Modeling and validation of high-temperature induced spikelet sterility in rice
Introduction
Global warming is unequivocal and surface air temperature is projected to rise by 1.4–5.8 °C at the end of this century (IPCC, 2007). The projected climate change characterized by the increase in both frequency and intensity of high temperature along with its large variability is expected to become a major detrimental factor to rice production in most rice growing regions including temperate region in the future. Generally, high temperature stress effect on grain yield is greater during reproductive stage than during vegetative stage (Yoshida, 1981). High temperature during reproductive stage reduces the number of spikelets produced per unit dry weight or nitrogen absorbed (Yoshida, 1983), the spikelet fertility (Satake and Yoshida, 1978, Tashiro and Wardlaw, 1991, Kim et al., 1996, Matsui et al., 1997a, Matsui et al., 1997b), and grain weight by accelerating the panicle senescence (Kim et al., 2011), leading to the decrease of grain yield. High temperature-induced spikelet sterility has been an important factor to decrease rice yield and its variability only in tropical Asia (Osada et al., 1973) and Africa (Matsushima et al., 1982), but would become a prominent detrimental factor even in temperate rice growing regions in the future (Horie et al., 1995).
Sterility induction by high temperature is most sensitive at flowering time and next at meiotic stage of spikelet that falls on 12 days before flowering (Satake and Yoshida, 1978). During microsporogenesis the processes close to the meiotic stage are most sensitive to high temperature (Yoshida, 1981). A significant decrease in pollen production was found at 5 °C above ambient temperature (Prasad et al., 2006) that was attributed to impaired cell division of pollen mother cell (Takeoka et al., 1992). In rice, the reproductive processes that occur within one hour after anthesis–dehiscence of anther, shedding of pollen, germination of pollen grains on stigma, and elongation of pollen tubes, are most sensitive to high temperatures and are disrupted at day temperatures above 33.8 °C, leading to spikelet sterility (Satake and Yoshida, 1978). Therefore, an hour exposure of high temperature during flowering is enough to induce spikelet sterility (Jagadish et al., 2007, Satake and Yoshida, 1978) and spikelet opened beyond ±1 h of the high temperature exposure are not affected (Satake and Yoshida, 1978, Wassmann et al., 2009). Among these reproductive processes occurring within one hour after anthesis, anther dehiscence is the most susceptible process under high temperature (Matsui et al., 1999b). High temperatures at flowering inhibit swelling of the pollen grains (Matsui et al., 2000), which is the driving force for anther dehiscence in rice (Matsui et al., 1999a, Matsui et al., 1999b). Sterility is caused by poor anther dehiscence and low pollen production, and hence low numbers of germinating pollen grains on the stigma (Matsui et al., 2000, Matsui et al., 2001, Prasad et al., 2006). Weerakoon et al. (2008) reported that grain sterility increased with increased humidity under high temperature above the critical value that induces spikelet sterility in rice. Similarly, Matsui et al. (1997b) found that spikelet sterility was further aggravated with higher air humidity and higher wind velocity through disturbance of pollination process. He observed that the fertility of spikelets flowered at 37.5 °C was highest at 45% relative humidity (RH), followed by that at 60% RH, and lowest at 80% and wind speed over 0.85 m s−1 decreased spikelet fertility at 37.5 °C.
Many studies have shown that there are varietal differences in the tolerance to high temperature-induced sterility during flowering (Osada et al., 1973, Satake and Yoshida, 1978, Yoshida, 1981, Jagadish et al., 2007, Matsui et al., 2001, Matsui et al., 2005). For instance, Matsui et al. (2001) reported that difference of the temperature causing 50% spikelet sterility was about 3 °C between the tolerant variety “Akitakomatch” (40 °C) and the susceptible variety “Hinohikari” (37 °C). Although heat tolerant varieties have been found in both indica and japonica subspecies, it has been suggested that indica types are more tolerant to higher temperatures than japonica ones (Satake and Yoshida, 1978, Matsui et al., 2001).
Generally, spikelet sterility response to high temperature has been modeled using daily mean maximum temperature during 10 day period close to heading (Matsui and Horie, 1992, Horie et al., 1995), number of days with maximum temperature above 34 °C (Challinor et al., 2007), and daily maximum and minimum temperature (Krishnan et al., 2007). These models have taken into account the genotypic difference in the critical temperature causing sterility while they have not considered the temperature x duration interaction effect on spikelet sterility and the non-synchrony of the dates of panicle heading and thus flowering date and time in the field. However, Jagadish et al. (2007) reported an interaction between high temperature and duration of exposure was found in a heat-sensitive genotype “Azucena” but not in a moderately tolerant genotype “IR 64”, and the linear relationship between the logits of percent spikelet fertility and the accumulated hourly temperature above 33 °C.
As reviewed above, the effect of high temperature on spikelet sterility is seems to be limited only to the time of spikelet flowering and microsporogenesis and also spikelets in the field are exposed to different temperature at flowering time because flowering of rice in the field and even on the same panicle occurs over an extended time period of 15–20 and 7–10 days, respectively, due to the non-synchrony of tillering and thus heading date of panicles (Yoshida, 1981). Therefore, the accuracy of modeling the temperature effects on spikelet sterility depends on the diurnal time course of temperature and on the accuracy of the model in predicting the probability distribution of flowering date and time in the field. This is particularly true when temperature varies considerably from day to day. However, only a model (Shi et al., 2007) considered this flowering habit in predicting high temperature–induced sterility of rice, but this model also did not include high temperature-induced sterility at meiosis.
In this regards, a simulation model considering the flowering habit was constructed, calibrated, and validated for predicting spikelet sterility induced by high temperature during meiosis and flowering time of spikelet in the rice field.
Section snippets
Model description
Based on the literature review, we assumed that high temperature-induced sterility of spikelet is sensitive at meiotic stage and spikelet opening time (Satake and Yoshida, 1978, Yoshida, 1981), high temperature at one hour before and after flower opening does not induce sterility (Satake and Yoshida, 1978, Wassmann et al., 2009), and one hour exposure to high temperature during spikelet opening is enough to induce sterility (Jagadish et al., 2007, Satake and Yoshida, 1978). As assumed, not only
Heading date distribution of panicles
The heading dates of all the panicles from four pots for each temperature treatment were recorded every day from the initial heading date. Heading of panicles continued until about 12 days after initial heading in both cultivars and reached peak around five days and three days after initial heading in Hwaseongbyeo and Dasanbyeo, respectively (Table 1; Fig. 1). As this temporal courses of panicle heading were not significantly different among temperature treatments from initial heading
Discussion
The simulation model was comprised of equations to estimate the probability distributions of heading date of panicles in the field, flowering date of spikelets on a panicle, and flowering time of spikelets during the day time, and two sterility response functions to the temperature on the day of meiosis and at flowering time of a spikelet. To collect the data for model calibration, rice plant of a japonica “Hwaseongbyeo” and a Tongil type “Dasanbyeo” were grown under ambient temperature and
Acknowledgement
This work was funded by the Korea Meteorological Administration Research and Development Program under Grant Weather Information Service Engine(WISE) project, 153-3100-3133-302-350.
References (39)
- et al.
Variation in time of day of anthesis in rice in different climatic environments
Eur. J. Agron.
(2012) - et al.
Relationship between grain filling duration and leaf senescence of temperate rice under high temperature
Field Crop Res.
(2011) - et al.
Impact of elevated CO2 and temperature on rice yield and methods of adaptation as evaluated by crop simulation studies
Agric. Ecosyst. Environ.
(2007) - et al.
Effect of high temperature and CO2 concentration on spikelet sterility in indica rice
Field Crop Res.
(1997) - et al.
Mechanism of anther dehiscence in rice (Oryza sativa L.)
Ann. Bot.
(1999) - et al.
Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress
Field Crops Res.
(2006) - et al.
Effect of high temperature at meiosis stage on seed-setting rate in rice
Acta Agron. Sin.
(2008) - et al.
Climate change affecting rice production: the physiological and agronomic basis for possible adaptation strategies
Adv. Agron.
(2009) - et al.
Effect of heat stress during meiosis on grain yield of rice cultivars differing in heat tolerance and its physiological mechanism
Acta Agron. Sin.
(2008) - et al.
Assessing the vulnerability of food crop systems in Africa to climate change. Assessing the vulnerability of food crop systems in Africa to climate change
Clim. Chang.
(2007)
Characterization of Changes in Grain Filling and Sink/Source Ratio of Rice Cultivars in Response to Seeding Time
Modelling Potential Crop Growth Processes
Spikelet sterility of rice observed in the record hot summer of 2007 and the factors associated with its variation
J. Agric. Meteor.
The rice simulation model SIMRIW and its testing
The Growing Rice Plant: An Anatomical Monograph
Climate change 2007: impacts, adaptation and vulnerability
High temperature stress and spikelet fertility in rice (Oryza sativa L.)
J. Exp. Bot.
Effects of elevated CO2 concentration and high temperature on growth and yield of rice. II. The effect on yield and its components on Akihikari rice
Jpn. J. Crop Sci.
Effects of temperature, solar radiation, and vapor-pressure deficit on flower opening time in rice
Plant Prod. Sci.
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Both authors contributed equally to this work.