Mild preflowering drought priming improves stress defences, assimilation and sink strength in rice under severe terminal drought
R. N. Bahuguna A B , A. Tamilselvan A C , R. Muthurajan C , C. A. Solis A and S. V. K. Jagadish A D E
+ Author Affiliations
- Author Affiliations
A International Rice Research Institute, DAPO BOX 7777, Metro Manila 4030, Philippines.
B Indian Agricultural Research Institute, New Delhi 110012, India.
C Centre for Plant Molecular Biology, Tamil Nadu Agricultural University, Coimbatore 641003, India.
D Department of Agronomy, Kansas State University, Throckmorton Center, Manhattan, KS 66506, USA.
E Corresponding author. Email: kjagadish@ksu.edu
Functional Plant Biology 45(8) 827-839 https://doi.org/10.1071/FP17248
Submitted: 31 August 2017 Accepted: 5 February 2018 Published: 5 March 2018
Abstract
Drought stress is a prominent and persisting constraint for sustaining global rice (Oryza sativa L.) production. Priming with mild drought can be effective in reducing the impact of severe terminal drought stress affecting seed set and grain filling in rice. The cultivars N22 (drought tolerant), NSIC Rc222 and IR64 (high yielding, drought sensitive) were tested for short-term mild drought priming before flowering and subsequently exposed to severe drought stress either at the highly sensitive flowering or at the early grain filling stage under greenhouse conditions. Drought stress increased oxidative damage and reduced photosynthesis and sink enzymatic activity, ultimately reducing seed set (20–46%) and grain yield (22–68%) across cultivars. However, priming with mild drought significantly reduced oxidative damage, and increased photosynthesis, stomatal conductance and enzymatic activity, contributing to improved sink strength, thereby significantly reducing seed set (7–18%) and grain yield (12–59%) losses. The higher activity of key enzymes associated with sink strength such as cell wall invertase and sucrose synthase in primed plants probably reduced drought-induced losses at the grain filling stage. The findings support mild drought priming before flowering as a promising strategy for reducing yield penalty by providing partial protection against subsequent severe terminal drought stress. However, application of mild drought priming at the field level would need further investigation.
Additional keywords: enzymes, grain filling, Oryza sativa, oxidative damage, photosynthesis, seed set.
References
Ahmadi A, Baker DA (2001) The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat. Plant Growth Regulation 35, 81–91.| The effect of water stress on the activities of key regulatory enzymes of the sucrose to starch pathway in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVOltA%3D%3D&md5=2831ab632cdb605a4fa10ea4a33b7d95CAS |
Anjum SA, Xie X, Wang L, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. African Journal of Agricultural Research 6, 2026–2032.
Banik P, Zeng W, Bizimungu B, Tanino K (2016) Effects of drought acclimation on drought stress resistance in potato (Solanum tuberosum L.) genotypes. Environmental and Experimental Botany 126, 76–89.
| Effects of drought acclimation on drought stress resistance in potato (Solanum tuberosum L.) genotypes.Crossref | GoogleScholarGoogle Scholar |
Bäurle I (2016) Plant heat adaptation: priming in response to heat stress. F1000 Research 5, 694
| Plant heat adaptation: priming in response to heat stress.Crossref | GoogleScholarGoogle Scholar |
Bouman BAM, Humphreys E, Tuong TP, Barker R (2007) Rice and water. Advances in Agronomy 92, 187–237.
| Rice and water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktlyjsbc%3D&md5=f74ff32251a4854b1610bf51aba2cecfCAS |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=90b0b14534fb4b0d25711d896ae5505eCAS |
Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Science 173, 603–608.
| Stressful “memories” of plants: evidence and possible mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtF2hsbzE&md5=dc35023faf884216c216d144c92c9a1eCAS |
Counce PA, Gravois KA (2006) Sucrose synthase activity as a potential indicator of high rice grain yield. Crop Science 46, 1501–1507.
| Sucrose synthase activity as a potential indicator of high rice grain yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2jtbg%3D&md5=002aa3e801385bf7874289af92540791CAS |
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science 2, 53
| Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants.Crossref | GoogleScholarGoogle Scholar |
Ekanayake IJ, De Datta SK, Steponkus PL (1989) Spikelet sterility and flowering response of rice to water stress at anthesis. Annals of Botany 63, 257–264.
| Spikelet sterility and flowering response of rice to water stress at anthesis.Crossref | GoogleScholarGoogle Scholar |
Food and Agricultural Organization (2017) ‘The future of food and agriculture – trends and challenges.’ (Food and Agricultural Organization: Rome)
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agronomy for Sustainable Development 29, 185–212.
| Plant drought stress: effects, mechanisms and management.Crossref | GoogleScholarGoogle Scholar |
Farooq M, Hussain M, Siddique KHM (2014) Drought stress in wheat during flowering and grain-filling periods. Critical Reviews in Plant Sciences 33, 331–349.
| Drought stress in wheat during flowering and grain-filling periods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslOqtLc%3D&md5=3d7cbc30e9ccabd900a4e6c76d91b222CAS |
Farquhar GD, Sharkey TD (1982) Stomata1 conductance and photosynthesis. Annual Review of Plant Physiology 33, 317–345.
| Stomata1 conductance and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=7896d0b46634bc74b52a111a48deabbeCAS |
Feller U, Crafts-Brandner SJ, Salvucci E (1998) Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase activase-mediated activation of Rubisco. Plant Physiology 116, 539–546.
| Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase activase-mediated activation of Rubisco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXht1aju74%3D&md5=7cd5a8d35045582c1aef629d180f30f9CAS |
Filippou P, Tanou G, Molassiotis A, Fotopoulos V (2012) Plant acclimation to environmental stress using priming agents. In ‘Plant acclimation to environmental stress’. (Eds. N Tuteja, SS Gill) pp. 1–28. (Springer: New York)
Fu J, Huang B (2001) Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environmental and Experimental Botany 45, 105–114.
| Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXitF2msrg%3D&md5=d5d1313c58ac0032180d9222af550a96CAS |
Harb A, Krishnan A, Ambavaram MM, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiology 154, 1254–1271.
| Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsV2ntr%2FN&md5=ca612201b30fd07b7567bd59df660c5eCAS |
Hirose T, Takano M, Terao T (2002) Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling. Plant & Cell Physiology 43, 452–459.
| Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFKntrs%3D&md5=4770df89784c030d59db530725e25c68CAS |
Huber SC, Israel D (1982) Biochemical basis for the partitioning of photosynthetically fixed carbon between starch and sucrose in soybean leaves. Plant Physiology 69, 691–696.
| Biochemical basis for the partitioning of photosynthetically fixed carbon between starch and sucrose in soybean leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhsF2msrk%3D&md5=629ce5a831f90348650dedba5b116900CAS |
Pachauri RK, Meyer LA (Eds) (2014) ‘Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.’ (Intergovernmental Panel on Climate Change: Geneva)
Jagadish SVK, Craufurd PQ, Wheeler TR (2007) High temperature stress and spikelet fertility in rice. Journal of Experimental Botany 58, 1627–1635.
| High temperature stress and spikelet fertility in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeju7c%3D&md5=97a310a8bd08650d19bddd6c17a85600CAS |
Jagadish SK, Muthurajan R, Rang ZW, Malo R, Heuer S, Bennett J, Craufurd PQ (2011) Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22). Rice (New York, N.Y.) 4, 1–11.
| Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22).Crossref | GoogleScholarGoogle Scholar |
Jagadish SVK, Murty MVR, Quick WP (2015) Rice responses to raising temperatures: challenges, perspectives and future directions. Plant, Cell & Environment 38, 1686–1698.
| Rice responses to raising temperatures: challenges, perspectives and future directions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2M%2FjsFOnsg%3D%3D&md5=8e2be359753524c491b35309aff38933CAS |
Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiology 139, 267–274.
| Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVCgurzL&md5=3eb3975d06d7235af06294b82f697c68CAS |
Kadam NN, Yin X, Bindraban PS, Struik PC, Jagadish SVK (2015) Does morphological and anatomical plasticity during the vegetative stage make wheat more tolerant of water deficit stress than rice? Plant Physiology 167, 1389–1401.
| Does morphological and anatomical plasticity during the vegetative stage make wheat more tolerant of water deficit stress than rice?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlvVKks78%3D&md5=683c628a2a5f47f9a5e11eea6243f683CAS |
Keeling PL, Bacon PJ, Holt DC (1993) Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase. Planta 191, 342–348.
| Elevated temperature reduces starch deposition in wheat endosperm by reducing the activity of soluble starch synthase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXmsVGksro%3D&md5=053d531980063658326c5895c8a50780CAS |
Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235–246.
| Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjvVams7s%3D&md5=c7202d4f0a8cdde7006f12db334588ffCAS |
Kumar A, Dixit S, Ram T, Yadaw RB, Mishra KK, Mandal NP (2014) Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches. Journal of Experimental Botany 65, 6265–6278.
| Breeding high-yielding drought-tolerant rice: genetic variations and conventional and molecular approaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitl2gtr4%3D&md5=d8bbbd45a3e77710e7f22b5a1401497dCAS |
Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology 128, 682–695.
| Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVSqs7w%3D&md5=898f2d4288ff13e49480acbd3050770eCAS |
Li X, Liu F (2016) Drought stress memory and drought stress tolerance in plants: biochemical and molecular basis. In ‘Drought stress tolerance in plants, Vol. 1’ (MA Hossain et al., Eds) pp. 17–44. (Springer International Publishing: Switzerland)
Li J, Baroja-Fernández E, Bahaji A, Muñoz FJ, Ovecka M, Montero M, Sesma MT, Alonso-Casajús N, Almagro G, Sánchez-López AM, Hidalgo M, Zamarbide M, Pozueta-Romero J (2013) Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms. Plant & Cell Physiology 54, 282–294.
| Enhancing sucrose synthase activity results in increased levels of starch and ADP-glucose in maize (Zea mays L.) seed endosperms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVaisL8%3D&md5=a2437c0f5fd451cebdb8cba41d8d6d5eCAS |
Li X, Lawas LM, Malo R, Glaubitz U, Erban A, Mauleon R, Heuer S, Zuther E, Kopka J, Hincha DK, Jagadish KSV (2015) Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress. Plant, Cell & Environment 38, 2171–2192.
| Metabolic and transcriptomic signatures of rice floral organs reveal sugar starvation as a factor in reproductive failure under heat and drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsFGrt77K&md5=8653707dacd186611c8dd85965b16dd9CAS |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=7500af4eb02d39331b21594ff59edb15CAS |
Molinier J, Ries G, Zipfel C, Hohn B (2006) Transgeneration memory of stress in plants. Nature 442, 1046–1049.
| Transgeneration memory of stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVyhtbo%3D&md5=60178e90925e2cbdcff4086e081e74b3CAS |
Nakamura Y, Yuki K, Park SY, Ohya T (1989) Carbohydrate metabolism in the developing endosperm of rice grains. Plant & Cell Physiology 30, 833–839.
| Carbohydrate metabolism in the developing endosperm of rice grains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhtFGrsb8%3D&md5=034d3f5db584d5ae434c8e9f64d026f5CAS |
Nawaz A, Farooq M, Cheema SA, Yasmeen A, Wahid A (2013) Stay green character at grain filling ensures resistance against terminal drought in wheat. International Journal of Agriculture and Biology 15, 1272–1276.
Pandey V, Shukla A (2015) Acclimation and tolerance strategies of rice under drought stress. Rice Science 22, 147–161.
| Acclimation and tolerance strategies of rice under drought stress.Crossref | GoogleScholarGoogle Scholar |
Peng S, Buresh RJ, Huang J, Zhong X, Zou Y, Yang J, Wang G, Liu Y, Hu R, Tang Q, Cui K (2010) Improving nitrogen fertilization in rice by site-specific N management. A review. Agronomy for Sustainable Development 30, 649–656.
| Improving nitrogen fertilization in rice by site-specific N management. A review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFOnsr3O&md5=d4a09477633b4c71559a776f295f3a64CAS |
Raman A, Verulkar S, Mandal N, Variar M, Shukla V, Dwivedi J, Singh B, Singh O, Swain P, Mall A, Robin S (2012) Drought yield index to select high yielding rice lines under different drought stress severities. Rice (New York, N.Y.) 5, 31
| Drought yield index to select high yielding rice lines under different drought stress severities.Crossref | GoogleScholarGoogle Scholar |
Rang ZW, Jagadish SVK, Zhou QM, Craufurd PQ, Heuer S (2011) Effect of high temperature and water stress on pollen germination and spikelet fertility in rice. Environmental and Experimental Botany 70, 58–65.
| Effect of high temperature and water stress on pollen germination and spikelet fertility in rice.Crossref | GoogleScholarGoogle Scholar |
Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9, 606–613.
| Function and regulation of plant invertases: sweet sensations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVaksLvO&md5=082e5bcadf4fec65a52ea33b13929f0cCAS |
Saini HS, Westgate ME (1999) Reproductive development in grain crops during drought. Advances in Agronomy 68, 59–96.
| Reproductive development in grain crops during drought.Crossref | GoogleScholarGoogle Scholar |
Selote DS, Khanna-Chopra R (2006) Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings. Physiologia Plantarum 127, 494–506.
| Drought acclimation confers oxidative stress tolerance by inducing co-ordinated antioxidant defense at cellular and subcellular level in leaves of wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVKgsrc%3D&md5=a8ba058887926f1f9b55ba566ff847f5CAS |
Serraj R, McNally KL, Slamet-Loedin I, Kohli A, Haefele SM, Atlin G, Kumar A (2011) Drought resistance improvement in rice: an integrated genetic and resource management strategy. Plant Production Science 14, 1–14.
| Drought resistance improvement in rice: an integrated genetic and resource management strategy.Crossref | GoogleScholarGoogle Scholar |
Tanou G, Fotopoulos V, Molassiotis A (2012) Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Frontiers in Plant Science 3, 216
| Priming against environmental challenges and proteomics in plants: update and agricultural perspectives.Crossref | GoogleScholarGoogle Scholar |
Tomlinson KL, McHugh S, Labbe H, Grainger JL, Jame LE, Pomeroy KM, Mullin JW, Miller SS, Dennis DT, Miki BLA (2004) Evidence that the hexose-to-sucrose ratio does not control the switch to storage product accumulation in oilseeds: analysis of tobacco seed development and effects of overexpressing apoplastic invertase. Journal of Experimental Botany 55, 2291–2303.
| Evidence that the hexose-to-sucrose ratio does not control the switch to storage product accumulation in oilseeds: analysis of tobacco seed development and effects of overexpressing apoplastic invertase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVOkt7k%3D&md5=d75d36a751eac8dae496d00e40d55c91CAS |
Udayakumar M, Devendra R, Ramaswamy GS, Nageswara Rao RC, Roy SA, Gangadhar GC, Aftab Hussain IS, Wright GC (1998) Measurement of transpiration efficiency in field condition. Indian Journal of Plant Physiology and Biochemistry 1, 69–75.
Wang L, Ruan YL (2012) New insights into roles of cell wall invertase in early seed development revealed by comprehensive spatial and temporal expression patterns of GhCWIN1 in cotton. Plant Physiology 160, 777–787.
| New insights into roles of cell wall invertase in early seed development revealed by comprehensive spatial and temporal expression patterns of GhCWIN1 in cotton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFaksbnK&md5=f340f78c4e69cae3a680d9916396459dCAS |
Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B (2014) Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. Journal of Experimental Botany 65, 6441–6456.
| Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1Gis73L&md5=e064fdac4e96281f053aa9148954094cCAS |
Wang X, Vignjevic M, Liu F, Jacobsen S, Jiang D, Wollenweber B (2015) Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat. Plant Growth Regulation 75, 677–687.
| Drought priming at vegetative growth stages improves tolerance to drought and heat stresses occurring during grain filling in spring wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVers73J&md5=ad5c3e57589671e1fc2d7dfe5e9ce3e3CAS |
Xu Z, Zhou G, Shimizu H (2010) Plant responses to drought and rewatering. Plant Signaling & Behavior 5, 649–654.
| Plant responses to drought and rewatering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1alur0%3D&md5=a5ba148662bbff63f797f26dccdc8f71CAS |
Yang J, Zhang J (2010) Crop management techniques to enhance harvest index in rice. Journal of Experimental Botany 61, 3177–3189.
| Crop management techniques to enhance harvest index in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVymsb0%3D&md5=b816807b077b3d9dbf05faf9820cdb71CAS |
Yang J, Zhang J, Wang Z, Xu G, Zhu Q (2004) Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling. Plant Physiology 135, 1621–1629.
| Activities of key enzymes in sucrose-to-starch conversion in wheat grains subjected to water deficit during grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVOqs7g%3D&md5=8e78bb88a33902f0545ab61a7c5fedcfCAS |
