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Tansley Review No. 116 Cyanobacterium–plant symbioses

  • A. N. RAI (a1), E. SÖDERBÄCK (a2) and B. BERGMAN (a2)
    • Published online: 23 October 2000
Abstract

Summary 449

I. INTRODUCTION 450

II. THE PARTNERS 451

1. Cyanobionts and their role 451

2. Hosts and their role 453

3. Location of cyanobionts in their hosts 455

III. INITIATION AND DEVELOPMENT OF SYMBIOSES 458

1. Initiation of symbioses 458

2. Geosiphon pyriforme 458

3. Cyanolichens 459

4. Liverworts and hornworts 460

5. Azolla 460

6. Cycads 461

7. Gunnera 461

IV. THE SYMBIOSES 462

1. Geographical distribution and ecological significance 462

2. Benefits to the partners 462

(a) Benefits to the cyanobionts 462

(b) Benefits to the hosts 463

3. Duration and stability 463

4. Mode of transmission and perpetuation 463

5. Recognition between the partners 464

6. Specificity and diversity 464

7. Symbiosis-related genes 465

8. Modifications of the cyanobiont 466

(a) Growth and morphology 466

(b) Photosynthesis and carbon metabolism 467

(c) Glutamine synthetase 467

(d) Heterocysts 469

(e) N2 fixation 470

9. Nutrient exchange 471

(a) Carbon 471

(b) Nitrogen 472

V. EVOLUTIONARY ASPECTS 472

VI. ARTIFICIAL SYMBIOSES 474

VII. FUTURE OUTLOOK AND PERSPECTIVES 475

1. Cryptic symbioses 476

2. Developmental profile of symbiotic tissues 476

3. Sensing and signalling 476

4. Genetic aspects 476

5. Physiological and biochemical aspects of nutrient exchange 477

6. Microaerobiosis 477

7. Potential applications 477

Acknowledgements 477

References 477

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.

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Author for correspondence (fax +91 364 250076 or 250108; e-mail rai_amar@hotmail.com).
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