms, with EPH performance affected also by the delivery and management practices.
Plants, like other so-called higher organisms, do not exist as entities unto themselves. They are biotic systems which consist of the plant plus innumerable microorganisms, the plant microbiome. This review considers plant-associated bacteria and fungi, focusing on those that internally colonize plant roots as microbial endophytes. Plants, together with their associated microbiomes, function as complex multi-species entities, referred to in the literature as holobionts (
A number of mechanisms are involved in producing these effects, particularly plant-microbial interactions, but there are also various microbe-microbe interactions. Because they are not widely known, we are particularly interested here in the microbial production of organic molecules that interact with plant cell membranes and induce system-wide changes in plant physiology, altering both plant gene and protein expression. These molecules we refer to as Symbiont-Associated Molecular Patterns (SAMPs;
By enhancing yields, EPHs can contribute to maintaining food security and reducing hunger in the world. These goals will become more challenging in future decades as still-rising human populations must be supported from a diminishing natural resource base that will be further constrained by the changing climate. EPHs can help to mitigate this as increased plant photosynthesis with greater root growth can increase carbon sequestration from the atmosphere and larger root systems will increase carbon stores in the soil. Increases in soil carbon (SC), especially in soil organic matter (SOM), will improve soil health and fertility which are associated with greater plant health, crop yields, and ultimately human health.
Following this introduction, Section 2 (entitled the functioning of enhanced plant holobionts) describes in general terms the physical interactions of symbiotic microbes with plants, and especially the colonization of internal plant organs and the nature of the endophytic associations. Section 3 (mechanisms for enhanced plant holobionts) reviews mechanisms by which endophytes react with plants to protect plants’ health and support their growth, robustness, and productivity. Section 4 (biochemical and genetic effects associated with EPHs) discusses the biochemical effects associated with SAMPs and their gene and protein regulation, improvements in photosynthetic efficiency, and effects of internal cellular functioning.
Section 5 (benefits conferred on plants) considers benefits that this symbiotic association confers on plants, including the control of biotic stresses, including disease, insect pests, and nematodes, as well as the mitigation of abiotic stresses such as drought, salt, and adverse temperatures. Section 6 (agricultural and societal benefits) discusses higher-level agricultural and societal benefits, including improvements in soil health, enhancing sustainable food production, and creating environmental benefits such as carbon sequestration and storage, which can help to slow global warming by capturing and removing greenhouse gases such as CO2 from the atmosphere.
Section 7 (management and delivery systems for EPHs) addresses important aspects of the delivery and management of microbial agents, including the application of exogenous inoculum and the mobilization of existing soil populations. Section 8 (enhancing microbial endowments with changes in crop and soil management) then goes into management systems such as no-till cultivation that can have beneficial effects on the soil biota, and the system of rice intensification for which we have experimental evidence confirming the practicality of EPHs when modifying crop management. Section 9 summarizes the various components that contribute to the creation and cultivation of EPHs and to the benefits that these confer at both micro and macro levels. Section 9 is a summary of the paper.
Numerous fungi and bacteria may provide beneficial effects including endophytic fungi (
Many bacteria and fungi are beneficial to plants in various ways:
By improving their resistance to diseases and pests;
By mitigating abiotic stresses such as drought, salt, and adverse temperatures;
By improving plants’ nutritional status through better acquisition of nutrients from the soil, enhancing supply of nutrients such as through the fixation of nitrogen, and better nutrient-use efficiency;
By enhancement of plants’ photosynthetic capability; and
By maintaining internal cellular environments that are more conducive for the functioning of critical plant metabolic processes.
These services generally result in better growth of plants’ shoots and roots and thus in higher yields, especially under adverse conditions.
Numerous bacteria and fungi are known to improve plant performance, among them bacteria in the genus or families
Many of the most beneficial microbes live within the internal space of plant roots. In at least one case, they take up residence anywhere in the plant where they are applied, not limited to the roots. In two other cases, once established in the roots, the microbes become systemic throughout the plant. The beneficial species that are considered in this review do not cause disease or other deleterious effects. Not all, but many microorganisms living within plant organs and tissues have beneficial effects on plants’ growth, health, and productivity. Their symbiotic services to plants are similar to those that myriad microbes in the human microbiome confer on our species. These endophytes when introduced purposefully to augment whatever microbial populations exist naturally in the plants’ microbiomes create what we refer to as EPHs.
Colonization patterns differ as shown in
Examples of endophytic colonization by different bacteria or fungi.
Among the more complex interactions are those involving bacteria in the Rhizobiacae family of protobacteria. In leguminous plant species, these bacteria infect plant roots and form nitrogen-fixing nodules, structures composed of both plant and bacterial cells as shown in
Conversely, some of these same bacteria which fix nitrogen in the roots of clover plants can infect the roots of cereal plans like wheat or rice and become systemic throughout these plants (
Vascular-arbuscular mycorrhizal (VAM) fungi also form complex plant root-microbial structures. These fungi interact with plant roots to form arbuscules within the roots that are highly efficient in transferring nutrients such as phosphorus from the VAM to the plant and of nutrients from the plant to the VAM in return, as seen in
Some strains of
In certain plants, strains of
Chemical crosstalk between roots and root colonizing microbes is required for symbiotic relationships to occur. With maize, roots and
The ability of certain fungi to colonize and parasitize other fungi and Oomycetes has been known for almost 90 years. This capability of fungi does not per se lead to the formation of holobionts, but it is included here for reasons of completeness. In addition, some fungi that are mycoparasiitic are endophytes that form holobiontic associations with plants.
The events that occur in mycoparasitism have been well documented in interactions of
Once in contact with the target fungus,
For example, strains of
Numerous metabolites are produced by bacteria and fungi that are toxic to particular plant pathogens and pests. For example, certain strains of
Similarly, control of the take-all disease in wheat caused by
In another case, we searched for strains of
This strain was isolated from a soil that had been periodically cultivated with peas for over a century. The root rot caused by the water mold
In the cases mentioned above, the antibiotics are clearly associated with disease suppression. However, it should not be assumed that this antibiotic production is the only mechanism involved in disease control. Many or most microorganisms produce at least some antibiotic substances. While their antibiotics may be involved in biocontrol, in most cases other mechanisms may also be involved, as discussed in later sections.
Earlier, we mentioned fungitoxic enzymes from
For example, a search for
For many years, this has been considered one of the three main mechanisms for microbial disease control, along with antibiosis and mycoparasitism. It is obvious that competition occurs widely and can never be excluded as a mechanism of biocontrol, but it is hard to prove or disprove. In at least one case, the control of aflatoxin by heavy application of atoxigenic strains of
Competition for infection sites by nonharmful strains can be expected to exclude harmful strains or species that are deleterious. It is thus difficult to rule competition in or out, since many cases of biocontrol may include competition.
Siderophores are a class of microbial metabolites that sequester iron, binding to it very tightly and making it difficult for other microbes with a lower affinity for iron to compete with those that are producing siderophores with a very strong binding of iron (
Siderophores from fluorescent
This capability can be demonstrated through several methods, such as comparing the Fe-EDTA or EDDHA (
However, competition for iron prevented biocontrol of damping-off diseases by a strain of
The previous sections have described biocontrol by the action of one organism on another. However, it is becoming increasingly clear that a great deal of the control of diseases and pests, as well as control of abiotic stresses, is a result of the effects of the microbial agent on the plant, changing gene and protein expression that results in benefits from developing EPHs.
We noted above, for example, that
Evidence of induced resistance includes the ability to control abiotic or biotic stresses at a distance from where the agent is located (
A synoptic diagram of the interactions of plants and endophytes that result in the formation of EPHs. A similar diagram was presented in (
Other evidence comes from genetic studies. For example, the gene NPR1 is essential to functioning of both Systemic Acquired Resistance (SAR) and Induced Systemic Resistance (ISR). These are two separate biochemical pathways by which each kind of resistance is induced. In studies with strains of the plant
However, these strains are also potent inducers of systemic resistance in plants (
These two examples (many others could be cited) demonstrate that effects on plants of beneficial microbes occur as a consequence of microbial effects on plants, rather than just their effects on plant pathogens as provided in section 5. Most of the studies demonstrating this effect began to be published in the early 2000s cf. (
In almost all cases, the induction of systemic effects which protect plants from pathogenic losses is mediated by the production of signaling molecules by endophytic microbes that interact with plant cell membranes. This results in signal transduction that occurs, in many cases, through mitogen-activated protein (MAP) kinases (
As indicated in those and other references, wounding of plants by injury or insects, infection by pathogenic microorganisms, and especially the effects of endophytic beneficial organisms all result in induction of beneficial systemic effects as does the alleviation of the negative effects of abiotic stresses.
The signaling compounds produced by beneficial organisms are numerous and varied. The primary elicitors for Rhizobiace and AMFs are chitooligosaccarides, and these are part of the common symbiotic pathway (
Surfactins from
Signal transduction leads to systemic responses in plants (
This in turn leads to signal transduction that leads to systemic responses (
As mentioned above, systemic changes in plant gene and protein expression require signal transduction, at least in some cases, through the action of MAP kinases (
An important consideration in this up-regulation are the energy costs to the plant. The pathways involved require both energy and resources such as fixed carbon, nitrogen, and other components that also are necessary for plant growth and development (
This process may take the form of some modification of histones surrounding DNA or DNA methylation which are part of the plant’s regulatory machinery (
Conventional agriculture practices use chemical biocides in controlling plant diseases and pests. Unfortunately, this approach induces resistance in pathogens and pests during long-term use (
The development of high-throughput molecular techniques such as proteomics, genomics, metagenomics and metabolomics for microbe isolation and characterization have allowed for the identification of a variety of bacteria and fungi able to act beneficially when proliferating in the soil for disease control and plant-growth promotion. Multi-omics has also advanced our ability to strategically select for microorganisms that have unique host site-specific qualities that function in biological disease or pest control (
Application of microbes as biocontrol agents in the field can have many benefits without requiring extensive investment in plant breeding and genetics (
The
The ability of
Some endophytic fungi, particularly
Moreover, the presence of
Arbuscular mycorrhizal fungi (AMF), which are endosymbionts, are effective biocontrol agents against several soil-borne plant pathogens. AMF are obligate root symbionts that can offer many benefits and protect their host plant against pathogen infections (
The results also revealed that total soluble phenols, flavonoids contents, and the defense enzyme phenylalanine ammonia lyase (PAL) were increased with AMF colonization, indicating an enhancement of the plant immune system against
Finally, several plant growth-promoting bacteria (PGPR) also possess traits that make them well suited as biocontrol and growth-promoting agents. As a consequence, plants treated with PGPR may be larger and healthier and have greater yields than plants without such treatment (
Canola plants inoculated with
Microorganisms have developed mechanisms that increase their host fitness and provide a more stable ecological community by working effectively against a broad spectrum of pathogens and pests and for alleviation of the adverse effects of plant stress, which is discussed in the next section.
On a daily basis, plants are exposed to numerous harmful environmental conditions that significantly affect their growth (
Drought stress, one of the most destructive abiotic stresses, has increased in intensity over the past decades, endangering the world’s food security. Currently, 90% of global water consumption is used for agriculture, and water constraints are expected to intensify in the future (
There are various agronomic mechanisms that explain microbes’ contributions to reducing the impacts of drought: alterations in root architecture that result in improved water use efficiency; increases in the synthesis of osmolytes, particularly proline; increases in antioxidant enzymes that scavenge for ROS; manipulation of phytohormones; and modifying plant gene regulation (
Root colonization by
Inoculation of wheat with
The application of
Salinity is another major abiotic stress that limits the growth and productivity of plants in arid and semiarid environments (
Many studies have reported microbes’ abilities to induce salt stress in plants by modulating ROS production (
In another study, barley plants previously inoculated with
Cold stress also severely hampers the reproductive development of plants and will result in significant agricultural losses. The major negative effect of cold stress is that it induces severe membrane damage in plants (
During complete submergence, plants experience a strong decline in their photosynthesis rate and carbon availability. This is due to a lack of light or a reduced rate of CO2 diffusion, and to impaired respiration through reduced O2 availability (
Beneficial microorganisms induce plant growth and counteract flooding stress through production of ACC deaminase, discussed in section “salt stress.” Under flooded conditions, plant roots become hypoxic. In response to oxygen-limitation, the enzyme ACC synthase is synthesized in roots. Because there is limited oxygen, ACC cannot be converted into ethylene. Subsequently, the unused ACC is transferred to the shoots where oxygen is available, and ACC can be converted into ethylene. However, the overproduction of ethylene by plants results in their wilting, necrosis and chlorosis.
One way that beneficial microorganisms contribute to mitigate flooding-stress conditions is by their producing ACC deaminase that can convert ACC into
One other stress that is alleviated by microorganisms is heavy metal stress.
The ability of a gibberellin-producing endophytic strain of
Amelioration of other environmental toxicants may be accomplished by the use of endophytic fungi. Cyanides are frequently present in mine tailings. Endophytic
Soils polluted by oily wastes are a serious problem. Researchers in Canada utilized
An important component of higher-level functioning leading to EPHs is the maintenance of internal cellular processes critical for plant growth, development and induced resistance to both biotic abiotic stresses is the avoidance of damaging ROS by gene and protein upregulation of the pathways for alleviating and mitigating their damaging effects (see the preceding divisions of this section). This is a feature of many endophytic microorganisms discussed in this paper. Earlier in this review, we discussed the damage that ROS cause to cellular functioning, and these are described in (
Thus, these endophytes are able to create an internal environment that maintains a cellular environment that is conducive to efficient operation of photosynthesis and all the other metabolic processes necessary for plant growth and amelioration of stresses. We have coined the term Optimized Internal Redox Environment (OIRE;
The previous section described maintenance of cellular functions, including photosynthesis. However, photosynthesis is actually increased and improved by endophytes, which contribute to formation of EPHs. Within the genus
The global population is increasing rapidly and is predicted to be roughly 9 billion by the middle of this century. Concurrently, global agriculture is facing increasing competition for land, water, and energy in food production (
In any case, global food requirements in the 2050s are expected to be double those of 2005. Unfortunately, annual productivity gains have been decelerating over the past two decades, and crop production area has been decreasing due to industrialization, desertification, and urbanization, which further constrains future food production. Therefore, there is urgent need for new initiatives to mitigate these challenges to the global food supply. Much evidence shows that careful selection and augmentation of efficient soil microbial strains is a potentially sustainable solution for raising agricultural production and reducing hunger globally. As mentioned previously, soil microbes play vital roles in helping crops to cope with multiple stresses induced by climate change such as higher temperature, more flooding and drought, and containing pests and pathogens. Soil microbes can also help to rehabilitate degraded soils by improving soil nutrient availability, suppressing soil pathogens, cleansing the soil of pollution and heavy metal contaminants, and preventing soil erosion.
Long-term monoculture production systems are one of the major factors contributing to soil degradation and contamination with inorganic pesticides, chemicals, and herbicide. Depending upon their concentration, soil contaminants can have destructive consequences on soil ecosystems, on the abundance and diversities of soil microbial communities, and on soil health. Soil microorganisms are not only crucial in crop production and soil health, but are also becoming important tools for cleaning up environmental pollutants (
Several beneficial microbes have been reported to have high bioremediation potential for chemical pesticides, petroleum hydrocarbons, and heavy metal contaminants in the soil. Microbial services for soil rehabilitation are less costly, easier to employ, and more environmentally friendly than other methods now used such as the “muck, suck, and truck” approach. Bacterial and fungi species employed for bioremediation include
It is well-established that microorganisms play critical roles in determining the concentrations of greenhouse gases such as carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O) in the atmosphere (
On the other hand, the application of beneficial microbes as biofertilizers, bio-stimulants, or biocontrol agents reduces the need for agrochemicals including fertilizers. Also, it reduces the habitat and sustenance for methanogens and denitrifying bacteria by competition for space, nutrition, and ecological niches in the soil, thereby reducing microbial sources of GHG emissions. Furthermore, if beneficial microbes such as
For example, minimum tillage operations favor microbial communities dominated by fungi which decrease the microbial decomposition and respiration induced by soil disturbance during plowing. It has been reported that this could lead to sequestration of as much as 55 Pg organic carbon in the surface soil (
In China, a microbial preparation used with tea plants in their cultivation reduced emissions of N2O by 33.1–71.8%, while yield was increased by 16.2–62.2% relative to standard use of synthetic N fertilizers. These indicated once again that microbial enhancement of crop holobionts can reduce GHG emission from agriculture with favorable impact for less global warming with a gain rather than a sacrifice in production.
The previous sections review the potential of various microorganisms to improve plant productivity. However, results may be inconsistent and suboptimal unless the organisms are properly used. This includes appropriate means of delivery to maximize and ensure that the organisms are able to colonize, protect and enhance plant growth and development. In addition to delivery systems, the way that microbial formulations are assembled and delivered can make a large difference in whether or not the organisms are able to provide the benefits anticipated. These are formidable challenges for their successful use.
The major challenges to be dealt with in the commercialization of microbial agents for improving crop production are inconsistent efficacy of the biological material, having a delivery system that can maintain the viability of the material, and ensuring appropriate physiological conditions of the microbial inoculants during transportation and handling (
Based on considerations of survivability, mode of action, and local climatic conditions, there are several types of delivery systems for microbial inoculants. These can be directly applied to seeds by seed inoculation, to the roots by root dip methods, by drenching of young plants, to the plant and soil through drip irrigation or flooding, or to growing plants by foliar spray (
A diagram of different delivery systems employed in agriculture.
The basic characteristics of an effective delivery system include easy mode of delivery; enhancement of target activities with effective concentration; little or no ecotoxicity; time controlled release; solubility, stability, and effectiveness (
Previously, the peat, clay, and liquid-based delivery systems were well-established; however, peat and clay-based carriers have proven difficult to sterilize, and they have a high chance of external contamination, plus low stability and viability during storage and handling. Similarly, liquid-based formulations may not be sufficiently protective to bacterial products during storage, transportation, and application into the soil. Stable liquid formulations are easier to achieve with spore-formers such as fungal spores and with gram-positive bacteria that form endospores; they are more difficult with gram-negative bacteria that lack resistant spore types.
Commercial practice usually requires that preparations have at least a year of shelf life without refrigeration or other special handling. Furthermore, suspension-based inoculations have several other demerits, such as settling of the microbial inoculants, blockage of spray nozzles during the application, and abiotic stresses affecting the viability of the spores (
Recent advances in science have focused on developing various encapsulation technologies to deliver the microbial products more effectively and cheaply in the farming system. The processes of lengthening the cell viability of microbes by entrapping or coating them within polymeric materials that are permeable to nutrients, gases and metabolites is known as encapsulation. Encapsulation has been divided into two categories based on the bead size: (i) macro encapsulation (a few mm to cm), and (ii) microencapsulation (1–1,000 μm;
Synthetic polymer, biopolymer, and different kinds of organic/inorganic materials are used in encapsulating microbial cells for agricultural use. The three major benefits related to encapsulation technology compared to the traditional delivery system include: (i) enhanced efficacy due to increased surface area; (ii) enhanced microbial activity due to higher penetration efficiency; and (iii) higher dispersion on plant surfaces due to smaller particle size (
Bioformulation improves the performance of microorganisms by preserving them and delivering them to their targets more reliably. (
Microbial inoculants can be formulated as dust, seed dressing powder, micro-granules, water dispersal, wettable powder, emulsifiers, suspension concentrates, oil dispersion, emulsions, capsule suspension, and ultra-volume formulations (
Some researchers (
In the senior author’s experience, single strains or at most three strains can be effective if the strains are carefully selected, if the formulations are appropriate, and if they are used with appropriate management systems. Limiting the number of strains is essential if registration is required, since most registration requirements include toxicology evaluations that are very time-consuming and expensive. Full registration packets typically require several tens of thousand dollars for each strain, and if multiple strains are used the total cost can exceed a million dollars. Regardless of the strain(s), delivery system, or formulation used, it is essential that any product or strategy be tested rigorously to ensure reliable results in the field.
Obviously, the selection of effective microbial strains is critical in bio-based product development. These strains should be sufficiently competitive with indigenous soil microbial populations to survive, as well as being compatible with other inoculants and native microorganisms along with their colonization efficiency in plant rhizoplane (
As mentioned already, microbial species and strains have differential potentialities to serve the plant communities within and with which they reside, utilizing different mechanisms and colonizing different niches in the rhizosphere and rhizoplane regions. Many will inhabit the plants’ endospheres. The carefully-selected application of microbial strains can fill vacant niches in the soil and establish communication with plants and other strains differently than do the indigenous microbes that are already present in the soil. Some microbial strains can vigorously thrive in more variable environments than can others. These can quickly capture spaces and nutrients in the plant rhizosphere, making these resources unavailable to potential pathogenic invaders.
The effects from exogenous application of plant microbes are not always consistent across fields and crop species. However, research has been undertaken focusing on how to prepare and adapt the rhizosphere environment for colonization of specific exogenously-applied microbial strains by rhizosphere engineering (
Host variation along with plant variety will affect a plant’s response to beneficial microorganisms (
Agricultural soil is a vast reservoir of microbial biomass and diversity. It is estimated that 1 g of rhizosphere soil contains more than 100 species of microbes and 108–1011 viable cells (
High tillage, the use of pesticides and chemical fertilizers, continuous monoculture, flood irrigation, reduced crop rotation, and lack of organic matter in the soil all negatively impact the soil microbial population and its diversity. On the other hand, cover cropping, crop rotation, intercropping, minimum tillage, system of rice intensification methods, the addition of organic manure, and organic amendments to the soil all support microbial and microbiome diversity and population. The addition of microbial probiotics, biochar, and organic manure with these different agronomic practices has been reported to increase microbial abundance and activity in the soil. Thus, it is possible to increase the efficacy of indigenous microbial populations by complementary crop and soil management practices and by purposeful enhancement of the soil biota (
Rice is the staple food for more than 50% of the global population. A rice production system known as the system of rice intensification developed in Madagascar and validated in over 60 countries is currently gaining currency because of its higher productivity per seed grain, per drop of water, per unit area of land, and per unit cost of production. SRI relies on alternate wetting and drying (AWD) of rice paddies rather than on their continuous flooding, and it controls weeds by actively aerating the upper layer of soil around plants by use of a rotary weeder, rather than by using herbicides. It enhances soil nutrients by the addition of organic matter rather than with chemical fertilizer (
These SRI effects have been reported in over 1,000 papers and are already being achieved by around 20 million farmers using its methods in Asia, Africa and Latin America (SRI-Rice, n.d.). The productivity gains are achieved not by making changes in crop genetic potential and applying external agrochemical inputs but by making synergistic changes in soil, crop, and water management practices to create a more favorable environment for beneficial microbes such as mycorrhizal fungi and phosphorus-solubilizing microbes.
Continuous flooding has deleterious effect on rice plant physiology and anatomy as well as suppression of aerobic soil microbes. For example, flooding has deleterious effects on rice root systems by deforming cells in their cortex to create aerenchyma (air pockets) which affect the transport of water and nutrients (
The effects of inoculating SRI-grown rice plants with
There was a 58% average increase in yield from these varieties when they were managed with SRI methods but no microbial inoculation. However, yield was further increased by inoculation with
Research in Malaysia found similar results with a significant increase in seedling growth, germination rate, seed vigor index, and leaf chlorophyll content when rice plants grown under SRI management were inoculated with
There is growing interest in alternative cropping methods not only to reduce farmers’ costs of production but also to increase their yields and reduce adverse environmental impacts of farming, particularly soil erosion and agrochemical contamination of soil and water. What is known as conservation agriculture combines reduced mechanical tillage such as no-tillage or minimum tillage, plus crop residue retention on the soil, the use of cover crops, and crop rotation. It has been reported that about 13% of global croplands, 200 million ha in 80 countries, are covered by conservation tillage (
Both cover crops and reduced tillage practices improve soil systems’ physical and chemical properties, which has a positive impact in the biological properties of soil. Reduced tillage improves the soil’s structure through better aggregation, soil organic matter, water infiltration, water-holding capacity, and less soil erosion. Cover crops cultivation increase nutrient inputs through crop residue decomposition, biological N fixation, and root exudates, both for succeeding crops and microbial communities (
Conservation tillage greatly influences the soil microclimate, dissemination and decomposition of crop residues, and nutrient recycling. All of these changes have positive effects in soil microbial diversity and abundance (
This paper offers a comprehensive review of the knowledge and practice for using endophytic microorganisms to enhance and maintain more beneficial systems of crop production. Most of the cases reported involve endophytic bacteria and fungi symbiotically affecting the functioning of plants, but in some instances beneficial microorganisms’ principal means of benefitting agriculture and the environment are by other mechanisms such as competition and mycoparasitism.
The review considered first different patterns of endophytic root colonization (
Beneficial endophytes produce SAMPs that interact with cell membranes and result in signal transduction
These systemic responses also improve and maintain photosynthesis. This together with improved nutrient efficiency and acquisition, including N2 fixation, provide the essential components for plant growth and development. Improving photosynthesis is critically important. Plants require the energy and fixed carbon compounds to support both the numerous changes involved is systemic resistance systems and to provide the wherewithal for plant growth and development.
Provision of beneficial endophytes by itself cannot provide total reliability and results. There need to be management practices and good delivery methods that ensure viability and efficacy of applications. The components of effective delivery systems include effective seed treatments or soil applications, and effective organisms that must be selected from either single strains or consortia of different strains since only a few strains or species can enter into mutually-beneficial relationships with plants (
These changes in crop and soil management improve soil health and increase the organic matter in soils (
Summary of the various components and management systems that interact to provide optimal performance of plant agriculture.
All authors listed have made a substantial, direct and intellectual contribution to the work and approved it for publication.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.