Different Responses in Vascular Traits between Dutch Elm Hybrids with a Contrasting Tolerance to Dutch Elm Disease

Abstract

The ascomycetous fungus Ophiostoma novo-ulmi is the causative agent of the current Dutch elm disease (DED) pandemic, which has ravaged many tens of millions of European and North American elm trees. Host responses in vascular traits were studied in two Dutch elm hybrids, 'Groeneveld' and 'Dodoens', which show different vascular architecture in the secondary xylem and possess contrasting tolerances to DED. 'Groeneveld' trees, sensitive to DED, possessed a high number of small earlywood vessels. However, these trees showed a poor response to DED infection for the earlywood vascular characteristics. Following infection, the proportion of least vessels with a vessel lumen area less than 2500 µm² decreased from 65.4% down to 53.2%. A delayed response in the increasing density of vessels showing a reduced size in the latewood prevented neither the rapid fungal spread nor the massive colonisation of the secondary xylem tissues resulting in the death of the infected trees. 'Dodoens' trees, tolerant to DED, possessed a low number of large earlywood vessels and showed a prominent and fast response to DED infection. Vessel lumen areas of newly formed earlywood vessels were severely reduced together with the vessel size : number ratio. Following infection, the proportion of least vessels with a vessel lumen area less than 2500 µm² increased from 75.6% up to 92.9%. A trend in the increasing density of vessels showing a reduced size was maintained not only in the latewood that was formed in the year of infection but also in the earlywood that was formed in the consecutive year. The occurrence of fungal hyphae in the earlywood vessels that were formed a year following the infection was severely restricted, as revealed by X-ray micro-computed tomography imaging. Possible reasons responsible for a contrasting survival of 'Groeneveld' and 'Dodoens' trees are discussed.

Keywords: Ophiostoma novo-ulmi; X-ray micro-computed tomography; bordered pits; earlywood vessel; vascular architecture.

Figure 1

Scanning electron microscopy images of earlywood vessels in the sixth annual growth ring of ‘Groeneveld’ trees. (A) The non-infected tree, radial section, scale bar = 100 μm. (B) Densely spreading hyphae on the radial wall surface of an earlywood vessel, radial section, scale bar = 100 μm. (C) Both minute and large fungal hyphae spread through the lumen of an earlywood vessel, cross-section, scale bar = 20 μm. (D) A large number of small tyloses formed on the tangential wall surface of an earlywood vessel that was not capable of efficiently plugging the conduit, tangential section, scale bar = 20 μm. (E) The free penetration of the fungal hypha in an earlywood vessel, unrestricted by the bordered pit aperture size, radial section, scale bar = 10 μm. (F) Vegetative sporulation of the fungus on the radial wall surface of an earlywood vessel, radial section, scale bar = 10 μm.

Figure 2

Scanning electron microscopy images of earlywood vessels in the sixth annual growth ring of ‘Dodoens’ trees. (A) The non-infected tree, radial section, scale bar = 100 μm. (B) The hyphae (white arrow) spread on the radial wall surface of an earlywood vessel, radial section, scale bar = 50 μm. (C) An earlywood vessel occlusion through tyloses following the fungal infection, radial section, scale bar = 200 μm. (D) Rapid formation of a large number of narrow earlywood vessels as the immediate response to the fungal infection, radial section, scale bar = 100 μm.

Figure 3

Scanning electron microscopy images of the latewood vascular architecture in the sixth annual growth ring of the examined Dutch elm hybrids. (A) The non-infected tree of ‘Groeneveld’. (B) The infected tree of ‘Groeneveld’. (C) The non-infected tree of ‘Dodoens’. (D) The infected tree of ‘Dodoens’. Cross-sections, scale bars (A–D) = 500 μm.