**4. Conclusion**

Among all the multicellular eukaryotes, plants have the greatest need for the beneficial interaction with microorganisms, as they lack active movement and therefore cannot choose more advantageous habitat. That kind of restriction can be compensated by the ability of photosynthesis, as carbon compounds produced by plants are a significant stimulus for various microbes to cooperate with them. As a result of such cooperation, plant acquires an access to the adaptations of microsymbiont, and *vice versa*, according to a principle of genome complementarity that was recently formulated by Prof. I.A. Tikhonovich and Dr. N.A. Provorov (ARRIAM, Russia) [122]. It means that, in spite of lacking the nitrogenase genes in its own genome, plant "exploits" corresponding part of microorganism's genome in order to implement biological nitrogen fixation, while rhizobia "exploit" plant genes controlling photosynthetic apparatus, and so forth. Thereby the plant-microbe system acquires an advantage over plants and microbes that compete for survival separately.

ortholog of *Lotus NFR1*, but two closely related paralogs – *Sym37* and *Sym2* – are involved in genetic control of Nod-factor reception. This is not surprising, if we take into account the complexity of Nod-factor molecule and the importance of its proper recognition for successful

**Figure 4.** Hypothetical model for precise recognition of Nod-factor structure by receptor kinases in pea. The model is proposed by Dr. V.A. Zhukov (ARRIAM, St. Petersburg, Russia). At first step, less specific receptor (probably, Sym10) anchors NF molecule onto the membrane; then it presents it to Sym37, which tests the structure of the nonreducing end, and to Sym2, which tests the structure of reducing end. When both Sym37 and Sym2 bind NF, they activate

Among all the multicellular eukaryotes, plants have the greatest need for the beneficial interaction with microorganisms, as they lack active movement and therefore cannot choose more advantageous habitat. That kind of restriction can be compensated by the ability of photosynthesis, as carbon compounds produced by plants are a significant stimulus for various microbes to cooperate with them. As a result of such cooperation, plant acquires an access to the adaptations of microsymbiont, and *vice versa*, according to a principle of genome complementarity that was recently formulated by Prof. I.A. Tikhonovich and Dr. N.A. Provorov (ARRIAM, Russia) [122]. It means that, in spite of lacking the nitrogenase genes in its own genome, plant "exploits" corresponding part of microorganism's genome in order to implement biological nitrogen fixation, while rhizobia "exploit" plant genes controlling

development of symbiosis.

148 Plants for the Future

downstream components of signal transduction pathway.

**4. Conclusion**

The role of symbioses in the evolution of life, and plants in particular, cannot be underesti‐ mated. One can state that the tendency to establish mutually beneficial associations with microorganisms is an essential feature of plants, which has a wide variety of manifestations through a long coevolution of symbiotic partners. Photosynthesis itself, the main distinctive feature of plants, is provided by chloroplasts – the descendants of ancient symbiotic cyano‐ bacteria. According to modern conception, plant colonization of land was possible primarily due to the symbiotic association with arbuscular mycorrhiza fungi. AM, in turn, is considered as a basis for the development of highly specific root-nodule symbiosis characteristic for legume plants. The possible path of the AM origin and its connection with RN was largely understood by studying *Geosiphon pyriformis* – the only representative of the phylum *Glomer‐ omycota* that does not form symbiotic association with higher plants.. Instead, it contains intracellular symbiotic nitrogen-fixing cyanobacteria of the *Nostoc* genus which are essential for its proper nutrition and development [123, 124]. The intensive exchange of products of nitrogen, carbon, and phosphorus metabolism between partners indicates that mechanisms of reciprocal nutrients' transport probably emerged in symbiotic systems formed by *Geosiphon* and *Nostoc* ancestors and lately have been recruited in the evolution of AM [124, 125]. The transition from *Geosiphon-Nostoc*-type association to AM could occur through an intermediate "triple" symbiosis including plant, common ancestor of AM fungi, and *Geosiphon*, and ancestral forms of *Nostoc*, with subsequent loss of cyanobiont. It should be noted that ancient symbiotic fungi presumably carried additional bacterial symbionts both on the surface and in the cytoplasm. In the cells of modern *Glomeromycota*, including *Geosiphon*, various symbiotic bacteria are found, including those capable of nitrogen-fixation (close to β-proteobacteria of *Burkholderia* genus, some members of which were shown to form the RN symbiosis with legumes; see above) [126]. Thus, the AM symbiosis could be the direct "gateway" for intro‐ ducing symbiotic bacteria, including the ascendants of modern rhizobia, into plant tissues. This suggestion is also supported by the existence of CSP and the similarity of rhizobial and fungal signal molecules.

Emergence of Nod-factor signaling was among the most important factors that determined the evolutionary success of legume-rhizobial symbiosis. The wide variety of Nod-factors as well as finely tuned receptor system in plants ensure that only specific partners will meet each other in the soil and consequently form a superorganism with high level of genetic and metabolic integration. This appears to be a basis for evolution of the efficiency of symbiotic pairs, instead of single organisms – the results we now observe.

Legumes provide both an important food source for humanity and a unique model for investigation of the evolution and the underlying genetic mechanisms of mutualistic plantmicrobe symbioses. Further studies of the genetic bases of signal interactions between plants and microbes can provide more information about evolution of such a mutually beneficial association, as well as about spreading of the legumes across the world. Discovery of genes involved in recognition of partners, transduction of symbiotic signals and overall "manage‐ ment" of symbiosis will also provide a useful tool for agriculture, as the knowledge obtained from this studying will facilitate the creation of highly-effective specific symbiotic pairs between crop plants and nitrogen-fixing bacteria in field..
