Understanding the Disease

To better understand which environmental factors might be important regulators of P. gaeumannii abundance and how they affect the epidemiology of Swiss needle cast, it was essential to investigate the infection cycle of the pathogen and its mechanism of pathogenicity. Ascospores of P. gaeumannii mature and are released during early May through late July, coinciding with bud break and shoot elongation of Douglas-fir. Ascospores are the only infective propagule; there is no conidial anamorph. Newly emerging foliage of Douglas-fir is most susceptible to infection. Infection of 1-year-old needles during the same period also occurs but is much less frequent. Germinating ascospores produce appressoria above stomata, and penetration pegs enter needles via stomata. Colonization within needles is exclusively intercellular; no intracellular hyphae or haustoria are produced. Internal colonization occurs gradually during the fall and winter. Ascocarp (pseudothecia) primordia begin to form in substomatal chambers at 4 to 9 months following infection. Concurrently with the formation of pseudothecial primorida, epiphytic hyphae emerge from the periphery of developing pseudothecia. These hyphae grow across the needle surface, form numerous anastomoses, and reenter the needle by producing appressoria above unoccupied stomata (Stone and others 2007). The importance of epiphytic hyphae in needle colonization and epidemiology of Swiss needle cast is not fully understood.

Internal colonization of needles continues as long as they remain attached, so numbers of ascocarps increase as needles age. Normally, fruiting bodies of the fungus are more abundant on needles aged 3 years or older and are sparse or absent on younger foliage (Boyce 1940, Hood 1982). In recent years, however, trees having abundant fruiting bodies on current-year needles have been commonly observed in forest plantations along the Oregon coast, with older foliage being prematurely abscised due to the disease (Hansen and others 2000).

Relationship of net carbon dioxide uptake

The ascocarp primordia completely occupy the substomatal space, thereby rendering the stoma nonfunctional. Occlusion of the stomata by pseudothecia of P. gaeumannii impedes gas exchange and regulation of transpiration, causing impaired photosynthetic activity and is considered the primary mechanism of pathogenicity (Manter and others 2000, 2003). Disruption of host cells by hyphal penetration has not been observed in infected needles examined in SEM and TEM preparations (Stone and others 2007), and attempts to find evidence of fungal phytotoxins to date have been inconclusive. Estimates of the effect of P. gaeumannii on CO₂ assimilation indicate that occlusion of 25 percent of stomata results in negative needle carbon budgets, i.e., respiration exceeds assimilation, on an annual basis (see figure at right) (Manter and others 2003).

The abundance of pseudothecia is also highly correlated with needle abscission because of the effect on CO₂ assimilation. It has been suggested that foliage abscission occurs when needles switch from being carbon sources to carbon sinks (Cannell and Morgan 1990). The mechanism of pathogenicity of P. gaeumannii, therefore, can be accounted for by the physical blockage of the stomata and interference with photosynthetic gas exchange. The proportion of stomata occupied by pseudothecia on attached needles seldom exceeds 50 percent, suggesting that most needles are abscised before more than half the stomata are occluded by pseudothecia, regardless of needle age (Hansen and others 2000). Because the physiological effects of the disease (impaired CO₂ uptake and photosynthesis) are quantitatively related to the abundance of the pathogen (proportion of stomata occluded by ascocarps), pathogen ascocarp abundance is a suitable response variable for assessing effects of climatic factors on disease.