Xylella fastidiosa Infection and Ethylene Exposure Result in Xylem and Water Movement Disruption in Grapevine Shoots

Abstract

It is conventionally thought that multiplication of the xylem-limited bacterium Xylella fastidiosa (Xf) within xylem vessels is the sole factor responsible for the blockage of water movement in grapevines (Vitis vinifera) affected by Pierce's disease. However, results from our studies have provided substantial support for the idea that vessel obstructions, and likely other aspects of the Pierce's disease syndrome, result from the grapevine's active responses to the presence of Xf, rather than to the direct action of the bacterium. The use of magnetic resonance imaging (MRI) to observe the distribution of water within the xylem has allowed us to follow nondestructively the development of vascular system obstructions subsequent to inoculation of grapevines with Xf. Because we have hypothesized a role for ethylene produced in vines following infection, the impact of vine ethylene exposure on obstruction development was also followed using MRI. In both infected and ethylene-exposed plants, MRI shows that an important proportion of the xylem vessels become progressively air embolized after the treatments. The loss of xylem water-transporting function, assessed by MRI, has been also correlated with a decrease in stem-specific hydraulic conductivity (K S) and the presence of tyloses in the lumens of obstructed water conduits. We have observed that the ethylene production of leaves from infected grapevines is greater than that from healthy vines and, therefore, propose that ethylene may be involved in a series of cellular events that coordinates the vine's response to the pathogen.

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

“…Host ethylene perception and synthesis have been previously shown to be an important factor in development of wilt symptoms elicited by fungal vascular pathogens (Van der Molen et al, 1983;Lund et al, 1998;Robison et al, 2001). 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).…”

Vascular Occlusions in Grapevines with Pierce’s Disease Make Disease Symptom Development Worse

“…Pathogen infection has been reported to cause elevated ethylene production of host plants in many species (Pegg, 1976;Pegg and Cronshaw, 1976;Boller, 1991;Abeles et al, 1992), including grapevines infected with X. fastidiosa (Pérez-Donoso et al, 2007). Furthermore, ethylene promotes tylose formation in grapevines (Sun et al, 2007) and pectin gel accumulation in other species (VanderMolen et al, 1983).…”

“…Even though the specific mechanistic linkage of wounds and enhanced ethylene synthesis is not clear in all plant systems, it is easy to propose that the harm caused by pathogens like X. fastidiosa could be perceived as a biochemical/structural wound by the infected grapevine. Furthermore, because disruption of the cell wall PM fabric catalyzed by the bacterium's CWDEs occurs during PD development (Pérez-Donoso et al, 2007;Sun et al, 2011), it is reasonable to suggest that pectinderived oligosaccharides, generated by PG cleavage of the sparsely methylesterified homogalacturonans in the PMs, could be a signal intermediate. Such oligosaccharides are known to be generated in ripening tomato fruit and to promote fruit ethylene synthesis (Melotto et al, 1994).…”

“…One major aspect is to clarify the process of tylose development itself, in which an open vessel may be gradually sealed (Sun et al, 2006(Sun et al, , 2008. Our investigations of the initiation of tylose formation in grapevines have identified ethylene as an important factor (Pérez-Donoso et al, 2007;Sun et al, 2007). In terms of the relationship of tyloses to grapevine PD, studies have so far led to several controversial viewpoints that are discussed below (Mollenhauer and Hopkins, 1976;Fry and Milholland, 1990b;Stevenson et al, 2004a;.…”

In Vivo Visualizations of Drought-Induced Embolism Spread in Vitis vinifera

“…Despite the availability of NMR, studies using this technology are largely focused to the spread of embolism over long periods of time (e.g. weeks [Umebayashi et al, 2011] or months [Pérez-Donoso et al, 2007]) rather than the shortterm dynamics of embolism spread over the course of a few hours.…”