Tansley Review No. 116
Authors: RAI A. N. , SÖDERBÄCK E. , BERGMAN B. 
Published: March 2003

Cyanobacteria are an ancient, morphologically diverse group of prokaryotes with an oxygenic photosynthesis. Many cyanobacteria also possess the ability to fix N2. Although well suited to an independent existence in nature,
some cyanobacteria occur in symbiosis with a wide range of hosts (protists, animals and plants). Among plants,
such symbioses have independently evolved in phylogenetically diverse genera belonging to the algae, fungi,
bryophytes, pteridophytes, gymnosperms and angiosperms. These are N2‐fixing symbioses involving heterocystous cyanobacteria, particularly Nostoc, as cyanobionts (cyanobacterial partners). A given host species
associates with only a particular cyanobiont genus but such specificity does not extend to the strain level. The
cyanobiont is located under a microaerobic environment in a variety of host organs and tissues (bladder, thalli and
cephalodia in fungi; cavities in gametophytes of hornworts and liverworts or fronds of the Azolla sporophyte;
coralloid roots in cycads; stem glands in Gunnera). Except for fungi, the hosts form these structures ahead of the
cyanobiont infection. The symbiosis lasts for one generation except in Azolla and diatoms, in which it is
perpetuated from generation to generation. Within each generation, multiple fresh infections occur as new
symbiotic tissues and organs develop. The symbioses are stable over a wide range of environmental conditions,
and sensing–signalling between partners ensures their synchronized growth and development. The cyanobiont
population is kept constant in relation to the host biomass through controlled initiation and infection, nutrient supply and cell division. In most cases, the partners have remained facultative, with the cyanobiont residing
extracellularly in the host. However, in the water‐fern Azolla and the freshwater diatom Rhopalodia the association
is obligate. The cyanobionts occur intracellularly in diatoms, the fungus Geosiphon and the angiosperm Gunner a.
Close cell–cell contact and the development of special structures ensure efficient nutrient exchange between the
partners. The mobile nutrients are normal products of the donor cells, although their production is increased in
symbiosis. Establishment of cyanobacterial–plant symbioses differs from chloroplast evolution. In these
symbioses, the cyanobiont undergoes structural–functional changes suited to its role as provider of fixed N rather
than fixed C, and the level of intimacy is far less than that of an organelle. This review provides an updated account
of cyanobacterial–plant symbioses, particularly concerning developments during the past 10 yr. Various aspects
of these symbioses such as initiation and development, symbiont diversity, recognition and signalling,
structural–functional modifications, integration, and nutrient exchange are reviewed and discussed, as are
evolutionary aspects and the potential uses of cyanobacterial–plant symbioses. Finally we outline areas that require
special attention for future research. Not only will these provide information of academic interest but they will also
help to improve the use of Azolla as green manure, to enable us to establish artificial N2‐fixing associations with cereals such as rice, and to allow the manipulation of free‐living cyanobacteria for photobiological ammonia or hydrogen production or for use as biofertilizers.

contents

Summary
449

I.
introduction
450

II.
the partners
451

III.
initiation and development of symbioses
458

IV.
the symbioses
462

V.
evolutionary aspects
472

VI.
artificial symbioses
474

VII.
future outlook and perspectives
475

Acknowledgements
477

References
477