Impact of high temperature on pollen germination and spikelet sterility in rice: comparison between basmati and non-basmati varieties
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1 CSIRO PUBLISHING Crop & Pasture Science,, 61, Impact of high temperature on pollen germination and spikelet sterility in rice: comparison between basmati and non-basmati varieties Bidisha Chakrabarti A,C, P. K. Aggarwal A, S. D. Singh A, S. Nagarajan B, and H. Pathak A A Division of Environmental Sciences, Indian Agricultural Research Institute, New Delhi 1 12, India. B Nuclear Research Laboratory, Indian Agricultural Research Institute, New Delhi 1 12, India. C Corresponding author. bidisha2@yahoo.com Abstract. Increased temperature due to global warming may reduce pollen germination and induce spikelet sterility in rice crops. Anthesis is the most sensitive stage in rice and exposure to high temperature during this period may cause reduction in floral reproduction. Increased temperature will have different effects on different rice varieties. In the present study the effect of high temperature on pollen as well as on spikelet sterility in basmati (aromatic) and non-basmati (non-aromatic) rice varieties was quantified. Rice varieties were grown at 11 different sowing dates, to see the effect of varying temperature on pollen and spikelet sterility. Rise in temperature increased pollen sterility and reduced germination of pollen grains on the stigma. Temperature above 338C during anthesis gradually increased pollen sterility in all rice cultivars. At 35.58C, variety Pusa Sugandh 2 (basmati) recorded a pollen sterility of 17% and 26% reduction in pollen germination. The principal cause of sterility was reduced anther dehiscence and less pollen deposition on the stigma at higher temperature. Increased temperature during the grain-filling period also increased spikelet sterility in rice and variety Pusa Sugandh 2 was most affected. Nonbasmati rice varieties were less affected by increased temperature than basmati types. The study indicated that increasing temperature could limit rice yield by affecting pollen germination and grain formation. It also suggested that sensitivity of pollen grains to temperature damage could be taken as one of the most important parameters for predicting rice yield in warmer climates. Additional keywords: pollen sterility, basmati rice. Introduction Rice is cultivated around the world mainly in tropical and subtropical zones. Climate change resulting from increased atmospheric concentration of greenhouse gases will increase earth s surface temperature (IPCC 7). Hence, in the future, rice will be grown in much warmer environments (Battisti and Naylor 9) with a greater likelihood of high temperatures coinciding with heat-sensitive processes during the reproductive stage. This would significantly affect rice productivity, raising serious concerns about food security. Heading and flowering are the most sensitive stages of rice affected by high temperature (Tan et al. 1985). High temperature at flowering inhibits swelling of pollen grains, which is the driving force behind anther dehiscence (Matsui et al. ). Percentage of dehisced thecae is significantly correlated with the number of pollen grains deposited on the stigma. Spikelets at anthesis that were exposed to temperatures greater than 358C for ~5 days during the flowering period were sterile and set no seed (Satake and Yoshida 1978). Occurrence of sterile spikelets caused by air temperature above 358C is a constraint to rice productivity (Kim et al. 1996a, 1996b; Morokuma et al. 1996). Horie et al. (1996) concluded that high temperature at the flowering stage would induce floret sterility, negate the positive effects of elevated CO 2 concentration, and thus increase the instability of rice yield. A moderately large genetic variation in the tolerance to high temperature-induced spikelet sterility has been reported in both Indica and Japonica rice genotypes (Matsui et al. 1997a). Matsushima et al.(1982) reported the difference in susceptibility to high temperature among Indica rice varieties that were mainly cultivated in tropical Asian countries. Horie et al. (1996) demonstrated, using a crop simulation model, that adoption of high temperature-tolerant cultivars with fertility higher than 5% even when the daily maximum temperature of flowering is 38.28C is one of the most effective countermeasures to maintain high productivity and stability of rice production under climate change. Detrimental effects of rise in temperature on rice yield were reported by Baker et al. (1992). According to the study, grain yield of rice will decline by an average of 7 8% per 18C rise in temperature when daytime temperature varies between 288C and 348C. However, field validation of this modelling hypothesis was not done. The basmati varieties, known for their long grains and aroma and grown in the north-western region of India, require a relatively lower temperature during the grain-filling stage. CSIRO.71/CP //5363
2 364 Crop & Pasture Science B. Chakrabarti et al. Little information is available on the impact of increased temperature on growth and yield of these basmati rice types. The objectives of the study were to (1) determine temperature sensitivity of basmati rice compared with non-basmati cultivars, (2) quantify the impact of high temperature on pollen sterility and germination of pollen grains on the rice stigma, and (3) establish the relationship between spikelet sterility and germination of pollen grains on the rice stigma. Methods A field experiment was conducted in kharif (June October) and rabi (November April) seasons in 5 6 at the Indian Agricultural Research Institute farm, New Delhi (2884 N, E). Climate of the region is subtropical semi-arid with hot and dry summers and cold winters. Mean annual maximum temperature is 38C and the mean minimum temperature is 188C. Soil type of the experimental site was sandy loam. Five rice varieties (3 basmati and 2 non-basmati) were sown at 11 different sowing dates starting from the first week of May to mid-july at weekly interval (Table 1) in a randomised block design. Basmati varieties were Pusa Sugandh 2, Pusa Sugandh 4, and Super Basmati, and IR 64 and Pusa 44 were non-basmati cultivars. Transplanting was done at 15 cm spacing. Nitrogen was applied as urea (1 kg N/ha) in 3 equal splits. Phosphorus (3 kg P/ha) and potassium (3 kg K/ha) were applied uniformly to the puddled soil at the time of transplanting. Since time of sowing varied, flowering took place at different times, exposing the crops to different temperatures during anthesis. Rice florets ( per treatment) were sampled in the morning (9.. hours) just before anthesis. Sampling was done for 2 3 days during mid-flowering for all the dates of sowing. Florets were artificially opened by removing the lemma with the help of a needle and pollen grains were dusted from the anthers onto the slide with a brush. Pollen grains were stained with % iodine solution on a glass slide and observed under the microscope. Only fertile pollen grains were stained with iodine, while pollen grains which did not get stained were sterile. By counting the number of Sowing date Table 1. Sowing date of rice varieties Temperature Seasonal Anthesis Grain filling 1st 6.v C C C 2nd 13.v C C C 3rd.v C C C 4th 27.v C C C 5th 3.vi C C C 6th.vi C C C 7th 17.vi C C C 8th 27.vi C C C 9th 1.vii C C C th 8.vii C C C 11th 15.vii C C C stained as well as unstained grains, sterility percentage was calculated. In order to determine pollen germination percentage, 15 florets were sampled at hours. Pollen grains on the stigma were observed under a microscope by staining the stigma with cotton blue. Germinated pollen grains along with the pollen tubes were observed on the stigma. Total number of pollen grains deposited and number of pollen grains germinated on the stigma were counted to determine the pollen germination percentage. Pollen grains were observed in 5 6 randomly selected microscopic fields to determine both sterility and germination percentage of pollen grains. Ambient temperature during anthesis at 12.3 hours was recorded for each variety. Percentage of pollen germination on the stigma was correlated with the number of pollen grains deposited on the stigma. At physiological maturity, representative panicles were harvested from each plot. Percentage of sterile spikelets was determined by counting number of filled and unfilled grains in those panicles. Mean daily air temperature was recorded during the grain-filling period. Statistical analysis of data was done to determine whether differences between means were statistically significant (P <.5). Pollen sterility (%) 15 IR 64 SB PS 4 Pusa 44 PS 2 Basmati Non-basmati Basmati y = x R 2 =.542** 5 Non-basmati y =.55x R 2 = Temperature ( C) Fig. 1. Impact of temperature on pollen sterility in rice (** significant at P =.5).
3 High temperature and pollen germination and spikelet sterility Crop & Pasture Science SB IR 64 PS 4 Pusa 44 PS 2 Non-basmati Basmati Basmati y = 2.852x R 2 =.3643** Non-basmati y = 2.165x R 2 = Temperature ( C) Fig. 2. Impact of temperature on pollen germination percentage in rice (** significant at P =.5). Results and discussion Impact of temperature on pollen sterility Ambient temperature at the time of anthesis affected fertility of the pollen grains. Early sown crops took more days to flowering in all varieties. Higher temperature during anthesis increased sterility of the pollen grains (Fig. 1). This effect was greater in basmati varieties, with 21.5% sterility observed in Pusa Sugandh 4 at 34.38C. Temperature above 338C sharply increased pollen sterility in all rice cultivars. At 35.58C, Pusa Sugandh 2 recorded 17% pollen sterility. Osada et al. (1973) and Kim et al. (1996b) observed that a maximum day temperature above 358C at the flowering stage induced floret sterility in rice. In all three basmati cultivars there was a sharp increase in number of sterile pollen grains with increase in temperature, but non-basmati varieties were not much affected. At 358C, pollen sterility in Pusa Sugandh 4 was 19.4%, whereas in Pusa 44 and IR64 sterility was % and 5%, respectively. Satake and Yoshida (1978) reported that for a tolerant cultivar, floret fertility decreased to 5% at 398C, whereas a similar level of sterility for moderately tolerant and susceptible cultivars was at 36.58C and 33.58C, respectively. Impact of temperature on pollen germination Germination of pollen grains on the stigma decreased with a rise in temperature. When temperature was below 38C, more than Table 2. Pollen germination percentage of different rice varieties at three different temperature ranges Within columns, values followed by the same letter are not significantly different at P =.5 Variety Temperature range (8C) Super Basmati 56.3a 5.8b 43.8c Pusa Sugandh a 53.2ab 41.1c Pusa Sugandh a 53.8ab 44.3bc Pusa a 55.3a 49.4b IR a 57.8a 56a 5% of the pollen grains germinated on the stigma in all varieties. Pusa 44 variety recorded pollen germination of 73.9% on the stigma when mean temperature was around 298C during anthesis. But pollen germination decreased in all rice varieties above 328C (Fig. 2). Increase in temperature from 298C to 358C during anthesis caused % reduction in pollen germination. Maximum reduction in pollen germination (26%) occurred in Pusa Sugandh 2 with 68C rise in temperature at the time of flowering. Variety Pusa Sugandh 4 recorded the lowest pollen germination (32.4%) when temperature was 358C. Non-basmati cultivars showed less reduction in pollen germination than basmati types with increase in temperature. There was no y =.1849x R 2 =.76** Number of pollen grains on stigma Fig. 3. Relationship between pollen germination percentage and number of pollen grains deposited on the stigma (** significant at P =.5). Table 3. Variety Correlation between temperature, pollen sterility, and pollen germination percentage of different rice varieties Correlation coefficient Pollen sterility (%) Super Basmati Pusa Sugandh Pusa Sugandh Pusa IR
4 366 Crop & Pasture Science B. Chakrabarti et al. Spikelet sterility (%) PS 4 y = x R 2 =.599** Super basmati y = x R 2 =.197 PS 2 y = 3.55x R 2 =.6811** PS 2 PS 4 SB Pusa Sugandh 4 Pusa Sugandh 2 Super basmati T mean Fig. 4. Impact of temperature on spikelet sterility in basmati rice cultivars (** significant at P =.5). significant difference in pollen germination percentage among rice varieties when temperature at mid-flowering was C. As temperature increased, pollen germination percentage decreased in all varieties, with more reduction in basmati varieties. At a temperature of C, germination of pollen grains in Super Basmati was less than in Pusa 44 and IR 64. Further increase in temperature (33 358C) caused significant reduction in pollen germination in all three basmati varieties. At this temperature range, IR 64 showed significantly higher pollen germination (56%) on the stigma than all other varieties (Table 2). This variety was least affected in terms of pollen germination by a rise in temperature (6% reduction with 68C increase in temperature). Pollen germination in variety Pusa 44 was also significantly higher than in Super Basmati and Pusa Sugandh 4 at the highest temperature range. It proved that an increase in temperature caused reduction in pollen germination on the stigma in rice, with greater effect in basmati varieties. Matsui et al. (5) observed that viability of pollen grains for fertilisation was decreased by high temperature treatment at the time of flowering, and pollination of non-japonica cultivars was more susceptible to high temperature than that of Japonica-type cultivars. Pollen germination percentage was positively correlated with number of pollen grains deposited on the stigma irrespective of the varieties (P <.5) (Fig. 3). Matsui et al. (1997b) observed that both number of deposited and germinated pollen on the stigma were decreased at higher growth temperature in the rice crop. The principal cause of sterility at high temperature is the reduction in number of deposited pollen grains on the stigma (Satake and Yoshida 1978). More than germinated pollen grains are required for normal fertilisation of rice. Anther dehiscence is acutely sensitive to high temperature both before and during anthesis, and high temperature at flowering inhibits swelling of pollen grains (Matsui et al., 1a), which is the driving force behind anther dehiscence in rice. In the present study, increased temperature might have caused anther indehiscence, resulting in fewer pollen grains on the stigma, thereby reducing pollen germination. Mackill et al. (1982) reported that number of pollen grains per stigma at flowering is highly associated with fertility. Pollen sterility was positively correlated with temperature (P <.5). The correlation coefficient (r) between pollen sterility and increase in temperature varied from.57 to.84 in different rice cultivars. Increased temperature had the maximum effect in terms of increase in pollen sterility in Pusa Sugandh 4 (r =.84). Basmati varieties had a higher correlation with increased temperature than non-basmati varieties. A negative correlation between pollen germination on the stigma and increased temperature (P <.5) suggested that increased temperature decreased germination of pollen grains in all varieties, with a higher effect in basmati cultivars. The correlation coefficient between increased temperature and pollen germination percentage ranged from.48 to.68 (Table 3). Studies on the effect of high temperature and humidity on floral reproduction of Japonica rice cultivars by Morokuma and Yasuda (4) revealed that percentage of spikelets with few pollen grains on the stigma increased with increase in temperature and relative humidity. Varietal difference in pollination under high humidity at 318C was also observed. Impact of temperature on spikelet sterility Differential response of spikelet sterility to mean temperature during the grain-filling period was observed among rice cultivars. Spikelet sterility (%) y =.5285x R 2 =.4391** Fig. 5. Relationship between pollen germination and spikelet sterility in basmati rice cultivars (** significant at P =.5).
5 High temperature and pollen germination and spikelet sterility Crop & Pasture Science Yield 8 7 Yield (Mg ha 1 ) Fig. 6. Pollen germination percentage and yield of basmati rice cultivars. Increased temperature caused an increase in number of sterile spikelets in most of the basmati cultivars of rice. Spikelet sterility of 33.7% was observed in Pusa Sugandh 4 when mean temperature was 318C in the grain-filling period. There was a steep rise in spikelet sterility percentage with temperature increase in all three basmati rice varieties (Fig. 4). The correlation between increased temperature and spikelet sterility was greatest (r 2 =.68) in variety Pusa Sugandh 2. But the effect of increased temperature on spikelet sterility was relatively lower in Super Basmati than in the other two basmati cultivars. Similar results were reported by Oh-e et al. (7) who observed a positive correlation between the percentage of sterile spikelets and maximum temperature during the flowering period, and the percentage of sterile spikelets exceeded % when maximum temperature was around 378C. On the other hand, increased temperature had no significant effect on spikelet sterility in non-basmati varieties of rice. Both IR64 and Pusa 44 varieties were not affected by rise in temperature during the grain-filling period. In the present experiment, spikelet sterility was found to be negatively correlated with pollen germination on the stigma (Fig. 5) in basmati varieties. When pollen germination percentage was lower, high spikelet sterility was observed in all three basmati cultivars, indicating that rise in temperature reduced pollen deposition as well as pollen germination on the stigma, thereby inhibiting successful fertilisation and grain formation in basmati rice cultivars. Genotypic variation in spikelet sterility at high temperature was previously reported by several workers (Matsui et al. 1b; Nakagawa et al. 2; Prasad et al. 6). They also reported that sterility is caused by poor anther dehiscence and low pollen production; hence, low pollen germination on the stigma. Some rice cultivars have the ability to flower early in the morning, thus potentially avoiding the damaging effects of higher temperatures later in the day (Imaki et al. 1987). Matsui et al. (1997a) also revealed that flowering temperature above 368C induced spikelet sterility and a considerable cultivar difference existed in spikelet sensitivity to high temperature. The primary cause for the cultivar difference was the number of pollen grains shed on the stigma. Yield and pollen germination Increase in temperature reduced pollen deposition as well as pollen germination on the stigma, affecting yield of the rice crop. In basmati varieties a positive correlation was observed (R 2 =.41) between pollen germination percentage and yield. Higher pollen germination was accompanied by higher yield in basmati rice varieties. Highest yield (8.75 Mg/ha) was recorded in variety Pusa Sugandh 4 where pollen germination percentage was 72.7% (Fig. 6). In the same basmati variety, yield was only 3.1 Mg/ha when pollen germination percentage was only 32.4%. The same trend was followed by Pusa Sugandh 2 and Super Basmati, where highest yield (8. Mg/ha and 7.34 Mg/ha, respectively) occurred due to high pollen germination (64.7% and 61.7%) on the stigma. Yield of the basmati varieties was negatively correlated with spikelet sterility. In non-basmati varieties, however, no significant correlation was observed between yield and percentage pollen germination. Less deposition of pollen grains on the stigma and subsequently lower number of germinated pollen grains due to increased temperature affected successful fertilisation, thereby causing increased number of unfilled grains, thereby reducing yield of basmati rice. Conclusions This study showed that high temperature during flowering reduced fertility of the pollen grains as well as pollen germination on the stigma in rice crops. Reduction in pollen germination on the stigma was attributed to less deposition of pollen grains on the stigma at high temperature due to inadequate anther dehiscence. Reduced pollen germination resulted in poor grain setting, greater spikelet sterility, and reduced yield in rice. Rice varieties exhibited differential sensitivities to increased temperature. The harmful effect of high temperature was greater in basmati varieties than in non-basmati types. Besides reduced pollen germination, higher mean temperature during the grain-filling period also contributed to increased spikelet sterility in basmati rice varieties. The study suggested that improvement of high temperature tolerance during the pollination process is
6 368 Crop & Pasture Science B. Chakrabarti et al. required for maintaining high yields in basmati rice in global warming scenarios. References Baker JT, Allen LH, Boote KJ (1992) Response of rice to carbon dioxide and temperature. Agricultural and Forest Meteorology 6(3, 4), doi:.16/ (92)935-3 Battisti DS, Naylor RL (9) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323, doi:.1126/ science Horie T, Matsui T, Nakagawa H, Omasa K (1996) Effect of elevated CO 2 and global climate change on rice yield in Japan. In Climate change and plant in East Asia. (Eds K Omasa, K Kai, H Toda, Z Uchijima, M Yoshino) pp (Springer Verlag: Tokyo) Imaki T, Tokunaga S, Obara S (1987) High temperature induced spikelet sterility of rice in relation to flowering time. Japanese Journal of Crop Science 56(extra issue), 9 2. [In Japanese] IPCC (7) Climate change impacts, adaptation and vulnerability. In Technical Summary of Working Group II to Fourth Assessment Report of Inter-governmental Panel on Climate Change. (Eds ML Parry, OF Canziani, JP Paultikof, PJ van der Linden, CE Hanon) pp (Cambridge University Press: Cambridge, UK) Kim HY, Horie T, Nakagawa H, Wada K (1996a) Effect of elevated CO 2 and high temperature on growth and yield of rice I. The effect on development, dry matter production and some growth characteristics. Nihon Sakumotsu Gakkai Kiji 65, Kim HY, Horie T, Nakagawa H, Wada K (1996b) Effect of elevated CO 2 and high temperature on growth and yield of rice II. The effect on yield and its components of Akihikari rice. Nihon Sakumotsu Gakkai Kiji 65, Mackill DJ, Coffman WR, Rutjer JN (1982) Pollen shedding and combining ability for high temperature tolerance in rice. Crop Science 22, Matsui T, Kobayashi K, Kagata H, Horie T (5) Correlation between viability of pollination and length of basal dehiscence of the theca in rice under a hot and humid condition. Plant Production Science 8(2), doi:.1626/pps.8.9 Matsui T, Namuco OS, Ziska LH, Horie T (1997b) Effects of high temperature and CO 2 concentration on spikelet sterility in indica rice. Field Crops Research 51, doi:.16/s (96)3451-x Matsui T, Omasa T, Horie T (1997a) High temperature induced spikelet sterility of japonica rice at flowering in relation to air temperature, humidity and wind velocity. Nihon Sakumotsu Gakkai Kiji 66, Matsui T, Omasa K, Horie T () High temperature at flowering inhibit swelling of pollen grains, a driving force for thecae dehiscence in rice (Oryza sativa L.). Plant Production Science 3, doi:.1626/ pps.3.43 Matsui T, Omasa K, Horie T (1a) Comparison between anthers of two rice (Oryza sativa L.) cultivars with tolerance to high temperatures at flowering or susceptibility. Plant Production Science 4, doi:.1626/pps.4.36 Matsui T, Omasa K, Horie T (1b) The difference in sterility due to high temperature during the flowering period among japonica rice varieties. Plant Production Science 4, doi:.1626/pps.4.9 Matsushima S, Ikewada H, Maeda A, Honma S, Niki H (1982) Study on rice cultivation in the tropics. 1. Yielding and ripening response of the rice plant to the extremely hot and dry climate in Sudan. Japanese Journal of Tropical Agriculture 26, 19. Morokuma M, Yasuda S (4) Effect of high temperature and high humidity during the flowering period on spikelet fertility in Japonica rice. Nihon Sakumotsu Gakkai Kiji 73(1), doi:.1626/jcs Morokuma M, Yajima M, Yonemura S (1996) Effects of elevated CO 2 concentration and warming on growth and yield of rice. Nihon Sakumotsu Gakkai Kiji 65, Nakagawa H, Horie T, Matsui T (2) Effects of climate change on rice production and adaptive technologies. In Rice science: innovations and impact for livelihood. (Eds TW Mew, DS Brar, S Peng, D Dawe, B Hardy) pp (International Rice Research Institute: China) Oh-e I, Saitoh K, Kuroda T (7) Effects of high temperature on growth, yield and dry matter production of rice grown in the paddy field. Plant Production Science (4), doi:.1626/pps..412 Osada A, Sasiprapa V, Rahong M, Dhammanuvong S, Chakrabondho H (1973) Abnormal occurrence of empty grains of indica rice plants in the dry, hot season in Thailand. Proceedings Crop Science Society of Japan 42, 3 9. Prasad PVV, Boote KJ, Allen LH, Sheehy JE, Thomas JMG (6) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crops Research 95, doi:.16/j.fcr Satake T, Yoshida S (1978) High temperature induced sterility in indica rice at flowering. Nihon Sakumotsu Gakkai Kiji 47, Tan ZH, Lan TY, Ren CF (1985) Studies on high temperature injury on hybrid rice at flowering time and the strategy to avoid high temperature damage. Acta Agronomica Sinica 11, 3 8. Manuscript received 21 January, accepted 9 April
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