Auxin Carriers Localization Drives Auxin Accumulation in Plant Cells Infected by Frankia in Casuarina glauca Actinorhizal Nodules


Actinorhizal symbioses are mutualistic interactions between plants and the soil bacteria Frankia that lead to the formation of nitrogen-fixing root nodules. Little is known about the signaling mechanisms controlling the different steps of the establishment of the symbiosis. The plant hormone auxin has been suggested to play a role. Here we report that auxin accumulates within Frankia-infected cells in actinorhizal nodules of Casuarina glauca. Using a combination of computational modeling and experimental approaches, we establish that this localized auxin accumulation is driven by the cell-specific expression of auxin transporters and by Frankia auxin biosynthesis in planta. Our results indicate that the plant actively restricts auxin accumulation to Frankia-infected cells during the symbiotic interaction.

Actinorhizal symbioses are mutualistic associations between plants belonging to eight angiosperm families collectively called actinorhizal plants and the soil actinomycete Frankia. These interactions culminate with the formation of a new root organ, the actinorhizal nodule, where Frankia is hosted and fixes atmospheric nitrogen (Benson and Silvester, 1993). During intracellular infection (e.g. in Casuarina glauca or Alnus glutinosa), diffusible signals are emitted by Frankia at early stages of the interaction leading to root hair deformation. The chemical nature of these signals remains unknown but biochemical and genetic studies suggest that they are different from rhizobial Nod factors (Cérémonie et al., 1998; Normand et al., 2007). Frankia then infects some of the deformed root hairs through intracellular infection threads. A limited number of cell divisions are induced in the cortex close to the infection site leading to the formation of the prenodule. Frankia infects some prenodule cells and starts fixing nitrogen while new cell divisions occur in the pericycle close to a xylem pole forming a nodule primordium (Pawlowski and Bisseling, 1996). The nodule primordium subsequently grows and become infected with intracellular Frankia hyphae coming from the prenodule. Actinorhizal nodules have a central vasculature and the cortical symbiotic tissues containing infected and uninfected cells. Unlike legume nodules, actinorhizal nodules are structurally and developmentally related to lateral roots (Pawlowski and Bisseling, 1996).

Little is known about the signals exchanged between the two partners during the establishment of actinorhizal symbioses. The phytohormone auxin controls many developmental processes and has also been involved in plant-microbe interactions (Robert-Seilaniantz et al., 2007; Mathesius, 2008; Kazan and Manners, 2009). Recently, we studied the role of auxin influx activity during actinorhizal symbioses. Inhibition of auxin influx using the competitive inhibitor naphtoxyacetic acid perturbs actinorhizal nodule formation in C. glauca (Péret et al., 2007). Two genes encoding putative auxin influx carriers from C. glauca were cloned and characterized. One of these genes named CgAUX1 was shown to encode a functional auxin influx carrier by complementation of the Arabidopsis (Arabidopsis thaliana) aux1 mutant. Interestingly, CgAUX1 is expressed in Frankia-infected cells during actinorhizal nodule formation (Péret et al., 2007). These results together with previous data showing auxin production by Frankia suggest a role for auxin in infected cells during the symbiotic interaction (Mathesius, 2008; Péret et al., 2008; Grunewald et al., 2009).

The aim of this work was to further explore the involvement of auxin in the C. glauca-Frankia actinorhizal symbiosis. Using a combination of computational modeling and molecular and cell biology approaches, we establish that the cell-specific expression of auxin transporters leads to localized auxin accumulation in Frankia-infected cells in C. glauca nodules.

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Plant Physiology


American Society of Plant Biologists

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© 2010 American Society of Plant Biologists