Higher Temperature at Lower Elevation Sites Fails to Promote Acclimation or Adaptation to Heat Stress During Pollen Germination

Abstract

High temperatures associated with climate change are expected to be detrimental for aspects of plant reproduction, such as pollen viability. We hypothesized that (1) higher peak temperatures predicted with climate change would have a minimal effect on pollen viability, while high temperatures during pollen germination would negatively affect pollen viability, (2) high temperatures during pollen dispersal would facilitate acclimation to high temperatures during pollen germination, and (3) pollen from populations at sites with warmer average temperatures would be better adapted to high temperature peaks. We tested these hypotheses in Pinus edulis, a species with demonstrated sensitivity to climate change, using populations along an elevational gradient. We tested for acclimation to high temperatures by measuring pollen viability during dispersal and germination stages in pollen subjected to 30, 35, and 40°C in a factorial design. We also characterized pollen phenology and measured pollen heat tolerance using trees from nine sites along a 200 m elevational gradient that varied 4°C in temperature. We demonstrated that this gradient is biologically meaningful by evaluating variation in vegetation composition and P. edulis performance. Male reproduction was negatively affected by high temperatures, with stronger effects during pollen germination than pollen dispersal. Populations along the elevational gradient varied in pollen phenology, vegetation composition, plant water stress, nutrient availability, and plant growth. In contrast to our hypothesis, pollen viability was highest in pinyons from mid-elevation sites rather than from lower elevation sites. We found no evidence of acclimation or adaptation of pollen to high temperatures. Maximal plant performance as measured by growth did not occur at the same elevation as maximal pollen viability. These results indicate that periods of high temperature negatively affected sexual reproduction, such that even high pollen production may not result in successful fertilization due to low germination. Acquired thermotolerance might not limit these impacts, but pinyon could avoid heat stress by phenological adjustment of pollen development. Higher pollen viability at the core of the distribution could be explained by an optimal combination of biotic and abiotic environmental factors. The disconnect between measures of growth and pollen production suggests that vigor metrics may not accurately estimate reproduction.

Long-Term Studies Reveal Differential Responses to Climate Change for Trees Under Soil- or Herbivore-Related Stress

“…Our findings that male reproduction was negatively affected by drought supports other research documenting the potential sensitivity of pinyon pine reproduction to climate change. Cone production has declined broadly across the landscape (Redmond et al, 2012) and pollen germination is impaired by the temperatures that P. edulis is predicted to experience as climate changes (Flores-Renteria et al, 2018). In this long-term study, we also saw declines in the production of male strobili with drought.…”

“…Our data indicate that drought is likely to increase this difference; declining strobili production following drought suggest that resistant trees are even less likely to serve as pollen donors under drought. Research on pollen viability conducted on cinder soils showed that P. edulis pollen was highly sensitive to the temperatures predicted with climate change during both the dispersal and germination stages of development (Flores-Renteria et al, 2018). Further research is necessary to determine if resistant and susceptible trees now differ in pollen viability, potentially further shifting male function to moth susceptible, drought tolerant trees.…”

Heat stress leads to rapid lipid remodelling and transcriptional adaptations in Nicotiana tabacum pollen tubes

“…Various sorghum genotypes show in vitro pollen germination reductions of 2-95 % under different heat stresses (Sunoj et al, 2017). In vivo experiments with pollen from rice or the pine Pinus edulis gave similar results (Flores-Rentería et al, 2018;Shi et al, 2018).…”

A method for experimental warming of developing tree seeds with a common garden demonstration of seedling responses

“…Tree life history stages from reproduction through seedling establishment are vulnerable to abiotic stress related to climate warming [ 13 ]. High temperatures and drought can limit seed production [ 2 , 14 ] and seedling establishment [ 15 ]. Temperature affects the production and quality of tree seeds in forests ranging from dry temperate [ 14 ] to subarctic regions [ 16 ].…”

“…High temperatures and drought can limit seed production [ 2 , 14 ] and seedling establishment [ 15 ]. Temperature affects the production and quality of tree seeds in forests ranging from dry temperate [ 14 ] to subarctic regions [ 16 ]. Longer periods of seed development (e.g.…”