Structural and Functional Evidence for Xylem‐Mediated Water Transport and High Transpiration in <i>Agrobacterium tumefaciens</i>‐Induced Tumors of <i>Ricinus communis</i>*

Schurr, Ulrich; Schuberth, Bettina; Aloni, Roni; Pradel, Katja S.; Schmundt, Dominik; Jähne, Bernd; Ullrich, C.

doi:10.1111/j.1438-8677.1996.tb00590.x

Cited by 26 publications

(26 citation statements)

References 23 publications

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“…Residual epidermis, characterized by continuously widely open stomata, occurred only at the borders of the host stem. Schurr et al (1996) showed that similar changes in the enlarged tumor surface substantially increased transpiration to about 15 and 7.5 times higher at the tumor surface compared with host leaves and leaves of noninfected castor bean plants, respectively. Therefore, the combination of a decrease in vessel diameter in the host and an increased surface of the tumor, both induced by ethylene, ensures water-supply priority to fast-growing crown galls.…”

Section: Discussionmentioning

confidence: 93%

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

et al. 1998

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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. ...

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Section: Discussionmentioning

confidence: 93%

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

et al. 1998

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“…Reasons for the reduction in species abundance in summer might be higher temperatures and drought stress. It is known from the model plant Arabidopsis (63,64) and Ricinus communis (65) that crown gall growth is affected by drought stress. In graft unions without a crown gall, the diversity of the bacterial species was only marginally affected by the season.…”

Section: Discussionmentioning

confidence: 99%

Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota

Faist¹,

Keller

Hentschel³

et al. 2016

Appl Environ Microbiol

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Crown gall disease of grapevine is caused by virulent Agrobacterium strains and establishes a suitable habitat for agrobacteria and, potentially, other bacteria. The microbial community associated with grapevine plants has not been investigated with respect to this disease, which frequently results in monetary losses. This study compares the endophytic microbiota of organs from grapevine plants with or without crown gall disease and the surrounding vineyard soil over the growing seasons of 1 year. Amplicon-based community profiling revealed that the dominating factor causing differences between the grapevine microbiota is the sample site, not the crown gall disease. The soil showed the highest microbial diversity, which decreased with the distance from the soil over the root and the graft union of the trunk to the cane. Only the graft union microbiota was significantly affected by crown gall disease. The bacterial community of graft unions without a crown gall hosted transient microbiota, with the three most abundant bacterial species changing from season to season. In contrast, graft unions with a crown gall had a higher species richness, which in every season was dominated by the same three bacteria (Pseudomonas sp., Enterobacteriaceae sp., and Agrobacterium vitis). For in vitro-cultivated grapevine plantlets, A. vitis infection alone was sufficient to cause crown gall disease. Our data show that microbiota in crown galls is more stable over time than microbiota in healthy graft unions and that the microbial community is not essential for crown gall disease outbreak. IMPORTANCEThe characterization of bacterial populations in animal and human diseases using high-throughput deep-sequencing technologies, such as 16S amplicon sequencing, will ideally result in the identification of disease-specific microbiota. We analyzed the microbiota of the crown gall disease of grapevine, which is caused by infection with the bacterial pathogen Agrobacterium vitis. All other Agrobacterium species were found to be avirulent, even though they lived together with A. vitis in the same crown gall tumor. As has been reported for human cancer, the crown gall tumor also hosted opportunistic bacteria that are adapted to the tumor microenvironment. Characterization of the microbiota in various diseases using amplicon sequencing may help in early diagnosis, to serve as a preventative measure of disease in the future.

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“…Agrobacterium-induced plant tumors show increased water loss, resulting in a redirection of water flow and nutrient transport necessary for tumor development (Schurr et al, 1996;Wächter et al, 2003). On the contrary, increased water loss causes tissue desiccation.…”

Section: Discussionmentioning

confidence: 99%

“…Tumors display a ruptured surface that is devoid of a cuticle covered epidermal cell layer; as a result tumors exhibit an increased water loss (Schurr et al, 1996). Usually, this is prevented by specialized cell types that contain substantial amounts of aliphatic polymers like cutin or suberin: Cutin is a major component of the cuticle that covers all aerial primary organs and forms the interface between plant and atmosphere.…”

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confidence: 99%

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

Efetova¹,

Zeier²,

Riederer³

et al. 2007

Plant Physiology

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Crown gall tumors induced by Agrobacterium tumefaciens represent a sink that has to be provided with nutrients and water by the host plant. The lack of an intact epidermis or cuticle results in uncontrolled loss of water. However, neither the tumor nor the host plant displays wilting. This phenomenon points to drought adaptation in both tumors and the crown gall host plant. To understand the underlying molecular mechanisms of protection against desiccation the gene expression pattern of Arabidopsis (Arabidopsis thaliana) tumors was integrated with the profile of stress metabolites: Arabidopsis tumors accumulated high amounts of abscisic acid (ABA), the ethylene precursor aminocyclopropyl carboxylic acid, osmoprotectants, and form a suberized periderm-like protective layer. Suberization of the outer tumor cell layers most likely is mediated by ABA since external application of ABA induced suberization of Arabidopsis roots. However, the expression level of the classical marker genes, known to respond to drought stress and/or ABA, was lower in tumors. Instead another set of drought and/or ABAinducible genes was more highly transcribed. Elevated transcription of several ABA-dependent aquaporin genes might indicate that ABA controls the water balance of the tumor. The retarded tumor growth on abi and aba mutant plants underlined the importance of a tumor-specific ABA signaling pathway. Taken together, we propose that ABA is an important signal for protection of tumors against desiccation and thus supports tumor development.

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Structural and Functional Evidence for Xylem‐Mediated Water Transport and High Transpiration in Agrobacterium tumefaciens‐Induced Tumors of *Ricinus communis**

Cited by 26 publications

References 23 publications

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

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

Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota

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

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Structural and Functional Evidence for Xylem‐Mediated Water Transport and High Transpiration in Agrobacterium tumefaciens‐Induced Tumors of Ricinus communis*

Cited by 26 publications

References 23 publications

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

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

Grapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota

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

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Structural and Functional Evidence for Xylem‐Mediated Water Transport and High Transpiration in Agrobacterium tumefaciens‐Induced Tumors of *Ricinus communis**