Actinorhizal plant

Last updated

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.

Contents

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

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

ClassificationOrderFamiliyGenera
The Clade Angiosperm Actinorhizal Plants Cucurbitales Coriariaceae Coriaria
Datiscaceae Datisca
Fagales Betulaceae Alnus
Casuarinaceae Allocasuarina
Casuarina
Ceuthostoma
Gymnostoma
Myricaceae Comptonia
Myrica
Rosales Elaeagnaceae Elaeagnus
Hippophae
Shepherdia
Rhamnaceae Adolphia
Colletia
Discaria
Kentrothamnus
Retanilla
Talguenea
Trevoa
Ochetophila
Ceanothus
Rosaceae Cercocarpus
Chamaebatia
Cowania
Dryas
Purshia
Legumes Fabales Fabaceae Caesalpinia
Cercis
Detarium
Dialium
Duparquetia
Faboideae
Polygalaceae Polygala
Quillajaceae Dakotanthus
Quillaja
Surianaceae Suriana
Frankia Root Nodule from Alder Tree (Alnus) A sectioned alder root nodule gall.JPG
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

The distribution of actinorhizal plants. Actinorhizal Plant Distribution.svg
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

Evolutionary origin of nitrogen-fixing nodulation ArbreDicots.jpg
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

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

  1. 1 2 "Angiosperm Phylogeny Website". www.mobot.org. Retrieved 2024-03-07.
  2. 1 2 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. 1 2 Benson & Clawson 2000
  4. 1 2 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. 1 2 3 Wall 2000
  6. 1 2 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. 1 2 3 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. 1 2 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. 1 2 3 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.

Related Research Articles

Nitrogen fixation is a chemical process by which molecular nitrogen (N
2
), which has a strong triple covalent bond, is converted into ammonia (NH
3
) or related nitrogenous compounds, typically in soil or aquatic systems but also in industry. The nitrogen in air is molecular dinitrogen, a relatively nonreactive molecule that is metabolically useless to all but a few microorganisms. Biological nitrogen fixation or diazotrophy is an important microbe-mediated process that converts dinitrogen (N2) gas to ammonia (NH3) using the nitrogenase protein complex (Nif).

<span class="mw-page-title-main">Mycorrhiza</span> Fungus-plant symbiotic association

A mycorrhiza is a symbiotic association between a fungus and a plant. The term mycorrhiza refers to the role of the fungus in the plant's rhizosphere, its root system. Mycorrhizae play important roles in plant nutrition, soil biology, and soil chemistry.

<span class="mw-page-title-main">Leghemoglobin</span> Phytoglobin

Leghemoglobin is an oxygen-carrying phytoglobin found in the nitrogen-fixing root nodules of leguminous plants. It is produced by these plants in response to the roots being colonized by nitrogen-fixing bacteria, termed rhizobia, as part of the symbiotic interaction between plant and bacterium: roots not colonized by Rhizobium do not synthesise leghemoglobin. Leghemoglobin has close chemical and structural similarities to hemoglobin, and, like hemoglobin, is red in colour. It was originally thought that the heme prosthetic group for plant leghemoglobin was provided by the bacterial symbiont within symbiotic root nodules. However, subsequent work shows that the plant host strongly expresses heme biosynthesis genes within nodules, and that activation of those genes correlates with leghemoglobin gene expression in developing nodules.

<span class="mw-page-title-main">Rhizobia</span> Nitrogen fixing soil bacteria

Rhizobia are diazotrophic bacteria that fix nitrogen after becoming established inside the root nodules of legumes (Fabaceae). To express genes for nitrogen fixation, rhizobia require a plant host; they cannot independently fix nitrogen. In general, they are gram negative, motile, non-sporulating rods.

<span class="mw-page-title-main">Casuarinaceae</span> Family of plants

The Casuarinaceae are a family of dicotyledonous flowering plants placed in the order Fagales, consisting of four genera and 91 species of trees and shrubs native to eastern Africa, Australia, Southeast Asia, Malesia, Papuasia, and the Pacific Islands. At one time, all species were placed in the genus Casuarina. Lawrence Alexander Sidney Johnson separated out many of those species and renamed them into the new genera of Gymnostoma in 1980 and 1982, Allocasuarina in 1982, and Ceuthostoma in 1988, with some additional formal descriptions of new species in each other genus. At the time, it was somewhat controversial. The monophyly of these genera was later supported in a 2003 phylogenetic study of the family. In the Wettstein system, this family was the only one placed in the order Verticillatae. Likewise, in the Engler, Cronquist, and Kubitzki systems, the Casuarinaceae were the only family placed in the order Casuarinales.

Diazotrophs are bacteria and archaea that fix atmospheric nitrogen(N2) in the atmosphere into bioavailable forms such as ammonia.

<i>Ensifer meliloti</i> Species of bacterium

Ensifer meliloti are an aerobic, Gram-negative, and diazotrophic species of bacteria. S. meliloti are motile and possess a cluster of peritrichous flagella. S. meliloti fix atmospheric nitrogen into ammonia for their legume hosts, such as alfalfa. S. meliloti forms a symbiotic relationship with legumes from the genera Medicago, Melilotus and Trigonella, including the model legume Medicago truncatula. This symbiosis promotes the development of a plant organ, termed a root nodule. Because soil often contains a limited amount of nitrogen for plant use, the symbiotic relationship between S. meliloti and their legume hosts has agricultural applications. These techniques reduce the need for inorganic nitrogenous fertilizers.

<span class="mw-page-title-main">Root nodule</span> Plant part

Root nodules are found on the roots of plants, primarily legumes, that form a symbiosis with nitrogen-fixing bacteria. Under nitrogen-limiting conditions, capable plants form a symbiotic relationship with a host-specific strain of bacteria known as rhizobia. This process has evolved multiple times within the legumes, as well as in other species found within the Rosid clade. Legume crops include beans, peas, and soybeans.

<span class="mw-page-title-main">Nod factor</span> Signaling molecule

Nod factors, are signaling molecules produced by soil bacteria known as rhizobia in response to flavonoid exudation from plants under nitrogen limited conditions. Nod factors initiate the establishment of a symbiotic relationship between legumes and rhizobia by inducing nodulation. Nod factors produce the differentiation of plant tissue in root hairs into nodules where the bacteria reside and are able to fix nitrogen from the atmosphere for the plant in exchange for photosynthates and the appropriate environment for nitrogen fixation. One of the most important features provided by the plant in this symbiosis is the production of leghemoglobin, which maintains the oxygen concentration low and prevents the inhibition of nitrogenase activity.

<i>Frankia</i> Genus of bacteria

Frankia is a genus of nitrogen-fixing bacteria that live in symbiosis with actinorhizal plants, similar to the Rhizobium bacteria found in the root nodules of legumes in the family Fabaceae. Frankia also initiate the forming of root nodules.

<span class="mw-page-title-main">Rhizosphere</span> Region of soil or substrate comprising the root microbiome

The rhizosphere is the narrow region of soil or substrate that is directly influenced by root secretions and associated soil microorganisms known as the root microbiome. Soil pores in the rhizosphere can contain many bacteria and other microorganisms that feed on sloughed-off plant cells, termed rhizodeposition, and the proteins and sugars released by roots, termed root exudates. This symbiosis leads to more complex interactions, influencing plant growth and competition for resources. Much of the nutrient cycling and disease suppression by antibiotics required by plants occurs immediately adjacent to roots due to root exudates and metabolic products of symbiotic and pathogenic communities of microorganisms. The rhizosphere also provides space to produce allelochemicals to control neighbours and relatives.

Symbiotic bacteria are bacteria living in symbiosis with another organism or each other. For example, rhizobia living in root nodules of legumes provide nitrogen fixing activity for these plants.

<i>Chamaebatia</i> Genus of evergreen shrubs in the rose family

Chamaebatia, also known as mountain misery, is a genus of two species of aromatic evergreen shrubs endemic to California. Its English common name derives from early settlers' experience with the plant's dense tangle and sticky, strong-smelling resin. They are actinorhizal, non-legumes capable of nitrogen fixation through symbiosis with the actinobacterium, Frankia.

<i>Bradyrhizobium</i> Genus of bacteria

Bradyrhizobium is a genus of Gram-negative soil bacteria, many of which fix nitrogen. Nitrogen fixation is an important part of the nitrogen cycle. Plants cannot use atmospheric nitrogen (N2); they must use nitrogen compounds such as nitrates.

<i>Casuarina glauca</i> Species of tree

Casuarina glauca, commonly known as swamp she-oak, swamp buloke, swamp she-oak, marsh sheoak, grey she-oak, grey she-oak, native pine, or guman by the Gadigal people, is a species of flowering plant that is endemic to eastern Australia. It is a dioecious tree that often forms root suckers and has fissured and scaly bark, spreading or drooping branchlets, the leaves reduced to scales in whorls of 12 to 20, the fruit 9–18 mm (0.35–0.71 in) long containing winged seeds (samaras) 3.5–5.0 mm (0.14–0.20 in) long.

<span class="mw-page-title-main">Flavan</span> Chemical compound

The flavans are benzopyran derivatives that use the 2-phenyl-3,4-dihydro-2H-chromene skeleton. They may be found in plants. These compounds include the flavan-3-ols, flavan-4-ols and flavan-3,4-diols (leucoanthocyanidin).

<i>Frankia alni</i> Species of bacterium

Frankia alni is a Gram-positive species of actinomycete filamentous bacterium that lives in symbiosis with actinorhizal plants in the genus Alnus. It is a nitrogen-fixing bacterium and forms nodules on the roots of alder trees.

Mesorhizobium loti, formerly known as Rhizobium loti, is a Gram negative species of bacteria found in the root nodules of many plant species. Its name is a reference to Lotus corniculatus, a flowering plant from which it was originally isolated.

Martin Parniske is a German biologist with a specialisation in genetics, microbiology and biochemistry. He is university professor and head of the Institute of Genetics at the Faculty of Biology of the Ludwig Maximilian University of Munich. Parniske's scientific focus is on the molecular interaction between plants and symbiotic and pathogenic organisms including bacteria, fungi, oomycetes and insects.

<span class="mw-page-title-main">Symbiosome</span>

A symbiosome is a specialised compartment in a host cell that houses an endosymbiont in a symbiotic relationship.

References