Long-term impact of Ophiostoma novo-ulmi on leaf traits and transpiration of branches in the Dutch elm hybrid 'Dodoens'

Abstract

To better understand the long-term impact of Ophiostoma novo-ulmi Brasier on leaf physiology in 'Dodoens', a Dutch elm disease-tolerant hybrid, measurements of leaf area, leaf dry mass, petiole anatomy, petiole hydraulic conductivity, leaf and branch water potential, and branch sap flow were performed 3 years following an initial artificial inoculation. Although fungal hyphae were detected in fully expanded leaves, neither anatomical nor morphological traits were affected, indicating that there was no impact from the fungal hyphae on the leaves during leaf expansion. In contrast, however, infected trees showed both a lower transpiration rate of branches and a lower sap flow density. The long-term persistence of fungal hyphae inside vessels decreased the xylem hydraulic conductivity, but stomatal regulation of transpiration appeared to be unaffected as the leaf water potential in both infected and non-infected trees was similarly driven by the transpirational demands. Regardless of the fungal infection, leaves with a higher leaf mass per area ratio tended to have a higher leaf area-specific conductivity. Smaller leaves had an increased number of conduits with smaller diameters and thicker cell walls. Such a pattern could increase tolerance towards hydraulic dysfunction. Measurements of water potential and theoretical xylem conductivity revealed that petiole anatomy could predict the maximal transpiration rate. Three years following fungal inoculation, phenotypic expressions for the majority of the examined traits revealed a constitutive nature for their possible role in Dutch elm disease tolerance of 'Dodoens' trees.

Keywords: Huber value; LMA; anatomy; petiole; potential transpiration; sap flow; water potential gradient.

Figure 1.

Distribution of DED inside the xylem tissues of infected ‘Dodoens’ trees. (a) Wood disc cross section, 80 cm above the point of inoculation, showing distinct infection zones (red arrows) concentrated mostly in earlywood of the 2008 annual ring. (b) Formation of many narrowed latewood vessels in the 2009 annual ring in response to fungal infection; SEM, cross section, scale bar = 500 µm. (c) Wild-type pattern of latewood organization in the 2009 annual ring of non-infected trees; SEM, cross section, scale bar = 500 µm. (d) Ophiostoma novo-ulmisubsp. novo-ulmi × O. novo-ulmi subsp. americana hyphae (white arrows) inside an earlywood vessel of the 2009 annual ring; SEM, radial section, scale bar = 50 µm. (e) Fungal hyphae inside vessel elements of the leaf midrib primary xylem; SEM, cross section, scale bar = 10 µm. Image (a) is adapted from Ďurkovič et al. (2015); images (d) and (e) are adapted from Ďurkovič et al. (2013).

Figure 2.

Transpiration of infected and non-infected trees during the day of measurement (26 August 2011). Infected trees show a lower transpiration from the morning until late afternoon. Thick lines indicate average transpiration and grey background with dashed lines indicates SD. Abbreviations are given in Table 1.

Figure 3.

Leaf water potential in infected and non-infected trees from 06:00 to 18:00 hours during the day of measurement (26 August 2011). There is no difference in leaf water potential between infected and non-infected trees. Circles denote mean values and bars denote SD. Abbreviations are given in Table 1.

Figure 4.

Comparison between the maximal measured transpiration (E_max) and calculated potential transpiration (E_th). Open circles denote non-infected trees, and closed circles denote infected trees. Dashed line signifies 1 : 1 ratio.

Figure 5.

Linear dependencies of potential transpiration (E_th), xylem area-specific conductivity (k_x) and leaf area-specific conductivity (k_l) on LMA. Open circles denote non-infected trees, and filled circles denote infected trees.

Figure 6.

Linear dependencies of leaf area (A_l), petiole xylem area (A_xl), mean diameter of vessels (D₉₅), vessel lumen area percentage (N_A) and vessel density (N_n) on xylem area-specific hydraulic conductivity (k_x). Open circles denote non-infected trees, and filled circles denote infected trees.

Figure 7.

Positions of the examined branch and leaf traits plus positions of the examined trees on the first and second axes of the PCA. The bottom and left-hand axes refer to the examined traits; the top and right-hand axes refer to the examined trees. Percentages of variation explained by each of the axes are given in parentheses. I1–I4 denote infected trees; N1–N3 denote non-infected trees. Trait abbreviations are given in Table 1.