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Plant Signal Behav. Jul 2011; 6(7): 930–933.
Published online Jul 1, 2011. doi:  10.4161/psb.6.7.15315
PMCID: PMC3257764
How does timing, duration and severity of heat stress influence pollen-pistil interactions in angiosperms?
John L Snidercorresponding author1 and Derrick M Oosterhuis2
1USDA-ARS; Dale Bumpers Small Farms Research Center; Booneville, AR USA
2Department of Crop; Soil and Environmental Sciences; University of Arkansas; Fayetteville, AR USA
corresponding authorCorresponding author.
Correspondence to: John Snider; Email: john.snider/at/ars.usda.gov
Received February 28, 2011; Accepted March 1, 2011.
Reproductive development in sexual plants is substantially more sensitive to high temperature stress than vegetative development, resulting in negative implications for food and fiber production under the moderate temperature increases projected to result from global climate change. High temperature exposure either during early pollen development or during the progamic phase of pollen development will negatively impact pollen performance and reproductive output; both phases of pollen development are considered exceptionally sensitive to moderate heat stress. However, moderately elevated temperatures either before or during the progamic phase can limit fertilization by negatively impacting important pollen pistil interactions required for successful pollen tube growth toward the ovules. This mini-review identifies the impacts of heat stress on pollen-pistil interactions and sexual reproduction in angiosperms. A special emphasis is placed on the biochemical response of the pistil to moderately high temperature and the resultant influence on in vivo pollen performance and fertilization.
Key words: pollen-pistil interaction, carbohydrates, heat stress, fertilization, pollen tube growth, climate change
Sexual reproduction is substantially more sensitive to moderately high temperature stress than vegetative processes.1 Consequently, the yield of crops with valuable reproductive structures used for food (i.e., grain crops and horticultural crops) and fiber (i.e., cotton) would be especially sensitive to moderately elevated temperatures projected to result from global climate change. Sexual reproduction in angiosperms occurs in essentially three stages: gametophyte development (from meiosis to pollination), the progamic phase (from pollination to zygote formation) and embryo development (from zygote to seed).2 During the pro-gamic phase, a number of reproductive processes must occur in a highly concerted fashion for successful fertilization to occur. (1) Anther dehiscence allows mature pollen grains to be transferred to a receptive stigmatic surface; (2) pollen grains germinate and pollen tubes penetrate the stigmatic surface of the pistil; (3) pollen tubes grow through the transmitting tissue of the style and towards a sexually competent ovule; finally, (4) double fertilization produces a zygote and its associated endosperm. Inhibition of any one of the aforementioned processes during the progamic phase, will necessarily limit seed development.3
Although the timing and precise coordination of events during the progamic phase are strongly determined by genotype and occur in a unique and well-defined manner for a given species,4 the environment encountered either before or during the pro-gamic phase also exerts considerable control over the fertilization process, and can strongly influence reproductive success.5 Consequently, high temperature has been shown to substantially limit fertilization in vivo.5 Depending upon the timing, duration and severity, heat stress can limit fertilization5 by (1) inhibiting male6 and female5,7 gametophyte development, (2) inhibiting pollen germination,6,8,9 (3) limiting pollen tube growth,811 or (4) by altering the development of tissues required to carry out reproductive processes (i.e., anther and pistil tissues).1 Although the existing literature concerning heat stress and reproductive development in sexual plants is exhaustive (reviewed in ref. 1 and 2), the approaches used by various investigators to elucidate plant reproductive responses to high temperature vary substantially from study to study. Consequently, it is the aim of this review to characterize the impact of timing, duration and severity of heat stress on sexual processes occurring during the progamic phase. A special emphasis is placed on the biochemical response of the pistil to moderately high temperature and the resultant influence on in vivo pollen performance.
Given the importance of fertilization in determining yield, a number of reports have been aimed at identifying the most thermosensitive stage of reproductive development. For example, it was reported that short-term exposure (3 h) of tomato (Lycopersicon esculentum) plants to excessively high temperatures (40°C) during the meiotic phase of mega- and micro-gametophyte development (9–7 days prior to anthesis) resulted in degeneration of pollen tetrads and subsequent degeneration of the ovule.12 Additionally, the same high temperature treatment following pollination completely prevented fertilization and resulted in ovule abortion.13 These results illustrated that even short term exposure to extreme temperatures imposed at any point prior to fertilization will likely limit a broad spectrum of reproductive processes and consequently decrease or prevent fertilization. Saini et al. reported that exposing wheat plants to high temperature (30°C) for three days during the meiotic stage of pollen and megaspore mother cell meiosis did not alter pollen germinability, but pollen tube guidance to the ovules was prevented due to an increase in ovule abnormalities and a decrease in the proportion of functional ovules.
A number of subsequent studies utilizing moderately high temperature exposure at different reproductive stages of development have implicated pollen development as the most heat-sensitive process in plant sexual reproduction.1416 For example, Peet et al.14 showed that reproductive output (i.e., fruit and seed production) could be completely abolished when pistils of male sterile tomato plants grown under an optimal day/night temperature regime (28/22°C) were pollinated with pollen that had developed under a high (32/26°C) day/night temperature regime. In contrast, when male sterile pistils exposed to the high day/night temperature regime were pollinated with pollen that had developed under optimal conditions, fruit set and seed per fruit were maintained at 40 and 87% of the levels observed when both pollen and pistils were kept at the optimal growth temperature. For a number of species, the meiotic phase of pollen development has been reported as an exceptionally thermosensitive stage of the reproductive process.1519 High temperature exposure during this stage of pollen development can limit fertilization and subsequent seed development by (1) decreasing the number of mature pollen grains available for pollination;15,17,19 (2) causing abnormal pollen development, resulting in decreased viability and germinability of available pollen grains;1518 and (3) resulting in abnormal anther morphology, thereby limiting anther dehiscence at anthesis.1518 Under moderately elevated temperature exposure extending from microsporogenesis to anthesis, altered carbohydrate metabolism of developing anthers and pollen grains prevents the accumulation of carbohydrates needed to drive the initial phases of pollen tube growth and accounts for poor pollen viability at anthesis.6,1922
Many of the available reports investigating the effects of high temperature on plant sexual reproduction have been in vitro studies of pollen performance (i.e., pollen germination and pollen tube growth) and have allowed researchers to identify the temperature sensitivity of the fully mature male gametophyte in isolation from either parental or female reproductive tissues. In contrast with vegetative and pistil tissues, mature pollen does not exhibit acquired thermotolerance via a typical heat shock response and is extremely sensitive to high temperature exposure.2326 For example, Dupuis and Dumas25 reported that pre-exposure of mature maize pollen to high temperature (40°C) for 4 h prior to pollination abolished in vitro fertilization even when pollination was performed on spikelets maintained at 28°C throughout the experiment. In contrast, when spikelets, previously exposed to 40°C for 4 h, were pollinated with unstressed pollen, a 43% fertilization rate was obtained.25 Based on these and other reports citing the exceptional sensitivity of pollen to heat stress, pollen performance is considered substantially more sensitive to high temperature exposure during the progamic phase than mega-gametophyte function.1,2 Consequently, numerous researchers have identified in vitro pollen germination and tube growth responses to a range of temperatures,8,9,25,2729 and have used this information to identify thermotolerant genotypes of a number of important crop species, including Arachis hypogaea,30 Gossypium hirsutum,9,31 Glycine max29 and Capsicum sp.28
The previously discussed studies have characterized pollen development and function as exceptionally heat-sensitive processes; however, it is also important to note that under natural conditions, high temperature will simultaneously impact male and female reproductive tissues, resulting in a synergistic effect on reproductive output.1 Furthermore, it has been reported that in vivo pollen performance under high temperature can be modulated by the pistil tissue that the pollen tubes grow through.32 Because a number of complex physical and biochemical pollen-pistil interactions are required for successful pollen tube growth from the stigma to the ovules,3,3336 heat-induced changes in the pistil can be expected to exert considerable control over pollen performance in vivo.
Because mature pollen grains lacking a heat shock response and exposed on the stigmatic surface of the pistil are considered more vulnerable to heat stress than the deeply seated ovules,9 many authors have utilized in vitro pollen germination and tube growth assays to screen for heat tolerant genotypes.9,2831 However, it has been reported that in vitro pollen germination and tube growth responses to high temperature are not necessarily predictive of in vivo pollen performance under elevated temperature,32,37,38 and high temperature can also limit pollen germination through loss of stigmatic receptivity.39 Furthermore, under field conditions, it was recently reported that the diurnal pattern of pollen tube growth was strongly altered by moderately elevated temperature in G. hirsutum, where pollination occurred earlier in the day under higher diurnal temperatures.11 Interestingly, pistil and air temperatures were comparable during the estimated time of pollination (Fig. 1), and pollen germination was unaffected by high temperature.11 It is interesting to speculate that temperature-dependent anther dehiscence may have allowed for pollen to be deposited on the stigmatic surface when temperatures were favorable for pollen germination in G. hirsutum.
Figure 1
Figure 1
Diurnal air temperature (A) pistil temperature (B) and in vivo pollen tube growth (C) under optimal (Tmax = 29.9°C; open circles) and high (Tmax = 34.6°C; closed circles) air temperature conditions from 06:00 to 18:00 h in 3 h increments. (more ...)
In vivo pollen tube growth is sensitive to high temperature, where above optimal temperatures accelerate tube growth in some species10,40,41 and slow tube growth in others.11,42 Given the importance of pollen-pistil interactions in determining successful pollen tube growth to the ovules, biochemical responses of the pistil to high temperature will necessarily influence pollen tube growth and fertilization. For example, heat-induced declines in fertilization efficiency have been associated with increased oxidative stress in the pistil, declines in the soluble carbohydrate and ATP content of the pistil, and decreased source leaf photosynthesis under high temperature (38/20°C).5 Subsequent research suggested that genotypic fertilization thermostability was associated with thermostable source leaf photosynthesis43 and elevated antioxidant enzyme activity in cotton pistils prior to heat stress.44 However, under field conditions and much more moderate high temperature exposure (Tmax = 34.6°C), diurnal pollen tube growth rates were significantly slowed in G. hirsutum pistils11 without any alterations in oxidative stress and ATP content of the pistil or source leaf photosynthesis.45 In contrast, high temperature significantly decreased soluble carbohydrate supply in the pistil during pollen tube growth through the style and pollen tube growth rates were highly correlated with the soluble carbohydrate content of the pistil during pollen tube growth (Fig. 2).45 It is well established that pollen tube growth transitions from an autotrophic growth phase (utilizing carbohydrate reserves preexisting within the pollen grain at the time of anthesis) to a heterotrophic growth phase (utilizing carbohydrate reserves within the transmitting tissue of the style).3,33 Given that the energy requirements of actively growing pollen tubes are approximately ten-fold higher than those of vegetative tissues,46 it is to be expected that heat-induced declines in pistil carbohydrate supply should have a pronounced affect on in vivo pollen tube growth. Consequently, the carbohydrate balance of the pistil should be strongly influenced by the moderate temperature increases projected to result from global climate change.
Figure 2
Figure 2
The relationship between pistil soluble carbohydrate concentration and pollen tube growth rate in Gossypium hirsutum pistils sampled under optimal (Tmax = 29.9°C; open circles) and high (Tmax = 34.6°C; closed circles) air temperature conditions. (more ...)
The importance of maintaining pistil carbohydrate supply under high temperature in promoting thermostable pollen tube growth should be investigated further since the available literature in this area of research is sparse. This could be addressed by (1) conducting rescue experiments to determine if the exogenous addition of soluble carbohydrates under moderate heat stress could restore pollen tube growth rates to the levels observed under optimal conditions and (2) comparing the in vivo pollen tube growth responses to moderately elevated temperature of cultivars known to differ in their pistil carbohydrate concentrations at anthesis. Additionally, the possibility that temperature dependent anther dehiscence may protect pollen grains from high temperature exposure during germination should be investigated further under a broader range of controlled environment conditions and with diverse germplasm.
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