Temperature stress and plant sexual reproduction: uncovering the weakest links

Abstract

The reproductive (gametophytic) phase in flowering plants is often highly sensitive to hot or cold temperature stresses, with even a single hot day or cold night sometimes being fatal to reproductive success. This review describes studies of temperature stress on several crop plants, which suggest that pollen development and fertilization may often be the most sensitive reproductive stage. Transcriptome and proteomic studies on several plant species are beginning to identify stress response pathways that function during pollen development. An example is provided here of genotypic differences in the reproductive stress tolerance between two ecotypes of Arabidopsis thaliana Columbia (Col) and Hilversum (Hi-0), when reproducing under conditions of hot days and cold nights. Hi-0 exhibited a more severe reduction in seed set, correlated with a reduction in pollen tube growth potential and tropism defects. Hi-0 thus provides an Arabidopsis model to investigate strategies for improved stress tolerance in pollen. Understanding how different plants cope with stress during reproductive development offers the potential to identify genetic traits that could be manipulated to improve temperature tolerance in selected crop species being cultivated in marginal climates.

Fig. 1.

Diagram depicting the reciprocal crossing strategy employed in experiments to determine the reproductive tissue responsible for temperature stress sensitivity. The Pollen Donor Plant is represented by ‘♂’ and the Female Receptor Plant is represented by ‘♀’. The panel at the bottom highlighted in grey represents temperature-stressed male and female contributions. Arrows depict the possible combination of crosses. The dashed line represents temperature-stressed male contributions and the solid line represents the control temperature male contribution.

Fig. 2.

Distribution of seed set within a silique showing relative patterns of seed set reduction in Arabidopsis plants subjected to a stress of hot days and cold nights. (A) In comparison to the even distribution of seeds in the Col ecotype, the Hi-0 ecotype showed a seed set clustered towards the stigma end. (B) The percentage seed set in each silique quadrant for stressed plants was determined by comparison to control Col and Hi-0 plants grown with 16 h of light (at 20 °C) and 8 h of dark (at 18 °C), respectively. The hot/cold-stress was implemented by growing plants in a growth chamber with 16 h of light (day) and 8 h dark (night). Plants were subjected a hot/cold-stress regime continuously from the initiation of bolting until silique maturity. This regime involved a gradual shift from a day-time peak hot stress of 40 °C, to a night-time cold stress at –1 °C. Specifically, at daybreak the temperature was shifted over 5 h from –1 °C to a 1 h peak at 40 °C, followed by a drop to 10 °C for 10 h. At the onset of night, the temperature was dropped to –1 °C for 8 h. Error bars represent the ratio of standard errors of the experimental quadrant seed set over the standard errors of the control quadrant seed set.

Fig. 3.

Aniline blue staining of pistils shows Hi-0 pollen tubes with stress-dependent defects in growth potential and tropism. Arabidopsis ecotypes Hi-0 and Col were subjected to a hot/cold stress as described in Fig. 2. Pistils from self-fertilized flowers were stained with aniline blue to reveal the locations of pollen tubes. Flowers of Col and Hi-0 were collected at identical growth stages. (A) Pollen tubes in the Col ecotype showed a uniform targeting of ovules throughout the pistil. B) Pollen tubes in the Hi-0 ecotype were only occasionally observed to target the ovule, and only two pollen tubes extended beyond the first half of the pistil. The pistil halves are indicated by the white dotted line (1/2). The white arrows (designated ‘T’) point to examples of ovules successfully targeted by pollen tubes. The white arrows (designated ‘L’) specify the location of the longest pollen tube in the pistils. Images shown are representative of approximately 6–8 pistils analysed for each ecotype. (C) Distribution of ovules targeted by pollen for Col and Hi-0 Arabidopsis ecotypes grown under hot/cold conditions. Aniline blue-stained pistils were used to determine the percentage of pollen-targeted ovules in each pistil quadrant. Error bars represent the standard error.