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. 2018 Apr 30;9:536.
doi: 10.3389/fpls.2018.00536. eCollection 2018.

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

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Free PMC article

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

Lluvia Flores-Rentería et al. Front Plant Sci. .
Free PMC article

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.

Keywords: Pinus edulis; acclimation; elevational gradient; global climate change; heat stress; pollen development; pollen germination and viability; reproduction.

Figures

FIGURE 1
FIGURE 1
Experimental design. Experiment 1: Pollen from 24 trees was collected and warmed at different temperatures, pollen during the dispersal stage: 30, 35, 40, and 4°C which served as a control of optimal storage conditions (not shown in the figure). Reciprocal temperature treatments were also done during germination: 30, 35, and 40°C. This experiment was performed in 2012 from trees at the elevational gradient site 7. Experiment 2: Vegetation composition was determined at 11 sites along an elevational gradient (0–10). From sites 1–9, where pinyon pines were present, six trees per site were studied and pollen was warmed simulating the two temperature treatments, dispersal and germination, in a reciprocal fashion, as shown in the figure. Site 9 was excluded from the analysis because of its low pollen production. In the region of our study, there is a change in temperature of 4°C in a little over 200 m represented by the color gradient bar on the left, lower elevations experience higher temperature – red, compared to higher elevations – green.
FIGURE 2
FIGURE 2
Viable pollen with pollen tube germinating (right) and non-viable pollen without pollen tube (left). Bar = 50 μm.
FIGURE 3
FIGURE 3
Pollen viability/germinability from 2012 from trees at 2010 m of elevation experimentally subjected to (A) 30, (B) 35, and (C) 40°C. (D) Mean percentage pollen germination when pollen was incubated at 4, 30, 35, and 40°C during pollen dispersal as a precondition treatment and reciprocally germinated at 30 (green), 35 (yellow), and 40°C (red). Error bars represent one standard error from the mean.
FIGURE 4
FIGURE 4
The phase of pollen development observed in P. edulis at June 1 2013 across an elevational gradient near Sunset Crater Arizona. There is a negative relationship between pollen development and elevation. Temperature difference between low and high elevation in the elevational gradient for P. edulis was 4°C, with 28, 30, and 32°C for high, middle, and low elevation, respectively, when considering only daylight temperatures.
FIGURE 5
FIGURE 5
Elevation correlates negatively with (A) average shoot growth (cm) of Pinus edulis and (B) water stress inferred by isotopic δC13 preference. (C) Elevation correlates positively with C:N ratio. Each point represents the data for a single tree.
FIGURE 6
FIGURE 6
Quadratic distribution of pollen viability/germinability of P. edulis along an elevational gradient showing higher pollen germination from sites at middle elevation.
FIGURE 7
FIGURE 7
Mean percentage viability of pollen incubated at 30, 35, and 40°C at dispersal and reciprocally germinated at 30 (green), 35 (yellow), and 40°C (red) along the elevational gradient using all sites combined. Error bars were constructed using one standard error from the mean.

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