Hotter droughts alter resource allocation to chemical defenses in piñon pine

Abstract

Heat and drought affect plant chemical defenses and thereby plant susceptibility to pests and pathogens. Monoterpenes are of particular importance for conifers as they play critical roles in defense against bark beetles. To date, work seeking to understand the impacts of heat and drought on monoterpenes has primarily focused on young potted seedlings, leaving it unclear how older age classes that are more vulnerable to bark beetles might respond to stress. Furthermore, we lack a clear picture of what carbon resources might be prioritized to support monoterpene synthesis under drought stress. To address this, we measured needle and woody tissue monoterpene concentrations and physiological variables simultaneously from mature piñon pines (Pinus edulis) from a unique temperature and drought manipulation field experiment. While heat had no effect on total monoterpene concentrations, trees under combined heat and drought stress exhibited ~ 85% and 35% increases in needle and woody tissue, respectively, over multiple years. Plant physiological variables like maximum photosynthesis each explained less than 10% of the variation in total monoterpenes for both tissue types while starch and glucose + fructose measured 1-month prior explained ~ 45% and 60% of the variation in woody tissue total monoterpene concentrations. Although total monoterpenes increased under combined stress, some key monoterpenes with known roles in bark beetle ecology decreased. These shifts may make trees more favorable for bark beetle attack rather than well defended, which one might conclude if only considering total monoterpene concentrations. Our results point to cumulative and synergistic effects of heat and drought that may reprioritize carbon allocation of specific non-structural carbohydrates toward defense.

Keywords: Drought; Heat; Ips confusus (piñon engraver beetle); Monoterpenes; Non-structural carbohydrates.

Fig. 1

Differences in relative growth rate, net assimilation rate, non-structural carbohydrates (NSCs), and constitutive secondary metabolism across a gradient of resource availability as predicted by a the growth-differentiation balance hypothesis (modified from Fig. 1 of Herms and Mattson 1992). b Mid-day photosynthesis rate (A_max;), c shoot growth rate, d total needle NSCs, e needle total monoterpene concentrations, and f) woody tissue total monoterpene concentrations from our study are shown as a function of pre-dawn water potential. Each set of data represent all the time points available from 2012 to 2016 for that analysis and relationships between total monoterpenes and pre-dawn water potentials are on a 1-month lag. The best-fit repeated measures regression lines are displayed along with the corresponding equation, R², repeated measures correlation coefficient (r), P value, and sample sizes (n). Throughout, different colors refer to different trees

Fig. 2

Total monoterpene compound concentrations (mg g FW-1) in a Pinus edulis needles and b woody tissue across the four treatments averaged over nine sampling periods from 2012 to 2016. Bars are means ± SEM and significant differences between treatments is expressed using differing lowercase letters (α < 0.05)

Fig. 3

Time series data representing means (± SEM) of total monoterpene concentrations (mg g FW⁻¹) a needles and b woody tissue for Pinus edulis exposed to the four treatments across nine sampling dates from 2012 to 2016. Totals were calculated by summing all identified monoterpenes for each tree (n = 14 for needle tissue; n = 16 for woody tissue) within each treatment (n = 4) during each sampling period. Different colored asterisks represent a significant difference from ambient (⍺ < 0.05) for that treatment

Fig. 4

Repeated measures correlations between total monoterpene concentrations (mg g FW⁻¹) and primary shoot growth rates (mm day⁻¹) in a needles and b woody tissue in Pinus edulis from the four treatments for six sampling periods from 2013 to 2014. Solid lines represent the best-fit repeated measures regression line for the data and the linear equations, P values, repeated measures correlation coefficients (r), and sample sizes (n) are presented

Fig. 5

The relationships between a needle total monoterpene concentrations (mg g FW⁻¹) and starch content (% dry weight) measured during the same month, and between woody tissue total monoterpene concentration and b starch and c glucose + fructose on a 1-month time lag. Solid lines represent the best-fit repeated measures regression line for the data and the linear equations, P-values, repeated measures correlation coefficients (r), and sample sizes (n) are presented

Fig. 6

Nonmetric multidimensional scaling (NMDS) of treatment effect on monoterpene composition in Pinus edulis a needles and b woody tissue across the four treatments averaged over nine sampling periods (2012–2016). Ellipses encircle the centroids (diamonds) and the relative monoterpene composition of all the tree individuals from the same treatment

Fig. 7

Mean individual monoterpene concentrations (mg g⁻¹ FW) of six compounds found in Pinus edulis current and one-year old needle tissue across the four treatments averaged over nine sampling periods (2012–2016). a (−)-α-Pinene, b (+)-α -pinene, c β -myrcene, d δ-3-carene, e S-(-)-limonene, f) R-( +)-limonene. Compounds were chosen to highlight the variation in responses across treatments and tissues. Bars represent means ± SEM and significance between treatments is expressed using different lowercase letters (α < 0.05)

Fig. 8

Monoterpene concentrations (mg g⁻¹ FW) of six compounds in Pinus edulis woody tissue across the four treatments averaged over nine sampling periods (2012–2016). a (−)-α-Pinene, b (+)-α -pinene, c β -myrcene, d δ-3-carene, e S-(−)-limonene, f R-(+)-limonene. Compounds were chosen to highlight the variation in responses across treatments and tissues. Bars are means ± SEM and significance between treatments is expressed using different lowercase letters (α < 0.05)