Actinorhizal plants are a group of angiosperms characterized by their ability to form a symbiosis with the nitrogen fixing actinomycetota Frankia. This association leads to the formation of nitrogen-fixing root nodules.
Actinorhizal plants are distributed within three clades,[1] and are characterized by nitrogen fixation.[2] They are distributed globally, and are pioneer species in nitrogen-poor environments. Their symbiotic relationships with Frankia evolved independently over time,[3] and the symbiosis occurs in the root nodule infection site.[4]
Classification
editActinorhizal plants are dicotyledons distributed within 3 orders,[1] 8 families and 26 genera, of the angiosperm clade.[5][2]: Table S1
All nitrogen fixing plants are classified under the "Nitrogen-Fixing Clade",[6] which consists of the three actinorhizal plant orders, as well as the order fabales. The most well-known nitrogen fixing plants are the legumes, but they are not classified as actinorhizal plants. The actinorhizal species are either trees or shrubs, except for those in the genus Datisca which are herbs.[7] Other species of actinorhizal plants are common in temperate regions like alder, bayberry, sweetfern, avens, mountain misery and coriaria. Some Elaeagnus species, such as sea-buckthorns produce edible fruit.[8] What characterizes an actinorhizal plant is the symbiotic relationship it forms with the bacteria Frankia,[9] in which they infect the roots of the plant. This relationship is what is responsible for the nitrogen-fixation qualities of the plants, and what makes them important to nitrogen-poor environments.[10]
Distribution and ecology
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Actinorhizal plants are found on all continents except for Antarctica. Their ability to form nitrogen-fixing nodules confers a selective advantage in poor soils, and are therefore pioneer species where available nitrogen is scarce, such as moraines, volcanic flows or sand dunes.[11] Being among the first species to colonize these disturbed environments, actinorhizal shrubs and trees play a critical role, enriching the soil[12] and enabling the establishment of other species in an ecological succession.[5][11] Actinorhizal plants like alders are also common in the riparian forest.[11] They are also major contributors to nitrogen fixation in broad areas of the world, and are particularly important in temperate forests.[5] The nitrogen fixation rates measured for some alder species are as high as 300 kg of N2/ha/year, close to the highest rate reported in legumes.[13]
Evolutionary origin
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No fossil records are available concerning nodules, but fossil pollen of plants similar to modern actinorhizal species has been found in sediments deposited 87 million years ago. The origin of the symbiotic association remains uncertain. The ability to associate with Frankia is a polyphyletic character and has probably evolved independently in different clades.[3] Nevertheless, actinorhizal plants and Legumes, the two major nitrogen-fixing groups of plants share a relatively close ancestor, as they are all part of a clade within the rosids which is often called the nitrogen-fixing clade.[6] This ancestor may have developed a "predisposition" to enter into symbiosis with nitrogen fixing bacteria and this led to the independent acquisition of symbiotic abilities by ancestors of the actinorhizal and Legume species. The genetic program used to establish the symbiosis has probably recruited elements of the arbuscular mycorrhizal symbioses, a much older and widely distributed symbiotic association between plants and fungi.[14]
The symbiotic nodules
editAs in legumes, nodulation is favored by nitrogen deprivation and is inhibited by high nitrogen concentrations.[15] Depending on the plant species, two mechanisms of infection have been described: The first is observed in casuarinas or alders and is called root hair infection. In this case the infection begins with an intracellular penetration of a Frankia hyphae root hair, and is followed by the formation of a primitive symbiotic organ known as a prenodule.[4] The second mechanism of infection is called intercellular entry and is well described in Discaria species. In this case bacteria penetrate the root extracellularly, growing between epidermal cells then between cortical cells.[15] Later on Frankia becomes intracellular but no prenodule is formed. In both cases the infection leads to cell divisions in the pericycle and the formation of a new organ consisting of several lobes anatomically similar to a lateral root.[16] Cortical cells of the nodule are invaded by Frankia filaments coming from the site of infection/the prenodule. Actinorhizal nodules have generally an indeterminate growth, new cells are therefore continually produced at the apex and successively become infected.[16] Mature cells of the nodule are filled with bacterial filaments that actively fix nitrogen. No equivalent of the rhizobial nod factors have been found, but several genes known to participate in the formation and functioning of Legume nodules (coding for haemoglobin and other nodulins) are also found in actinorhizal plants where they are supposed to play similar roles.[16] The lack of genetic tools in Frankia and in actinorhizal species was the main factor explaining such a poor understating of this symbiosis, but the recent sequencing of 3 Frankia genomes and the development of RNAi and genomic tools in actinorhizal species[17][18] should help to develop a far better understanding in the following years.[19]
Notes
edit- ^ a b "Angiosperm Phylogeny Website". www.mobot.org. Retrieved 2024-03-07.
- ^ a b Li, Hong-Lei; Wang, Wei; Mortimer, Peter E.; Li, Rui-Qi; Li, De-Zhu; Hyde, Kevin D.; Xu, Jian-Chu; Soltis, Douglas E.; Chen, Zhi-Duan (November 2015). "Large-scale phylogenetic analyses reveal multiple gains of actinorhizal nitrogen-fixing symbioses in angiosperms associated with climate change". Scientific Reports. 5 (1): 14023. Bibcode:2015NatSR...514023L. doi:10.1038/srep14023. PMC 4650596. PMID 26354898.
- ^ a b Benson & Clawson 2000
- ^ a b Rascio, N.; La Rocca, N. (2013-01-01), "Biological Nitrogen Fixation☆", Reference Module in Earth Systems and Environmental Sciences, Elsevier, ISBN 978-0-12-409548-9, retrieved 2024-03-08
- ^ a b c Wall 2000
- ^ a b Shen, Defeng; Bisseling, Ton (2020), Kloc, Malgorzata (ed.), "The Evolutionary Aspects of Legume Nitrogen–Fixing Nodule Symbiosis", Symbiosis: Cellular, Molecular, Medical and Evolutionary Aspects, vol. 69, Cham: Springer International Publishing, pp. 387–408, doi:10.1007/978-3-030-51849-3_14, ISBN 978-3-030-51849-3, PMID 33263880, retrieved 2024-03-15
- ^ Kumari, Rima (2023). "Advances in plant-pathogen interactions in terms of biochemical and molecular aspects". Chapter 6 - Advances in plant-pathogen interactions in terms of biochemical and molecular aspects. pp. 111–122. doi:10.1016/B978-0-323-91875-6.00021-9. ISBN 978-0-323-91875-6. Retrieved March 15, 2023.
- ^ Wang, Zhen; Zhao, Fenglan; Wei, Panpan; Chai, Xiaoyun; Hou, Guige; Meng, Qingguo (2022-12-06). "Phytochemistry, health benefits, and food applications of sea buckthorn (Hippophae rhamnoides L.): A comprehensive review". Frontiers in Nutrition. 9: 1036295. doi:10.3389/fnut.2022.1036295. ISSN 2296-861X. PMC 9763470. PMID 36562043.
- ^ Diagne, Nathalie; Arumugam, Karthikeyan; Ngom, Mariama; Nambiar-Veetil, Mathish; Franche, Claudine; Narayanan, Krishna Kumar; Laplaze, Laurent (2013-11-11). "Use of Frankia and Actinorhizal Plants for Degraded Lands Reclamation". BioMed Research International. 2013: e948258. doi:10.1155/2013/948258. ISSN 2314-6133. PMC 3844217. PMID 24350296.
- ^ Normand, Philippe; Lapierre, Pascal; Tisa, Louis S.; Gogarten, Johann Peter; Alloisio, Nicole; Bagnarol, Emilie; Bassi, Carla A.; Berry, Alison M.; Bickhart, Derek M.; Choisne, Nathalie; Couloux, Arnaud; Cournoyer, Benoit; Cruveiller, Stephane; Daubin, Vincent; Demange, Nadia (January 2007). "Genome characteristics of facultatively symbiotic Frankia sp. strains reflect host range and host plant biogeography". Genome Research. 17 (1): 7–15. doi:10.1101/gr.5798407. ISSN 1088-9051. PMC 1716269. PMID 17151343.
- ^ a b c Schwintzer & Tjepkema 1990
- ^ Restoration, Society for Ecological. "Society for Ecological Restoration (SER)". Society for Ecological Restoration. Retrieved 2024-03-15.
- ^ Zavitovski & Newton 1968
- ^ Kistner & Parniske 2002
- ^ a b Ferguson, Brett J.; Lin, Meng-Han; Gresshoff, Peter M. (2013-03-01). "Regulation of legume nodulation by acidic growth conditions". Plant Signaling & Behavior. 8 (3): e23426. Bibcode:2013PlSiB...8E3426F. doi:10.4161/psb.23426. ISSN 1559-2316. PMC 3676511. PMID 23333963.
- ^ a b c Pawlowski, Katharina; Demchenko, Kirill N. (October 2012). "The diversity of actinorhizal symbiosis". Protoplasma. 249 (4): 967–979. doi:10.1007/s00709-012-0388-4. ISSN 1615-6102. PMID 22398987. S2CID 254082345.
- ^ Hocher, Valérie; Auguy, Florence; Argout, Xavier; Laplaze, Laurent; Franche, Claudine; Bogusz, Didier (February 2006). "Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root". New Phytologist. 169 (4): 681–688. doi:10.1111/j.1469-8137.2006.01644.x. ISSN 0028-646X. PMID 16441749.
- ^ Gherbi, Hassen; Markmann, Katharina; Svistoonoff, Sergio; Estevan, Joan; Autran, Daphné; Giczey, Gabor; Auguy, Florence; Péret, Benjamin; Laplaze, Laurent; Franche, Claudine; Parniske, Martin; Bogusz, Didier (2008-03-25). "SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria". Proceedings of the National Academy of Sciences. 105 (12): 4928–4932. doi:10.1073/pnas.0710618105. ISSN 0027-8424. PMC 2290763. PMID 18316735.
- ^ Bethencourt, Lorine; Vautrin, Florian; Taib, Najwa; Dubost, Audrey; Castro-Garcia, Lucia; Imbaud, Olivier; Abrouk, Danis; Fournier, Pascale; Briolay, Jérôme; Nguyen, Agnès; Normand, Philippe; Fernandez, Maria P.; Brochier-Armanet, Céline; Herrera-Belaroussi, Aude (2019). "Draft genome sequences for three unisolated Alnus-infective Frankia Sp+ strains, AgTrS, AiOr and AvVan, the first sequenced Frankia strains able to sporulate in-planta". Journal of Genomics. 7: 50–55. doi:10.7150/jgen.35875. PMC 6775861. PMID 31588247.
References
edit- Wall, L. (2000), "The actinorhizal symbiosis", Journal of Plant Growth and Regulation, 19 (2): 167–182, doi:10.1007/s003440000027, hdl:11336/71779, PMID 11038226, S2CID 12887261
- Schwintzer, C. R.; Tjepkema, J. (1990), The Biology of Frankia and Actinorhizal Plants, Academic Press, ISBN 978-0-12-633210-0
- Benson, D. R.; Clawson, M. L. (2000), "Evolution of the actinorhizal plant nitrogen-fixing symbiosis", in Triplett, E. (ed.), Prokaryotic Nitrogen Fixation: A Model System for the Analysis of a Biological Process, Norfolk, UK: Horizon Scientific Press, pp. 207–224, ISBN 978-1-898486-19-0
- Zavitovski, J.; Newton, M. (1968), "Ecological importance of snowbrush Ceanothus velutinus in the Oregon cascade", Ecology, 49 (6): 1134–1145, Bibcode:1968Ecol...49.1134Z, doi:10.2307/1934497, JSTOR 1934497
- Kistner, C.; Parniske, M. (2002), "Evolution of signal transduction in intracellular symbiosis", Trends in Plant Science, 7 (11): 511–518, doi:10.1016/S1360-1385(02)02356-7, PMID 12417152
- Laplaze, L.; Duhoux, E.; Franche, C.; Frutz, T.; Svistoonoff, S.; Bisseling, T.; Bogusz, D.; Pawlowski, K. (2000), "Casuarina glauca prenodule cells display the same differentiation as the corresponding nodule cells", Molecular Plant-Microbe Interactions, 13 (1): 107–112, doi:10.1094/MPMI.2000.13.1.107, PMID 10656591
- Vessey, J. K.; Pawlowski, K.; Bergman, B. (2005), "Root-based N2-fixing symbioses: Legumes, actinorhizal plants, Parasponia sp. and cycads", Plant and Soil, 266 (1): 205–230, Bibcode:2005PlSoi.266..205V, doi:10.1007/s11104-005-0871-1, S2CID 35247396
- Gherbi, H.; Markmann, K.; Svistoonoff, S.; Estevan, J.; Autran, D.; Giczey, G.; Auguy, F.; Péret, B.; Laplaze, L.; Franche, C.; Parniske, M.; Bogusz, D. (2008), "SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria", Proceedings of the National Academy of Sciences, 105 (12): 4928–4932, doi:10.1073/pnas.0710618105, PMC 2290763, PMID 18316735
- Hocher, V.; Auguy, F.; Argout, X.; Laplaze, L.; Franche, C.; Bogusz, D. (2006), "Expressed sequence-tag analysis in Casuarina glauca actinorhizal nodule and root", New Phytologist, 169 (4): 681–688, doi:10.1111/j.1469-8137.2006.01644.x, PMID 16441749
- Normand, P.; Lapierre, P.; Tisa, L. S.; Gogarten, J. P.; Alloisio, N.; Bagnarol, E.; Bassi, C. A.; Berry, A. M.; Bickhart, D. M.; Choisne, N.; Couloux, A.; Cournoyer, B.; Cruveiller, S.; Daubin, V.; Demange, N.; Francino, M. P.; Goltsman, E.; Huang, Y.; Kopp, O. R.; Labarre, L.; Lapidus, A.; Lavire, C.; Marechal, J.; Martinez, M.; Mastronunzio, J. E.; Mullin, B. C.; Niemann, J.; Pujic, P.; Rawnsley, T.; Rouy, Z. (2006). "Genome characteristics of facultatively symbiotic Frankia sp. Strains reflect host range and host plant biogeography". Genome Research. 17 (1): 7–15. doi:10.1101/gr.5798407. PMC 1716269. PMID 17151343.
External links
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