Carbon Costs of Constitutive and Expressed Resistance to a Non-Native Pathogen in Limber Pine

Abstract

Increasing the frequency of resistance to the non-native fungus Cronartium ribicola (causative agent of white pine blister rust, WPBR) in limber pine populations is a primary management objective to sustain high-elevation forest communities. However, it is not known to what extent genetic disease resistance is costly to plant growth or carbon economy. In this study, we measured growth and leaf-level physiology in (1) seedling families from seed trees that have previously been inferred to carry or not carry Cr4, the dominant R gene allele conferring complete, gene-for-gene resistance to WPBR in limber pine, and (2) populations that were and were not infected with C. ribicola. We found that, in the absence of C. ribicola exposure, there was no significant difference in carbon relations between families born from seed trees that harbor the resistance allele compared to those that lack it, either to plant growth and phenology or leaf-level photosynthetic traits. However, post-infection with C. ribicola, growth was significantly reduced in inoculation survivors expressing complete resistance compared to uninoculated seedlings. Furthermore, inoculation survivors exhibited significant increases in a suite of traits including photosynthetic rate, respiration rate, leaf N, and stomatal conductance and a decrease in photosynthetic water-use efficiency. The lack of constitutive carbon costs associated with Cr4 resistance in non-stressed limber pine is consistent with a previous report that the R gene allele is not under selection in the absence of C. ribicola and suggests that host resistance may not bear a constitutive cost in pathosystems that have not coevolved. However, under challenge by C. ribicola, complete resistance to WPBR in limber pine has a significant cost to plant growth, though enhanced carbon acquisition post-infection may offset this somewhat. These costs and effects on performance further complicate predictions of this species’ response in warmer future climates in the presence of WPBR.

The future of subalpine forests in the Southern Rocky Mountains: Trajectories for Pinus aristata genetic lineages

“…Currently, the disease has only been found on bristlecone pine in south-central Colorado [ 72 ] in the area that contains lineage group 3 [ 22 ]. Genetic resistance to WPBR is not distributed uniformly within the five-needle pine species, including bristlecone pine [ 22 ], and how disease resistance traits are associated with abiotic stress tolerances is unclear but may be significant [ 73 , 74 ]. Consequently, the climate space of five-needle pines may be shifting under directional selection for resistance to WPBR [ 73 , 74 ], further complicating climate change projections.…”

“…Genetic resistance to WPBR is not distributed uniformly within the five-needle pine species, including bristlecone pine [ 22 ], and how disease resistance traits are associated with abiotic stress tolerances is unclear but may be significant [ 73 , 74 ]. Consequently, the climate space of five-needle pines may be shifting under directional selection for resistance to WPBR [ 73 , 74 ], further complicating climate change projections. Range-wide genetic collections (seed and tissues) of bristlecone pine have been made and these efforts are the first proactive coordinated range-wide genetic collection design and forest health assessment for a threatened, but not yet heavily impacted, tree species [ 21 ].…”

Is Resistance to Mountain Pine Beetle Associated with Genetic Resistance to White Pine Blister Rust in Limber Pine?

“…Genetic resistance in a species to a novel biotic stress for which it has not co-evolved may be neutral or carry a benefit to the host via a function that offers adaptive benefit for environmental factor(s), biotic or abiotic, under which it co-evolved [47]. Knowing the complete resistance status of trees in populations naïve to WPBR enables us to assess if adaptations to other stresses are associated with complete resistance and may provide insights into the evolutionary history of this resistance trait [47,48]. We hypothesized that MPB may be such a stress for limber pine, however, our data on resin duct traits suggest otherwise.…”

“…This may occur in populations with trees with complete resistance but is less likely for trees with quantitative resistance. Complete (qualitative) resistance (i.e., Cr4) prevents WPBR from developing, however, there is still a carbon cost to the tree for expressing the immunity response upon infection by C. ribicola [48] which may be sufficiently high to affect MPB attack. Trees with quantitative resistance still develop the WPBR disease, albeit more slowly [65], and may therefore be preferentially attacked by MPB.…”

“…In the Southern Rocky Mountains the frequency of the Cr4 allele in limber pine is estimated at 5.0% and shows greater range among sites (0% to 13.9%) [39] than current data on Cr2 in western white pine (<0.1%; range of 0% to 0.8%) [45] and Cr1 in sugar pine range-wide (2.2%; range of 0% to 8.9%) [46]. Without past exposure to and selection pressure by WPBR, the origins of the Cr alleles remain enigmatic [39,40,45,47,48].…”