Tree genetics defines fungal partner communities that may confer drought tolerance

Abstract

Plant genetic variation and soil microorganisms are individually known to influence plant responses to climate change, but the interactive effects of these two factors are largely unknown. Using long-term observational studies in the field and common garden and greenhouse experiments of a foundation tree species (Pinus edulis) and its mutualistic ectomycorrhizal fungal (EMF) associates, we show that EMF community composition is under strong plant genetic control. Seedlings acquire the EMF community of their seed source trees (drought tolerant vs. drought intolerant), even when exposed to inoculum from the alternate tree type. Drought-tolerant trees had 25% higher growth and a third the mortality of drought-intolerant trees over the course of 10 y of drought in the wild, traits that were also observed in their seedlings in a common garden. Inoculation experiments show that EMF communities are critical to drought tolerance. Drought-tolerant and drought-intolerant seedlings grew similarly when provided sterile EMF inoculum, but drought-tolerant seedlings grew 25% larger than drought-intolerant seedlings under dry conditions when each seedling type developed its distinct EMF community. This demonstration that particular combinations of plant genotype and mutualistic EMF communities improve the survival and growth of trees with drought is especially important, given the vulnerability of forests around the world to the warming and drying conditions predicted for the future.

Keywords: climate change; drought; ectomycorrhizal fungi; host genetics; plant-soil feedback.

Fig. 1.

(A) Nonmetric multidimensional scaling ordination of P. edulis EMF community composition showing that seed source (symbol color), but not inoculum source (symbol shape), influenced the EMF community composition of P. edulis seedlings. Light orange symbols represent seeds from drought-intolerant mothers, and light green symbols represent seeds from drought-tolerant mothers. Squares represent inoculum from drought-tolerant mothers and diamonds represent inoculum from drought-intolerant mothers. Points are the centroid of the EMF community, with lines depicting ±1 SE. The closer centroids are to one another, the more similar the EMF community. (B) Nonmetric multidimensional scaling ordination of the EMF communities of drought-tolerant and drought-intolerant adult trees in the field and seedlings grown from the seeds of drought-tolerant and drought-intolerant trees. The communities of adult trees are shown by large circles (dark green, drought tolerant; dark orange, drought intolerant), and the communities of seedlings are indicated by smaller squares (light green, seeds from drought-tolerant trees; light orange, seeds from drought-intolerant trees). Points are centroids, with lines depicting ±1 SE. Icons show the morphology of adult drought-intolerant (tall, upright) and drought-tolerant (prostrate, shrub-like) trees.

Fig. 2.

Mean (+1 SE) dry biomass of seedlings from drought-intolerant (light orange bars; tree icon with upright architecture) and drought-tolerant (light green bars; tree icon with shrub-like architecture) mothers grown with live EMF or sterilized EMF inoculum in drought conditions. Seedlings grown from drought-tolerant seeds received inoculum from drought-tolerant trees (live vs. sterile), and seedlings grown from drought-intolerant seeds received inoculum from drought-intolerant trees (live vs. sterile).

Fig. S1.

Positive relationship between the relative abundance of Geopora ectomycorrhizas and biomass in seedlings of drought-intolerant mothers from the Greenhouse EMF drought experiment (R² = 0.367; F_1,8 = 5.65; P = 0.05). Please see the text of the manuscript for Methods.

Fig. 3.

Mean shoot (±1 SE) growth of drought-intolerant (orange bars) and drought-tolerant adult trees (green bars) during a 20-y period (n = 11 trees/group). Predrought bars illustrate 10-y mean shoot growth from 1986 to 1995, when conditions were relatively moist, and drought bars represent the 10-y mean shoot growth from 1997 to 2006, when drought conditions prevailed.

Fig. 4.

Similar patterns of mortality and growth of adult drought-intolerant (dark orange bars) and drought-tolerant (dark green bars) trees at the field site and of seedlings of these trees in a common garden (light orange bars, seedlings from drought-intolerant mothers; light green bars, seedlings from drought-tolerant mothers). Mortality data for adult trees resulted from extreme drought in 2002 and were previously published (17). Growth data for adult trees are mean shoot length in millimeters (+1 SE) of drought-tolerant and drought-intolerant trees over the course of 10 y of drought (1997–2006). These data are shown in Fig. 3 but are presented here for comparison with seedling data. Seedling mortality data are mean mortality (±1 SE) over the course of 2 y, and seedling growth is mean cumulative total shoot growth in centimeters (±1 SE) during the same 2 y. The photograph shows common garden seedlings from a drought-intolerant mother (within circle on left) and a drought-tolerant mother (within circle on right) to illustrate size differences.