Plant Physiol. Journal of Pharmacology and Experimental Therapeutics
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Published on August 19, 2005; 10.1104/pp.105.064931


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Received April 30, 2005
Returned for revision June 30, 2005
Accepted July 11, 2005

Nitrogen Deprivation Stimulates Symbiotic Gland Development in Gunnera manicata

Wan-Ling Chiu *, Gerald A. Peters , Germain Levieille , Patrick C. Still , Sarah Cousins , Bruce Osborne , and Jeff Elhai

Department of Biology, Virginia Commonwealth University, Richmond, Virginia, 23284
Department of Botany, University College Dublin, Belfield, Dublin 4, Ireland
Department of Biology, Virginia Commonwealth University, Richmond, Virginia, 23284; Center for the Study of Biological Complexity, Virginia Commonwealth University, Richmond, Virginia, 23284

* Corresponding author; email: wchiu{at}vcu.edu.

Gunnera is the only genus of angiosperms known to host cyanobacteria and the only group of land plants that hosts cyanobacteria intracellularly. Motile filaments of cyanobacteria, known as hormogonia, colonize Gunnera plants through cells in the plant's specialized stem glands. It is commonly held that Gunnera plants always possess functional glands for symbiosis. We found, however, that stem gland development did not occur when Gunnera manicata plants were grown on nitrogen (N)-replete medium but, rather, was initiated at predetermined positions when plants were deprived of combined N. While N status was the main determinant for gland development, an exogenous carbon source (sucrose) accelerated the process. Furthermore, a high level of sucrose stimulated the formation of callus-like tissue in place of the gland under N-replete conditions. Treatment of plants with the auxin transport inhibitor 1-naphthylphthalamic acid prevented gland development on N-limited medium, most likely by preventing resource reallocation from leaves to the stem. Optimized conditions were found for in vitro establishment of the Nostoc-Gunnera symbiosis by inoculating mature glands with hormogonia from Nostoc punctiforme, a cyanobacterium strain for which the full genome sequence is available. In contrast to uninoculated plants, G. manicata plants colonized by N. punctiforme were able to continue their growth on N-limited medium. Understanding the nature of the Gunnera plant's unusual adaptation to an N-limited environment may shed light on the evolution of plant-cyanobacterium symbioses and may suggest a route to establish productive associations between N-fixing cyanobacteria and crop plants.




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[Abstract] [Full Text] [PDF]




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