Engineering of crop plants to facilitate bottom-up innovation: A possible role for broad host-range nitroplasts and neoplasts

Abstract

The astonishing gains in agricultural output since the 1960's has come at an environmental cost. It has also failed to bring much benefit to sub-Saharan Africa, the region of the world that is predicted to have the greatest population increase in the coming decades and greatest agricultural need. The increase in productivity required to feed the billions that will soon be added to the world's population is more likely to succeed if creative direction lies in the hands of those most intimately acquainted with local agricultural concerns. Nitrogen has been a major limitation, particularly in sub-Saharan agriculture, and I look here at the prospect for extending biological nitrogen fixation to the crops and practices of local interest. A source of optimism in this historically intractable problem is the discovery in certain algae of natural organelles – nitroplasts – derived from unicellular cyanobacteria that fix N2. Transferring nitroplasts to land plants seems possible only if the organelles rely little on their hosts. A survey of the metabolic capabilities of three of them indicate different degrees of independence. The nitroplast from the diatom Rhopalodia gibberula may need nothing from its host except a source of carbon (the nature of which is explored). The nitroplast from another diatom, Epithema turgida, is somewhat less independent, while the nitroplast from Braarudosphaera bigelowii (called UCYN-A) requires a great deal from its host, including imported protein. The evolutionary route to acquire proteins may have been greatly simplified if nitroplasts share proteins with chloroplasts, a co-resident cyanobacteria-derived organelle. The genomes of the diatom nitroplasts suggest the presence of a few enzymes that are rare in cyanobacteria but seemingly well suited to the special needs of a nitrogen-fixing organelle. I describe how the host-range of nitroplasts might be explored and how a stripped down version, called a neoplast, might simplify strain modification to such a degree that the process becomes accessible to academic researchers with limited resources, even to individual farmers.

Nitrogen-fixing organelle in a marine alga

“…Although it has been suggested that there is no reason why an N 2 -fixing organelle could not be maintained in the cell, such organelles have yet to be described ( 51 ). The findings of this study, along with the regulation of spheroid body size ( 17 ) and coevolution of B. bigelowii and UCYN-A ( 53 ), suggest that the evolution of the nitroplast is underway and establish B. bigelowii as an important model system of great interest for understanding organellogenesis, with implications for contemporary efforts to engineer N 2 -fixing capabilities into agricultural plants ( 10 , 57 ).…”

“…Several presumed endosymbiotic interactions have been described that involve unicellular eukaryotic algae and N 2 -fixing intracellular spheroid bodies that are evolutionarily related to cyanobacteria ( 6 ), including diatom symbionts ( 7 ) and the Candidatus Atelocyanobacterium thalassa (UCYN-A) symbiosis with a haptophyte alga ( 8 ). However, it has remained unclear where these symbiotic relationships fall along the spectrum of endosymbiosis to organelle, and no N 2 -fixing organelle has yet been discovered ( 9 , 10 ).…”