![]() | |||
Research paper Botanica Pacifica. A journal of plant science and conservation 2024. Preprint Article first published online: 23 OCT 2024 | DOI: 10.17581/bp.2024.13212 Root microbiomes of Zygophyllaceae in the Kazakhstan desert: a weak evidence for rhizobial nitrogen fixation Vladimir G. Onipchenko 1 ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() 1 Lomonosov Moscow State University, Faculty of Biology, Dept. Ecology and Plant Geography, Moscow, Russia 2 Winogradsky Institute of Microbiology, Research Centre of Biotechnology RAS, Moscow, Russia 3 Altyn-Emel National Park, Basshi Village, Jetysu Region, Kazakhstan 4 Makhambet Utemisov West Kazakhstan University, Uralsk, Kazakhstan 5 A.N. Severtsov Institute of Ecology and Evolution, Moscow, Russia The plants of the Zygophyllaceae family are often considered to be capable of symbiotic atmosphere nitrogen fixation, forming rhizobial nodules similar to those of Fabaceae and Urticaceae. In four species of Zygophyllaceae and the related Peganum harmala (hereafter called Z-plants), collected in Dzungarian deserts (Kazakhstan), we analyzed the prokaryotic component of the root microbiome and the 15N and 13C content in the leaves of these Z-plants compared with neighboring dicots belonging to other families (R-plants). Among all studied Zygophyllum fabago root samples only one was found to have the root nodule, however the microbiome of this sample was similar to that found in other Z. fabago root samples where nodulation was not observed. If compared to Z-plants, the R-plants had a significantly higher relative abundance of bacteria of genera Glycomyces, Massilia and Streptomyces, while the Z-plants had a higher relative abundance of the representatives of genera Actinomadura, Nocardia and Pseudonocardia. Unidentified representatives of the family Rhizobiaceae were present in some of R and Z plants, being most abundant in soil samples. On average, the Z- and the R-plants did not differ in their δ13С and δ15N. Overall, the results do not allow us to consider the studied Zygophyllaceae plants as species with effective atmospheric nitrogen fixation due to rhizobial symbiosis – a characteristic feature of the most legumes. Онипченко В.Г., Клюкина А.А., Кубланов И.В., Бонч-Осмоловская Е.А., Мусабеков М.Т., Бисенгазиева А.С., Тиунов А.В., Цуриков С.М., Ахметжанова А.А., Елумеева Т.Г. Корневой микробиом Zygophyllaceae в пустыне Казахстана: слабые свидетельства ризобиальной азотфиксации. Растения семейства Zygophyllaceae часто рассматриваются как группа, способная симбиотически фиксировать атмосферный азот, образуя ризобиальные клубеньки, аналогичные таковым у Fabaceae и Urticaceae. Для четырех видов семейства Zygophyllaceae и Peganum harmala (Z-растения) из Джунгарских пустынь (Казахстан) проведен анализ корневого микробиома (состав прокариот) и содержания изотопов 15N и 13C в листьях этих растений в сравнении с соседними двудольными из других семейств (R-растения). Только в одном случае был найден корневой клубенёк (у Zygophyllum fabago), однако, этот образец корней не имел каких-либо существенных отличий от других по составу микробиома. При сравнении микробиомов Z- и R-растений выяснилось, что в ризосфере R-растений повышено относительное содержание бактерий родов Glycomyces, Massilia and Streptomyces, в то время как у Z-растений выше относительное содержание представителей родов Actinomadura, Nocardia и Pseudonocardia. Неидентифицированные представители семейства Rhizobiaceae присутствовали в микробиомах некоторых R- and Z-растений, однако наиболее высокое их содержание было в образцах почвы. В среднем Z- и R- растения не отличались по содержанию 13С и 15N. Проведенные исследования не позволяют нам относить изученных представителей семейства Zygophyllaceae к видам эффективно фиксирующим атмосферный азот на базе ризобиального симбиоза, как это имеет место у большинства бобовых. Keywords: Zygophyllaceae, microbial communities, δ13С, δ15N, nitrogen fixation, микробные сообщества, азотфиксация References APG. [= Angiosperm Phylogeny Group] IV 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of Linnean Society 181:1-20. CrossRef Allen, E.K. & O.N. Allen 1950. The anatomy of nodular growth on the roots of Tribulus cistoides L. Proceedings of Soil Science Society of America 14:179-183. CrossRef Athar, M. & A. Mahmood 1972. Root nodules in some members of Zygophyllaceae growing at Karachi university campus. Pakistan Journal of Botany 4(2):209-210. Athar, M. & A. Mahmood 1981. Extension of Rhizobium host range to Zygophyllaceae. In: Current perspectives in nitrogen fixation (A.H. Gibson & W.E. Newton, eds), p. 481, Australian Academy of Science, Canberra. Becking, J.H. 1970. Plant-endophyte symbiosis in nonleguminous plants. Plant and Soil 32:611-654. CrossRef Bolyen, E., J.R. Rideout, M.R. Dillon, N.A. Bokulich, C.C. Abnet, G.A. Al-Ghalith, H. Alexander, E.J. Alm, M. Arumugam, F. Asnicar, et al. 2019. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37:852-857. CrossRef Bulgarelli, D., K. Schlaeppi, S. Spaepen, E.V.L. van Themaat & P. Schulze-Lefert 2013. Structure and functions of the bacterial microbiota of plants. Annual Reviews of Plant Biology 64: 807-838. CrossRef Craine, J.M., A.J. Elmore, M.P. Aidar, M. Bustamante, T.E. Dawson, E.A. Hobbie, A. Kahmen, M.C. Mack, K.K. McLauchlan, A. Michelsen, G.B. Nardoto, L.H. Pardo, J. Penuelas, P.B. Reich, E.A.G. Schuur, W.D. Stock, P.H. Templer, R.A. Virginia, J.M. Welker & I.J. Wright 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytologist 183: 980-992. CrossRef Friesen, M.L., S.S. Porter, S.C. Stark, E.J. von Wettberg, J.L. Sachs & E. Martinez-Romero 2011. Microbially mediated plant functional traits. Annual Review of Ecology, Evolution, and Systematics 42:23-46. CrossRef Gao J., S. Chen, Y. Wang, J. Qi, X. Li, G. Wei & S. Jiao 2022. Variation in soybean root-associated microbiome between lateral roots with and without nodules. Plant and Soil 479(1-2):481-494. CrossRef Gohl, D.M., A. MacLean, A. Hauge, A. Becker, D. Walek & K.B. Beckmann 2016. An optimized protocol for high-throughput amplicon-based microbiome profiling. Protocol Exchange 1-15. CrossRef Gutierrez, J.R., P.L. Meserve, L.C. Contreras, H. Vasquez & F.M. Jaksic 1993. Spatial distribution of soil nutrients and ephemeral plants underneath and outside the canopy of Porlieria chilensis shrubs (Zygophyllaceae) in arid coastal Chile. Oecologia 95:347-352. CrossRef Hardoim, P.R., L.S. van Overbeek, G. Berg, A.M. Pirttila, S. Compant, A. Campisano, M. Dorling & A. Sessittsch 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79(3):293-320. CrossRef Hassani, M.A., P. Duran & S. Hacquard 2018. Microbial interactions within the plant holobiont. Microbiome 6(58):1-17. CrossRef Högberg, P. 1997. 15N natural abundance in soil-plant systems. New Phytologist 137(2):179-203. CrossRef Hugerth, L.W., H.A. Wefer, S. Lundin, H.E. Jakobsson, M. Lindberg, S. Rodin, L. Engstrand & A.F. Andersson 2014. DegePrime, a program for degenerate primer design for broad-taxonomic-range PCR in microbial ecology studies. Applied and Environmental Microbiology 80(16):5116-5123. CrossRef Hu, Y.-K., G.-F. Liu, X. Pan, Y.B. Song, M. Dong & J.H.C. Cornelissen 2022. Contrasting nitrogen cycling between herbaceous wetland and terrestrial ecosystems inferred from plant and soil nitrogen isotopes across China. Journal of Ecology 110(6):1259-1270. CrossRef Hurek, T., L. Handley, B. Reinhold-Hurek & Y. Piche 1998. Does Azoarcus sp. fix nitrogen with monocots? In: Biological nitrogen fixation for the 21st century. Current Plant Science and Biotechnology in Agriculture, vol. 31 (C. Elmerich, A. Kondorosi & W.E. Newton, eds.), p. 407, Springer, Dordrecht. CrossRef Isachenko, B.L. 1913. On nodules on the roots of Tribulus terrestris L. Izvestiya S.-Peterburgskogo Botanicheskogo Sada 13(1-2):23-31 (in Russian). [Исаченко Б.Л. 1913. О клубеньках на корнях Tribulus terrestris L. // Известия Санкт-Петербургского ботанического сада. Вып. 13, № 1-2. С. 23-31]. Kaplan, D., M. Maymon, C.M. Agapakis, A. Lee, A. Wang, B.A. Prigge, M. Volkogon & A.M. Hirsch 2013. A survey of the microbial community in the rhizosphere of two dominant shrubs of the Negev Desert highlands, Zygophyllum dumosum (Zygophyllaceae) and Atriplex halimus (Amaranthaceae), using cultivation-dependent and cultivation-independent methods. American Journal of Botany 100(9):1713-1725. CrossRef Kivlin, S.N., M.A. Mann, J.S. Lynn, M.R. Kazenel, D.L. Taylor & J.A. Rudgers 2022. Grass species identity shapes communities of root and leaf fungi more than elevation. ISME Communications 2(25):1-14. CrossRef Lauterbach, M., R. Zimmer, A.C. Alexa, S. Adachi, R. Sage, T. Sage, T. MacFarlane, M. Ludwig & G. Kadereit 2019. Variation in leaf anatomical traits relates to the evolution of of C4 photosynthesis in Tribuloideae (Zygophyllaceae). Perspectives in Plant Ecology, Evolution and Systematics 39:125463. CrossRef Mahmood, A. & M. Athar 2006. Scanning electron microscopic observations on micro-organisms in the root nodules of Tribulus terrestris L. (Zygophyllaceae). Scanning 28:233-235. CrossRef Makarov, M.I., V.G. Onipchenko, T.I. Malysheva, R.S.P. van Logtestijn, N.A. Soudzilovskaia & J.H.C. Cornelissen 2014. Determinants of 15N natural abundance in leaves of co-occurring plant species and types within an alpine lichen heath in the Northern Caucasus. Arctic, Antarctic, and Alpine Research 46(3):581-590. CrossRef Meade, C.V., C.P. Bueno de Mesquita, S.K. Schmidt & K.N. Suding 2020. The presence of a foreign microbial community promotes plant growth and reduces filtering of root fungi in the arctic-alpine plant Silene acaulis. Plant Ecology and Diversity 13(5-6):377-390. CrossRef Merkel, A.Y., I.Y. Tarnovetskii, O.A. Podosokorskaya & S.V. Toshchakov 2019. Analysis of 16S rRNA primer systems for profiling of thermophilic microbial communities. Microbiology 88(6):671-680. CrossRef Mostafa, M. & M. Mahmoud 1951. Bacterial isolates from root nodules of Zygophyllaceae. Nature 167:446-447. CrossRef Moyes, A.B., L.M. Kueppers, J. Pett-Ridge, D.L. Carper, N. Vandehey, J. O'Neil & A.C. Frank 2016. Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer. New Phytologist 210(2):657-668. CrossRef Onipchenko, V.G. 2019. Functional phytocenology: plant synecology. Krasand, Moscow, 567 pp. (in Russian). [Онипченко В.Г. 2019. Функциональная фитоценология: синэкология растений. М.: Красанд. 567 с.]. Pangesti, N., A. Pineda, S.E. Hannula & T.M. Bezemer 2020. Soil inoculation alters the endosphere microbiome of chrysanthemum roots and leaves. Plant and Soil 455(1-2):107-119. CrossRef Parker, L.W., H.G. Fowler & G. Ettershank 1982. The effects of subterranean termite removal on desert soil nitrogen and ephemeral flora. Journal of Arid Environment 5(1):53-59. CrossRef Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Core Team 2021. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-152. URL: http://CRAN.R-project.org/package=nlme>. Pyankov, V., H. Ziegler, A. Kuz'min & G. Edwards 2001. Origin and evolution of C4 photosynthesis in the tribe Salsoleae (Chenopodiaceae) based on anatomical and biochemical types in leaves and cotyledons. Plant Systematics and Evolution 230:43-74. CrossRef Quast, C., E. Pruesse, P. Yilmaz, J. Gerken, T. Schweer, P. Yarza, J. Peplies & F.O. Glöckner 2013. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research 41(D1):D590-D596. CrossRef Sabet, Y. 1946. Bacterial root nodules in the Zygophyllaceae. Nature 157:656-657. CrossRef Santi, C., D. Bogusz & C. Franche 2013. Biological nitrogen fixation in non-legume plants. Annals of Botany 111(5):743-767. CrossRef Sheahan, M.C. 2007. Zygophyllaceae. In: The families and genera of vascular plants, vol. 9 (K. Kubitzki, ed.), pp. 488-500, Springer, Berlin. Sprent, J.I. 2005. Biological nitrogen fixation associated with angiosperms in terrestrial ecosystems. In: Nutrient acquisition by plants: An ecological perspective (Ecological studies, vol. 181) (H. BassiriRad, ed.), pp. 89-115, Springer, Berlin. CrossRef Sprent, J.I., J. Ardley & E.K. James 2017. Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytologist 215(1):40-56. CrossRef Tedersoo, L., L. Laanisto, S. Rahimlou, A. Toussaint, T. Hallikma & M. Partel 2018. Global database of plants with root-symbiotic nitrogen fixation: NodDB. Functional Ecology 29(3):560-568. CrossRef Yu, J. & Y. Steinberger 2011. Vertical distribution of microbial community functionality under the canopies of Zygophyllum dumosum and Hammada scoparia in the Negev Desert, Israel. Microbial Ecology 62(1):218-227. CrossRef Zhang, J., S. Sun, G. Wang, P. Chen, Z. Hu & X. Sun 2022. Composition and diversity of endophytic diazotrophs within the pioneer plants in a newly formed glacier floodplain on the eastern Tibetan Plateau. Plant and Soil 481(1-2):253-267. CrossRef
|