Further insights into the components of resistance to Ophiostoma novo-ulmi in Ulmus minor: hydraulic conductance, stomatal sensitivity and bark dehydration

Abstract

Dutch elm disease (DED) is a vascular disease that has killed over 1 billion elm trees. The pathogen spreads throughout the xylem network triggering vessel blockage, which results in water stress, tissue dehydration and extensive leaf wilting in susceptible genotypes. We investigated the differences between four Ulmus minor Mill. clones of contrasting susceptibility to Ophiostoma novo-ulmi Brasier regarding morphological, anatomical and physiological traits affecting water transport, in order to gain a better understanding of the mechanisms underlying DED susceptibility. We analyzed the differential response to water shortage and increased air vapor pressure deficit (VPD) to investigate whether resistance to water stress might be related to DED tolerance. Sixteen plants per clone, aged 2 years, were grown inside a greenhouse under differential watering. Stomatal conductance was measured under ambient and increased VPD. Growth, bark water content and stem hydraulic and anatomical parameters were measured 22 days after starting differential watering. Vessel lumen area, lumen fraction and hydraulic conductance were highest in susceptible clones. Stomatal conductance was lowest under low VPD and decreased faster under increased VPD in resistant clones. We found a negative relationship between the decrease in stomatal conductance at increased VPD and specific hydraulic conductance, revealing a narrower hydraulic margin for sustaining transpiration in resistant clones. The effect of water shortage was greater on radial stem growth than on leaf area, which could be explained through an extensive use of capacitance water to buffer xylem water potential. Water shortage reduced stomatal conductance and vessel lumen area. Bark water content under conditions of water shortage only decreased in susceptible clones. Higher hydraulic constraints to sap flow in resistant clones may determine higher stomatal sensitivity to VPD and so contribute to DED resistance by limiting pathogen expansion and reducing water loss and metabolic impairment in cells involved in fighting against infection.

Xylem characteristics in Ulmus americana cultivars and their potential use as a preliminary screening method for Dutch elm disease resistance

“…Since vessel density and vessel diameter showed strong correlations with disease severity (Table 2), there may be opportunities for using these characteristics in preliminary screening procedures. Findings from this study support those of previous authors that resistant elm genotypes generally have smaller vessel diameters/lumens compared with susceptible genotypes (Elgersma, 1970;McNabb et al, 1970;Pita et al, 2018;Sinclair et al, 1975a;Solla & Gil, 2002a). However, the relationship between vessel diameter and disease resistance is not perfect as evident by the correlation (r s = 0.76, p = 0.049) ( Although much of the focus on preliminary screening methods has been on vessel diameter (Sinclair et al, 1975a;Solla & Gil, 2002a), the strongest correlation found in our study between the xylem characteristics examined and mean disease severity rating was for vessel density (r = −0.77, p = 0.04; Table 2).…”

“…However, in a separate study on Ulmus minor, Martín et al (2009) found that the susceptible group had greater mean vessel density in the earlywood compared with the resistant group, but the difference in the latewood was not significant. Additionally, Pita et al (2018) found that under low watering conditions one of the two susceptible cultivars of Ulmus minor examined had significantly greater vessel density than the two resistant cultivars. Vessel density has been associated with resistance to vascular wilts in other woody plants as well.…”

“…Based on local weather data from the National Oceanic and Atmospheric Administration, from April to June there were 578 mm of precipitation in 2014 and only 275 mm in 2015. In a study on Ulmus minor, Pita et al (2018) found that water stress resulted in a significant effect on average vessel lumen area. Additionally, it has been shown in other woody species that water availability can impact xylem development.…”

“…A potential explanation for the underutilization of this method may be due to concern over the variability in xylem characteristics. Factors such as the age of the plant material (Leal et al., 2011; Martín et al., 2013; Solla et al., 2005), the amount of moisture available (Arend & Fromm, 2007; Lovisolo & Schubert, 1998; Pita et al., 2018; Solla & Gil, 2002b) and sun exposure (Lemoine et al., 2002) have all been shown to affect xylem development in tree species. Another potential explanation for its limited use is the lack of experimental testing with American elm cultivars that have been confirmed to be resistant to DED.…”

Breeding and scientific advances in the fight against Dutch elm disease: Will they allow the use of elms in forest restoration?

“…The differences in numerous xylem characteristics between tolerant individuals and susceptible ones are probably related to slower propagation of the pathogen in the former. Lower vessel grouping, vessel diameter, proportion of large vessels, pit membrane diameter and pit abundance per vessel-wall area directly restrict pathogen axial and radial spreading (McNabb et al 1970;Solla and Gil 2002a;Martín et al 2009) and indirectly restrict spreading by favoring early closure of stomata in response to mild water stress that prevents bark dehydration (Pita et al 2018). The combination of chemical, physiological and anatomical defenses helps to compartmentalize the pathogen, while initial fungal contention results in greater capacity to maintain fungal restriction later on due to lower declines in sap flow, bark water content, photosynthesis and energy available to fuel secondary metabolism.…”