CC BY
44
simbiogenetics
49
© I. A. Tikhonovich,
N. A. Provorov
All-Russia Research Institute for Agricultural Microbiology
' The molecular mechanism of the agronomically important nutritional and defensive plant-microbe symbioses are reviewed. These symbioses are based on the signaling interactions which result in the development of novel tissue/cellular structures and of extended metabolic capacities in the partners which improve greatly the adaptive potential of plants due to an increased tolerance to biotic or abiotic stresses. The molecular, genetic and ecological knowledge on plant-microbe interactions provide a strategy for a sustainable crop production based on substituting the agrochemicals (mineral fertilizers, pesticides) by the microbial inoculants. An improvement of plant-microbe symbioses should involve the coordinated partners’ modifications resulted in complementary combinations of their genotypes.
' Key words: beneficial plant-microbe interactions; symbiotic nitrogen fixation, arbuscular mycorrhiza, nodule bacteria, cyanobacteria, ergot fungi, endophytes, biocontrol of pathogens and phytophagans, sustainable plant production
MOLECULAR STRATEGIES AND AGRONOMIC IMPACTS OF PLANT-MICROBE SYMBIOSES
1. INTRODUCTION
Genetic, molecular and ecological research of the beneficial plant-microbe interactions comprises an exiting and swiftly developing field in modern biology. These interactions may be classified into two categories: nutritional and defensive (Table 1). The first category involves: (1) mycorrhizal symbioses responsible for supplying the plants with soil nutrients; (2) nitrogen-fixing symbioses which are most effective in legumes inoculated with rhizobia. The second category is represented by the broad spectrum of endo- and epiphytic associations in which different bacteria and fungi protect their hosts from pathogens or phytophagans.
2. NITROGEN-FIXING SYMBIOSES
Being the principle sources of fixed carbon in the majority of terrestrial ecosystems, plants usually suffer a deficiency of nitrogen because they are devoid of nitrogenase enzyme required for N2 fixation: distribution of this enzyme (and of nif genes encoding for its synthesis) is restricted to prokaryotes. This is why many plants balance their N/C ratio due to symbioses with different N2-fixing bacteria.
2.1. Legume-rhizobia symbiosis
Being highly diverse (17000-19000 globally distributed species), legumes (Fabaceae) in collaboration with rhizobia make the largest contribution into N balance in natural and agricultural ecosystems (Allen, Allen, 1981). N2 fixation occurs within the root (sometimes, stem) nodules the formation of which represents the sequential process based on the tightly coordinated expression of the specialized plant and bacterial genes.
2.1.1. Development and regulation
The legume-rhizobia interactions vary in the specificity which may be classified into the narrow and broad types (Table 2). The legumes grown in temperate areas (Pisum, Medicago, Lotus, Trifolium) are inoculated by specific groups of a-proteobacteria (Rhizobium, Sinorhizobium species close to pathogenic Agrobacterium). Interactions between the tropical legumes and their microsymbionts are less specific: they involve several distant groups of a-proteobacteria (including Azorhizobium close to Xanthobacter, and Brady-rhizobium close to Rhodopseudomonas) and some p-proteobacteria (Bal-anchadar et al., 2007).
The specificity of interactions is controlled by the lipo-chito-oligosaccha-ride Nod factors (NFs) the synthesis and functions of which will be addressed by a special paper in this volume (Dolgikh et al., 2008). Here we shall point only that NFs responsible for contrast types of symbiotic specificity have different structures in the acyl chains: narrow specificity is related to poly-unsaturated (2—4 double C=C bounds per 16—20 C atoms) while for broad specificity is related to the saturated or mono-unsaturated acyl chains. The signaling processes initiated in plant roots by NFs involve many stages common to plant-pathogen interactions. For example, NFs are recognized by the receptor-like kinases (RLK) containing the LysM domains and afterwards the signal information is transmitted to the internal messengers (Madsen et al., 2003; Radutoiu et al., 2003) including RLK which contain the leucine rich repeats (LRR) being similar to the products of plant R-genes responsible for the resistance to pathogens (Michelmore, Meyers, 1998). The signaling cascade induces the early nodulin (ENOD) genes for some of which the products are
Table 1
The major types of beneficial plant-microbe interactions
Types of symbiosis Beneficial impacts on plants Mechanisms Best studied symbioses
Supply of nitrogen Fixation of atmospheric N2 Nodule bacteria (rhizobia) with legumes; actinomycetes Frankia with some dicots; filamentous cyanobacteria (Nostoc, Ana-baena) with diverse land plants
Nutritional Extraction of N from soils (including mineralization of organic compounds) Ectomycorrhizal (EC) fungi (Basidiomy-cota, Ascomycota) with some angio-sperms and gymnosperms (mainly, trees and shrubs)
Supply of phosphorous Adsorption of soil phosphates and their transfer into plants Arbuscular mycorrhizal (AM) fungi (Glomeromycota) with 80-90 % of plants
Extraction of P from insoluble soil compounds EC and AM fungi, phosphate solubilizing bacteria (Bacillus)
Defensive Suppression of pathogens Competitive exclusion of pathogens (e. g., synthesis of antibiotics), induction of systemic resistance in plants Plant growth promoting rhizobacteria (PGPR), p-endophytes (Phialophora, Gliocladium), mycorrhizal fungi
Suppression of phytophagans Synthesis of toxins Clavicipitacean (ergot) fungi (Ascomycota), gram-positive bacteria (Clavi-bacter)
Table 2
Examples of narrow and broad specificity in the rhizobia-legume interactions
Symbiotic specificity Rhizobia strains Legume hosts (taxonomy is given according to: Allen, Allen, 1981)
Narrow (cross- Rhizobium galegae Legumes representing the same genus: Galega
inoculation groups) Rhizobium leguminosarum bv. trifolii Legumes representing the same genus: Trifolium
Rhizobium leguminosarum bv. viceae Legumes representing the same tribe of subfamily Papilionoi-deae: Vicieae (Pisum, Vicia, Lathurus, Lens)
Sinorhizobium meliloti, S. medicae Legumes representing the same tribe of subfamily Papilionoi-deae: Trifolieae (Medicago, Melilotus, Trigonella)
Broad Bradyrhizobium sp., Mesorhizobium loti (18 strains) 1 Legumes representing different tribes of subfamily Papilionoi-deae: Galegeae (Astragalusglycyphyllus, Caragana arbore-scens), Genisteae (Lupinus densiflorus), Hedysareae (Orni-thopus sativus), Trifolieae (Ononis repens), Loteae (Anthyllis vulneraria, Lotus corniculatus, L. uliginosus)
Bradyrhizobium japonicum (102 strains) 2 Legumes representing different subfamilies of the Fabaceae: Caesalpinioideae: Cassieae (Cassia nictitans); Papilionoideae: Genisteae (Crotalaria sagittalis, Genista tinctoria), Hedysareae (Desmodium paniculatum, Lespedeza hirta, L. frutescens), Phaseoleae (Amphicarpaea bracheata, Dolichos lablab), Podalyrieae (Baptisia tinctoria),
Rhizobium tropici 3 Legumes representing different subfamilies of the Fabaceae: Mimosoideae: Eumimoseae (Leucaena leucocephala); Papilionoideae: Phaseoleae (Phaseolus vulgaris)
Sinorhizobium fredii (strain NGR234) 4 Legumes representing 112 genera from all three subfamilies of the Fabaceae as well as the non-legume Parasponia (Ulmaceae)
1 Jensen, 1967 (referred as Rhizobium lupini and Rhizobium spp.).
2 Conklin, 1936 (referred as Rhizobium japonicum).
3 Brom et al., 1988 (referred as Rhizobiumphaseoli, symbiotype 2)
4 Broughton, Perret, 1999.
similar to PR (pathogen-regulated) proteins and extensins (Brewin, 2004; Ovtsyna, Staehelin, 2005).
However, the developmental impacts of signaling processes responsible for nodulation are quite different from the pathogenic interactions. In Pisum, Medicago and Lotus species the symbiosis ontogeny starts from the rhizobia penetration into the root hairs leading to their curling and development of the special tunnel structures called infection threads (ITs) (Brewin, 1991). ITs grow inter- and intra-cel-lularly into the cortex wherein the mitotic reactivation occurs in some cells and the nodule primordium is established which differentiates into several tissue types some of which (located in the centre of emerging nodule) are infected by ITs. Several ENOD genes (e. g., ENOD5, ENOD12) are involved in the IT growth since their products are located in the IT walls (Franssen et al., 1992). This development is culminated in the release of rhizobia into the plant cell cytoplasm where they are surrounded by the host membrane and form the organelle-like symbiosomes (Roth, Stacey, 1989). Inside them, rhizobia differentiate in the bacteroids in which the nitrogense enzyme is synthesized and N2 fixation occurs.
At present, nearly all nodulation stages are dissected using the plant mutations arresting IT growth and tissue differentiation. The functional sequence of the involved genes was revealed due to analysis of complementary and epistatic gene interactions in the double mutant lines which combine different developmental mutations (Borisov et al., 1997; Tsyganov et al., 1998). The revealed plant genes are expressed in a tight cooperation with the bacterial symbiotic genes which compose the functionally integrated, super-organism gene network. Its integrity is illustrated by the data demonstrating that similar developmental defects may be obtained due to the plant and bacterial mutations (Provorov et al., 2002; Borisov et al., 2004). Characteristically, the plant Nod- and Fix- mutations usually do not influence the resistance to pathogens, while establishment of the other mutualistic symbiosis, arbuscular mycorrhiza (AM) may be arrested by many of these mutations (Section 3).
The major prerequisite for an efficient legume-rhizobia interaction is the very stringent control over the bacterial performance within the root nodules. It starts just at the first steps of invasion when the IT walls isolate the bacterial cells from the cytoplasm of infected root hairs. During IT growth in the epidermis and cortex a range of defenselike reactions are induced including synthesis of pheno-lics, flavonoids, lytic enzymes and reactive oxygen species (Gamas et al., 1998; Santos et al., 2001; Brewin, 2004). Due to these reactions, nodule development which is quite different from the pathogenic interactions at the organ/ tissue levels, appeared to be similar to them at the cellular/molecular levels. These similarities may be enhanced greatly if the structures of bacterial exopolysaccharides, li-popolysaccharides or cyclic p-glucans are changed by mu-
tations demonstrating that these surface components are responsible for suppressing the host immune responses (Breedveld, Miller, 1994; Niehaus et al., 1998; Kannenberg et al., 1998).
At the very beginning of nodule ontogeny, systemic regulation of nodulation is switched on to balance the symbiosis with the nutritional and energy status of the plant organism (Kinkema et al., 2006). This balance is reached due to the autoregulation of nodulation (AON) induced by a hypothetical signal transmitted from the emerging nodule primordium into the shoots and eliciting the feedback response which prevents formation of the excessive nodules. Mutations in the genes controlling AON lead to a supernodulation (Nod++) phenotype and the plant biomass can be decreased in spite of an increased total N2-fixing activity (Novak et al., 1997). These mutants are usually able to nodulate effectively under a sufficient nitrate supply leading to Nts (Nitrate tolerant symbiosis) phenotype. Therefore, important function of AON is to arrest symbiosis when its formation does not lead to an adaptive gain by host. The involved plant genes (e. g., NARK) are close to CLAVATA genes regulating of meristimatic activities and having no homologues among the resistance (R) genes (Beveridge et al., 2007). However, after inducing AON, some processes common to Systemic Acquired Resistance (SAR) are detected in legumes, including salicilate and jasmonate syntheses (Kinkema et al., 2006).
2.1.2. Nitrogen fixation and assimilation
Due to cooperation between the legumes and rhizobia, two fundamental processes are combined in the super-organism system: fixation of N2 and of CO2. A highly integrated network of partners’ C and N metabolic pathways is formed in nodules responsible for acquiring by plant of a novel adaptive property — symbiotrophic nitrogen nutrition. For this, partners fulfill a range of functions responsible for a high efficiency of cooperation: the amount of N2 obtained symbiotically by some leguminous crops (Medicago sativa, Galega orientalis) may reach 550-600 kg/ha per season (Provorov, Tikhonovich, 2003).
In order to fuel the energy consuming biochemical machinery in nodules the host should spend up to 30 % of its photosynthesis products. About a half of them is lost for respiration that supplies ATP for nitrogenase and for building the symbiotic structures. Another half is a reversible investment used to assimilate fixed N and to transport it to the shoots (Phillips, 1980; Vance, Heichel, 1991; Fisher, 1994).
The photosynthesis products supplied to the infected nodule cells are fermented in an unusual way, not to pyruvate but to malate that can be used immediately in the tricarboxylic acid (TCA) cycle in bacterial cells. Malate together with some other C4-dicarboxylic acids (succinate, fumarate) are up-taken by bacteroids via the DctA permease (Jording et al., 1994). Nearly all ATP produced in bacteroids is used to supply energy to nitrogenase en-
zyme the immediate product of its which, NH4+ is excreted into the host cytoplasm since the enzymes for its assimilation (glutamine synthethase, glutamate synthase) are repressed in bacteroids (Kahn et al., 1998; Kaminski et al., 1998).
In indeterminate nodules, N compounds which are exported to shoots are mainly glutamine and asparagine that contain 2 N atoms per 4-5 C atoms. However, in some legumes forming the determinate nodules (e. g., soybean or common bean) the assimilation is more specialized and the transport forms are represented by ureids (allantoine and allantoic acid) in which N:C ratio is close to 1:1. These compounds are synthesized in the plant cells that are not infected by rhizobia but are located in a close contact to the infected cells (Brewin, 1991).
One of the basic properties of nitrogenase is its high oxygen sensitivity: N2 can be fixed only under microaerobic (< 50 nM of O2) conditions required for nitrogenase stability. In the legume nodules, two barriers are created to protect N2-fixing bacteroids from O2: structural and biochemical. The first one, called the diffusion barrier, consists of a tightly packed layer(s) of thick-walled cells in nodule parenchyma that isolates physically the infected central zone from O2 (Brewin, 1991). The second one consists of the leghe-moglobin (Lb) which may constitute more than 50 % of total proteins produced by the infected plant cells. Both parts of Lb molecule (polypeptide and heme) are encoded by the plant genes (O’Brian, 1996).
The principle strategy for formation of the integrated biochemical system in nodule is represented by the strictly coordinated expression of the partners’ symbiotic genes. This expression was visualized as the synthesis of multiple “late nodulins” represented by Lb and by nodule-specific forms of C- and N-metabolic enzymes synthesized after a decrease of O2 tension in nodules (Vance, Heichel, 1991; Hennecke, 2004). It looks probable that this expression is controlled by some signals coming from the bacteria cells. For example, in legume Sesbania the promoter of Lb3 gene contains two sites specific for the bacterial gene regulators. In Azorhizobium caulinodans (the Sesbania symbiont) the proteins were identified which bind these sequences and the bacterial mutations that knockout these proteins lead to a decrease in Lb synthesis and in N2-fixing activity (De Bruijn et al., 1994).
2.2. Symbioses with N2-fixing cyanobacteria
Some filamentous cyanobacteria (Nostoc, Anabaena) interact with plants forming the symbioses that differ in many respects from the legume nodules. These cyanobacteria can fix N2 in free-living state using the products of their own photosynthesis. Many mechanisms of the free-living N2 fixation are involved in symbioses, but here they are controlled by hosts due to localization of cyanobacteria within special structures. In water fern Azolla, cyanobacteria are located within the leaf cavities, in gymnosperm Cycas — within the intercellular spaces of coralloid roots,
in angiosperm Gunnera — within cells in the glands at the bases of leaf petiols (Bergman et al., 1994; Meeks, El-hai, 2002).
When transferred into N-free medium, 5-10 % of cells distributed regularly along the filaments of free-living Nostoc and Anabaena are differentiated into the heterocysts that are (like the rhizobia bacteroids) devoid of reproductive ability. Heterocysts are enlarged and have thick walls blocking the oxygen entry. Due to arrest of photosynthesis, microaerobic conditions are reached inside heterocysts permitting the nitrogenase synthesis. In free-living cyanobacteria, glutamine synthetase (GS) is expressed along with nitrogenase and the primary product of NH4+ assimilation (glutamine) is exported from heterocysts to the vegetative (photosynthetic) cells. The major source of ATP for nitrogenase reaction is photosystem I that, in contrast to photosystem II and Calvin cycle, retains its activity in heterocysts.
Development of cyanobacteria-plant symbioses is usually started with preinfection contacts, and the massive formation of motile hormogonia is induced in cyanobacteria that colonize the plant interiors. Within Gunnera glands, cyanobacteria propagate actively and infect the plant cells. After entering their cytoplasm, cyanobacteria are encapsulated into the symbiosome membranes and up to 80 % of cells are converted into N2-fixing heterocycts (Bergman et al., 1994). They differ from free-living heterocysts since in symbiosis with Gunnera, the GS activity is lost by Nostoc and NH4+ is exported into the plant cells. The principal sources of C skeletons and energy for heterocyst are the sugars provided by plant host since the own photosynthesis in symbiotic cyanobacteria is almost absent (Meeks, Elhai, 2002).
A unique feature of N2-fixation in cyanobacteria is constituted by the programmed rearrangements of nif genes. In the vegetative Anabaena cells the nitrogense structural gene nifD is split by a 11 kb DNA segment, and integrity of this gene is restored during the heterocyst differentiation. This restoration is controlled by the site-specific endonuclease xisA gene located within the 11 kb segment which may be found as a plasmid in the N2-fixing heterocysts (Golden et al., 1991).
When we compare legume-rhizobia and plant-cyano-bacteria symbioses a range of contrasts may be revealed with respect to structures and biochemical activities of partners’ cells. However, the important general principles of the symbioses operation are evident too (Table 3). In both of them the microbial N2 fixation is combined with the plant photosynthesis resulting in integrated partners’ C/N biochemical pathways. During symbioses, the energy supply of microbial N2-fixing machinery as well as assimilation of NH4+are implemented mainly by hosts. Deep and mainly irreversible cellular differentiation before the onset of N2 fixation occurs in rhizobia (bacteroids) and in cyanobacteria (heterocysts).
Table S
Comparison of two types of N2-fixing plant-microbe symbiosis
Properties Symbioses between
rhizobia and legumes cyanobacteria and plants
Specificity of interaction Narrow: great majority of rhizobia inoculate only the restricted groups of legumes Broad: Nostoc inoculates different types of plants
Impacts of plant signals on microbes Activation of nod-genes (by plant flavonoids) Massive formation of motile hormogonia
Plant structures which contain microsymbionts Develop de novo in the result of symbiotic interaction (root or stem nodules) Exist before symbiotic interaction although are fully developed after colonization by bacteria (glands, tissue cavities, coralloid roots)
Differentiation of nitrogen-fixing bacterial cells Only in plants (bacteroids) In plants and in free-living state (heterocysts)
Penetration of micro-symbionts into plant cells In the majority of legumes Only in Gunnera glands
Rearrangements of nif-genes prior to N2 fixation onset Not shown Typical
Source of ATP for nitrogenase reaction Respiratory chain Photosystem I
Protection of nitrogenase from oxygen Mainly by plants (leghemoglobin and diffusion barrier in nodules) Mainly by bacteria (cell wall of heterocysts)
3. ARBUSCULAR MYCORRHIZA
Mycorrhizae represent the universal type of plant-microbe symbiosis formed by the root-colonizing fungi wherein a part of mycobiont is inside the root while the other part is outside of it (Smith, Read, 1997). Separation of the mycobiont into intra- and extra-radical portions reflects the basic function of mycorrhizae as of intermediates between plant and soil. This function is of global ecological importance since only few plants (mainly short-living herbs and aquatic forms) cover their demands in nutrients and water without an aid of mycobionts. Based on their anatomy, mycorrhizae are classified into endomycorrhizae (the major part of mycobiont is located inside the root; the fungal hyphae penetrate the plant cells and develop the specialized sub-cellular compartments) and ectomycorrhizae (the roots contain a minor part of mycobiont the distribution of which is restricted to intercellular spaces).
The first type is represented by the well studied and ecologically most important arbuscular mycorrhiza (AM) formed by the great majority (> 80 %) of land plants. The genetic organization of the AM-fungi reclassified recently as Glomeromycota (Schußler, 2002) looks intriguing since they combine the absence of sexual reproduction with extremely high genetic diversity (Dodd et al., 1996) and inability to propagate independently of plants with the huge (100 — 1000 Mb) genome size (Tunlid, Talbot, 2002). The heterocaryotic mycelia and spores of AM fungi harbor thousands of genetically variable haploid nuclei (Lloyd-MacGilp et al., 1996). These features complicate greatly the genetic
analysis of AM fungi and nearly all information on the control of this symbiosis is obtained by means of plant genetics.
3.1. Development
AM development involves pre-infection, formation of intra-radical (intercellular) mycelium, development of subcellular symbiotic structures and of sporulating extraradical mycelium (Hahn, Mendgen, 2001). This development starts with the germination of the fungal spores and the brunching growth of germ tubes elicited by the plant exudates. Recently the plant signals (“branching factors”) inducing these processes were elucidated in the model legume Lotus japonicus as strigolactones which are close to the inducers for germination of seeds in parasitic angio-sperms Striga and Orobanche (Akiyama et al., 2005). The pre-infection fungal growth induced by these signals is reversible: if do not attach a root within 5-7 days, the germ tubes abort and the nutrients are returned into spore (Bago et al., 1999). The huge size (up to 0.5 mm) and high metabolic potential of spores permits AM fungi to repeat several times their attempts to reach the root.
After the root is found, the germ tubes form the attachment structures, appressoria from which the infective hyphae start and colonize outer and inner cortex but never cross the pericycle. After establishing a network of intercellular hyphae, fungus develops arbuscules which penetrate the plant cells and fill a sufficient parts of their volumes.
The plant cells containing arbuscules undergo a pronounced differentiation to ensure hosting of the mycobiont. The vacuole is reduced or degraded, the amount of a-tu-
bulin is increased, the nucleus is deformed (sometimes it becomes surrounded by the branches of arbuscule) and chromatin is decondensed due to its high transcriptional activity. The amount of endoplasmic reticulum and Golgi vesicles is increased greatly ensuring the biogenesis of peri-arbuscular membranes. The latter are separated from the fungus surface by an apoplast that contains polysaccharides and enzymes of the mixed (plant and fungal) origins (Harrison, 1998). The arbuscules are short-living structures: every 4-7 days they are digested by plant cells and the novel arbuscules may be developed (Harrison, 1999).
The final developmental stage in AM is represented by formation of the extra-radical hyphae that are of crucial importance for both partners. For the host, nutritional functions of these hyphae (absorption of soil nutrients) are important, while for the mycobiont the reproductive function (sporulation) is indispensable. The extended system of extra-radical hyphae (70-80 m per 1 m of root length) permits the mycobiont to explore carefully the soil around roots scavenging the nutrients. An important property of the extra-radical hyphae is represented by their ability to penetrate the roots of neighboring plants, enabling the allocation of nutrients and energy across the plant community resulting in its stability and diversity (Smith, Read, 1997).
Development of AM fungi within the root is controlled strictly by host; the regulatory processes induced within the root cortex during AM development include: modification of the cell walls, synthesis of flavonoid phytoalexins, accumulation of callose and pathogen-regulated (PR) proteins, including peroxidases and lytic enzymes (Gianinazzi-Pear-son et al., 1996). However, upon Glomus inoculation the intensity of these defence-like reactions is low, they are less prolonged and more differentiated in time and space since the plant defence reactions are repressed by some fungal signals (Kapulnik et al., 1996; Provorov et al., 2002).
The analyses of plant control over AM development have been started using the legume mutants defective in early nodule development since these mutants are often arrested in AM formation (Duc et al., 1989; Borisov et al., 1992). The resulted phenotypes were classified into two groups: Myc-1 and Myc-2. The first one is composed of mutants in which AM development is blocked just after formation of appressoria and the infective hyphae are aborted when penetrating the epidermis. Phenotype Myc-1 was revealed in legume mutants defective in the root hair curling which occurs after rhizobia inoculation. The Myc-2 mutants form apressoria and intercellular mycelium after Glomus inoculation, however arbuscules are not developed. Myc-2 phenotype was identified in the legume mutants arrested at the later stages of nodule development (e. g., rhizobia endocy-tosis into plant cells) (Buttery, Park, 1993).
The analysis of the legume mutants allowed researches to identify a range of genes involved in control of both mutualistic symbioses (Hahn, Mendgen, 2001). However, this approach does not cover the whole AM developmental
program since the defects in pre-infection processes were not identified in the nodulation-arrested legume mutants. The mutants defective in eliciting spore germination and appressoria formation were obtained via a direct selection of AM- phenotypes in legumes (Medicago truncatula) and non-legumes (tomato, maize) (Klingler et al., 1995; Cordi-er et al., 1998; Barker et al., 1988; David-Schwartz et al.,
2001, 2003; Marsh et al., 2006).
From the practical viewpoint, the plant genotypes with an increased AM development look attractive. Some of them were selected among the legume Nod++ mutants impaired in AON suggesting the common mechanisms for systemic regulation of nodulation and mycorrhization (Krussel et al.,
2002). An enhanced AM development was detected in Medicago truncatula lines with an increased activity of chi-tinase class III (MtChit-3) gene (Hause et al., 2002) or of ENOD40 gene involved in the hormonal control of nodulation (Staehelin et al., 2001). Expression of these genes in the cells infected by arbuscules suggest their roles in development of these endosymbiotic structures.
Numerous similarities between AM and nodulation were revealed at the molecular level. Mycorrhization stimulates the de novo synthesis of proteins (mycor-rhizins) which are absent in non-inoculated roots. They comprise 4-5 % of the total root proteins, and in the legumes some of them are common to early nodulins (ENOD2, ENOD11, ENOD12, EN0D40) and to Lb which is weakly synthesised in the plant cells containing arbuscules (Gianinazzi-Pearson, Gianinazzi, 1995). In M. truncatula roots, 300-400 genes are induced during AM, and about 100 of then are common to the nodulation program (Küster et al., 2007). A range of common genes are involved in signalling cascades regulating root nodulation and development of AM in legumes (Hahn, Mendgen, 2001). These data suggest that in the course of legume evolution, some genes were recruited from the ancient AM program into the more young nodulation program (Gianinazzi-Pearson, 1996).
3.2. Metabolism
The adaptive gains obtained by plants and fungi from AM formation are based on their active exchange by nutrients. Due to the ability for intensive osmotrophic nutrition, mycobiont collects broad spectrum of macro-and micro-elements required by host, however, the most pronounced effects pertain the phosphorous nutrition (Smith, Read, 1997). This function is very important for the plant survival because the major part of P in soils is represented by unsolvable compounds that can not be assimilated by roots directly (Vance, 2001). In Pisum sativum genotypes the comparative (%) increases in the P content obtained by plants due to inoculation with Glomus are sufficiently more than the increases in N and K contents or in plant biomass (Martensson, Rydberg, 1994; Jakobi et al., 2000) suggesting the specific mechanisms for P assimilation.
The biochemical data support this suggestion since the uptake of P from soils (which occurs in soluble forms, mainly as Н2РО4- addressed as P.) involves several transport systems some of which have an extremely high affinity for p. (Ezawa et al., 2002). After transporting into hyphae, the major part of P. is included into polyphosphates — linear chains of p. (polymerization is catalyzed by the polyphosphate kinase). The granules rich in polyphosphates and in the P-containing esters move along the hyphae being packed into cylindrical vacuoles the transport of which is facilitated by tubulin fibrils (Ashford, 2002). After reaching the arbuscules, P-compounds are destroyed by phosphatases and the released P. cross the partners’ interface. The crucial role of arbuscules in P. export was proved by the dependence of their development on the soil P status: arbuscules are formed actively under the limited or moderate P. supply, while the absence or excess of P. block their formation.
Inoculation by AM fungi can improve also the N content in plants. An interesting hypothesis concerning this improvement may be deduced from the data demonstrating that some AM fungi harbor obligatory endosymbiotic bacteria close to Burkholderia. In these bacteria, nif genes encoding for nitrogenase were found and their in planta expression was demonstrated that may result in N2 fixation (Minerdi et al., 2002). Its real impact on the plant growth needs precise evaluation, however, high adaptive potential of this tripartite symbiosis is evident since the active P accumulation may lead to an imbalanced plant metabolism if not accompanied by an improved N supply.
In order to support the mycobiont activity, reverse flow of C compounds from host occurs via arbuscules and interfaces between plant cells and intercellular hyphae. Fungi receive these products as the hexoses which resulted from destruction of sucrose by acid invertases located on the plant cell surfaces (Bago et al., 2000). The major part of carbon obtained by fungus is included into the storage and transport forms: lipids, glycogen and trehalose. They are packed into the granules suitable to transport from intrato extra-radical mycelium. The major part of plant-derived C-compounds is used to provide energy for developing the external mycelium as well as for its osmotrophic and spore forming activities.
4. DEFENSIVE SYMBIOSES
One of the basic strategies in plant-microbe interactions is to restrict the activities of hosts’ natural enemies: pathogenic microbes and phytophagans. The defensive symbioses differ from the nutritional ones (N2-fixing symbioses and mycorrhizae): protective functions do not require the bilateral metabolic exchange since the symbiotically essential microbial compounds are produced in tiny dosages and are used not to feed the host but to suppress the antagonistic organisms. A potential to be used in ecologically friendly
agriculture for biocontrol of various pests attracts a great attention to the defensive symbioses. Since the defense from fungal pathogens by plant growth promoting bacteria (PGPR) and by endophytic bacteria will be covered in this volume by the other authors (Lugtenberg and Kamilova, 2008; Berg et al., 2008), we shall concentrate here on the defense of plants from phytophagans.
Plants support in their tissues a variety of endophytic or epiphytic microbes which synthesize the protective substances against invertebrate or vertebrate phytophagans. The best studied are ergot fungi (Clavicipitaceae, Ascomy-cota): Claviceps, Neotyphodium (formerly Acremonium) and Epichloe. They implement the complicated living cycles including asexual and sexual reproduction and a very interesting phenomenon of obligatory involvement of insects into the conidia dispersal (Schardl et al., 1997).
For Neotyphodium and some Epichloe genotypes, vertical transmission through the host generations was demonstrated which can ensure the maintenance of endophytes in the plant populations. Infections by these fungi may result in diverse impacts on the plant fitness including not only beneficial but some deleterious effects too. Interactions with Neotyphodium are predominantly mutualis-tic: endophytes synthesize alkaloids lolins and peramins which make the plant toxic to some insect pests (aphids, weevils, larvae of beetles and butterflies). The gene cluster controlling the synthesis of insecticidal nor-loline was recently mapped and sequenced in N. uncinatum (Spiering et al., 2005). In addition, Neotyphodium induce vegetative plant development and improve resistance to some abiotic stresses, for example to drought (Schardl, 2001; Schardl et al., 2004). However, the related Epichloe spp. often combine the protective and pathogenic effects (e. g., chock disease resulted in suppression of developing the reproductive tillages in cereals).
Unfortunately, many Neotyphodium strains produce alkaloids loliterm B and ergovaline deleterious for cattle; the latter compound is produced also by the ergot fungus Claviceps (Tudzynski, Scheffer, 2004). However, Neotyphodium strains devoid of vertebrate-toxic compounds may be constructed and introduced into the plants since the genes encoding for toxicity are not required for the host colonization (Spiering et al., 2005). The “unarmed” strains may be used to exclude the inoculation of commercial cereal varieties by the toxin-producing endophytes.
An interesting group of plant protectors is represented by Clavicipitaceaen genus Cordyceps, a symptom-less or moderately pathogenic epiphytes which cause the lethal infections in phytophagous insects. These infections are initiated by feeding the insects on epiphyte-harboring plants and are resulted in development of mycelia and fruiting bodies just in the killed pests (White et al., 2002).
As one can conclude from the data on Clavicipitaceae fungi, the analyses of defensive symbioses are required not only to organize the biocontrol of pests but also to avoid the
plant toxicity for domestic animals and for humans. The importance of the latter approach is valid for the plant infections by the Gram-positive coryneform bacterium Cla-vibacter toxicus which was found in the broad spectrum of crops including grain, fodder and vegetable ones (Dorofeeva et al., 2002). In the natural communities, this endophyte if disseminated mainly via nematodes Anguina spp. Presence of C. toxicus in the shoots of fodder crops (ryegrass, fescues) often leads to the “staggers” in cattle, the annual lost from which in New Zealand, Australia and USA is estimated in hundreds of million dollars. A potential of A. tritici to transmit C. toxicus from the fodder cereals to wheat may be dangerous for humans (Riley, Reardon, 1995). The bacterial production of “corynetoxins” is dependent on some bacteriophages which may encode for essential stages of the toxin biosynthesis or for its regulation (Metzler et al., 1997).
5. CONSTRUCTION OF SUSTAINABLE AGROSYSTEMS
Intensive genetic, molecular and ecological research on plant-microbe symbioses demonstrate that the plant organism should be investigated and manipulated not as a chemical machinery which synthesize the organic compounds using the solar energy but as an organizer of the symbiotic communities where many vital (trophic, defensive, some regulatory) functions are delegated from hosts to their microsymbionts (Tikhonovich, Provorov, 2007). This approach opens broad prospects for the symbioses improvement and application in the sustainable agricultural systems in which the high crop productivity may be reached under a minimized application of mineral fertilizers and plant protecting dyes.
Unfortunately, beneficial plant-microbe systems was imbalanced greatly in the cultured flora. During the domestication and breeding of plants, the humans learned to implement many of their vital functions using agrochemicals (mineral fertilizers, pesticides) and agrotechni-cal procedures. The broad application of these techniques underlies the “intensive agriculture” strategy, however, the ecological price of its development expressed as a global pollution of environment appeared to be unexpectedly high (Vance, 2001). A sufficient part of it is due to the chemical transformations of N and P fertilizers the products of which accumulate in soil and water leading to the adverse ecological changes. The plant-protective dyes and the products of their degradation may be transformed into toxic substances that reach humans through the food chains. The real alternatives to these agrochemicals are represented by microbial inoculants without which no ecologically friendly agriculture is possible (Sessitsch et al., 2002). Of course, these inoculants will not substitute totally the fertilizers or pesticides but may decrease manyfold the levels of their application.
Broad analysis of variation in the agronomically important symbiotic traits in plant-microbial systems suggests some general approaches which should underlie their genetic improvement. The first one may be deduced from the data demonstrating that many of the broadly used legume crops are defective in the responsiveness to rhizobial inoculation (Provorov, Tikhonovich, 2003). For example, “old” crops having a prolonged history of cultivation and breeding (alfalfa Medicago sativa, pea Pisum sativum, soybean Glycine max, polebean Phaseolus vulgaris) grow better under the combined N supply than under inoculation with rhizobia strains. However, some “young” crops (Kura clover Trifolium ambiguum, hairy vetch Vicia villosa, goats’ rue Galega orientalis) usually prefer to use symbiotically fixed N2. Moreover, in pea and alfalfa, the wild-growing genotypes and local varieties exceed the agronomically advanced cultivars in the N2-fixing activity. Similar difference between wild-growing and cultivated plant genotypes were reported for AM symbiosis in pea (Jakobi et al., 2000) and for PGPR associations in wheat (Kravchenko, Leonova, 1993).
These data suggest that during domestication and breeding, plants lost their symbiotic potential, and the special efforts from breeders and gene engineers are required to improve it using the genetic resources of wild-growing germplasm. A validity of this approach was demonstrated in polebean: introduction of genes for high N2-fixing activity from wild-growing (climbing) lines into agronomically advanced (bush) cultivars created the commercially attractive genotypes which combine the “cultured” phenotype with high N2-fixing activity (Bliss, 1993).
An important prerequisite for improving the efficiency of symbiotic systems is the coordination of genetic modifications in plants and their microsymbionts. Two-factor analysis of variance of the data on interactions between different plant cultivars and rhizobia strains suggests that the symbiotic efficiency is controlled by genotypes of both partners. However, the highly effective symbioses are formed when the non-additive genetypic effects resulted from the specific cultivar-strain interactions are most pronounced (Rengel, 2002; Provorov, Tikhonovich, 2003). Therefore, coordinated improvement of partners should be aimed at creating the optimal (complementary) combinations of plant and microbial genotypes. The potential output of this work is very high: in major legume crops the amount of fixed nitrogen may be increased by 3—4 times by means of different genetic manipulations (Provorov, Tikhonovich, 2003). The specific approaches and techniques to be used in this work are broadly reviewed in the literature (Barnes et al., 1984; Rengel, 2002; Sessitch et al., 2002; Provorov, Tikhonovich,
2003)
6. CONCLUSION
Molecular research demonstrated that different types of plant-microbe symbiosis (nutritional and defensive) are
based on the deep functional integration of the partners’ genes which is mediated by the signaling interactions. The symbiosis-specific phenotypes acquired by partners are expressed as the development of novel tissue/cellular structures, metabolic functions and adaptive capacities. It is important to note that in order to cooperate with beneficial microbes the plants use a range of universal factors permitting them to avoid a hyper-complications in their genomes which would be required to harbor genes for multiple adaptive functions. Instead, the plants retain a restricted number of genes for hosting various microorganisms, evolutionary reorganizing these genes to adapt the new symbiotic partners and to meet the novel environmental challenges.
From the study of plant-microbe interactions, a novel view of sustainable crop production is suggested as of a methodology of substituting the agrochemicals (mineral fertilizers, plant protective dyes) by the microbial metabolites. An improvement of plant-microbe symbioses should involve the reorganizations of the integrated genetic systems based on a coordinated modifications in the plant and microbial genotypes. In future, the sustainable agriculture should switch from growing the plants to the cultivation of genetically constructed plant-microbial communities which can reach a high productivity under the restricted energy and chemical investments and with the minimal pressures on the environment. However, at present we are still at the beginning of this construction and much more co-operation of experts on the plant and microbial genetics, molecular biology and ecology is required to reach a pronounced success in purchasing the sustainable microbial-based agrotechnologies.
ACKNOWLEDGEMENTS
The research presented in this paper is supported by grants from Russian Foundation of Basic Research (04-0448457, 06-04-48800, 06-04-89000NWO); NWO Centre of Excellence: 047.018.001.
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Молекулярные стратегии и сельскохозяйственное использование растительно-микробных симбиозов
Тихонович И. А., Проворов Н. А.
' РЕЗЮМЕ: Рассматриваются молекулярные механизмы симбиотических взаимодействий между сельскохозяйственно-значимыми растениями и микроорганизмами, играющих важную роль в питании и защите растений. Такие симбиозы основаны на сигнальных взаимодействиях, приводящих к развитию новых тканевых/клеточных структур, а также к расширению метаболических возможностей у партнеров, что в значительной степени улучшает адаптивный потенциал растений вследствие устойчивости к биотическому или абиотическому стрессу. Данные, касающиеся молекулярных, генетических или экологических особенностей растительно-микробных взаимодействий, обеспечивают методологию создания устойчивых сельскохозяйственных культур, основанную на замещении химикатов (минеральных удобрений и пестицидов) микробиологическими препаратами. Усовершенствование растительно-микробных симбиозов должно включать согласованные изменения обоих партнеров, обеспечивающие создание комплементарных сочетаний их генотипов.
' КЛЮЧЕВЫЕ СЛОВА: полезные растительно-микробные взаимодействия, симбиотическая фиксация азота, арбускулярная микориза, клубеньковые бактерии, цианобактерии, спорыньевые грибы, эндофиты, биоконтроль патогенов и фитофагов, создание устойчивых растений
