The Never ripe Mutant Provides Evidence That Tumor-Induced Ethylene Controls the Morphogenesis ofAgrobacterium tumefaciens-Induced Crown Galls on Tomato Stems1,2

Abstract

We confirm the hypothesis that Agrobacterium tumefaciensinduced galls produce ethylene that controls vessel differentiation in the host stem of tomato (Lycopersicon esculentum Mill.). Using an ethylene-insensitive mutant, Never ripe (Nr), and its isogenic wild-type parent we show that infection by A. tumefaciens results in high rates of ethylene evolution from the developing crown galls. Ethylene evolution from isolated internodes carrying galls was up to 50-fold greater than from isolated internodes of control plants when measured 21 and 28 d after infection. Tumor-induced ethylene substantially decreased vessel diameter in the host tissues beside the tumor in wild-type stems but had a very limited effect in the Nr stems. Ethylene promoted the typical unorganized callus shape of the gall, which maximized the tumor surface in wild-type stems, whereas the galls on the Nr stems had a smooth surface. The combination of decreased vessel diameter in the host and increased tumor surface ensured water-supply priority to the growing gall over the host shoot. These results indicate that in addition to the well-defined roles of auxin and cytokinin, there is a critical role for ethylene in determining crown-gall morphogenesis.Infection of sensitive plants by Agrobacterium tumefaciens is known to induce crown galls. Tumor growth is initiated by the integration and expression of the T-DNA of the bacterial Ti plasmid within the plant nDNA. The T-DNA encodes enzymes catalyzing the synthesis of high levels of auxin, cytokinin, and opines (Weiler and Spanier, 1981;Zambryski et al., 1989;Schell et al., 1994). Aloni et al. (1995) found that an A. tumefaciens-induced crown gall caused the development of pathologic xylem in the centripetal direction within the host stem of castor bean. This pathologic xylem was characterized by narrow vessels, giant rays, and an absence of fibers. A similar anatomy was induced experimentally in stems of elm seedlings by the ethylene-releasing agent ethrel (Yamamoto et al., 1987), indicating the possible involvement of the hormone ethylene in crown-gall development. Therefore, Aloni et al. (1995) suggested that the high auxin levels induced by the T-DNA-encoded genes iaaM and iaaH (Thomashow et al., 1984(Thomashow et al., , 1986 stimulate ethylene synthesis at the base of the crown gall, where high auxin streams originating in the tumor merge. Therefore, tumor-induced ethylene might affect crown-gall morphogenesis and differentiation of host tissues adjacent to the tumor.A. tumefaciens-induced crown galls cause poor xylem development in grapevine, which impairs water flow to the young parts of the shoot above the gall (Agrios, 1988). Aloni et al. (1995) proposed the "gall-constriction hypothesis" to explain the mechanism that gives water-supply priority to the growing gall over the host shoot. The hypothesis proposes that the growing gall retards the development of its host shoot by decreasing vessel diameter in the host, substantially reducing the supply of water to the upper parts of the shoot. ...

Tomato Transcriptional Changes in Response toClavibacter michiganensissubsp.michiganensisReveal a Role for Ethylene in Disease Development

“…Interestingly, ethylene treatment of various plant species causes xylem occlusion, which leads to the wilt phenotype of vascular diseases (Van der Molen et al, 1983;Perez-Donoso et al, 2007). In addition, it was shown that ethylene produced by galls of Agrobacterium-infected tomato plants decreases the diameter of xylem vessels in the stem adjacent to the tumor (Aloni et al, 1998). In light of these observations, it is tempting to speculate that ethylene emission by Cmminfected tissues may contribute to the development of wilt symptoms by affecting physical properties of xylem vessels in the host plant.…”

Agrobacterium tumefaciensPromotes Tumor Induction by Modulating Pathogen Defense inArabidopsis thaliana

“…It has been demonstrated that auxin and ET control vascular development in plants as well as in tumors (Aloni et al, 1998, and it is well known that high auxin levels induce ET emission. Besides their action in pathogen defense during initiation of infection with agrobacteria, this may imply an additional role for these phytohormones in regulating vascular development at later stages of tumor development.…”

“…JA and ET accumulate in response to pathogen infection or herbivore damage, resulting in the activation of distinct sets of pathogenesis-related genes (PR). It has been reported that along with auxin and cytokinin (Weiler and Schroeder, 1987;Zambryski et al, 1989;Malsy et al, 1992), the phytohormone ET is a limiting factor of crown gall morphogenesis because ET deficiency or insensitivity leads to inhibition of tumor growth (Aloni et al, 1998;Wachter et al, 2003). SAmediated defense responses provide protection from biotrophic fungi, oomycetes, and bacteria, including Erysiphe orontii, Peronospora parasitica, and Pseudomonas syringae.…”

A Central Role of Abscisic Acid in Drought Stress Protection of Agrobacterium-Induced Tumors on Arabidopsis

“…From tumors of castor bean (Ricinus communis) it was proposed that the synthesis of auxin and cytokinin promotes an increased production of ethylene. Communication between the tumor and the host plant might well be provided by this gaseous factor, which in turn triggers synthesis of high ABA content in leaves of the host plant (Aloni et al, 1998;Wächter et al, 1999;Veselov et al, 2003). Since Arabidopsis tumors produce increased levels of the ethylene precursor ACC and develop very close to rosette leaves, ethylene diffusion seems very likely.…”