Abstract
All plants in the ecosystem are found in close association with complex group of microbes both belowground and aboveground surfaces. Reports suggest that the association can be harmful, neutral, or beneficial to the plants depending upon the category of colonizing microbes. It is among them that certain microorganisms bring about modification in the plant metabolome, maneuvering to modifications in the biosynthetic pathway of plant metabolites of known and unknown origin. Plant secondary metabolites are exceptional group of chemicals released as an end product of biosynthetic pathways which have numerous secondary roles in survival and growth of the plants. Among the multifarious roles played by the metabolites, some of the important traits include repulsion of pathogens and attraction of beneficial group of microbes. The present chapter thus summarizes the till-date understanding of the role of root microbiome on the secondary metabolic status of plants, how the remodeling affects the health and defense status of the concerned plants, and finally the knowledge hiatus that needs to be fulfilled for harnessing the full potential of microbes.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
16.1 Introduction
Host-associated microbial populations are reported to be engaged in elementary roles like nutrition status, different developmental phases, and immunity of both animal and plant kingdom. The different factors which help in architecturing the host–microbiome interactions are inadequately understood, which hold an important place in evolutionary and ecological sciences (Fitzpatrick et al. 2018). Talking about the plants, the roots bring together two different microbial sections namely rhizosphere and the endosphere. The colonization at the rhizospheric surface by microbes can either be beneficial, neutral, or harmful associations, depending upon the relationship they share with the host plant. With the advancement in technologies, especially pertaining to sequencing, the picture of different root-associated microbiomes is getting clearer day by day (Rout and Southworth 2013). The most recent information which is coming out from the experimental evidences is that the role of microbiome differs not only with plant tissues but also with the change in environmental conditions too (Yu et al. 2019). The Next Generation Sequencing (NGS) data clearly demonstrates that amazing number of taxonomically dissimilar microbes colonize the plant system, whose density can be sometimes much higher than the plant cells figures (Mendes et al. 2013; Panke-Buisse et al. 2015). The colonization affects the plant system either directly or indirectly either by facilitating nutrient uptake, phytohormone production, induction of systemic resistance, formation of physical barriers, and changes in secondary metabolite status of concerned plants (Etalo et al. 2018). The most recent area of current research in plant–microbe interaction is changes in metabolomic status of plants leading to alteration in some key metabolites of agricultural and medical importance (Etalo et al. 2018). Hence, it is hypothesized that exploring plant–microbe communication will pave way for not only boosting production of metabolites of pharmaceutical importance but other unknown secondary metabolites too. The current chapter has thus been written with the aim to provide exhaustive information about the key players involved in alteration of secondary metabolites in plants with special emphasis on beneficial microbes, root exudates, and bioactive metabolites.
16.2 Root Microbes
Microorganisms have been defined as smallest organisms that cannot be seen with the naked eye and can only be seen with a special equipment called microscope. Among the diverse range of microbes, we in this chapter have specifically discussed about the microbes colonizing the root zone of plants. Microorganisms are mostly found as free-living microbes and when they stick around the plant roots and root hairs, they are called root microbes.
Root microbes are classified into two types:
-
1.
Beneficial microbes are those microbes which work toward enhancing the yield and overall well-being of plants and which can easily perform plant growth promotion, for example Pseudomonas, Bacillus, etc.
-
2.
Harmful microbes are the category of root microbes that inhibits the growth of plants by destroying the plant cells, making the plants nutrients deficient, and killing the beneficial microbes.
16.2.1 Beneficial Root Microbes
In the early 1904, Lorenz Hiltner observed and stated that there are numerous microorganisms which live in the soil near the rhizospheric region than the distant part of soil (Hiltner 1904). Soil is been widely accepted as the home for array of microbial species, fungi, invertebrates, archaea, and mostly bacteria (Tringe et al. 2005). Hiltner gave the term Rhizosphere for that region where microbial population was the highest near plant roots. It has also been derived that some region of soil which is conventionally benefitted by root secretion and associated with microbes of soil is referred to as root microbiome. Moreover, plant root system always expands through the soil and penetrates it, resulting in release of water-soluble materials such as amino acids, organic molecules, certain sugars, and carbohydrate derivatives which are essential for microorganism to survive.
Surprisingly, plant physiologists noted that soil plays a role in providing nutrients to plants, but they forgot to add that soil is a different complex ecological system having a huge species like protists, animals, bacteria, and fungi specially (Bonkowski et al. 2009; Müller et al. 2016). The microorganisms’ living in soil are the basic invisible mangers of soil fertility, and it doesn’t matter if the soil condition or crop species favour them or not, because it is the nature which promotes microbes to become root symbionts. These symbionts promote plant growth and increase yield by different actions like nutrient uptake and nitrogen metabolism resulting in nitrogen fixation, and these particular activities help plants to counter pests, diseases, and biotic and abiotic stresses (Fig. 16.1). Collectively, by the enhancement of plant capacity in photosynthesis and production of organic acids, plants derive their health and the microbes which helped throughout this process are referred as “beneficial root microbes.”
16.2.1.1 Types of Beneficial Root Microbes
The beneficial root microbes have been basically categorized into five different types, namely actinomycetes, bacteria, fungi, protozoans, and nematodes. The detailed information about these microbes has been discussed in the following sections.
16.2.1.1.1 Bacteria
Bacteria are the smallest living organisms and major key player of soil in bringing together the simpler forms around the root system so that the plants can firmly take up all the nutrients important to their growth and development, for examples macronutrients like nitrogen, phosphorus, potassium, etc. Phosphorus is usually not found in available form for the plants in soil, but some of the beneficial bacteria turns the nonavailable phosphorus into available form which a plant can easily utilize. In soil system there are huge number of bacteria which enhance plant growth and have thus been referred to as plant growth–promoting rhizobacteria (PGPR) (Bonkowski et al. 2009). Moreover, in obligate symbionts, PGPRs can easily interact with the host plants and enhance growth of the plant either by direct benefit via nitrogen fixation (Müller et al. 2016; Kloepper and Schroth 1987) or indirectly by secreting certain enzymes and hormones which can suppress other pathogens’ activity (Soyano et al. 2014; Ferguson and Mathesius 2014). The root hierarchy is also dependent upon PGPRs, as the structural modification in root results in better conduction of molecules into plant parts which is inversely proportional to better crop yield (Pérez-Montaño et al. 2014; Lugtenberg and Kamilova 2009; Uga et al. 2013). The projectile PGPR activity and plant growth promotion attributes are also reviewed in some articles (Ogawa et al. 2014; Ning et al. 2014).
Example – Indole-3-acetic acid production by the Rhizobium leguminosarum has been discussed in literature for playing a key role in promoting certain effects on rice seedlings (Biswas et al. 2000). In the same way, Azotobacter has been reported to do the job for maize seedlings (Zahir et al. 2000).
16.2.1.1.2 Actinomycetes
Actinomycetes are spore-forming, gram-positive aerobic bacteria which form thread-like structures called filaments, and work in cycling or turning up the organic matters, mainly by decomposition of complex mixtures found from decomposed plants, animals, or fungal sheets over rocks. Somehow these enzymes and hormones also help in suppressing certain plant pathogens which pose threat to plants, for example Streptomyces sp. have been found responsible for nutrient uptake and plant growth in rice and chickpea plants (Gopalakrishnan et al. 2014, 2015). Likewise, Frankia has been found to be responsible for nitrogen fixation in Alnus plant (Simonet et al. 1990).
16.2.1.1.3 Fungi
Fungi are multicellular, eukaryotic, heterotrophic organisms that have absorptive mode of nutrition. They live in the root zone of plants and act like natural recycling bins, help in reabsorbing soil nutrients from dead organic matter, and redistributing them back to plants roots. In addition, they also help in making nutrients available to plants through formation of siderophores. For example, mycorrhizal association is a mutual relationship which exists between roots of plant and fungus for sharing the benefits. The association is usually two ways – ectomycorrhizal when the fungus resides outside of root, or endomycorrhizal when the fungus penetrates inside of the root. It is well reported in literature that most of the rhizospheric fungus produces metabolites for the inhibition of plant pathogens (Ali et al. 2015; Saraf et al. 2014).
Example – Plant defense mechanisms can directly or indirectly be controlled by arbuscular mycorrhizal fungi (AMF) (Di Benedetto et al. 2017). Trichoderma harzianum are involved in active colonization of tomato root and induced systemic resistance-like defense in Arabidopsis. (Engelberth et al. 2001). Likewise, Trichoderma viride has been found to be responsible for elicitation of jasmonic acid and salicylic acid biosynthesis in lima bean (Morán-Diez et al. 2009).
16.2.1.1.4 Protozoa
Protozoa are single-celled, microscopic, eukaryotic, and heterotrophic organisms (using organic carbon as a source of energy). They are non-filamentous and restricted to moist or aquatic habitats. Protozoans play important roles in the fertility of soils by eating soil bacteria and maintaining bacterial populations. Protozoans sometime help in promoting plant health by the mineralization of nutrients and alteration in the hierarchy or activity of plant root–associated families (Bonkowski 2004). It was also stated and reported that predation of some of the different plant pathogenic species has an inverse effect on the plant growth hormone production (Krome et al. 2010) or sometimes they support the beneficial microbes to survive (Jousset et al. 2010; Müller et al. 2013). Protozoans also excrete nitrogen in the form of ammonium and phosphorus as products of their metabolism, and it is because of this reason that the presence of protozoans in soil has been reported to enhance plant growth and development.
Example – Acanthamoeba castellanii grazing has been reported to maintain the bacterial population in the rhizospheric soil by consumption etc.
16.2.1.1.5 Nematodes
Nematodes are microscopic worms which live around or inside the plant and periodically rely and feed over bacteria, fungus, and other soil microbes. Nematodes can easily carry live microbes over their bodies and also inside their digestive systems, and by this activity wherever they go nematodes deliver microbes over the roots of plant or in soil. Few nematodes are also disease causing, while others feed over disease-causing organisms which can be identified as potential biocontrol agents.
Example – Steinernema, Risbravis, Rhabditis, etc., are the useful nematodes responsible for decomposing the organic matter and managing attack on insects and other pests.
16.3 How Useful Root Microbes Boost Crop Productivity?
Beneficial root microbes present in the rhizospheric soil near plant roots ameliorate plant productivity and its performance in a variety of ways like deterioration of pathogens, providing resistance against any infection, and help in plant growth promotion. The major mode action involves following steps:
16.3.1 Nutrient Availability
Rhizospheric microorganisms always take part in obtaining trace elements which are found in insoluble forms, where microbes turn this into soluble form and make them available to plants. By the use of certain molecules, like siderophore, iron chelation and conversion of complex to simpler form takes place (Aznar and Dellagi 2015). Most of the bacterial community works as key component to unlock the nutrients which are locked in the form of hydrocarbons essential for the plants. Some of the saprotrophs and fungi have been reported as nutrient extractors through solubilization or reabsorption processes, among which actinomycetes play a significant role in decaying organic matter to make it in available form (Aznar and Dellagi 2015).
16.3.2 Plant Growth Promotion
In a different manner we have seen PGPRs playing essential role in plant growth promotion where they produce metabolites which eventually trigger the release of plant hormones reported to play beneficial role for plants. Apart from working as PGPRs, some microbes work as bio-remediators. As a biocontrol trait, microbes effect plant pathogens through the different synthesis like regulation of ethylene level in plant, siderophore activity, acquired systemic resistance, antibiosis, quorum sensing, etc. (Babalola 2010; Olanrewaju et al. 2017). In addition, the beneficial microbes are reported to increase photosynthesis and production of hormones and enzymes as a result of improvement in crop growth. They also control various insects and plant diseases as a consequence improvement in crop quality. The use of such kinds of microorganisms leads to reduction in the usage of chemical fertilizers.
16.4 Root Exudates: Role in Shaping Root Microbiome
In natural environment, plants health status mainly depends on complex and active microbial community present in the rhizospheric soil. In plants, root system is the essential part for nutrient and water conduction, which is inhabited and encircled by a major microbial community called root microbiota or rhizomicrobiome (Del Carmen Orozco-Mosqueda et al. 2018; Hacquard et al. 2015). Complex microbial community present in the root microbiome is referred to as plant’s second genomic part which consists of total rhizosphere community’s interactions present in relation to plant health (Berendsen et al. 2012). Crop growth and yield inside natural environment depends on microbial interactions, that is, bacteria and fungi, actinomycetes, etc. (Schmidt et al. 2016). Attachment of microbial diversities was preferred to be connected in two steps:
16.4.1 Rhizosphere
Rhizosphere as a term was first coined by Lorentz Hiltner (Hiltner 1904) and reconsidered by Pinton as the zone around the plant roots in the soil which is colonized by microbial community (Morgan et al. 2005; Pinton et al. 2007).
Example – Azotobacter, Nitrobacter, Proteobacteria, Rhizobacteria, Actinobacteria, Pseudomonas are some of the ruling populations of bacteria over rhizosphere (Sylvia and Prévost 2005).
16.4.2 Rhizoplane
Region of surface of the plant roots with epidermis and mucilage which is direct contact with the soil and colonized by microbial community.
Example – Burkholderia, Acidobacterium, Dyella, and Edaphobacter are the major genera abundant in the rhizoplane.
The soil–microbe interactions are usually specific and depend upon coevolutionary dilemma (Dobbelaere et al. 2003; Duffy et al. 2004); (Morgan et al. 2005). In the underground world, the specific plant–microbe interactions hold a very important place in various processes governing ecosystem, just like carbon metabolism, sequestration, and nutrient cycling (Singh et al. 2004).
For the export and secretion of molecules into the rhizospheric soil, plants use a hierarchical transport technique where plant roots along with root hairs and adventitious part release root exudates either by passive or active diffusion/secretion mechanism (Badri et al. 2009; Weston et al. 2012).
Root exudates are usually referred to as a group of chemical molecules in rhizosphere which are secreted by plant root systems. They are a mixture of complex substances like sugars, organic acids, enzymes, amino acids, etc., which act as major source of organic carbon specifically obtained from rhizospheric soil (Hütsch et al. 2002; Nguyen 2003). Usually quality and quantity of root exudates depends upon plant species and is variable in different plants, individual plant’s age, and some external factors like biotic and abiotic stresses. Knudson (1920) and Lyon and Wilson (1921) were the first who had provided indication regarding root exudation and microbe abundance in rhizosphere of the plants. Some of the important exudates usually found in the rhizosphere have been mentioned in Table 16.1.
16.5 Requirement of Root Exudates in Plant–Microbe Interactions
Phytochemicals secreted by plant roots mediate certain number of interactions like
-
Plant–plant interaction
-
Plant–microbe interaction
-
Microbe–microbe interaction
Microorganisms live in the rhizospheric soil where they interact with roots and their components to enhance the plant health (Berendsen et al. 2012; Panke-Buisse et al. 2015). The interaction might be neutral in some ways and either advantageous or harmful in others (Mercado-Blanco and Bakker 2007; Raaijmakers et al. 2009). Most probably, depending on the environment, microbes also turn the table from pathogenesis to symbiotic association (Newton et al. 2010). In different examples, Rhizobia includes Bradyrhizobium, Azorhizobium, symbiotic nitrogen, and nitrogen-fixing bacteria like Sinorhizobium and Mesorhizobium (Davidson and Robson 1986; Zahran 1999). In nitrogen-limiting conditions, attraction and intimation of legume–rhizobia symbiosis result in secretion of flavones and flavonols by legumes (Coronado et al. 1995; Zhang et al. 2009). In the same way equal exchange of plant nutrients benefit both the partners like the mycorrhizal associations which is a common association found in alomost 80 percent of the plant species (Kiers et al. 2011).
16.6 Effect of Microbe–Microbe Interactions on the Soil Microbial Communities
For plants, rhizospheric zone is a kind of nutrient-rich site where the competition for food among microbes always takes place. Secondary metabolites produced by microbes are released in the environment to overcome other competitors which fight to occupy similar zone for establishing firmly itself outside or within the roots (Thomashow and Weller 1988; van Loon and Bakker 2005; Pierson and Pierson 2010; Kim et al. 2011). The metabolites released in environment consist of siderophore, lytic enzymes, toxic elements, and antibiotics (Bais et al. 2006). Some rhizospheric microbes hold a variety of genes for the production of siderophores and other antibiotics like Bacillus amyloliquefaciens (Chen et al. 2007) and few species of Pseudomonas (Paulsen et al. 2005). Antibiotics like 2,4-diacetylphloroglucinol (DAPG) and oomycin are also products of microbes (van Loon and Bakker 2005). The referred antibiotics play a significant role in restraining the pathogenic microbes (Aminov 2009; Pierson and Pierson 2010; Thomashow and Weller 1988; Kim et al. 2011).
Besides antibiotics, plant secondary metabolites also work toward altering signaling pathway and metabolic activity of plants (Přikryl et al. 1985; Brazelton et al. 2008; Costacurta and Vanderleyden 1995; Kim et al. 2011). These kinds of microbial attributes sometime change the root exudates’ composition, leading to the selective enhancement of any particular microbial partner in the rhizosphere (Přikryl et al. 1985; Bulgarelli et al. 2013). The whole scenario of communication between two bacterial communities results in release of signaling molecules which are relatively recognized by other communities via inter- and intra-species communication (An et al. 2014). In bacteria this scenario comprises of biofilm formation, motility, and cell adhesion (Sperandio et al. 2002; Chu et al. 2011); production of the virulence-associated factors; and cell proliferation. This kind of density-dependent stimulus and exchange of signals is referred to as quorum sensing (Fuqua et al. 1994; Miller and Bassler 2001; Atkinson and Williams 2009; An et al. 2014) (Yajima 2014).
In fungi, two important molecules namely farnesol and tyrosol have been reported for regulating quorum sensing–controlled traits like biofilm formation, resistance to drugs, and morphogenesis (Chen et al. 2007; Enjalbert and Whiteway 2005; Albuquerque and Casadevall 2012). Likewise, tryptophol has been reported to control morphogenetic behavior in Saccharomyces cerevisiae through both density-dependent approach as well via nutritional trigger (Chen and Fink 2006).
16.7 Coevolutionary Relationship of Root Exudates with the Rhizosphere
Microbial communities present in the soil are involved in multilevel intercommunication which are known to influence vital environmental activities, like biogeochemical cycling of nutrients, soil quality, and plant well-being (Barea et al. 2005; Giri 2005).
The age of the plants, crop species, and types of soil determine the variation in microbial communities present in the rhizospheric soil (Wieland et al. 2001; Buyer et al. 2002); (Kowalchuk et al. 2002). In some recent evidences it was observed that specific plant species cultivate their own soil fungal community and diversity composition, and this “culture” is mediated by root exudates (Broeckling et al. 2008).
Example – In native soil, when Arabidopsis thaliana and Medicago truncatula were grown at different places, it was observed that Arabidopsis and Medicago maintained its own fungal community in their resident soil. When the plants were grown in other soil different from the native soil that did not promote Arabidopsis or Medicago plants, the microbial communities in those soils decreased considerably. Similarly, when root exudates were added to the soil, the same response was observed, thus showing that plants secrete root exudates to drive these responses and this interaction has a coevolutionary component.
16.8 Bioactive Metabolites
Plants play a variety of roles either in metabolism or metabolites, which are required for the sustainability of plant system. These plant metabolites could be made up of proteins, lipids, carbohydrates, or nucleic acids which are then known as primary metabolites. Metabolites are primarily known as helping hand for plant system which directly intervenes in the growth and development (Ballhorn et al. 2009). The metabolites produced by plants have been broadly categorized into two groups namely:
16.8.1 Primary Metabolites
Primary metabolites are certain compounds which directly benefitted the plants for their overall growth. They have been classified as carbohydrates, lipids, proteins, etc., which are likely used by the plants directly for different works (Schafer and Wink 2009).
16.8.2 Secondary Metabolites
Plant secondary metabolites are those compounds which do not having any direct role in plant metabolism and are often useful in respect to defense-related properties. They are usually low molecular weight around 3000 dalton (Osbourn et al. 2003). The production and secretion of secondary metabolite varies from species to species and somehow difference between natural products and secondary metabolites is hard to define (Vasconsuelo and Boland 2007).
In so many different ways, secondary metabolites are involved in upregulation of primary metabolism and act as triggers for signaling any known process. Secondary metabolites often maintain the balance of plant molecules with the environment either via adaptation mechanism or by making a complementary framework to intricate fine balance (Osbourn et al. 2003; Berni et al. 2018; Grayson 1998).
16.9 Principal Groups of Secondary Metabolites
Plant secondary metabolites have been majorly categorized into four major classes (Goldberg 2003). These four categories include terpenoids, nitrogen-containing compounds, phenolics, and sulfur-containing compounds (GSH, defensins, and lectins) (Mazid et al. 2011).
16.9.1 Terpenes
Terpenoids are the on the whole most varied class of plant secondary metabolites as they have approximately 40,000 dissimilar compounds, and thus they stand out as the biggest class of important plant metabolites (Bohlmann and Keeling 2008).
16.9.2 Phenolics
Phenolics are molecules that have an aromatic ring bound with one or more hydroxyl groups (Nicholson and Hammerschmidt 1992). By the chemical formula and its structure, it differs from simple phenols like catechol to catechol melanins through a long chain polymer. Phenolic compounds are reported to guard plants from different herbivores and pathogens. Apart from protecting plants from above-mentioned stressors, phenolics also protect plants from UV radiation, heat shock, and frost situation (Parr and Bolwell 2000).
16.9.3 Alkaloids
Alkaloids are amino acids–derived nitrogen-containing compounds just like tyrosine and tryptophan. They also present in huge amount but take 20% of total metabolites (Hegnauer 1988). Alkaloids occupy a major share in drug industry and are being mainly used as narcotics or in pharmaceuticals (Hesse 2002; Yao et al. 2004). The most common alkaloids derived from plant sources are vincristine and vinblastine, morphine, and codeine (Crozier et al. 2006).
16.9.4 Sulfur-Containing Secondary Metabolites
Sulfur-containing metabolites are derived from two different ways; one group is formed from hydrolyzation of glucosinolates by myrosinase enzyme. Second group is made up of allin by alliinase enzyme found basically in onion and garlic. Both of these groups are in nature for a purpose which we always face off with and help in guarding plants from the herbivores (Ober et al. 2003).
16.10 Role of Rhizospheric Microbiome on Plant Growth Promotion
Microbial communities are well acclaimed for playing a crucial part in the overall development and growth of plants by manipulating diverse physiological processes. The shaping of rhizospheric microbiome is a mutual process which is largely influenced by the rhizodeposits (Sharma and Chauhan 2017). Recently, people have started focusing on studying the microbiome associated with host plants in order to expand sustainable farming customs via the utilization of microbial biopesticides and biofertilizers. Within a given set of soil type, the indigenous plants restructure and reframe the native rhizospheric microbial community by applying a selective pressure. It is exhaustively reported in literature that within a given set of soil type, the indigenous plants put forth a selective pressure on this immense biodiversity pool, thereby reshaping the rhizospheric microbial community structure.
Manipulation of bacterial microbiome has attracted more attention of researchers in recent times than the other groups of organisms, as it has helped the scientists in altering numerous plant beneficial activities, namely enhancement in growth and yield, as well as suppression of phytopathogens with final effect on the usage of chemical fertilizers which is considerably reduced (Adesemoye and Kloepper 2009). Microorganisms living belowground are known to affect composition and total yield of natural plant communities directly and indirectly (Van Der Heijden et al. 2008; Turner et al. 2013). It is because of this reason that the soil microbial richness has been directly linked with the diversity and productivity aboveground plant (Lau and Lennon 2011; Wagg et al. 2011).
16.11 Role of Rhizospheric Microbiome on Plant Secondary Metabolite Status
The interconnection between plants and their microbial communities is active practice in which plants interact to their surrounding environment and accordingly respond to the changes (Chaparro et al. 2012). Microbes play important role in agriculture in order to maintain environmental equilibrium (Fig. 16.2). Both the shoot and root systems of plant are directly or indirectly contact with diverse group of microorganisms. Due to the presence of infinite number of microbes, various mechanisms occur around the plant root, and one of them is secretion by root exudate. The root exudation comprises the secretion of carbon-containing compounds that are primary and secondary metabolites products and many more molecules (Uren 2000).
Elicitors are chemical compounds for stress factors which when applied in minute quantity to a living being enhances the biosynthesis of metabolites, mainly secondary metabolites (Radman et al. 2003). In context to the plant system, elicitors play vital role in defense process against pathogens and environmental stress. The biotic elicitors include bacteria, fungi, and viruses whereas abiotic elicitors involve metal, ions, and inorganic molecules. Thus, PGPR can produce elicitors which in turn will originate the synthesis of secondary metabolites (Sekar and Kandavel 2010) [Table 16.2]. The herbaceous plant Catharanthus roseus, which is commonly called rose periwinkle, belonging to family Apocynaceae releases bioactive compound ajmalicine under drought stress (Jaleel et al. 2009). Likewise, in another study Pseudomonas fluorescens, a plant growth–promoting rhizobacteria was reported to increase the production of ajmalicine under drought stress. This bacterium also increased plant biomass and helped in protecting the plants against stress condition. C. roseus is also reported to secrete some metabolites like serpentine, catharanthine, tabersonine, and vindoline but among all of them ajmalicine content was found to be maximally increased (Jaleel et al. 2009).
The perennial plant Crocus sativus, commonly called saffron crocus, secretes crocetin, picrocrocin, and safranal compounds. In a study it was found that the contents were increased when plants were inoculated with Bacillus subtilis FZB24 (Sharaf-Eldin et al. 2008). Among all the compounds, crocetin was found to be increased maximally. Trichoderma belonging to fungal genera is usually present in almost all soil types (Hermosa et al. 2012). It has property to kill other harmful bacteria and fungi that act as biocontrol agent for the plant (Druzhinina et al. 2011). Trichoderma acts as a biotic elicitor for oleanolic acid which is secreted by Calendula officinalis plant. Oleanolic acid amount is intensified by application of Trichoderma viride (Wiktorowska et al. 2010).
Scopolia parviflora is a flowering plant belonging to family Solanaceae, which produces scopolamine compound whose concentration was found to be increased along with the amount of tropane alkaloids by different microbes such as Bacillus cereus and Pseudomonas aeruginosa (Jung et al. 2003). Tropane alkaloids concentration is high in roots as compared to stem and leaves. Tropane has cyclic amine group which has piperidine and pyrrolidine ring with single nitrogen atom and two carbon atoms (Hanuš et al. 2005). They are used as anesthetics, bronchodilators, and mydriatics (Grynkiewicz and Gadzikowska 2008).
Apart from PGPRs, endophytes are those bacterial or fungal microbes that live their entire life with living cells of plant without causing any disease to the host (Wilson 1995; Sturz et al. 2000). Nowadays endophytes have been considered as an important source for secondary metabolites which include phenols, alkaloids, and terpenoids products. For example, hypericin is a bioactive compound which was isolated from Hypericum perforatum and whose production was increased upon inoculation of Thielavia subthermophila (Kusari et al. 2008, 2009).
Plumbago rosea L., commonly called Indian leadwort, is classified under angiosperms. It is used for medicinal purposes like in curing of certain kinds of chronic diseases, skin diseases, and used as an anticancer plant (Parimala and Sachdanandam 1993). It releases useful metabolite compound plumbagin from its root and Aspergillus niger, Rhizopus oryzae, Bacillus subtilis, and Pseudomonas aeruginosa have been reported to be its elicitor. Among the above-mentioned genera, fungal elicitors enhanced the content of plumbagin, whereas bacteria elicitors were not so effective (Komaraiah et al. 2002) The maize crop (Zea mays) discharges a compound named benzoxazinoid whose amount changed by rhizobacterium Pseudomonas putida KT2440, which protects the plant from pathogenic microorganism (Neal et al. 2012). These compounds function naturally toward the protection of plants. In cell culture roots of Taverniera cuneifolia (shrub), glycyrrhizic acid content was intensified when treated with bacteria Rhizobium leguminosarum as compared to the control roots. Other bacterial origin elicitors observed in Taverniera cuneifolia are B. aminovorans, B. cereus, and Agrobacterium rhizogenes which were also found to increase the amount of glycyrrhizic acid. But when it is treated with Agrobacterium tumefaciens, no significant increase in glycyrrhizic acid was found. In another plant, namely Hypericum perforatum compound hypericin and pseudohypericin is released, whose concentration is reported to be increased by Rhizobacterium (Mañero et al. 2012).
Alfalfa (Medicago sativa) belonging to family Fabaceae is a medicinal plant, which is a rich source of vitamins A, B, and C (Rashmi and Sarkar 1997). Luteolin is a bioactive compound released by alfalfa plant whose production is enhanced by plant growth rhizobacteria Rhizobium meliloti (Peters et al. 1986). Likewise, in Datura metel, Bacillus cereus and Staphylococcus aureus were found to increase the content of atropine, a compound largely used for relieving pain (Shakeran et al. 2015).
16.12 Conclusion and Future Prospects
Owing to the presence of diverse variety and multidimensional role of secondary metabolites, we can assume that these organic compounds are of immense importance for the growth, development, defense, and survival of plants. Plants preferably produce these compounds when they encounter herbivores or pathogen attacks. In totality, these compounds are also produced when plants face challenges like abiotic stresses, that is, salinity, drought, UV radiations, heavy metals, and harsh climate. In addition to the above, the biotic elicitors, namely rhizospheric microbes many times positively change the status of plant secondary metabolites production. Additionally, being relatively an unexplored area, the rhizospheric microbiome offers a huge potential for not only manipulating the plant growth but also the secondary metabolite status of plants too.
Therefore, though significance of the microbiome present in the rhizosphere has been identified way back, but still tremendous efforts needs to be put in to explore the potential of organisms which might have good properties for our plants and surrounding environment. Pairing traditional techniques with high-end, next-generation sequencing techniques for identifying cues, exudates and other molecules will really help in understanding the complex underground communication existing between plants and microbes.
References
Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12
Albuquerque P, Casadevall A (2012) Quorum sensing in fungi–a review. Med Mycol 50:337–345
Ali GS, Norman D, El-Sayed AS (2015) Soluble and volatile metabolites of plant growth-promoting rhizobacteria (PGPRs): role and practical applications in inhibiting pathogens and activating induced systemic resistance (ISR). In: Advances in botanical research, vol 75. Academic Press, pp 241–284
Aminov RI (2009) The role of antibiotics and antibiotic resistance in nature. Environ Microbiol 11:2970–2988
An JH, Goo E, Kim H, Seo YS, Hwang I (2014) Bacterial quorum sensing and metabolic slowing in a cooperative population. Proc Natl Acad Sci 111:14912–14917
Atkinson S, Williams P (2009) Quorum sensing and social networking in the microbial world. J R Soc Interface 6:959–978
Awad V, Kuvalekar A, Harsulkar A (2014) Microbial elicitation in root cultures of Taverniera cuneifolia (Roth) Arn. for elevated glycyrrhizic acid production. Ind Crop Prod 54:13–16
Aznar A, Dellagi A (2015) New insights into the role of siderophores as triggers of plant immunity: what can we learn from animals. J Exp Bot 66:3001–3010
Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570
Badri DV, Weir TL, Van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant–microbe interactions. Curr Opin Biotechnol 20:642–650
Bais HP, Walker TS, Schweizer HP, Vivanco JM (2002) Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiol Biochem 40:983–995
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266
Ballhorn DJ, Kautz S, Heil M, Hegeman AD (2009) Cyanogenesis of wild lima bean (Phaseolus lunatus L.) is an efficient direct defence in nature. Plant Signal Behav 4:735–745
Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778
Bassam BJ, Djordjevic MA, Redmond JW, Batley M, Rolfe BG (1988) Identification of a nodD-dependent locus in the Rhizobium strain NGR234 activated by phenolic factors secreted by soybeans and other legumes. Mol Plant-Microbe Interact 1:161–168
Berendsen RL, Pieterse CM, Bakker PA (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Berni R, Cantini C, Romi M, Hausman JF, Guerriero G, Cai G (2018) Agrobiotechnology goes wild: Ancient local varieties as sources of bioactives. Int J Mol Sci 19:2248
Biswas JC, Ladha JK, Dazzo FB, Yanni YG, Rolfe BG (2000) Rhizobial inoculation influences seedling vigor and yield of rice. Agron J 92:880–886
Bohlmann J, Keeling CI (2008) Terpenoid biomaterials. Plant J 54:656–669
Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631
Bonkowski M, Villenave C, Griffiths B (2009) Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 321:213–233
Brazelton JN, Pfeufer EE, Sweat TA, Gardener BBM, Coenen C (2008) 2, 4-Diacetylphloroglucinol alters plant root development. Mol Plant-Microbe Interact 21:1349–1358
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744
Brooks CJ, Watson DG, Freer IM (1986) Elicitation of capsidiol accumulation in suspended callus cultures of Capsicum annuum. Phytochemistry 25:1089–1092
Bulgarelli D, Schlaeppi K, Spaepen S, Van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838
Buyer JS, Roberts DP, Russek-Cohen E (2002) Soil and plant effects on microbial community structure. Can J Microbiol 48:955–964
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499
Chen H, Fink GR (2006) Feedback control of morphogenesis in fungi by aromatic alcohols. Genes Dev 20:1150–1161
Chen XH, Koumoutsi A, Scholz R, Eisenreich A, Schneider K, Heinemeyer I, Junge H (2007) Comparative analysis of the complete genome sequence of the plant growth–promoting bacterium Bacillus amyloliquefaciens FZB42. Nat Biotechnol 25:1007
Chodisetti B, Rao K, Gandi S, Giri A (2013) Improved gymnemic acid production in the suspension cultures of Gymnema sylvestre through biotic elicitation. Plant Biotechnol Rep 7:519–525
Chu W, Jiang Y, Yongwang L, Zhu W. (2011) Role of the quorum-sensing system in biofilm formation and virulence of Aeromonas hydrophila. Afr J Microbiol Res 5: 5819–5825
Coronado C, Zuanazzi JS, Sallaud C, Quirion JC, Esnault R, Husson HP, Ratet P (1995) Alfalfa root flavonoid production is nitrogen regulated. Plant Physiol 108:533–542
Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18
Crozier A, Jaganath IB, Clifford MN (2006) In: Crozier A, Clifford MN, Ashihara H (eds) Plant secondary metabolites: occurrence, structure and role in the human diet. Blackwell Publishing Limited. ISBN-13: 978-1-4051-2509-3
Davidson IA, Robson MJ (1986) Effect of contrasting patterns of nitrate application on the nitrate uptake, N2-fixation, nodulation and growth of white clover. Ann Bot 57:331–338
Del Carmen Orozco-Mosqueda M, del Carmen Rocha-Granados M, Glick BR, Santoyo G (2018) Microbiome engineering to improve biocontrol and plant growth-promoting mechanisms. Microbiol Res 208:25–31
Di Benedetto NA, Corbo MR, Campaniello D, Cataldi MP, Bevilacqua A, Sinigaglia M, Flagella Z. (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat, 3: 413–434
Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149
Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Kubicek CP (2011) Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 9:749
Duffy B, Keel C, Défago G (2004) Potential role of pathogen signaling in multitrophic plant-microbe interactions involved in disease protection. Appl Environ Microbiol 70:1836–1842
Engelberth J, Koch T, Schüler G, Bachmann N, Rechtenbach J, Boland W (2001) Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol 125:369–377
Enjalbert B, Whiteway M (2005) Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryot Cell 4:1203–1210
Etalo DW, Jeon JS, Raaijmakers JM (2018) Modulation of plant chemistry by beneficial root microbiota. Nat Prod Rep 35:398–409
Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume-rhizobia interactions. J Chem Ecol 40:770–790
Firmin JL, Wilson KE, Rossen L, Johnston AWB (1986) Flavonoid activation of nodulation genes in Rhizobium reversed by other compounds present in plants. Nature 324:90
Fitzpatrick CR, Copeland J et al (2018) Assembly and ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci 115:E1157–E1165
Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269
Ghorbanpour M, Hosseini NM, Rezazadeh S, Omidi M, Khavazi K, Etminn A (2010) Hyoscyamine and scopolamine production of black henbane (Hyoscyamus niger) infected with Pseudomonas putida and Pseudomonas. fluorescens strains under water deficit stress. Planta Med 76:P167
Giri BF (2005) In: Varma A (ed) Microorganisms in soils: roles in genesis and functions (pp. 139–153). Springer, Germany
Goldberg G (2003) Plants: diet and health. The report of a British nutrition foundation task force, vol 347. Blackwell Publishing Limited, Oxford, U.K.
Gopalakrishnan S, Vadlamudi S, Bandikinda P, Sathya A, Vijayabharathi R, Rupela O, Varshney RK (2014) Evaluation of Streptomyces strains isolated from herbal vermicompost for their plant growth-promotion traits in rice. Microbiol Res 169:40–48
Gopalakrishnan S, Srinivas V, Alekhya G, Prakash B, Kudapa H, Varshney RK (2015) Evaluation of Streptomyces sp. obtained from herbal vermicompost for broad spectrum of plant growth-promoting activities in chickpea. Org Agric 5:123–133
Grayson DH. (1998) Monoterpenoids. Natl Prod Rep. 5:497–521
Grynkiewicz G, Gadzikowska M (2008) Tropane alkaloids as medicinally useful natural products and their synthetic derivatives as new drugs. Pharmacol Rep 60:439
Hacquard S, Garrido-Oter R, González A, Spaepen S, Ackermann G, Lebeis S, Schulze-Lefert P (2015) Microbiota and host nutrition across plant and animal kingdoms. Cell Host Microbe 17:603–616
Hanuš LO, Řezanka T, Spížek J, Dembitsky VM (2005) Substances isolated from Mandragora species. Phytochemistry 66:2408–2417
Hartwig UA, Maxwell CA, Joseph CM, Phillips DA (1990) Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol 92:116–122
Hegnauer R (1988) Biochemistry, distribution and taxonomic relevance of higher plant alkaloids. Phytochemistry 27:2423–2427
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25
Hesse M (2002) Alkaloids: Nature’s Curse or Blessing? Wiley- VCH, New York
Hiltner LT (1904) Uber nevere Erfahrungen und Probleme auf dem Gebiet der Boden Bakteriologie und unter besonderer Beurchsichtigung der Grundungung und Broche. Arbeit Deut Landw Ges Berlin 98:59–78
Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407
Jaleel CA, Gopi R, Gomathinayagam M, Panneerselvam R (2009) Traditional and non-traditional plant growth regulators alters phytochemical constituents in Catharanthus roseus. Process Biochem 44:205–209
Jousset A, Rochat L, Scheu S, Bonkowski M, Keel C (2010) Predator-prey chemical warfare determines the expression of biocontrol genes by rhizosphere-associated Pseudomonas fluorescens. Appl Environ Microbiol 76:5263–5268
Jung HY, Kang SM, Kang YM, Kang MJ, Yun DJ, Bahk JD, Choi MS (2003) Enhanced production of scopolamine by bacterial elicitors in adventitious hairy root cultures of Scopolia parviflora. Enzyme Microb Tech 33:987–990
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Palmer TM (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882
Kim YC, Leveau J, Gardener BBM, Pierson EA, Pierson LS, Ryu CM (2011) The multifactorial basis for plant health promotion by plant-associated bacteria. Appl Environ Microbiol 77:1548–1555
Kloepper JW, Schroth MN (1987) Plant growth-promoting rhizobacteria on radishes. Proc 4th Int Conf Plant Path Bact Angers:879–882
Knudson L (1920) The secretion of invertase by plant roots. Am J Bot 7:371–379
Komaraiah P, Amrutha RN, Kishor PK, Ramakrishna SV (2002) Elicitor enhanced production of plumbagin in suspension cultures of Plumbagorosea L. Enzyme MicrobTechnol 31:634–639
Kosslak RM, Bookland R, Barkei J, Paaren HE, Appelbaum ER (1987) Induction of Bradyrhizobium japonicum common nod genes by isoflavones isolated from Glycine max. Proc Natl Acad Sci 84:7428–7432
Kowalchuk GA, Buma DS, de Boer W, Klinkhamer PG, van Veen JA (2002) Effects of above-ground plant species composition and diversity on the diversity of soil-borne microorganisms. Antonie Van Leeuwenhoek 81:509
Krome K, Rosenberg K, Dickler C, Kreuzer K, Ludwig-Müller J, Ullrich-Eberius C, Bonkowski M (2010) Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants. Plant Soil 328:191–201
Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71:159–162
Kusari S, Zühlke S, Kosuth J, Cellarova E, Spiteller M (2009) Light-independent metabolomics of endophytic Thielavia subthermophila provides insight into microbial hypericin biosynthesis. J Nat Prod 72:1825–1835
Lau JA, Lennon JT (2011) Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits. New Phytol 192:215–224
Lugtenberg B, Kamilova F (2009) Plant-Growth-Promoting Rhizobacteria. Annu Rev Microbiol 63:541–556
Lyon TL, Wilson JK (1921) Liberation of organic matter by roots of growing plants, vol 40. Cornell University
Mañero FJG, Algar E, Gómez MS, Sierra MD, Solano BR (2012) Elicitation of secondary metabolism in Hypericum perforatum by rhizosphere bacteria and derived elicitors in seedlings and shoot cultures. Pharm Biol 50:1201–1209
Mazid M, Khan TA, Mohammad F (2011) Role of secondary metabolites in defense mechanisms of plants. Biol Med 3:232–249
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Mercado-Blanco J, Bakker PA (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92:367–389
Messens E, Geelen D, Van Montagu M, Holsters M (1991) 7, 4-Dihydroxyflavanone is the major Azorhizobium nod gene-inducing factor present in Sesbania rostrata seedling exudate. Mol Plant-Microbe Interact 4:262–267
Miller MB, Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199
Ming Q, Su C, Zheng C, Jia M, Zhang Q, Zhang H, Qin L (2013) Elicitors from the endophytic fungus Trichoderma atroviride promote Salvia miltiorrhiza hairy root growth and tanshinone biosynthesis. J Exp Bot 64:5687–5694
Morán-Diez E, Hermosa R, Ambrosino P, Cardoza RE, Gutiérrez S, Lorito M, Monte E (2009) The ThPG1 endopolygalacturonase is required for the Trichoderma harzianum–plant beneficial interaction. Mol Plant-Microbe Interact 22:1021–1103
Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739
Müller MS, Scheu S, Jousset A (2013) Protozoa drive the dynamics of culturable biocontrol bacterial communities. PLoS One 8:e66200
Müller DB, Vogel C, Bai Y, Vorholt JA (2016) The plant microbiota: systems-level insights and perspectives. Annu Rev Genet 50:211–234
Namdeo AG (2004) Investigation on pilot scale bioreactor with reference to the synthesis of bioactive compounds from cell suspension cultures of Catharanthus roseus Linn. Devi Ahilya Vishwavidyalaya, Indore
Namdeo A, Patil S, Fulzele DP (2002) Influence of fungal elicitors on production of ajmalicine by cell cultures of Catharanthus roseus. Biotechnol Prog 18:159–116
Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PLoS One 7:e35498
Newton AC, Fitt BD, Atkins SD, Walters DR, Daniell TJ (2010) Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol 18:365–373
Nguyen C (2003) Rhizodeposition of organic C by plants: Mechanisms and controls. Agronomie 23:375–396
Nicholson RL, Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30:369–389
Ning P, Li S, Li X, Li C (2014) New maize hybrids had larger and deeper post-silking root than old ones. Field Crop Res 166:66–67
Ober D, Harms R, Witte L et al (2003) Molecular evolution by change of function. Alkaloid specific homospermidine synthase retained all properties of deoxyhypusine synthase except binding the eIF5A precursor protein. J Biol Chem 278:12805–12812
Ogawa S, Valencia MO, Ishitani M, Selvaraj MG (2014) Root system architecture variation in response to different NH4+ concentrations and its association with nitrogen-deficient tolerance traits in rice. Acta Physiol Plant 36:2361–2372
Ohno A, Ano T, Shoda M (1995) Production of a lipopeptide antibiotic, surfactin, by recombinant Bacillus subtilis in solid state fermentation. Biotechnol Bioeng 47:209–214
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197
Osbourn AE, Qi X, Townsend B, Qin B (2003) Dissecting plant secondary metabolism- constitutive chemical defences in cereals. New Phytol 159:101–108
Panke-Buisse K, Poole AC, Goodrich JK, Ley RE, Kao-Kniffin J (2015) Selection on soil microbiomes reveals reproducible impacts on plant function. Microb Ecol J 9:980
Parimala R, Sachdanandam P (1993) Effect of Plumbagin on some glucose metabolising enzymes studied in rats in experimental hepatoma. Mol Cell Biochem 125:59–63
Parr AJ, Bolwell GP (2000) Phenols in the plant and in man. The potential for possible nutritional enhancement of the diet by modifying the phenols content or profile. J Sci Food Agric 80:985–1012
Paulsen IT, Press CM, Ravel J, Kobayashi DY, Myers GS, Mavrodi DV, Dodson RJ (2005) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 23:873
Pérez-Montaño F, Alías-Villegas C, Bellogín RA, Del Cerro P, Espuny MR, Jiménez-Guerrero I, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336
Peters NK, Frost JW, Long SR (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977–980
Pierson LS, Pierson EA (2010) Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol 86:1659–1670
Pinton R, Varanini Z, Nannipieri P (2007) The rhizosphere: biochemistry and organic substances at the soil-plant interface. CRC press
Přikryl Z, Vančura V, Wurst M (1985) Auxin formation by rhizosphere bacteria as a factor of root growth. Biol Plant 27:159–163
Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Locco Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361
Radman R, Saez T, Bucke C, Keshavarz T (2003) Elicitation of plants and microbial cell systems. Biotechnol Appl Biochem 37:91–102
Rashmi R, Sarkar MV (1997) Cultivation of alfalfa (Medicago sativa L). Anc Sci Life 17:117
Redmond JW, Batley M, Djordjevic MA, Innes RW, Kuempel PL, Rolfe BG (1986) Flavones induce expression of nodulation genes in Rhizobium. Nature 323:632
Rout ME, Southworth D (2013) The root microbiome influences scales from molecules to ecosystems: the unseen majority1. Am J Bot 100:1689–1691
Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol Res 169:18–29
Schafer H, Wink M (2009) Medicinally important secondary metabolites in recombinant microorganisms or plants: progress in alkaloid biosynthesis. Biotechnol J 4:1684–1703
Schmidt JE, Bowles TM, Gaudin A (2016) Using ancient traits to convert soil health into crop yield: impact of selection on maize root and rhizosphere function. Front Plant Sci 7:373
Sekar S, Kandavel D (2010) Interaction of plant growth promoting rhizobacteria (PGPR) and endophytes with medicinal plants “New Avenues for Phytochemicals”. J Phytol 91:100
Shakeran Z, Keyhanfar M, Asghari G, Ghanadian M (2015) Improvement of atropine production by different biotic and abiotic elicitors in hairy root cultures of Datura metel. Turk J Biol 39:111–118
Sharaf-Eldin M, Elkholy S, Fernández JA, Junge H, Cheetham R, Guardiola J, Weathers P (2008) Bacillus subtilis FZB24® affects flower quantity and quality of saffron (Crocus sativus). Planta Med 74:1316–1320
Sharma R, Chauhan A (2017) Rhizosphere microbiome and its role in plant growth promotion. In: Mining of microbial wealth and metagenomics. Springer, pp 29–56
Simonet P, Normand P, Moiroud A, Bardin R (1990) Identification of Frankia strains in nodules by hybridization of polymerase chain reaction products with strain-specific oligonucleotide probes. Arch Microbiol 153:235–240
Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere–microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393
Soyano T, Hirakawa H, Sato S, Hayashi M, Kawaguchi M (2014) Nodule inception creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production. Proc Natl Acad Sci 111:14607–14612
Sperandio V, Torres AG, Kaper JB (2002) Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43:809–821
Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30
Sylvia AH, Prévost D (2005) Ecology of plant growth promoting rhizobacteria. In: PGPR: Biocontrol and Biofertilization. Springer, Dordrecht, pp 1–38
Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170:3499–3508
Tringe SG, Von Mering C, Kobayashi A, Salamov AA, Chen K, Chang HW, Bork P (2005) Comparative metagenomics of microbial communities. Science 308:554–557
Turner TR, James EK et al (2013) The plant microbiome. Genome Biol 14:209
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, Inoue H (2013) Control of root system architecture by deeper rooting 1 increases rice yield under drought conditions. Nat Genet 45:1097
Uren NC (2000) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In: The Rhizosphere. CRC Press, pp 35–56
Van Der Heijden MG, Bardgett RD et al (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310
Van Loon LC, Bakker PAHM (2005) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: PGPR: Biocontrol and Biofertilization. Springer, Dordrecht, pp 39–66
Vasconsuelo A, Boland R (2007) Molecular aspects of the early stages of elicitation of secondary metabolites in plants. Plant Sci 172:861–875
Wagg C, Jansa J et al (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009
Weston LA, Ryan PR, Watt M (2012) Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere. J Exp Bot 63:3445–3454
Wieland G, Neumann R, Backhaus H (2001) Variation of microbial communities in soil, rhizosphere, and rhizoplane in response to crop species, soil type, and crop development. Appl Environ Microbiol 67:5849–5854
Wiktorowska E, Długosz M, Janiszowska W (2010) Significant enhancement of oleanolic acid accumulation by biotic elicitors in cell suspension cultures of Calendula officinalis L. Enzym Microb Technol 46:14–20
Wilson D (1995) Endophyte: the evolution of a term, and clarification of its use and definition. Oikos:274–276
Yajima A (2014) Recent progress in the chemistry and chemical biology of microbial signaling molecules: quorum-sensing pheromones and microbial hormones. Tetrahedron Lett 55:2773–2780
Yao LH, Jiang YM, Shi J, Tomás-Barberán FA, Datta N, Singanusong R et al (2004) Flavonoids in food and their health benefits. Plant Foods Hum Nutr 59:113–122
Yu K, Pieterse CM et al. (2019) Beneficial microbes going underground of root immunity. Plant Cell Environ 42:2860–2870
Zaat SA, Schripsema J, Wijffelman CA, Van Brussel AA, Lugtenberg BJ (1989) Analysis of the major inducers of the Rhizobium nod A promoter from Vicia sativa root exudate and their activity with different nodD genes. Plant Mol Biol 13:175–188
Zahir ZA, Abbas SA, Khalid M, Arshad M (2000) Substrate dependent microbially derived plant hormones for improving growth of maize seedlings. Pak J Biol Sci 3:289–291
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Zhang J, Subramanian S, Stacey G, Yu O (2009) Flavones and flavonols play distinct critical roles during nodulation of Medicago truncatula by Sinorhizobium meliloti. Plant J 57:171–183
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Singapore Pte Ltd.
About this chapter
Cite this chapter
Singh, A., Chaubey, R., Srivastava, S., Kushwaha, S., Pandey, R. (2021). Beneficial Root Microbiota: Transmogrifiers of Secondary Metabolism in Plants. In: Singh, K.P., Jahagirdar, S., Sarma, B.K. (eds) Emerging Trends in Plant Pathology . Springer, Singapore. https://doi.org/10.1007/978-981-15-6275-4_16
Download citation
DOI: https://doi.org/10.1007/978-981-15-6275-4_16
Published:
Publisher Name: Springer, Singapore
Print ISBN: 978-981-15-6274-7
Online ISBN: 978-981-15-6275-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)