Ecological Conditions and Molecular Determinants Involved in Agrobacterium Lifestyle in Tumors

Abstract

The study of pathogenic agents in their natural niches allows for a better understanding of disease persistence and dissemination. Bacteria belonging to the Agrobacterium genus are soil-borne and can colonize the rhizosphere. These bacteria are also well known as phytopathogens as they can cause tumors (crown gall disease) by transferring a DNA region (T-DNA) into a wide range of plants. Most reviews on Agrobacterium are focused on virulence determinants, T-DNA integration, bacterial and plant factors influencing the efficiency of genetic transformation. Recent research papers have focused on the plant tumor environment on the one hand, and genetic traits potentially involved in bacterium-plant interactions on the other hand. The present review gathers current knowledge about the special conditions encountered in the tumor environment along with the Agrobacterium genetic determinants putatively involved in bacterial persistence inside a tumor. By integrating recent metabolomic and transcriptomic studies, we describe how tumors develop and how Agrobacterium can maintain itself in this nutrient-rich but stressful and competitive environment.

Keywords: Agrobacterium tumefaciens; competition; crown gall; molecular traits; plant defense; tumor lifestyle.

Figure 1

Schematic representation of the plant reactions to the stresses caused by tumor development. T-DNA integration into the plant genome induces auxin and cytokinin production. High concentrations of these two phytohormones accelerate cell proliferation and tumor growth. ACC synthase expression is also induced and triggers ethylene production. Ethylene has two main roles in the tumor: it reduces plant vessel diameter around the tumor to ensure its hydration, and it triggers abscisic acid synthesis. The latter induces the polymerization of suberin that forms a protective layer around the tumor. (A) Drought stress in the tumor: under drought stress, FAD3 produces α-linolenic acid, an unsaturated fatty acid, to maintain lipid membrane integrity. (B) Hypoxic stress in the tumor: when the drought stress is more severe (i.e., in old tumors), abscisic acid triggers stomatal closure. This implies H₂O₂ production and leads to a decreased oxygen rate. Under low oxygen, SAD6 also contributes to the production of unsaturated fatty acids to maintain lipid membrane integrity in the transformed cells.

Figure 2

Model of the regulation of siderophore gene cluster expression according to iron availability. In an iron-limited environment, due to the low heme and Fe-S concentrations, the Irr protein is abundant and represses rirA. Consequently, SigI, which is under the negative control of RirA, is expressed and can induce siderophore synthesis. In an iron-rich environment, Irr is negatively regulated by the high heme concentration. In these conditions, RirA is abundant and its binding to Fe-S allows for the repression of sigI, which leads to the very low expression of siderophore biosynthesis genes.