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Symbiogenetics Underway: from Genetic Analysis to Genetic Synthesis

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Symbiogenetics Underway: from Genetic Analysis to Genetic Synthesis EDITORIAL Symbiogenetics underway: from genetic analysis to genetic synthesis Symbiogenetics is a completely new research field aimed at studying the variabil- ity and heredity in superorganismal systems composed by distant species during intimate symbiotic interactions. The emergence and swift progress of this field are based on the genetic analysis of inter-species interactions, which play a crucial role in the development, adaptation and evolution of nearly all living creatures. However, we do not consider symbiogenetics as a paraphrasing for “genetics of symbiosis”: it is a fundamental area of biology which represents a holistic ap- proach to studying the genomic integration of distant species. This approach, aimed at analyzing superorganismal genetic systems (Tikhonovich and Provorov, 2009), complements the traditional reductionist methodology of genetic analysis based on the dissection of hereditary material into the elementary units — genes, cistrons, mutons, recons, codons, etc. (Benzer, 1957; Lobashev, 1967; Inge-Vech- tomov, 1983). Historically, symbiogenetics emerged at the border of ecological genetics, which addresses the impacts of environmental factors on genetic processes (Inge- Vechtomov, 2015), and the symbiogenesis theory, which proposes that eukary- otic cells originated via integration of distant prokaryotic forms (Mereschkowsky, 1910; Margulis, 1996; Provorov et al., 2018). This is why symbiogenetics consid- ers the tight integration of diverse species as their fundamental adaptive strategy based on the immanent properties of genetic material expressed at all levels of its organization. The universal mechanisms for maintenance, transmission and expression of hereditary information provide opportunities for merging the ge- nomes of distant organisms (prokaryotes and eukaryotes, bacteria and archaea), which results in functionally and structurally integrated systems. Previously we suggested that in symbiotic systems, the elementary units of heredity are represented not by individual genes (as in free-living organisms Citation: Provorov, N. and Tikhonovich, I. subjected to conventional genetic analysis) but by extra-gene systems, at least by 2021. Symbiogenetics underway: from genetic analysis to genetic synthesis. pairs of genes belonging to the interacting partners (Tikhonovich and Provorov, Bio. Comm. 66(1): 3–5. https://doi. 2012). Developing an approach coined by W. Q. Loegering (1978), who suggest- org/10.21638/spbu03.2021.101 ed for symbiosis a specific phenotype represented by the “emergent traits” (von Authors’ information: Nikolay Provorov, Dr. of Sci. in Biology, Professor, Director of Bertalanffy, 1968), we proposed for symbiosis a distinct genotype based on the ARRIAM, orcid.org/0000-0001-9091-9384; Igor Tikhonovich, RAS Academician, Dr. of integration of partners’ genomes. Preliminarily, it may be addressed in terms of Sci. in Biology, Professor, Director for the partners’ genomic complementation (Tikhonovich et al., 2015), although the Science of ARRIAM, Dean of Faculty, orcid. org/0000-0001-8968-854X resulting integrative evolution should not be restricted to the genome interaction: Manuscript Editor: Pavel Skutschas, in the course of partners’ co-adaptation, communalized systems for variability Department of Vertebrate Zoology, Faculty and heredity are emerging. of Biology, Saint Petersburg State University, Saint Petersburg, Russia To address these composite genomes, the notion of “hologenome” has been Received: May 17, 2020; introduced, which denotes an integral genetic system composed of all genes har- Revised: July 15, 2020; bored by the eukaryotic host and its associated microbial community (Zilber- Accepted: August 10, 2020. Rosenberg and Rosenberg, 2008). However, this definition cannot be considered Copyright: © 2021 Provorov and universal since symbiotic interactions implemented in the communities formed Tikhonovich. This is an open-access article distributed under the terms of the License by plants or animals with their microbial cohabitants are extremely diverse: they Agreement with Saint Petersburg State University, which permits to the authors range from sporadically emerging, transient associations to strictly obligatory, unrestricted distribution, and self-archiving vertically transmitted ones. This is why we consider a “symbiogenome” as a ma- free of charge. jor product of facultative symbiosis in which the specialized partners’ genes are Funding: Supported by the Russian Science Foundation, Grants 19-16-00081 (genomic involved. In a historical perspective, the provisionally emerged symbiogenomes integration) and 17-76-30016 (signaling tend to be reorganized into obligatory hologenomes in which the permanent co- interactions). Competing interests: The authors have existence of diverse organisms assumes the participation of the whole partners’ declared that no competing interests exist. genomes in a cooperative interaction. 4 BIOLOGICAL COMMUNICATIONS, vol. 66, issue 1, January–March, 2021 | https://doi.org/10.21638/spbu03.2021.101 In the model N2-fixing legume- natural history, land plants acquired and antagonistic communications. rhizobia association, the symbioge- a system for hosting and managing Importantly, in some pathosystems, nome involves the partners’ genes the beneficial symbionts which were partners’ interactions are very tight, used in signal interactions (e.g., diversified broadly to meet the phy- as illustrated by the microbe → host bacterial nod genes for the synthe- logenetic and ecological radiation of transfer of effector proteins mainly sis of lipo-chito-oligosaccharidic microbial partners. During adapta- via different secretion systems, or Nod factors + plant NFR genes for tion to various environments, plants even of symbiotically essential genes their reception) and in the meta- gained a range of mechanisms for (e.g., in Agrobacterium responsible bolic exchange (e.g., bacterial nif/fix recruiting the beneficial symbionts for plant onco-transformation), genes for nitrogenase synthesis/op- from external sources (e.g., from suggesting excellent models for co- eration + plant GS/GTS/AAT genes soils) and from the associated (e.g., operative adaptation and integrative for assimilating the nitrogenase re- endophytic) communities providing evolution covering different levels of action products). For these genes, to their hosts the urgent nutritional, genomic organization. coevolution was demonstrated at defensive and regulatory functions. Finally, we are going to demon- the population and phylogenetic In this special issue of Biological strate that the integrative approaches levels (Andronov et al., 2015; Shats- Communications, we are going to il- provided by symbiogenetics have a kaya et al., 2019), which resulted in lustrate the major ideas of symbio- pronounced applied potential aimed a marked increase of symbiogenome genetics using the models of tightly at constructing the superspecific complexity and integrity. integrated microbe–plant and mi- systems for agricultural, biomedical Analysis of the diverse mi- crobe–animal symbioses in which and environmental purposes. crobe–plant interactions, includ- the micropartners colonize the in- Acknowledgements ing legume–rhizobia symbiosis, ternal niches of host organisms. Since the major ideas of symbioge- arbuscular mycorrhizae and the Given that many beneficial sym- netics have originated as a summary endophytic/epiphytic associations, bioses are closely related to parasitic of genetic research on plant–microbe demonstrate that at least some genes interactions (de Bary, 1879; Provo- symbioses implemented in the All-Rus- used by plants for cross-talking with rov, 2019), we will address several sia Research Institute for Agricultural Microbiology during the last 40 years of microbial cohabitants are universal examples of host–pathogen systems its 90-year history, the authors are cor- (Tikhonovich et al., 2015). It seems which allow us to dissect the evo- dially grateful to all colleagues who con- that from the very beginning of their lutionary continuum of mutualistic tributed to this exciting development. Nikolay Provorov and Igor Tikhonovich, Guest Editors of this Special Issue of “Biological Communications” References Andronov, E. E., Igolkina, A. A., Kimeklis, A. K., Vorobyov, N. I., and Provorov, N. A. 2015. Characteristics of natural selection in populations of nodule bacteria (Rhizobium leguminosarum) interacting with different host plants.Russian Journal of Genet- ics 51(10):949–956. https://doi.org/10.1134/S1022795415100026 Benzer, S. 1957. The elementary units of heredity. In McElroy, W. D., Glass B. (eds.). The chemical basis of heredity. Baltimore, Maryland: Johns Hopkins Press, pp. 70–93. de Bary, A. 1879. Die erscheinung der symbiose. Strassburg: Verlag Von K. J. Trübner. https://doi.org/10.1515/9783111471839 Inge-Vechtomov, S. G. 1983. Introduction into molecular genetics. Moscow, Russia: Higher School. Inge-Vechtomov, S. G. 2015. Genetics in retrospect. St.-Petersburg, Russia: N.-L. Publ. (In Russian) Lobashev, M. E. 1967. Genetics. Leningrad, Russia: Leningrad Univ. Publ. (In Russian) Loegering, W. Q. 1978. Current concepts of inter-organismal genetics. Annual Review of Phytopathology 16:309–320. https://doi. org/10.1146/annurev.py.16.090178.001521 Margulis, L. 1996. Archaeal-eubacterial mergers in the origin of Eukarya: phylogenetic classification of life. Proceedings of the National Academy of Sciences USA 93(3):1071–1076. https://doi.org/10.1073/pnas.93.3.1071 Mereschkowsky, C. 1910. Theorie
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