Actinorhizal plant
Encyclopedia
Actinorhizal plants are a group of angiosperms characterized by their ability to form a symbiosis
with the nitrogen fixing actinobacteria
Frankia
. This association leads to the formation of nitrogen-fixing root nodules.
s distributed among four angiosperm orders
(Fagales
, Cucurbitales
, Fabales
and Rosales
), 8 families
and 24 genera
(Betulaceae
: Alnus
; Casuarinaceae
: Gymnostoma, Casuarina
, Allocasuarina
, Ceuthostoma; Coriariaceae: Coriaria
; Datiscaceae
: Datisca, Elaeagnaceae
: Eleagnus, Hippophae, Shepherdia; Myricaceae
: Myrica
, Comptonia
; Rhamnaceae
: Colletia
, Discaria
, Kenthrothammus, Retanilla, Talguenea, Trevoa
, Ceanothus
; Rosaceae
: Dryas
, Purshia
, Cowania, Cercocarpus, Chamaebatia
). Actinorhizal species are trees or shrubs, except for the genus Datisca.
Many are common plants in temperate regions like alder
, bayberry
, sweetfern
, Avens
, mountain misery and Coriaria
. Some Elaeagnus
species and Sea-buckthorn
s produce edible fruit. In tropical regions, Casuarina
s are widely cultivated, becoming invasive species
in some areas like Casuarina glauca
in Florida
.
that colonize young soils where available nitrogen is scarce like moraine
s, volcanic flows or sand dunes. Being among the first species to colonize these disturbed environments, actinorhizal shrubs and trees play a critical role, enriching the soil and enabling the establishment of other species in an ecological succession
. Actinorhizal plants like alders are also common in the riparian forest
.
Actinorhizal plants are the major contributors to nitrogen fixation in broad areas of the world, and are particularly important in temperate forests. The nitrogen fixation rate measured for some alder species is as high as 300 kg of N2/ha/year, close to the highest rate reported in Legumes.
s. Nevertheless, actinorhizal plants and Legumes, the two major nitrogen-fixing groups of plants share a relatively close ancestor, as they all part of a clade
within the rosids which is often called the nitrogen-fixing clade. This ancestor may have developed a "predisposition" to enter in 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 mycorrhiza
l symbioses, a much older and widely distributed symbiotic association between plants and fungi.
and is followed by the formation of a primitive symbiotic organ lacking any particular organization, a prenodule. 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. 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. This organ is the actinorhizal nodule also called actinorhizae. Cortical cells of the nodule are invaded by Frankia filaments coming from the site of infection or the prenodule. Actinorhizal nodules have generally an indeterminate growth, new cells are therefore continually produced at the apex and successively become infected. Mature cells of the nodule are filled with bacterial filaments that actively fix nitrogen.
Little information is available concerning the mechanisms leading to nodulation. No equivalent of the rhizobial Nod factor
s have been found, but several genes known to participate in the formation and functioning of Legume nodules (coding for heamoglobin and other nodulins) are also found in actinorhizal plants where they are supposed to play similar roles. 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 should help to a far better understanding in the following years.
Symbiosis
Symbiosis is close and often long-term interaction between different biological species. In 1877 Bennett used the word symbiosis to describe the mutualistic relationship in lichens...
with the nitrogen fixing actinobacteria
Actinobacteria
Actinobacteria are a group of Gram-positive bacteria with high guanine and cytosine content. They can be terrestrial or aquatic. Actinobacteria is one of the dominant phyla of the bacteria....
Frankia
Frankia
Frankia is a genus of nitrogen fixing, filamentous bacteria that live in symbiosis with actinorhizal plants, similar to the Rhizobia bacteria that are found in the root nodules of legumes in the Fabaceae family. Bacteria of this genus also form root nodules.The genus Frankia was originally named by...
. This association leads to the formation of nitrogen-fixing root nodules.
Classification
Actinorhizal plants are dicotyledonDicotyledon
The dicotyledons, also known as dicots, are a group of flowering plants whose seed typically has two embryonic leaves or cotyledons. There are around 199,350 species within this group...
s distributed among four angiosperm orders
Order (biology)
In scientific classification used in biology, the order is# a taxonomic rank used in the classification of organisms. Other well-known ranks are life, domain, kingdom, phylum, class, family, genus, and species, with order fitting in between class and family...
(Fagales
Fagales
The Fagales are an order of flowering plants, including some of the best known trees. The order name is derived from genus Fagus, Beeches. They belong among the rosid group of dicotyledons...
, Cucurbitales
Cucurbitales
The Cucurbitales are an order of flowering plants, included in the rosid group of dicotyledons. This order mostly belongs to tropical areas, with limited presence in subtropic and temperate regions. The order includes shrubs and trees, together with many herbs and climbers...
, Fabales
Fabales
Fabales is an order of flowering plants. It is included in the rosid group of the eudicots in the Angiosperm Phylogeny Group II classification system...
and Rosales
Rosales
Rosales is an order of flowering plants. It is one of the four orders in the nitrogen fixing clade of the fabids and is sister to a clade consisting of Fagales and Cucurbitales. It contains about 7700 species, distributed into about 260 genera. Rosales comprises nine families, the type family...
), 8 families
Family (biology)
In biological classification, family is* a taxonomic rank. Other well-known ranks are life, domain, kingdom, phylum, class, order, genus, and species, with family fitting between order and genus. As for the other well-known ranks, there is the option of an immediately lower rank, indicated by the...
and 24 genera
Genus
In biology, a genus is a low-level taxonomic rank used in the biological classification of living and fossil organisms, which is an example of definition by genus and differentia...
(Betulaceae
Betulaceae
Betulaceae, or the Birch Family, includes six genera of deciduous nut-bearing trees and shrubs, including the birches, alders, hazels, hornbeams and hop-hornbeams, numbering about 130 species...
: Alnus
Alder
Alder is the common name of a genus of flowering plants belonging to the birch family . The genus comprises about 30 species of monoecious trees and shrubs, few reaching large size, distributed throughout the North Temperate Zone and in the Americas along the Andes southwards to...
; Casuarinaceae
Casuarinaceae
Casuarinaceae is a family of dicotyledonous flowering plants placed in the order Fagales, consisting of 3 or 4 genera and approximately 70 species of trees and shrubs native to the Old World tropics , Australia, and the Pacific Islands...
: Gymnostoma, Casuarina
Casuarina
Casuarina is a genus of 17 species in the family Casuarinaceae, native to Australasia, southeast Asia, and islands of the western Pacific Ocean. It was once treated as the sole genus in the family, but has been split into three genera .They are evergreen shrubs and trees growing to 35 m tall...
, Allocasuarina
Allocasuarina
Allocasuarina is a genus of trees in the flowering plant family Casuarinaceae. They are endemic to Australia, occurring primarily in the south. Like the closely related genus Casuarina, they are commonly called sheoaks or she-oaks, they are notable for their long, segmented branchlets that...
, Ceuthostoma; Coriariaceae: Coriaria
Coriaria
Coriaria is the sole genus in the family Coriariaceae. It includes about 30 species of subshrubs, shrubs and small trees, with a widespread but disjunct distribution across warm temperate regions of the world, occurring as far apart as the Mediterranean region, southern and eastern Asia, New...
; Datiscaceae
Datiscaceae
Datiscaceae are a family of Dicotyledonous plants, containing two species of the genus Datisca. Two other genera, Octomeles and Tetrameles are now classified in the Tetramelaceae family....
: Datisca, Elaeagnaceae
Elaeagnaceae
Elaeagnaceae, the oleaster family, is a plant family of the order Rosales comprising small trees and shrubs, native to temperate regions of the Northern Hemisphere, south into tropical Asia and Australia. The family has 45-50 species in three genera....
: Eleagnus, Hippophae, Shepherdia; Myricaceae
Myricaceae
The Myricaceae is a small family of dicotyledonous shrubs and small trees in the order Fagales. There are three genera in the family, although some botanists separate many species from Myrica into a fourth genus Morella...
: Myrica
Myrica
Myrica is a genus of about 35–50 species of small trees and shrubs in the family Myricaceae, order Fagales. The genus has a wide distribution, including Africa, Asia, Europe, North America and South America, and missing only from Australasia...
, Comptonia
Comptonia
Comptonia is a monotypic genus in the family Myricaceae, order Fagales. It is native to eastern North America, from southern Quebec south to the extreme north of Georgia, and west to Minnesota. The common name is Sweetfern or Sweet-fern, a confusing name as it is not a fern.It is a deciduous...
; Rhamnaceae
Rhamnaceae
Rhamnaceae, the Buckthorn family, is a large family of flowering plants, mostly trees, shrubs and some vines.The family contains 50-60 genera and approximately 870-900 species. The Rhamnaceae have a worldwide distribution, but are more common in the subtropical and tropical regions...
: Colletia
Colletia
Colletia is a genus of flowering plants in the family Rhamnaceae, with 15 to 17 species of spiny shrubs. All species of this genus are native to southern South America. They are non-legume nitrogen fixers.-Selected species:*Colletia armata...
, Discaria
Discaria
Discaria is a genus of about 12 species of flowering plants in the family Rhamnaceae, native to temperate regions of the Southern Hemisphere, in Australia, New Zealand and South America....
, Kenthrothammus, Retanilla, Talguenea, Trevoa
Trevoa
Trevoa is a genus of actinorhizal plants; these dicotyledon flora are trees or small shrubs. The genus was first proposed by Miers in 1825, but was not fully described until 1830 by Sir William Jackson Hooker. Genus members are notable for their ability to fix nitrogen. Species of this genus are...
, Ceanothus
Ceanothus
Ceanothus L. is a genus of about 50–60 species of shrubs or small trees in the buckthorn family Rhamnaceae. The genus is confined to North America, the center of its distribution in California, with some species in the eastern United States and southeast Canada, and others extending as far south...
; Rosaceae
Rosaceae
Rosaceae are a medium-sized family of flowering plants, including about 2830 species in 95 genera. The name is derived from the type genus Rosa. Among the largest genera are Alchemilla , Sorbus , Crataegus , Cotoneaster , and Rubus...
: Dryas
Dryas (plant)
Dryas is a genus of dwarf perennial herbaceous plants in the rose family Rosaceae, native to the arctic and alpine regions of Europe, Asia and North America. The genus is named after the Greek nymph Dryas. The classification of Dryas within the Rosaceae has been unclear...
, Purshia
Purshia
Purshia is a small genus of 5-8 species of flowering plants in the family Rosaceae, native to western North America, where they grow in dry climates from southeast British Columbia in Canada south throughout the western United States to northern Mexico. The classification of Purshia within the...
, Cowania, Cercocarpus, Chamaebatia
Chamaebatia
The plant genus Chamaebatia includes two species of aromatic evergreen shrubs known as mountain misery. This common name in English refers to the strong aroma resulting from brushing against the foliage...
). Actinorhizal species are trees or shrubs, except for the genus Datisca.
Many are common plants in temperate regions like alder
Alder
Alder is the common name of a genus of flowering plants belonging to the birch family . The genus comprises about 30 species of monoecious trees and shrubs, few reaching large size, distributed throughout the North Temperate Zone and in the Americas along the Andes southwards to...
, bayberry
Myrica
Myrica is a genus of about 35–50 species of small trees and shrubs in the family Myricaceae, order Fagales. The genus has a wide distribution, including Africa, Asia, Europe, North America and South America, and missing only from Australasia...
, sweetfern
Comptonia
Comptonia is a monotypic genus in the family Myricaceae, order Fagales. It is native to eastern North America, from southern Quebec south to the extreme north of Georgia, and west to Minnesota. The common name is Sweetfern or Sweet-fern, a confusing name as it is not a fern.It is a deciduous...
, Avens
Dryas (plant)
Dryas is a genus of dwarf perennial herbaceous plants in the rose family Rosaceae, native to the arctic and alpine regions of Europe, Asia and North America. The genus is named after the Greek nymph Dryas. The classification of Dryas within the Rosaceae has been unclear...
, mountain misery and Coriaria
Coriaria
Coriaria is the sole genus in the family Coriariaceae. It includes about 30 species of subshrubs, shrubs and small trees, with a widespread but disjunct distribution across warm temperate regions of the world, occurring as far apart as the Mediterranean region, southern and eastern Asia, New...
. Some Elaeagnus
Elaeagnus
Elaeagnus , silverberry or oleaster, is a genus of about 50–70 species of flowering plants in the family Elaeagnaceae.The vast majority of the species are native to temperate and subtropical regions of Asia. Elaeagnus triflora extends from Asia south into northeastern Australia, while E...
species and Sea-buckthorn
Sea-buckthorn
The sea-buckthorns are deciduous shrubs in the genus Hippophae, family Elaeagnaceae. The name sea-buckthorn is hyphenated here to avoid confusion with the buckthorns...
s produce edible fruit. In tropical regions, Casuarina
Casuarina
Casuarina is a genus of 17 species in the family Casuarinaceae, native to Australasia, southeast Asia, and islands of the western Pacific Ocean. It was once treated as the sole genus in the family, but has been split into three genera .They are evergreen shrubs and trees growing to 35 m tall...
s are widely cultivated, becoming invasive species
Invasive species
"Invasive species", or invasive exotics, is a nomenclature term and categorization phrase used for flora and fauna, and for specific restoration-preservation processes in native habitats, with several definitions....
in some areas like Casuarina glauca
Casuarina glauca
Casuarina glauca, commonly known as the swamp she-oak, is a species of Casuarina native to the east coast of Australia. It is found from central Queensland south to southern New South Wales. It has become naturalised in the Everglades in Florida where it is considered a weed.The larvae of the...
in Florida
Florida
Florida is a state in the southeastern United States, located on the nation's Atlantic and Gulf coasts. It is bordered to the west by the Gulf of Mexico, to the north by Alabama and Georgia and to the east by the Atlantic Ocean. With a population of 18,801,310 as measured by the 2010 census, it...
.
Distribution and ecology
Actinorhizal plants are found on all continents except for Antarctica. Their ability to form nitrogen-fixing nodules confers a selective advantage in poor soils. Most actinorhizal plants are therefore pioneer speciesPioneer species
Pioneer species are species which colonize previously uncolonized land, usually leading to ecological succession. They are the first organisms to start the chain of events leading to a livable biosphere or ecosystem...
that colonize young soils where available nitrogen is scarce like moraine
Moraine
A moraine is any glacially formed accumulation of unconsolidated glacial debris which can occur in currently glaciated and formerly glaciated regions, such as those areas acted upon by a past glacial maximum. This debris may have been plucked off a valley floor as a glacier advanced or it may have...
s, volcanic flows or sand dunes. Being among the first species to colonize these disturbed environments, actinorhizal shrubs and trees play a critical role, enriching the soil and enabling the establishment of other species in an ecological succession
Ecological succession
Ecological succession, is the phenomenon or process by which a community progressively transforms itself until a stable community is formed. It is a fundamental concept in ecology, and refers to more or less predictable and orderly changes in the composition or structure of an ecological community...
. Actinorhizal plants like alders are also common in the riparian forest
Riparian forest
A riparian forest is a forested area of land adjacent to a body of water such as a river, stream, pond, lake, marshland, estuary, canal, sink or reservoir. -Etymology:...
.
Actinorhizal plants are the major contributors to nitrogen fixation in broad areas of the world, and are particularly important in temperate forests. The nitrogen fixation rate measured for some alder species is as high as 300 kg of N2/ha/year, close to the highest rate reported in Legumes.
Evolutionary origin
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 cladeClade
A clade is a group consisting of a species and all its descendants. In the terms of biological systematics, a clade is a single "branch" on the "tree of life". The idea that such a "natural group" of organisms should be grouped together and given a taxonomic name is central to biological...
s. Nevertheless, actinorhizal plants and Legumes, the two major nitrogen-fixing groups of plants share a relatively close ancestor, as they all part of a clade
Clade
A clade is a group consisting of a species and all its descendants. In the terms of biological systematics, a clade is a single "branch" on the "tree of life". The idea that such a "natural group" of organisms should be grouped together and given a taxonomic name is central to biological...
within the rosids which is often called the nitrogen-fixing clade. This ancestor may have developed a "predisposition" to enter in 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 mycorrhiza
Mycorrhiza
A mycorrhiza is a symbiotic association between a fungus and the roots of a vascular plant....
l symbioses, a much older and widely distributed symbiotic association between plants and fungi.
The symbiotic nodules
As in legumes, nodulation is favored by nitrogen deprivation and is inhibited by high nitrogen concentrations. 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 infection of a root hairRoot hair
A root hair, the rhizoid of a vascular plant, is a tubular outgrowth of a trichoblast, a hair-forming cell on the epidermis of a plant root. That is, root hairs are lateral extensions of a single cell and only rarely branched, thus invisible to the naked eye. They are found only in the region of...
and is followed by the formation of a primitive symbiotic organ lacking any particular organization, a prenodule. 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. 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. This organ is the actinorhizal nodule also called actinorhizae. Cortical cells of the nodule are invaded by Frankia filaments coming from the site of infection or the prenodule. Actinorhizal nodules have generally an indeterminate growth, new cells are therefore continually produced at the apex and successively become infected. Mature cells of the nodule are filled with bacterial filaments that actively fix nitrogen.
Little information is available concerning the mechanisms leading to nodulation. No equivalent of the rhizobial Nod factor
Nod factor
Nodulation factors are signaling molecules produced by bacteria known as rhizobia during the initiation of nodules on the root of legumes. A symbiosis is formed when legumes take up the bacteria...
s have been found, but several genes known to participate in the formation and functioning of Legume nodules (coding for heamoglobin and other nodulins) are also found in actinorhizal plants where they are supposed to play similar roles. 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
RNAI
RNAI is a non-coding RNA that is an antisense repressor of the replication of some E. coli plasmids, including ColE1. Plasmid replication is usually initiated by RNAII, which acts as a primer by binding to its template DNA. The complementary RNAI binds RNAII prohibiting it from its initiation role...
and genomic tools in actinorhizal species should help to a far better understanding in the following years.