Abstract
It is reported that high temperatures (HT) would cause a marked decrease in world rice production. In tropical regions, high temperatures are a constraint to rice production and the most damaging effect is on spikelet sterility. Boron (B) plays a very important role in the cell wall formation, sugar translocation, and reproduction of the rice crop and could play an important role in alleviating high temperature stress. A pot culture experiment was conducted to study the effect of B application on high temperature tolerance of rice cultivars in B-deficient soil. The treatments comprised of four boron application treatments viz. control (B0), soil application of 1 kg B ha−1 (B1), soil application of 2 kg B ha−1 (B2), and foliar spray of 0.2% B (Bfs); three rice cultivars viz. Annapurna (HT stress tolerant), Naveen, and Shatabdi (both HT stress susceptible); and three temperature regimes viz. ambient (AT), HT at vegetative stage (HTV), and HT at reproductive stage (HTR). The results revealed that high temperature stress during vegetative or flowering stage reduced grain yield of rice cultivars mainly because of low pollen viability and spikelet fertility. The effects of high temperature on the spikelet fertility and grain filling varied among cultivars and the growth stages of plant when exposed to the high temperature stress. Under high temperature stress, the tolerant cultivar displays higher cell membrane stability, less accumulation of osmolytes, more antioxidant enzyme activities, and higher pollen viability and spikelet fertility than the susceptible cultivars. In the present work, soil application of boron was effective in reducing the negative effects of high temperature both at vegetative and reproductive stages. Application of B results into higher grain yield under both ambient and high temperature condition over control for all the three cultivars; however, more increase was observed for the susceptible cultivar over the tolerant one. The results suggest that the exogenous application of boron had a substantial effect on cell membrane stability, sugar mobilization, pollen viability, and spikelet fertility, hence the yield. The cultivars due to their variation in the tolerance level for high temperature stress behaved differently, and at high temperature stress, more response of the application of boron was seen in susceptible cultivars.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Afuakwa JJ, Crookston RK, Jones RJ (1984) Effect of temperature and sucrose availability on kernel black layer development in maize. Crop Sci 24:285–288. https://doi.org/10.2135/cropsci1984.0011183X002400020018x
Agarie S, Hanaoka N, Kubota F, Agata W, Kaufman PB (1995) Measurement of cell membrane stability evaluated by electrolyte leakage as a drought and heat tolerance test in rice (Oryza sativa L.). J Fac Agric Kyushu Univ 40:233–240.
Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Blevins D, Lukaszewski K (1998) Boron in plant structure and function. Annu Rev Plant Physiol Plant Mol Biol 49:481–500. https://doi.org/10.1146/annurev.arplant.49.1.481
Blum A (1988) Plant breeding for stress environments. CRC Press Inc., Boca Raton
Cakmak I, Marschner H (1992) Magnesium deficiency and high light intensity enhance activities of superoxide dismutase, ascorbate peroxidase, and glutathione reductase in bean leaves. Plant Physiol 98:1222–1227. https://doi.org/10.1104/pp.98.4.1222
Cakmak I, Romheld V (1997) Boron deficiency-induced impairments of cellular functions in plants. Plant Soil 193:71–83. https://doi.org/10.1023/A:1004259808322
Cao YY, Duan H, Yang LN, Wang ZQ, Liu LJ, Yang JC (2009) Effect of high temperature during heading and early filling on grain yield and physiological characteristics in indica rice. Acta Agron Sin 35:512–521. https://doi.org/10.1016/S1875-2780(08)60071-1
Cheng F, Zhong L, Zhao N, Liu Y, Zhang G (2005) Temperature induced changes in the starch components and biosynthetic enzymes of two rice varieties. Plant Growth Regul 46:87–95. https://doi.org/10.1007/s10725-005-7361-6
Christiansen MN (1978) The physiology of plant tolerance to temperature extremes. In: Crop tolerance to suboptimal land conditions. American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America, pp 173–191
CRRI (2012) Evaluation of germplasm and genotypes for heat stress tolerance. In: CRRI annual report 2011–12. Central Rice Research Institute, Cuttack, Odisha, India, pp 25–25
Dell B, Huang L (1997) Physiological response of plants to low boron. Plant Soil 193:103–120. https://doi.org/10.1023/A:1004264009230
Dinar M, Rudich J (1985) Effect of heat stress on assimilate partitioning in tomato. Ann Bot 56:239–248. https://doi.org/10.1093/oxfordjournals.aob.a087008
Driedonks N, Rieu I, Vriezen WH (2016) Breeding for plant heat tolerance at vegetative and reproductive stages. Plant Reprod 29:67–79
Dubois M, Gilles K, Hamilton JK, Rebers PA, Smith F (1951) A colorimetric method for the determination of sugars. Nature 168:167
Farooq M, Wahid A, Siddique KHM (2012) Micronutrient application through seed treatments: a review. J Soil Sci Plant Nutr 12:125–142. https://doi.org/10.4067/S0718-95162012000100011
Fokar M, Blum A, Nguyen HT (1998) Heat tolerance in spring wheat. II. Grain filling. Euphytica 104:1–8. https://doi.org/10.1023/a:1018322502271
García-Hernández d ER, Cassab López GI (2005) Structural cell wall proteins from five pollen species and their relationship with boron. Braz J Plant Physiol 17:375–381. https://doi.org/10.1590/S1677-04202005000400005
Garg OK, Sharma AN, Kona GRSS (1979) Effect of boron on the pollen vitality and yield of rice plants (Oryza sativa L. Var. Jaya). Plant Soil 52:591–594
Guilioni L, Wery J, Tardieu F (1997) Heat stress-induced abortion of buds and flowers in pea: is sensitivity linked to organ age or to relations between reproductive organs? Ann Bot 80:159–168. https://doi.org/10.1006/anbo.1997.0425
Gupta AS, Heinen JL, Holaday a S, Burke JJ, Allen RD (1993) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci U S A 90:1629–1633. https://doi.org/10.1073/pnas.90.4.1629
Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. https://doi.org/10.3390/ijms14059643
IPCC (2007) An assessment of the intergovernmental panel on climate change. IPCC, Geneva
Ito S, Hara T, Kawanami Y, Watanabe T, Thiraporn K, Ohtake N, Sueyoshi K, Mitsui T, Fukuyama T, Takahashi Y, Sato T, Sato A, Ohyama T (2009) Carbon and nitrogen transport during grain filling in rice under high-temperature conditions. J Agron Crop Sci 195:368–376. https://doi.org/10.1111/j.1439-037X.2009.00376.x
Jagadish SVK, Craufurd PQ, Wheeler TR (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot 58:1627–1635. https://doi.org/10.1093/jxb/erm003
Jagadish SVK, Craufurd P, Shi W, Oane R (2014) A phenotypic marker for quantifying heat stress impact during microsporogenesis in rice (Oryza sativa L.). Funct Plant Biol 41:48–55. https://doi.org/10.1071/FP13086
Keeling P, Banisadr R, Barone L, Wasserman B, Singletary G (1994) Effect of temperature on enzymes in the pathway of starch biosynthesis in developing wheat and maize grain. Aust J Plant Physiol 21:807. https://doi.org/10.1071/PP9940807
Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8:e26374. https://doi.org/10.4161/psb.26374
Krishnan P, Ramakrishnan B, Reddy KR, Reddy VR (2011) High-temperature effects on rice growth, yield, and grain quality. Adv Agron 111:87–206. https://doi.org/10.1016/B978-0-12-387689-8.00004-7
Levitt J (1980) Responses of plant to environmental stresses, vol 2. Academic Press, New York
Loomis WD, Durst RW (1992) Chemistry and biology of boron. Biofactors 3:229–239
Lordkaew S, Konsaeng S, Jongjaidee J, Dell B, Rerkasem B, Jamjod S (2013) Variation in responses to boron in rice. Plant Soil 363:287–295. https://doi.org/10.1007/s11104-012-1323-3
Maavimani M, Jebaraj S, Raveendran M, Vanniarajan C, Balakrishnan K, Muthamilan M (2014) Cellular membrane thermostability is related to rice (Oryza sativa L) yield under heat stress. Int J Trop Agric 32:201–208
Matsui T, Omasa K (2002) Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Ann Bot 89:683–687. https://doi.org/10.1093/aob/mcf112
Matsui T, Namuco OS, Ziska LH, Horie T (1997) Effects of high temperature and CO2 concentration on spikelet sterility in indica rice. Field Crop Res 51:213–219. https://doi.org/10.1016/S0378-4290(96)03451-X
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Mohammed AR, Tarpley L (2009a) Impact of high nighttime temperature on respiration, membrane stability, antioxidant capacity, and yield of rice plants. Crop Sci 49:313–322. https://doi.org/10.2135/cropsci2008.03.0161
Mohammed AR, Tarpley L (2009b) High nighttime temperatures affect rice productivity through altered pollen germination and spikelet fertility. Agric For Meteorol 149:999–1008. https://doi.org/10.1016/j.agrformet.2008.12.003
Prasad PVV, Boote KJ, Allen LH, Sheehy JE, Thomas JMG (2006) Species, ecotype and cultivar differences in spikelet fertility and harvest index of rice in response to high temperature stress. Field Crop Res 95:398–411. https://doi.org/10.1016/j.fcr.2005.04.008
Prasad PVV, Bheemanahalli R, Jagadish SVK (2017) Field crops and the fear of heat stress-opportunities, challenges and future directions. Field Crop Res 200:114–121. https://doi.org/10.1016/j.fcr.2016.09.024
Rashid A, Yasin M (2004) Boron deficiency in calcareous soil reduces rice yield and impairs grain quality. Int Rice Res Notes 29:57–59
Redfern SK, Azzu N, Binamira JS (2012) Rice in Southeast Asia: facing risks and vulnerabilities to respond to climate change. In: Meybeck A, Lankoski J, Redfern S, Azzu N, Gitz V (eds) Building resilience for adaptation to climate change in the agriculture sector. FAO, Rome, pp 295–314
Rehman A, Farooq M, Cheema ZA, Nawaz A, Wahid A (2014) Foliage applied boron improves the panicle fertility, yield and biofortification of fine grain aromatic rice. J Soil Sci Plant Nutr 14:723–733
SAS (2008) SAS Software of the SAS System for Windows. SAS Institute Inc., Cary
Satake T, Yoshida S (1978) High temperature-induced sterility in indica rices at flowering. Jpn J Crop Sci 47:6–17
Shkolnik MY (1984) Trace elements in plants. Elsevier, New York
Shorrocks VM (1997) The occurrence and correction of boron deficiency. Plant Soil 193:121–148. https://doi.org/10.1023/A:1004216126069
Singletary GW, Banisadr R, Keeling PL (1994) Heat stress during grain filling in maize: effects on carbohydrate storage and metabolism. Aust J Plant Physiol 21:829–841. https://doi.org/10.2135/cropsci1999.3961733x
Sullivan CY (1972) Mechanisms of heat and drought resistance in grain sorghum and methods of measurement. In: Rao N, House L (eds) Sorghum in seventies. Oxford & IBH Publishing Co., New Delhi, pp 248–264
Tang RS, Zheng JC, Jin ZQ, Zhang DD, Huang YH, Chen LG (2008) Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA, GAs and ABA in rice (Oryza sativa L.). Plant Growth Regul 54:37–43. https://doi.org/10.1007/s10725-007-9225-8
Teixeira EI, Fischer G, Van Velthuizen H, Walter C, Ewert F (2013) Global hot-spots of heat stress on agricultural crops due to climate change. Agric For Meteorol 170:206–215. https://doi.org/10.1016/j.agrformet.2011.09.002
Wahid A, Close TJ (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol Plant 51:104–109. https://doi.org/10.1007/s10535-007-0021-0
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223
Waraich E, Ahmad R, Halim A, Aziz T (2012) Alleviation of temperature stress by nutrient management in crop plants: a review. J Soil Sci Plant Nutr 12:221–244. https://doi.org/10.4067/S0718-95162012000200003
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(DOCX 21 kb)
Rights and permissions
About this article
Cite this article
Shahid, M., Nayak, A.K., Tripathi, R. et al. Boron application improves yield of rice cultivars under high temperature stress during vegetative and reproductive stages. Int J Biometeorol 62, 1375–1387 (2018). https://doi.org/10.1007/s00484-018-1537-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-018-1537-z