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Actinorhizal plant

April 12, 2024

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 edit

Actinorhizal plants are dicotyledons distributed within 3 orders,[1] 8 families and 26 genera, of the angiosperm clade.[5][2]: Table S1 

 
Frankia Root Nodule from Alder Tree (Alnus)

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 edit

 
The distribution of actinorhizal plants.

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 edit

 
Evolutionary origin of nitrogen-fixing nodulation

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 edit

As 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

  1. ^ a b "Angiosperm Phylogeny Website". www.mobot.org. Retrieved 2024-03-07.
  2. ^ 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.
  3. ^ a b Benson & Clawson 2000
  4. ^ 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
  5. ^ a b c Wall 2000
  6. ^ 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
  7. ^ 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.
  8. ^ 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.
  9. ^ 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.
  10. ^ 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.
  11. ^ a b c Schwintzer & Tjepkema 1990
  12. ^ Restoration, Society for Ecological. "Society for Ecological Restoration (SER)". Society for Ecological Restoration. Retrieved 2024-03-15.
  13. ^ Zavitovski & Newton 1968
  14. ^ Kistner & Parniske 2002
  15. ^ 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.
  16. ^ 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.
  17. ^ 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.
  18. ^ 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.
  19. ^ 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 edit

 
Wikimedia Commons has media related to Actinorhizal plants.
 
Look up actinorhizal plant in Wiktionary, the free dictionary.
 
Scholia has a profile for actinorhizal plant (Q422276).

    April 12, 2024
    actinorhizal, plant, group, angiosperms, characterized, their, ability, form, symbiosis, with, nitrogen, fixing, actinomycetota, frankia, this, association, leads, formation, nitrogen, fixing, root, nodules, distributed, within, three, clades, characterized, n. 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 Contents 1 Classification 2 Distribution and ecology 3 Evolutionary origin 4 The symbiotic nodules 5 Notes 6 References 7 External linksClassification editActinorhizal plants are dicotyledons distributed within 3 orders 1 8 families and 26 genera of the angiosperm clade 5 2 Table S1 Classification Order Familiy GeneraThe Clade Angiosperm Actinorhizal Plants Cucurbitales Coriariaceae CoriariaDatiscaceae DatiscaFagales Betulaceae AlnusCasuarinaceae AllocasuarinaCasuarinaCeuthostomaGymnostomaMyricaceae ComptoniaMyricaRosales Elaeagnaceae ElaeagnusHippophaeShepherdiaRhamnaceae AdolphiaColletiaDiscariaKentrothamnusRetanillaTalgueneaTrevoaOchetophilaCeanothusRosaceae CercocarpusChamaebatiaCowaniaDryasPurshiaLegumes Fabales Fabaceae CaesalpiniaCercisDetariumDialiumDuparquetiaFaboideaePolygalaceae PolygalaQuillajaceae DakotanthusQuillajaSurianaceae Suriana nbsp Frankia Root Nodule from Alder Tree Alnus 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 edit nbsp The distribution of actinorhizal plants 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 edit nbsp Evolutionary origin of nitrogen fixing nodulationNo 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 amp 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 amp Tjepkema 1990 Restoration Society for Ecological Society for Ecological Restoration SER Society for Ecological Restoration Retrieved 2024 03 15 Zavitovski amp Newton 1968 Kistner amp 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 amp 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 Valerie 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 Daphne Giczey Gabor Auguy Florence Peret 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 Jerome Nguyen Agnes Normand Philippe Fernandez Maria P Brochier Armanet Celine 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 editWall 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 12887261Schwintzer C R Tjepkema J 1990 The Biology ofFrankiaand Actinorhizal Plants Academic Press ISBN 978 0 12 633210 0Benson 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 0Zavitovski 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 1934497Kistner 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 12417152Laplaze 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 10656591Vessey 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 35247396Gherbi H Markmann K Svistoonoff S Estevan J Autran D Giczey G Auguy F Peret 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 18316735Hocher 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 16441749Normand 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 edit nbsp Wikimedia Commons has media related to Actinorhizal plants nbsp Look up actinorhizal plant in Wiktionary the free dictionary nbsp Scholia has a profile for actinorhizal plant Q422276 Frankia and Actinorhizal plant Website Retrieved from https en wikipedia org w index php title Actinorhizal plant amp oldid 1216230786, wikipedia, wiki, book, books, library,

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