My lab studies the signaling networks that regulate symbiosis between plants of the legume family and soil bacteria collectively called rhizobium. This mutually beneficial interaction results in the formation of nitrogen-fixing nodules on roots of the host plant. Inside the nodule rhizobia fix atmospheric nitrogen into ammonia, acting as a natural source of fertilizer for the plant. In exchange, the plant provides the resident bacteria with carboxylic acids and other nutrients.

How did legume root nodules evolve?
There are several models for the origin of nodulation. Experiments in our lab are directed to testing two of these models, which address different aspects of nodule evolution. These models are not mutually exclusive, but rather address different aspects of the rhizobium-legume symbiosis.

Model 1: Could nodules have evolved from a preexisting developmental program? Rather than evolve new genes to control these very common developmental processes in a nodule, might legumes have recruited existing genes used for other aspects of plant development and reused them to help form a nodule?

We have identified several mutants in the model legume, Medicago truncatula, that have defects both in plant development and nodule formation. The latd mutant is defective in both nodule formation and root development. In particular, lateral root development is strongly affected. Based on a similar developmental origin, people have long speculated that nodules might have evolved from a lateral root blueprint. Our data provides strong support for nodules and lateral roots sharing a common evolutionary origin. We are characterizing the physiology of latd mutants and using a positional cloning approach to identify the LATD gene. In addition, mutant screens in our lab have identified a number of other plant genes that play a role in nodulation. We have begun to characterize two supernodulating mutants that we identified, giraffe and eve.

Model 2: Could the rhizobium-legume symbiosis have evolved from a pathogenic relationship? Plant defenses present a formidable barrier to invading bacteria. Successful pathogens have evolved ways to bypass these defenses. Somehow, beneficial Rhizobium bacteria are also able to infect the plant and penetrate the developing nodule primordia. Might Rhizobium have evolved from a pathogenic ancestor? Phylogenetic analysis suggests this is possible since most of Rhizobium’s closest relatives are pathogens.

We have shown that the plant hormone, Jasmonic Acid (JA), which is known to regulate plant responses to wounding, herbivory, necrotrophic pathogens as well as modulate root growth, also inhibits nodule formation by modulating the very earliest steps in rhizobium-legume signaling, before infection begins. We are currently trying to examine JA signaling in M. truncatula using a combined genetic and molecular approach.

The model legume Medicago truncatula

Nodules and lateral roots have a similar developmental origin.

Harris, Jeanne Marie* and Dickstein, Rebecca*. (2010). Review: Control of root architecture and nodulation by the LATD/NIP transporter. *Joint corresponding authors. Plant Signaling and Behavior, 5(11): 1386 – 1390.

Yendrek, C. †, Yi-Ching Lee†, Viktoriya Morris†, Yan Liang, Catalina I. Pislariu, Graham Burkart, Matthew H. Meckfessel, Mohammad Salehin, Hilary Kessler, Heath Wessler, Melanie Lloyd, Heather Lutton, Alice Teillet, D. Janine Sherrier, Etienne-Pascal Journet, Harris, J. M*. and R. Dickstein*. (2010). A putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula. †Co-first authors *Joint corresponding authors. The Plant Journal, 62(1): 100-112. (Cover photo of journal accompanies article.)

Ding, Y., Kalo, P., Yendrek, C., Sun, J., Liang, Y., Marsh, J., Harris, J. M. and Oldroyd, G. E. D. (2008). Abscisic acid coordinates Nod factor and cytokinin signaling during the regulation of nodulation. The Plant Cell, 20: 2681-2695.

Liang, Yan, Mitchell, David M. and Jeanne M. Harris. (2007). Abscisic Acid rescues the root meristem defects of the Medicago truncatula latd mutant. Developmental Biology, 304 (1): 297-307

Sun, J., Cardoza, J., Mitchell, D. M., Bright, L., Oldroyd, G. and J. M. Harris. Crosstalk between Jasmonic acid, ethylene and Nod factor signaling allows integration of diverse inputs for regulation of nodulation. The Plant Journal (2006) 46: 961-970.

Liang, Y. and J. M. Harris Response of root branching to Abscisic Acid is correlated with nodule formation both in legumes and non-legumes. American Journal of Botany, (2005) 92: 1675-1683

Bright, L. J., Liang, Y., Mitchell, D. M. and J. M. Harris. (2005). The LATD gene of Medicago truncatula is required both for nodule and root development. Molecular Plant-Microbe Interactions (2005) 18(6): 521-532.

* indicates equal contribution