Symbioses with beneficial microorganisms constitute the universal and ecologically highly effective strategy of adaptation of plants towards nearly all types of environmental challenges. Representatives of many groups of fungi and bacteria participate in plant-microbial symbioses (PMS) wherein they can colonize the plant surfaces, tissues or intra-cellular compartments using two basic adaptive strategies: nutritional and defensive. Construction of niches for hosting the symbiotic microbes involves the complicated developmental programs implemented under the joint control by plant and microbial partners and based on the cross-regulation of their genes.
Legume plants (family Fabaceae) are known to form symbioses with extremely broad range of beneficial soil microorganisms (BSM), representing examples of almost all plant-microbe mutualistic systems. Different groups of beneficial microbes improve host mineral nutrition, acquisition of water, promote the plant development and offer protection from pathogens and pests. For ecology and agriculture, the most important beneficial legume symbioses are arbuscular mycorrhiza (AM) and root nodule (RN) symbiosis. These symbioses demonstrate high level of genetic and metabolic integrity, compared with other interactions of legumes with plant growth-promoting rhizosphere bacteria (PGPR) and/or beneficial endophytic bacteria.
High integrity of AM and RN symbioses implies highly specific mutual recognition of partners, formation of special complex symbiotic compartments and integration of partners’ metabolic pathways. In the symbioses, legume plant plays a role of the organizing center of the system as it performs functions of coordination and regulation of all developmental processes. During last decade, a significant progress has been achieved in revealing the genetic bases of symbioses formation and functioning, so the knowledge of the plant genetic control over symbioses can effectively facilitate breeding new varieties of legumes that are needed for modern sustainable agriculture. In this chapter, we describe the present state of the developmental genetics of legume symbioses and depict the potential to organize the multi-component symbioses to be used for optimizing the broad spectrum of plant adaptive functions and to improve the sustainability of legume crop production.
2. Mechanisms of positive effect of BSM on the environment and health and yield of the legume plant
2.1. Legume-rhizobia Root-Nodule (RN) symbiosis
Leguminous plants are able to grow in the soil/substrate without any combined nitrogen due to the fixation of atmospheric nitrogen by symbiotic nodule bacteria (collectively called rhizobia). In collaboration with rhizobia, legumes make a large contribution to the global nitrogen balance in natural and agricultural ecosystems . Nitrogen fixation occurs within special plant organs, root nodules (in some associations stem nodules are also formed). Development of these organs represents a well-organized process based on the tightly coordinated expression of specialized symbiotic plant and bacterial genes. The legume nodules provide an ecological niche for bacteria, as well as structure for metabolic/signal exchange between the partners and for the control of symbionts by the hosts .
Family Fabaceae contains 17000-19000 species divided between three sub-families (Caesalpinioideae, Mimosoideae and Papilionoideae) and more than 700 genera of world-wide distribution . With a single exception (
By contrast to legumes, their nitrogen-fixing microsymbionts do not constitute a taxonomically coherent group of organisms. The majority of rhizobia belong to the α-proteobacteria assigned into the Rhizobiaceae family solely on the basis of their ability to nodulate the legumes (e.g.
Root-nodule symbiosis is well known as highly specific plant-microbe interaction. According to the early surveys of symbiotic specificity , legumes were suggested to comprise a range of taxonomically restricted cross-inoculation groups within which the free cross inoculation occurs, while the species from different groups do not cross-inoculate. The best studied examples of this classification are represented by four cross-inoculation groups: “
The specificity of legume-rhizobia interactions is expressed just during the pre-infection stage when rhizobia recognize the roots of appropriate host plants and colonize their surfaces. The interaction starts when the root-excreted signals, in particular, flavonoids, activate the rhizobial nodulation genes (
The main enzyme of nitrogen fixation in nodules is a nitrogenase that has a complex structure [18, 19]. Synthesis of nitrogenase (the enzyme catalysing reduction of N2 into NH4+) and other proteins involved in nitrogen fixation is induced in bacterial cells after they differentiate into a specific form called bacteroids. Bacteroids are embedded into a membrane structure named symbiosome, which formation as well as bacteroid differentiation is induced by plant . These symbiosomes are organelle-like units of plant cell responsible for nitrogen fixation [21, 22]. Peri-bacteroid membrane (PBM) that surrounds bacteroids is an active interface of RN symbiosis where exchange of metabolites between symbionts occurs .
A pronounced differentiation is typical for rhizobia-infected plant cells, such as an increase in internal membrane structures participating in the PBM formation and biosynthetic processes. Polyploidization and chromatin decondensation are typical for these cells correlating with an elevated transcription activity . Biochemically plant cell differentiation is expressed as a
Rhizobial cells also undergo differentiation, but its level varies in different legume species. The terminal bacteroid differentiation (when bacteroids increase their size and DNA content and lack the capacity to divide) is specific for legumes belonging to the inverted repeat–lacking clade (IRLC) such as
It was also found that nodules where terminal bacteroid differentiation takes place are more efficient in terms of energy use. Oono and Denison  reported that legume species with terminal bacteroid differentiation (such as peas (
2.2. Arbuscular Mycorrhiza (AM)
Arbuscular mycorrhiza (AM) is formed by at least 80% of contemporary terrestrial plants with fungi of phylum Glomeromycota. The Glomeromycota are unique as the only monophyletic mycorrhizal fungus lineage that has co-evolved with land plants throughout their history. They are obligate biotrophs that colonize plant roots obtaining photosynthates, such as carbohydrates (hexoses), and niches for both their growth and reproduction. The AM is evolved more than 400 million years ago and was considered to play a decisive role in plants achieving a terrestrial existence [32-34]. The AM is supposed to be “the mother of plant root endosymbioses” . Since legumes originated long after AM, about 60 million years ago , it may be assumed that all of them have the potential to produce this type of symbioses.
Specificity of AM symbiosis is relatively low . Symbiosis establishment starts with molecular dialogue between the partners. Plant roots release sesquiterpenes (also known as inducers of parasitic plant seed germination) as well as different phenolic compounds, including flavonoids, which induce fungal hypha growth and branching [40, 41]. Similar to rhizobia, AM-fungi produce signal molecules termed Myc factors (mycorrhization factors) , which can be recognized by the plant. They are a mixture of several lipochitooligosaccarides, the structure of which is close to that of rhizobial Nod factors, but is presumably more universal for different plant-fungus combinations . Both sesquiterpenes and Myc factors are released constitutively and in the absence of physical contact with symbiotic partner .
The AM-fungi penetrate the root to colonize inner cortical cells. Plant plays an active role in fungus hosting inside the root tissues using cellular mechanisms similar to those used during rhizobial invasion, such as nucleus reposition, cytoplasm aggregation, special cytoskeletal tunnel assembly and symbiotic membrane formation (reviewed in: ). A special intracellular compartment of AM providing tight metabolic exchange between the partners is arbuscule, which is highly branched fungal hypha surrounded by membrane of plant origin  similar to symbiosome of RN symbiosis [35, 46].
Inner-root and outer parts of mycelium remain bound with arbuscules and are a single continuum
Phosphorous (P) is one of the mineral nutrients essential for the plant growth (constituting up to 0.2% of the dry weight of the plant cell) and development. It plays the diverse regulatory, structural, and energy transfer roles and consequently is required in significant amounts [48, 49]. The plants can acquire soluble forms of phosphorous directly from soil through the plant specific phosphate transporters (PTs). The dominant available forms in soil (orthophosphate ions, Pi) are very poorly mobile because of the abundance of cations such as Ca2+, Fe3+ and Al3+ . In such environments where inorganic phosphorous is the predominant form in soil, a range of root adaptations, most of them primarily involved in mobilization and assimilation of phosphorous, are described including plant dependence on arbuscular mycorrhizas (see for review: [34, 51]). In most cases there is a preferential uptake
After transporting into hyphae, the major part of Pi is polymerized by polyphosphate kinase into polyphosphates (poly-P), the linear chains of Pi. The granules rich in poly-P together with phosphorous-containing esters are packed into the cylindrical vacuoles which are transported along the hyphae by tubulin fibrils. After reaching the arbuscules, phosphorous compounds are destroyed by phosphatases and the released Pi cross the partners’ interface [56-58]. The arbuscule is the site of phosphate transfer from fungus to plant. It is well documented that plants possess many classes of phosphate transport proteins, including those which are expressed only in AM symbiosis [59-61]. It was discovered that five plant and one fungal PT genes are consistently expressed inside the arbusculated cells . A plant phosphate transporter MtPt4 was shown to be expressed specifically on the peri-arbuscular membrane in
The mycorrhizal Pi uptake pathway is controlled by the plant host. Many results suggest that the plant phosphorous status is a major regulator controlling induction/repression of plant PT genes at both the soil-root interface and the inner-root symbiotic interface [63-65]. It was shown that high phosphorous concentrations counteract the induction of the mycorrhizal Pi transporter genes by phospholipid extracts from mycorrhizal roots containing the mycorrhiza signal lysophosphatidylcholine . The efflux of Pi probably occurs in coordination with its uptake and the fungus, on its side, might exert the control over the amount of Pi delivered to the plant .
Although Pi acquisition receives more attention, the important advances in investigations on nitrogen uptake by AM-fungi have been made in recent years. AM-fungi directly uptake ammonium (NH4+), nitrate and amino acids  with preference to NH4+ . The first step in the nitrogen uptake requires the activity of specific transporters located at the interface between the soil and extraradical mycelium. A fungal transporter gene (
Inorganic nitrogen that was taken up by the extraradical mycelium should then be incorporated into the amino acids and translocated to the intraradical mycelium, mainly as arginine (Arg) since this is the predominant free amino acid in the external hyphae . The glutamine synthetase/glutamate synthase (GS/GOGAT) cycle is possibly responsible for a subsequent NH4+ assimilation in AM extraradical hyphae [70, 71], although the involvement of glutamate dehydrogenase has not been experimentally excluded. Arg similar to Poly-P is stored and is translocated along hyphae in vacuoles and is later released to the plant apoplast .
A mycorrhizal-specific NH4+ transporter
The plants colonized by AM-fungi have been demonstrated to manifest an increased resistance to attack of some pathogenic microorganisms, such as fungi, nematodes, bacteria, phytoplasma, and plant viruses (reviewed in: ) as well as to plant feeding insects [74, 75]. However, it is still unknown whether such increased resistance to pathogens is a consequence of improved plant overall fitness or it is due to the specific defense responses induced by AM-fungi.
Actually, a range of processes occurring as a result of pathogen invasion (plant defense responses) also takes place in mycorrhized root tissues. They include the signal perception, signal transduction and defense-related gene activation [76-80]. The elements of hypersensitive responses have been observed to take place at both compatible and non-compatible combinations of plants with AM-fungi; reactions similar to the “oxidative burst” are typical for AM during fungus penetration into the epidermal cell . In AM, as in other compatible biotrophic interactions, the defense-like response appears to be weak and occurs transitorily during the early phases of colonization, suggesting that the suppression of plant defense responses by the fungal signals may contribute to successful, compatible AM fungal colonization [76, 82]. AM-fungi are known to alter both constitutive and induced defenses in foliar tissues [83-85].
Drought stress is a major agricultural constraint in the semi-arid tropics. In most cases symbiosis with AM-fungi has been shown to increase host plant growth rates during drought stress and plant resistance to drought. Several mechanisms explaining this phenomenon have been proposed: an influence of AM on plant hormone profiles, increasing intensity of gaseous exchange and photosynthesis in leaves, direct water transport via fungal hyphae from soil into the host plant, enhanced water uptake through improved hydraulic conductivity and increasing leaf conductance and photosynthetic activity, nitrate assimilation by fungal hyphae, enhanced activity of plant enzymes involved in defence against oxidative stress, plant osmosis regulation, and changes in cell-wall elasticity (reviewed in: [86-89]).
The AM fungal hyphae grow into the soil matrix and create conditions conducive to the formation of microaggregates and then their packing into macroaggregates due to production copious amounts of the glycoprotein glomalin [90, 91]. Through AM-fungi-mediated effects on soil structure, it seems logical to suggest that AM colonization of a soil might affect its moisture retention properties and, in turn, the behaviour of plants growing in the soil, particularly when it is relatively dry .
AM-fungi were found to play an important role in heavy metal detoxification and the establishment of vegetation in strongly polluted areas (see for review: ). Fungal strains isolated from old zinc wastes also decrease heavy metal uptake by plants growing on metal rich substrates, limiting the risk of increasing the levels of these elements in the food chain . Phytoremediation of metal contaminated areas attracts the increasing interest as a cheaper alternative to chemical methods, more friendly for environment and nondestructive to soil biota. The effectiveness of the bioremediation techniques depends on the appropriate selection of both the plant and the fungal partners. Plants conventionally introduced in contaminated areas disappear relatively soon, while those appearing during natural succession are better adapted to harsh conditions. Much more stable are plants that appear on the wastes spontaneously, but, it takes a long time till they establish and form stable communities. Symbiotic partners selected on the basis of such research are often the best choice for future phytoremediation technologies [93-96]. Introduction of plants from xerothermic grasslands into the soils contaminated with industrial metal rich wastes is supposed to be a new solution for waste revegetation . Further improvements can be obtained by optimization of diverse microbiota including various groups of rhizospheric bacteria and shoot endophytes .
2.3. Associations of roots with Plant Growth-Promoting Rhizobacteria (PGPR)
Plant Growth Promoting Rhizobacteria (PGPR) are the taxonomically diverse group including different bacteria (
Similar to rhizobia,
Many PGPR are able to solubilize sparingly soluble phosphates, usually by releasing chelating organic acids. Phosphate solubilizing bacteria (PSB) have been identified, but their effectiveness in the soil-plant system is unclear. The ability of an inoculated PSB to supply phosphopous to plant may be limited, either because the compounds released by PSB to solubilize phosphate are rapidly degraded or because the solubilized phosphate is re-fixed before it reaches the root surface .
The best studied examples of bacteria providing efficient defense from phytopathogens are:
The best studied mechanism is the competitive exclusion of pathogens often related to their direct suppression by the bacterial antibiotic substances: phenazine-1-carboxamide, 2,4-diacetylphloroglucinol, kanosamine, oligomycin A, oomycin A, pyoluterin, pyrrolnitrin, xanthobaccin, zwittermycin A, volatile dyes (HCN) and cyclic lipopeptides [98, 104, 105].
An important mechanism for the suppression of pathogens by biocontrol microbes may result from competition for iron or other metals, that involves bacterial siderophores which may possess much greater affinities for ferric ions than those for fungal siderophores [104, 105]. The value of siderophores in biocontrol effects under natural conditions is predominantly associated with their ability to induce forms of systemic resistance in plant [98, 106].
Competitive exclusion of pathogens by PGPR is best achieved when the bacteria exhibit high root-colonizing activity. Application of the technique of genetic labeling with Green Fluorescent Protein (GFP) suggested that these bacteria do not regularly colonize the root interiors, and only rarely they can be observed inside the outer root tissues . Most PGPR cells are concentrated on the root surface where the micro-colonies [98, 104] or bio-films are formed . Since the interactions of plants with root-associated bacteria are not specific, the bacteria will colonize the roots of a broad spectrum of hosts. Specificity of the defensive association may be expressed however, at the point when antimicrobial compounds are being synthesized and this does not always correlate with bacteria taxonomy; many strains of
Microscopic observations demonstrated that suppression of fungi may be correlated with bacterial attachment to pathogen hyphae. As a result of this attachment, some PGPR strains commence their biocontrol functions by behaving as hyper-parasites of pathogenic fungi. This suppression may be related to the production of bacterial enzymes which destroy the pathogen cell walls [104, 105, 110, 111].
Sometimes the biocontrol activities of PGPR do not correlate with intensive colonization of host roots and plant protection results from only a small number of bacteria cells. This occurs when PGPR inoculation induces the systemic resistance mechanisms that make the root non-accessible by pathogens. Initially this effect of PGPR was called ISR (Induced Systemic Resistance) and was attributed exclusively to nonpathogenic systems ; SAR (Systemic Acquired Resistance) reactions, by contrast, were considered to be typical for the interactions with plant pathogens. Nevertheless, it was later found that the reactions of both types occur in either pathogen or nonpathogen systems and are distinguished by the nature of their endogenous elicitors (reviewed in: [106, 113]). The conventional SAR reaction is characterized by an accumulation of salicylic acid as signal molecules and pathogenesis-related proteins (PR-proteins), whereas ISR reaction is based on signal transduction pathways regulated by jasmonates and ethylene. The systemic defence responses of both types may be elicited exogenously by PGPR cells attached to the roots or penetrating their outer tissues. Some molecules produced by PGPR (cell wall and cyclic lipopolysaccharides, flagella components, exoenzymes, phytohormones, type III secretion system (TTSS) effectors, siderophores, salicylic acid, and toxins) may be perceived by the plant and elicit a defensive response .
It has been reported that PGPR which produce an enzyme which is involved in the catabolism of 1-aminocyclopropane-1-carboxylate (ACC) – the ACC deaminase, can lower ethylene concentration in a developing or stressed plant, protecting it against the deleterious effects of ethylene induced stress and facilitating the formation of longer roots [114, 115]. This demonstrates that ethylene is negative regulator of plant interaction with PGPR.
Despite relatively low specificity of plant associations with PGPR, plant genotype has been shown to influence their effectiveness (i.e. genetic integration exists between the partners), and a series of genome loci (QTL) was identified controlling its quantitative variation [106, 116, 117]. The most pronounced plant species-specificity has been observed in the manifestation of ISR reactions caused by PGPR [118, 119].
Both highly effective direct promotion of plant growth and biocontrol may be due to an ability of the host to regulate PGPR functions by modulating the composition of root exudates. Root-excreted organic acids, but not sugars, are optimal for support of different types of PGPR [120-122]. Additionally, some plants (including the legumes, pea and alfalfa) regulate their PGPR functions by exudating specialised signals from the roots which mimic the bacterial “quorum sensing” regulators required for root colonization and antifungal activities . These observations suggest that improvement of biocontrol functions in root-PGPR associations may be achieved
2.4. Mutually beneficial associations of plants with endophytic bacteria
Healthy naturally propagated plants grown in the field or in pot cultures are colonized by populations of endophytic bacteria. The spectrum of endophytic bacteria isolated from the roots of various plants covers a wide range of species; representatives of the genera
Some endophytes are seed-borne, but others have mechanisms for colonizing plants that have yet to be elucidated . Although there are occasional poorly substantiated reports of intracellular colonization of bacteria providing a consistent and effective increase in the productivity of crops, it is still considered that the intercellular apoplastic space is the most suitable niche for endophytes . It is suggested that many bacterial ‘endophytes’ may not colonize the living tissues, but occupy protective niches in dead surface tissues or closely adhering soil of rhizosheaths. Consistent entry of endophytes into living root tissues in the field is supposed to require a bacterial capability to hydrolyse the hydrophobic incrustations of the walls of epidermal, hypodermal, endodermal, and other cortical cells .
Plant associations with endophytic bacteria can increase plant growth and promote general development or improve plant resistance to pathogens and other environmental stresses enhancing the host’s ability to acquire nutrients, or by production of plant growth-regulating, allelopathic or antibiotic compounds [127, 129]. Sometimes improved plant resistance can be linked to induced systemic resistance caused by bacterial elicitors coming from the endophyte .
It is necessary to study the natural associations between bacterial endophytes and their hosts for the purposes of employing such systems most productively in sustainable agriculture . Delivery of endophytes to the environment or agricultural fields should be carefully evaluated to avoid introducing plant, animal and human pathogens .
2.5. Synergistic effect of microbes in rhizosphere
Microorganisms in the rhizosphere are under the influence of root exudates and plant as a whole as well as of interspecies interactions with each other. Many fungi including AM-fungi can interact with different bacterial species which frequently attach to fungal mycelium (reviewed in: [103, 132, 133]). For those bacteria known to stimulate mycelial growth of mycorrhizal fungi and/or enhance root mycorrhization the term ‘mycorrhiza-helper-bacteria’ has been proposed [133, 134]. Particularly, the bacteria may encourage growth of AM-fungi at the perisymbiotic stage of development, which precedes the establishment of a direct contact of the microsymbiont with the plant root [103, 135]. On the other hand, AM-fungi directly modify the environment due to mycelial exudation , forming the so-called ‘mycorrhizosphere’ . In addition, the stimulation of root exudation as a result of interactions with AM-fungi leads to qualitative and quantitative changes of the bacterial community in the rhizosphere (reviewed in: [103, 132]).
Synergistic effect between RN and AM symbioses of legumes was described by many authors [95, 138-142]. AM formation is known to promote nodule development and nitrogen fixation by rhizobia, in particular, by means of improvement of mineral (predominantly phosphorous) host plant nutrition (see for review: ). AM-fungi also manifest synergism during interactions with PGPR (both indigenous and introduced), which perform biocontrol, nitrogen fixation, and phosphate mobilization during double and complex inoculation [103, 132]. The synergetic effect of plant inoculation by rhizobia and PGPR (
Thus, the potential of microbial synergism allows us to speak about high prospects of biotechnologies focused on creation multicomponent symbioses (MCS) that increase the fertility and quality of agricultural legume and nonlegume crops. At the same time, the results of experiments with plant symbioses with AM-fungi, rhizobia and PGPR, including multimicrobial systems, show the important role of physiological and genetic adaptation of microorganisms to local environmental conditions [92, 94, 95, 144]. Hence, during the development of such biotechnologies, it is recommended to use a complex of local microbial isolates adapted to particular environmental conditions.
3. Plant genetic control over development and functioning of mutualistic symbioses of legumes
3.1. Legume genes involved in development of RN and AM symbioses
The complex developmental processes which lead to the formation of intercellular and sub-cellular symbiotic compartments in RN and AM symbioses are controlled by both macro- and microsymbiont. Genetic systems of the symbionts are highly integrated, because some genes and gene products of one partner can switch certain genetic programs in another partner, still the development and function of the symbioses is reliant to the greatest extent on the plant. Developmental genetics of RNS is now well described because both plants and nodule bacteria can be subjected to genetic analysis during nitrogen-fixing nodule formation and functioning. There has been less investigation of AM systems. Mainly this is due to the difficulties encountered in culturing AM-fungi, caused by their obligate symbiotic lifestyle and impossibility of using selective media. Additionally, genetic analysis of AM fungi is more complex because of their heterokaryotic nature and lack of sexual process [34, 145].
The plant genes involved in development of RN and AM symbioses may be divided into two groups, according to approach which was used for the gene identification. The first group,
Genes of these groups are suspected to play different roles in the processes which may be referred collectively as “management of microsymbionts” inside plant roots. Specifically, the products of some nodulin genes represent the structural elements of newly constructed temporary compartments developed during symbiosis . The other nodulin genes may play essential roles in modulating the hormonal status of the developing nodules [152, 153]. Resently,
Still, most of nodulins, mycorrhizins and symbiosins seem to play a subordinate role in the regulatory scheme of symbiosis, nevertheless being indispensable for its functionality and stability. In turn, the major, regulatory role in realization of symbiotic programmes is to be assigned to
The large sizes of genomes of crop legumes (e.g. soybean
Genetic analysis in model legumes as well as in crop legumes was started with experimental mutagenesis. Large-scale programs of insertion, chemical and X-rays mutagenesis, performed by different research groups, resulted in generation of numerous symbiotic mutants in
3.2. Common Symbiosis Pathway (CSP)
The data obtained during the last fifteen years allowed reconstruction the symbiotic signaling pathway which starts in RN and AM symbioses with recognition the Nod and Myc factors, respectively, and goes on as the signal transduction inside the root. In legumes Nod and Myc factors are most likely perceived by specific receptor complexes . The receptor for NF is considered to be a heterodimer composed of at least two LysM containing receptor kinases [166-168]. Alike, receptor for Myc factor (which is not known yet) also supposed to be consisted of similar receptor kinases, or even include one or more kinases participating in Nod factor signaling . The system of receptor kinases perceiving signal molecules of microsymbionts seems to be complicated, with some receptor complexes being necessary not only for starting the interactions, but also on later stages, during penetration bacteria into the root cortex through root hair. Moreover, some receptor kinases could non-specifically bind Nod and Myc factors, which results in intensified growth of lateral roots [43, 169]. Probably, the diversity of receptor kinases should complement the variability of soil microorganisms and increase the specificity of interactions with mutually beneficial ones.
After the first step of reception of Nod or Myc factor, the symbiotic signal is being transmitted to the common pathway, named Common Symbiosis Pathway . The first player in this pathway is LRR-receptor kinase, or SymRK (symbiotic receptor kinase), which is required for both RN and AM symbioses development [171, 172]. The ligand for this receptor kinase is not known yet. Interestingly, the activity of this kinase is also required for proper progression of late symbiotic stages, at least for rhizobial infection . SymRK kinase domain has been shown to interact with 3-hydroxy-3-methylglutaryl CoA reductase 1 (HMGR1) from
The symbiosis receptor kinase SymRK acts upstream of the Nod and Myc factor-induced Ca2+ spiking in the perinuclear region of root hairs within a few minutes after NF application . Perinuclear calcium spiking involves the release of calcium from a storage compartment (probably the nuclear envelope) through as-yet-unidentified calcium channels. To date it is known that the potassium-permeable channels might compensate for the resulting charge imbalance and could regulate the calcium channels in plants [179-183]. Also, nucleoporins NUP85 and NUP133 (to date described only in
The calcium spiking is characteristic for both RN and AM symbioses formation . These Ca2+ spikes are supposed to activate a calcium- and calmodulin-dependent protein kinase (CCaMK) that is also required for NF signaling and AM development . This kinase contains an autoinhibition domain, removing of which leads to a spontaneous activation of downstream transcription events and induction of nodule formation in the absence of rhizobia . Thus, CCaMK appears to be a general manager for both symbioses activating different cascades of signaling for N2-fixing symbiosis and AM in response to different Ca2+ spiking, because the next steps of nodulation signaling are independent from those of AM: the mutations in downstream
The calcium-calmodulin-dependent protein kinase (CCaMK) is supposed to be also involved in legume interactions with PGPR and/or endophytic bacteria as it was shown using inoculation of
The CCaMK is known to form a complex with CYCLOPS, a phosphorylation substrate, within the nucleus .
It is supposed that CCaMK with help of CYCLOPS probably phosphorilates the specific transcription factors already present in cell: NSP1 and NSP2, which influence the changes of expression in several genes related to the symbiosis development [192, 193]. The activity of these proteins leads to the transcriptional changes in root tissues, for instance, increasing the level of early nodulins ENOD40, ENOD11, ENOD12, ENOD5, which are known to be the potential regulators of infection thread growth and nodule primordium formation [165, 194, 195). Also, the changes in cytokinin status of plant are detected, followed by up-regulation of genes encoding for RN symbiosis-specific cytokinin receptors [196-198]. Moreover, transcription regulators NIN and ERN are to be induced specifically downstream of the early NF signaling pathway in order to coordinate and regulate the correct temporal and spatial formation of root nodules [199-202].
The presented genes are responsible for the signal cascade which is aimed to induce the nodulin, mycorrhizin and symbiosin genes responsible for building the symbiotic structures and implementing their biochemical functions. It is supposed that the signaling pathway did not appear
3.3. Autoregulation of symbioses formation
Autoregulation of symbiosis development is an important process that takes place after successful mutual partners’ recognition and signal exchange. For RN symbiosis, it is considered that legume host controls the root nodule numbers by sensing the external and internal cues. A major external cue is the soil nitrate, whereas a feedback regulatory system in which earlier formed nodules suppress further nodulation through shoot-root communication is an important internal cue. The latter is known as the autoregulation of nodulation (AON), and is believed to consist of two long-distance signals: a root-derived signal that is generated in infected roots and transmitted to the shoot; and a shoot-derived signal that inhibits nodulation systemically [203, 204]. Therefore, AON represents a strategy through which the host plant can balance the symbiotrophic N nutrition with the energetically more “cheap” combined N nutrition.
Recent findings on autoregulation of nodulation suggest that the root-derived ascending signals to the shoot are short peptides belonging to the CLE peptide family [205, 206]. The leucine-rich repeat receptor-like kinase HAR1 of
Very little is still known about the plant regulation of mycorrhization process. In split-root systems on alfalfa (
3.4. Next stage of development the genetics of symbioses
The next-coming step of development the genetics of symbioses is studying gene networks on intergenomic level, i.e. the coordinated expression of plant and microbe genes. For AM, with use of the new molecular approaches, in particular transcriptomics, a series of AM fungal genes has been identified, having altered expression levels during the AM formation [216-219]. Still it is not well studied at which stages of fungal-plant interaction the complementary partners’ genes are induced or repressed, and so the use of plant mutants impaired at different steps of AM development might be a challenging approach to reveal the pattern of plant and fungal genetic cooperation . The same research aimed at identification of plant-rhizobial gene interactions with the use of plant and microbe mutants is also in progress.
It has been recently observed that
According to these data, genes encoding for enzymes of malate synthesis should be good candidates for markers to be used as selection and breeding aimed at improvement of symbiotic properties in
4. New approaches of application of mutually beneficial plant-microbe systems in sustainable agriculture
4.1. Development of multicomponent inocula containing BSM
An existence of plant genes [148, 150, 222] and their molecular products  common for both AM and RN symbioses led to a conclusion that system of legume symbiotic genes should be considered as a single whole, controlling the development of a tripartite symbiosis (legume plant + AM fungi + rhizobia). This fact along with the demonstration of synergistic activity in beneficial soil microbes (reviewed in: ) and a suggestion that plant genetic systems controling the development of RN and, probably, of some other beneficial plant-microbe associations evolved on the basis of that of AM  have great importance for the application of tripartite or even multi-partite symbiotic systems in low-input sustainable environmentally-friendly agrotechnologies.
The use in sustainable agriculture of inocula based on beneficial soil microbes as described above allows the improvement crop productivity with decreased doses of mineral fertilizers and pesticides (reviewed in: [224, 225]). These days the majority of commercial inocula contain pure cultures of single microorganisms and only occasionally multiple combinations. There are several objections to the use of mono-inoculation. Firstly, endemic microbial communities are stable and the introduced microbe may be allowed to occupy a very small niche in the whole community or even get lost in a first week after introduction. Secondly, genetic material in microbes is very plastic, and consequently strains introduced into natural ecosystems can rapidly lose their beneficial traits. Thirdly, the existence of microbial cooperation in the rhizosphere  as well as in natural synergistic associations of different microbes including those between AM fungi and their endocellular or superficial symbionts [103, 132] question the possibility and expediency of applying mono-inoculants and even use of the term ‘mono-inoculation’ itself. Finally, plants possess relatively stable genomes and this fact contributes significantly to the effectiveness of symbiosis . Therefore, for industrial plant production in sustainable systems we should use plants having highly effective interactions with all kinds of beneficial soil microbes, which can encourage the development of multiple niches hosting microbes and regulating their activity. For this it is necessary to develop new multi-component microbial inocula which increase the content and biodiversity of beneficial soil microbes in agricultural land.
There is experimental evidence of the effectiveness of simultaneous inoculation of legumes with AM fungi and nodule bacteria leading to increased productivity and quality of the yield, e.g. groundnut , pea [139-141, 227], albaida (
There is an example of application of triple inoculum (AM fungi, rhizobia and PGPR) to the legume
It is possible, therefore, to develop effective multi-microbial inoculants, but it is necessary to use local communities of beneficial microbes because this exploits the natural biological and genetical adaptations of the partners to their environment [94, 231].
4.2. Breeding for improving legume symbiotic effectiveness
During development of plant-microbe systems for low-input sustainable ecologically friendly plant cultivation it is necessary to be guided by conclusions of EC experts about global productivity of legumes (http://www.grainlegumes.com/aep/; http://ec.europa.eu/research/biosociety/food_quality/projects/002_en.html) for sustainable agriculture. The use of legumes in agriculture is leading to: improved soil fertility and increased diversity of crops and soil microbial communities; reductions in the use of non-renewable natural resources; decreased negative effects from intensive agrotechnologies on the natural environment due to decreased requirement for mineral fertilizers and pesticides and decreased production of animal protein and associated wastes; local production of pollution-free food and forage; and a more stable income for the agricultural producers. This is why it is necessary to breed legumes which have highly effective interactions with beneficial soil microbes.
For more than twenty five years the authors’ laboratory has specialized in the genetics of plant-microbe interactions using pea (
4.3. Analysis of genetic variability of pea with respect to its effectiveness of interactions with beneficial soil microbes
A high level of genetic variability was demonstrated in analyses of the symbiotic effectiveness under double inoculation with AM fungi and nodule bacteria of 99 land-races and outclassed heritage cultivars of
The most promising highly symbiotically effective pea genotypes previously selected and different commercial pea cultivars created without consideration of symbiotic effectiveness were involved in three-year field trials (Orel district) . Seed productivity and plant dry weight were chosen as the main criteria for the evaluation of symbiosis effectiveness in legume crops. The double (actually multiple, see above comments on the nature of AM fungi) inoculation was shown to increase seed productivity and plant dry weight in most of the pea genotypes studied and sometimes this could exceed the effect of mineral fertilizers. The effectiveness of legume breeding to improve the symbiotic potential of legume cultivars was proven therefore under field conditions and the genotypes to be used in such breeding programmes were identified. The genotype K-8274 (non-commercial) was selected as a standard of symbiotic effectiveness. Additionally, it was demonstrated that highly effective genotypes can be also found among commercial pea cultivars created without consideration for effectiveness of interactions with beneficial soil microbes. Taking into account that most commercial legume cultivars have accidentally lost their abilities for symbiotrophic nutrition without selective pressure during breeding of intensive crops, the latter constitutes a very important finding for plant breeders and gives them the possibility for concurrent generation of cultivars with required pea plant architecture, other agriculturally important traits and high effectiveness of interactions with all types of beneficial soil microbes in a single breeding programme.
4.4. Breeding to improve pea symbiotic effectiveness
In order to cultivate plants with improved symbiotic potential a special breeding nursery was created in the experimental trials ground of ARILGC on land where for the 5 years before nursery establishment mineral fertilizers had not been applied. To reduce the incidence and severity of root pathogens a 6-field crop rotation was used where cultivation of winter wheat was followed by peas. The multi-component preparation BisolbiMix was used for the inoculation of test plants.
Using the breeding nursery as well as a breeding protocol developed from long-term collaboration of ARRIAM with ARILGC the first (in the whole history of legume breeding) pea cultivar “Triumph” having increased potential of interactions with beneficial soil microbes was intentionally created . It arose as a result of crossing a commercial cultivar ‘Classic’ (donor of agriculturally important traits) and the genotype K-8274 (donor of symbiotic effectiveness trait) and subsequent individual selection of genotypes with high productivity and capacity for supporting various beneficial microbes.
The cultivar “Triumph” is of middle stem height, semi-leafless and has stable productivity under different climate conditions, it is comparatively resistant to root rots and pests. Its productivity is not lower than those of the productivity standards for Orel district using the conventional production technologies and 10% greater in comparison with the standard cultivars when inoculated with BisolbiMix. As a result of two-year state trials (2007-2008) the productivity of “Triumph” was shown to be comparable with those of standard regional cultivars enabling recommendation for commercial cultivation in the Central region of Russian Federation (unpublished results). Thus, the innovative concept of the authors’ research team for plant breeding (applicable not only for legumes, but also for non-legumes) is bearing its first fruits.
Intimate associations of beneficial soil microbes with the host plants described above in detail are applicable in sustainable crop production if taken either separately or in combination. Many authors are now recognizing the need for using the multi-microbial plant inoculants and the advantages of using the indigenous plants (or varieties of local breeding) and microbes.
The authors’ team proposes its own concept which offers fundamentally new approaches to plant production. Firstly, it is necessary to consider plant genetic systems controlling interactions with different beneficial soil microbes in unison. Secondly, plants used as a component of this complex plant-microbe system controlling its effectiveness should be bred to improve the effectiveness of interactions with all types of beneficial soil microbes. Increases of plant biomass production due to plant-microbe symbiosis should be used as the main parameter for an evaluation of plant effectiveness in interactions with beneficial soil microbes. The plant production should be done with inoculation composed of multi-component microbial inocula consisting of AM fungi, rhizobia, PGPR and/or beneficial endophytic bacteria. Finally, taking into consideration the importance of legumes for global agriculture, greater emphasis should be placed on plant-microbial systems in the development of low-input agro-biotechnologies enabling wider cultivation of leguminous crops.
Molecular markers are considered to be a convenient tool to facilitate breeding via MAS (marker-assisted selection) approach. But, search for suitable markers that are associated with symbiotic effectiveness trait is rather complicated problem. To our knowledge, there was no direct link between sequences of symbiotic genes and symbiotic effectiveness, and there are only a few examples of successful use of QTL analysis in legumes to trace loci associated with some symbiotic traits in pea  and
Key words and abbreviations
arbuscular mycorrhiza (AM),
beneficial soil microorganisms (BSM),
defense of plants from pathogens,
evolution of symbiosis,
Nod factor (NF),
phosphate transporter (PT),
plant growth promoting rhizobacteria (PGPR),
plant-microbe symbioses (PMS),
root nodule (RN)
root nodule symbiosis (RNS),
root nodule bacteria (rhizobia),
symbiotrophic plant nutrition,
AcknowledgmentsWe thank Dr. Margarita A. Vishnyakova (N.I. Vavilov All-Russia Research Institute of Plant Industry, St-Petersburg, Russian Federation), Dr. Tatiana S. Naumkina (All-Russia Institute of Legumes and Groat Crops, Orel, Russian Federation) and Dr. Vladimir K. Chebotar (“Bisolbi-Inter” Ltd., St-Petersburg, Russian Federation) for the long-term collaboration in the fields of legume breeding and microbial inocula development. We are also grateful to Victoria Semenova (Komarov Botanical Institute, St-Petersburg, Russian Federation) for critical reading the manuscript. This work was supported by the grants of RFBR (10-04-00961, 10-04-01146, 12-04-01867), Grant to support leading Russian science school (HIII–337.2012.4) and Governmental contracts for research with Ministry of Science and Education of Russian Federation (II1304, 16.512.11.2155, #8109).
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