Bacteria belonging to the genera Rhizobium, Mesorhizobium, Sinorhizobium, Bradyrhizobium, and Azorhizobium (collectively referred to as rhizobia) grow in the soil as free-living organisms but can also live as nitrogen-fixing symbionts inside root nodule cells of legume plants. The interactions between several rhizobial species and their host plants have become models for this type of nitrogen-fixing symbiosis. Temperate legumes such as alfalfa, pea, and vetch form indeterminate nodules that arise from root inner and middle cortical cells and grow out from the root via a persistent meristem. During the formation of functional indeterminate nodules, symbiotic bacteria must gain access to the interior of the host root. To get from the outside to the inside, rhizobia grow and divide in tubules called infection threads, which are composite structures derived from the two symbiotic partners. This review focuses on symbiotic infection and invasion during the formation of indeterminate nodules. It summarizes root hair growth, how root hair growth is influenced by rhizobial signaling molecules, infection of root hairs, infection thread extension down root hairs, infection thread growth into root tissue, and the plant and bacterial contributions necessary for infection thread formation and growth. The review also summarizes recent advances concerning the growth dynamics of rhizobial populations in infection threads.

Infection and Invasion of Roots by Symbiotic, Nitrogen-Fixing Rhizobia during Nodulation of Temperate Legumes

Rhizobium-legume nodulation: life together in the underground.

that are expressed before the onset of nitrogen fixation and are involved in infection and nodule development. The products of the late nodulin genes are involved in the interaction with the endosymbiont and in the metabolic specialization of the nodule (Nap and Bisseling, 1990). In the first part of this review, we describe the early steps of the interaction between rhizobia and legumes that result in the formation of a nitrogen-fixing nodule. We focus on the role of specific lipooligosaccharides secreted by rhizobia in the induction of these early steps. In the second part, we describe nodule functioning and compare actinorhizal and legume nodules.

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Symbiotic Nitrogen Fixation.

Nitrogen is generally considered one of the major limiting nutrients in plant growth. The biological process responsible for reduction of molecular nitrogen into ammonia is referred to as nitrogen fixation. A wide diversity of nitrogen-fixing bacterial species belonging to most phyla of the Bacteria domain have the capacity to colonize the rhizosphere and to interact with plants. Leguminous and actinorhizal plants can obtain their nitrogen by association with rhizobia or Frankia via differentiation on their respective host plants of a specialized organ, the root nodule. Other symbiotic associations involve heterocystous cyanobacteria, while increasing numbers of nitrogen-fixing species have been identified as colonizing the root surface and, in some cases, the root interior of a variety of cereal crops and pasture grasses. Basic and advanced aspects of these associations are covered in this review.

/pdf/nitrogen-fixing-bacteria-associated-with-leguminous-and-non-1gzxmeeigu.pdf

Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants

Elementary ecology texts tell us that organisms interact in three fundamental ways, generally given the names competition, predation, and mutualism. The third member has gotten short shrift (264), and even its name is not generally agreed on. Terms that may be considered synonyms, in whole or part, are symbiosis, commensalism, cooperation, protocooperation, mutual aid, facilitation, reciprocal altruism, and entraide. We use the term mutualism, defined as "an interaction between species that is beneficial to both," since it has both historical priority (311) and general currency. Symbiosis is "the living together of two organisms in close association," and modifiers are used to specify dependence on the interaction (facultative or obligate) and the range of species that can take part (oligophilic or polyphilic). We make the normal apologies concerning forcing continuous variation and diverse interactions into simple dichotomous classifications, for these and all subsequent definitions. Thus mutualism can be defined, in brief, as a -b/qinteraction, while competition, predation, and eommensalism are respectively -/-, -/q-, and -t-/0. There remains, however, the question of how to define "benefit to the

https://kuscholarworks.ku.edu/bitstream/handle/1808/677/annurev.es.13.110182.pdf?sequence=1

The Ecology of Mutualism

The soil actinomycete causing formation of nitrogen-fixing symbiotic nodules on roots of the woody angiosperm Comptonia peregrina (L.) Coult. (Myricaceae) has been isolated from surface-sterilized root nodules after incubation and enzyme maceration. The filamentous bacterium grows slowly in pure culture on a yeast extract medium, producing sporogenous bodies which form large numbers of ovoid spores. Reinfection of sand-grown or aeroponically grown seedlings of Comptonia was achieved repeatedly with inocula prepared from suspensions of the Comptonia isolate. The same actinomycete has been reisolated from these seedling nodules. The induced nodules are highly active in the acetylene-reduction assay, and plants grow vigorously without an exogenous supply of fixed nitrogen.

http://science.sciencemag.org/content/sci/199/4331/899.full.pdf

Isolation and Cultivation in vitro of the Actinomycete Causing Root Nodulation in Comptonia

Root hair infection of Trifolium repens L. by Rhizobium trifolii was investigated with regard to the structural basis of infection thread origin. Most infected root hairs were shown to have in comm...

/pdf/the-structural-basis-for-infection-of-root-hairs-of-47tpsw2l6y.pdf

The structural basis for infection of root hairs of Trifolium repens by Rhizobium

The infection process leading to the development of root nodules of Comptonia peregrina, Casuarina cunning hamiana, Myrica gale, and M cerifera was studied by light and electron microscopy. Deformed growth of root hairs was observed as early as 24 h after seedlings grown aeroponically or hydroponically were inoculated with suspensions of crushed nodules or cultures of the actinomycetous endophyte of Comptonia The extent of root hair deformation showed a positive correlation with the number of nodules which subsequently developed The essential features of infection in each of these species were very similar. The actinomycete entered a deformed root hair of the host in a region of folding of the cell wall A convoluted elaboration of the root hair wall which occurred at this presumptive penetration site was continuous with the more evenly deposited capsule of the endophytic actinomycete An associated feature of this wall deposition was thickening of the cell wall of the infected root hair and the adjacent pr...

Root Hair Infection in Actinomycete-Induced Root Nodule Initiation in Casuarina, Myrica, and Comptonia

Seedlings of the sweet fern, Comptonia peregrina (L.) Coult., grown aeroponically, were inoculated with a nodule suspension to allow infection by the actinomycete-like organism which causes nodule ...

https://harvardforest.fas.harvard.edu/sites/harvardforest.fas.harvard.edu/files/publications/pdfs/Callahan_CAJBotany_1977.pdf

Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae)

The filamentous bacterium Frankia sp. CpI1 of the Actinomycetales, responsible for symbiotic nitrogen fixation in the nodules of certain woody dicots, also fixes dinitrogen when grown independently...

https://harvardforest.fas.harvard.edu/sites/harvardforest.fas.harvard.edu/files/publications/pdfs/Torrey_CanJMicrobiology_1982.pdf

Dale Callaham

Papers

Isolation and Cultivation in vitro of the Actinomycete Causing Root Nodulation in Comptonia

The structural basis for infection of root hairs of Trifolium repens by Rhizobium

Root Hair Infection in Actinomycete-Induced Root Nodule Initiation in Casuarina, Myrica, and Comptonia

Prenodule formation and primary nodule development in roots of Comptonia (Myricaceae)

Structural features of the vesicle of Frankia sp. CpI1 in culture