Skip to main content

Advertisement

Log in

Phenotyping and characterization of heat stress tolerance at reproductive stage in rice (Oryza sativa L.)

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Rice crop is known to be sensitive to heat stress particularly at the flowering stage. Breeding approaches for improving heat tolerance in rice needs understanding of heat tolerance mechanisms and suitable heat tolerance donors. A study was planned for screening of rice genotypes and identification of novel heat tolerant donor(s) and physiologically characterize the component traits using contrasting set of genotypes in green house environment. Genotypes were categorized as tolerant and sensitive to heat stress using heat susceptibility index and cumulative stress response index for spikelet fertility, pollen viability, and grain yield. Among the set of genotypes screened, IET 22218 recorded high spikelet fertility (> 85%), pollen viability (> 95%) at high temperature (39–44 °C) with relative humidity (> 60–80%). This genotype recorded higher photosynthesis, canopy temperature depression, and accumulation of endogenous level of polyamines both under optimum and heat stress environments. Moreover, IET 22218 genotype recorded lower H2O2 accumulation, membrane damage and higher activity of antioxidant enzymes. Heat stress tolerance in IET 22218 was at par with heat tolerant checks, i.e., Nagina22 (N22) and Nerica L-44 (NL-44). Interestingly, IET 22218 also maintained lower chalkiness (< 34%) and higher head rice yield (> 85%) under heat stress. Based on above traits IET 22218 was selected as the novel donor for heat tolerance. The study concludes that induced polyamines and antioxidant enzymes activity in IET 22218 under stress were associated with lowering oxidative stress and maintained higher pollen viability and spikelet fertility under heat stress environment. However, more studies are recommended to understand the role of polyamines in heat stress tolerance specifically in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adu-Kwarteng EE, Oduro WO, Manful JT (2003) Rice grain quality: a comparison of local varieties with new varieties under study in Ghana. Food Control 14:507–514

    Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    CAS  Google Scholar 

  • Ayeneh A, Ginkel V, Reynolds MP, Ammar K (2002) Comparison of leaf, spike, peduncle and canopy temperature depression in wheat under heat stress. Field Crops Res 79:173–184

    Google Scholar 

  • Bahuguna RN, Jagadish KSV (2015) Temperature regulation of plant phenological development. Environ Exp Bot 111:83–90

    CAS  Google Scholar 

  • Bahuguna RN, Solis CA, Shi W, Jagadish KSV (2017) Post-flowering night respiration and altered sink activity account for high night temperature-induced grain yield and quality loss in rice (Oryza sativa L.). Physiol Plant 159:59–73

    CAS  PubMed  Google Scholar 

  • Bahuguna RN, Tamilselvan A, Muthurajan R, Solis CA, Jagadish SVK (2018) Mild preflowering drought priming improves stress defences, assimilation and sink strength in rice under severe terminal drought. Fun Plant Biol 45:827–839

    Google Scholar 

  • Bahuguna RNJ, Pal J, Shah M, Lawas D, Lovely MF, Khetarpal S, Jagadish SVK (2015) Physiological and biochemical characterization of NERICA-L-44: a novel source of heat tolerance at the vegetative and reproductive stages in rice. Physiol Plant 154:543–559

    CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Google Scholar 

  • Blum A, Shpiler L, Golan G, Mayer J (1989) Yield stability and canopy temperature of wheat genotypes under drought-stress. Field Crops Res 22(4):289–296

    Google Scholar 

  • Challinor AJ, Watson J, Lobell DB, Howden SM, Smith DR, Chhetri N (2014) A meta-analysis of crop yield under climate change and adaptation. Nat Clim Change 4:287

    Google Scholar 

  • Chaturvedi AK, Bahuguna RN, Shah D, Pal M, Jagadish SVK (2017) High temperature stress during flowering and grain filling offsets beneficial impact of elevated CO2 on assimilate partitioning and sink-strength in rice. Sci Rep 7:8227

    PubMed  PubMed Central  Google Scholar 

  • Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945

    PubMed  PubMed Central  Google Scholar 

  • Conrath U, Chen Z, Ricigliano JR, Klessig DF (1995) Two inducers of plant defense responses, 2, 6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. Proc Nat Acad Sci 92(16):7143–7147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Counce PA, Bryant RJ, Bergman CJ, Bautista RC, Wang YJ, Siebenmorgen TJ, Moldenhauer KAK, Meullenet JFC (2005) Rice milling quality, grain dimensions, and starch branching as affected by high night temperatures. Cereal Chem 82:645–648

    CAS  Google Scholar 

  • Dai Q, Shaobing P, Chavez AQ, Vergara BS (1994) Intraspecific responses of 188 rice cultivars to enhanced UV-B radiation. Environ Exp Bot 34:433–442

    Google Scholar 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53

    Google Scholar 

  • Dat JF, Lopez-Delgado H, Foyer CH, Scott IM (1998) Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings. Plant Physiol 116(4):1351–1357

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Azevedo Neto AD, Prisco JT, Enéas-Filho J, de Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94

    Google Scholar 

  • Do PT, Degenkolbe T, Erban A, Heyer AG, Kopka J et al (2013) Dissecting rice polyamine metabolism under controlled long-term drought stress. PLoS ONE 8(4):e60325. https://doi.org/10.1371/journal.pone.0060325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Do PT, Drechsel O, Heyer AG, Hincha DK, Zuther E (2014) Changes in free polyamine levels, expression of polyamine biosynthesis genes, and performance of rice cultivars under salt stress: a comparison with responses to drought. Front Plant Sci 5:182. https://doi.org/10.3389/fpls.2014.00182

    Article  PubMed  PubMed Central  Google Scholar 

  • Dong W, Chen J, Wang L, Tian Y, Zhang B, Lai Y, Meng Y, Qian C, Guo J (2014) Impacts of night time post-anthesis warming on rice productivity and grain quality in East China. The Crop J 2:63–69

    Google Scholar 

  • FAO (2014) (Food and Agriculture Organization). http://www.fao.org/faostat/en/?#home. Accessed 5 Jan 2018

  • Fischer R, Maurer R (1978) Drought resistance in spring wheat cultivars. I. Grain yield responses. Aust J Agril Res 29:897–912

    Google Scholar 

  • Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fukuoka M, Yoshimoto M, Hasegawa T (2012) MINCER: A novel instrument for monitoring the micrometeorology of rice canopies. J Agril Meteorol 68:135–147

    Google Scholar 

  • Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    CAS  PubMed  Google Scholar 

  • Ikbal FE, Hernández JA, Barba-Espín G, Koussa T, Aziz A, Faize M, Diaz-Vivancos P (2014) Enhanced salt-induced antioxidative responses involve a contribution of polyamine biosynthesis in grapevine plants. J Plant Physiol 171:779–788

    CAS  PubMed  Google Scholar 

  • Jagadish SVK, Cairns J, Lafitte R, Wheeler TR, Price AH, Craufurd PQ (2010) Genetic analysis of heat tolerance at anthesis in rice. Crop Sci 50:1633–1641

    CAS  Google Scholar 

  • Jagadish SVK, Craufurd PQ, Wheeler TR (2008) Phenotyping parents of mapping populations of rice for heat tolerance during anthesis. Crop Sci 48(3):1140–1146

    Google Scholar 

  • Jagadish SVK, Craufurd PQ, Wheeler TR (2007) High temperature stress and spikelet fertility in rice (Oryza sativa L.). J Exp Bot 58:1627–1635

    CAS  PubMed  Google Scholar 

  • Jagadish SVK, Murty MV, Quick WP (2015) Rice responses to rising temperatures—challenges, perspectives and future directions. Plant Cell Environ 38:1686–1698

    CAS  PubMed  Google Scholar 

  • Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410

    CAS  PubMed  Google Scholar 

  • Juliano BO (1971) A simplified assay for milled-rice amylose. Cereal Sci Today 16:334–360

    Google Scholar 

  • Kadam NN, Xiao G, Melgar RJ, Bahuguna RN, Quinones C, Tamilselvan A, Prasad PVV, Jagadish KS (2014) Agronomic and physiological responses to high temperature, drought, and elevated CO2 interactions in cereals. Adv Agron 127:111–156

    Google Scholar 

  • Khatun S, Flowers TJ (1995) Effects of salinity on seed set in rice. Plant, Cell Environ 18:61–67

    Google Scholar 

  • Khush GS, Paule CM, Dela Cruz NM (1978) Rice grain quality evaluation and improvement at IRRI. In: Proceedings of the workshop on chemical aspects of rice grain quality. Los Banos, Philippines, International Rice Research Institute 1979.

  • Koti S, Reddy KR, Kakani VG, Zhao D, Gao W (2007) Effects of carbon dioxide, temperature and ultraviolet-B radiation and their interactions on soybean (Glycine max L.) growth and development. Environ & Exp Bot 60(1):1–10

    CAS  Google Scholar 

  • Krishnan P, Ramakrishnan B, Reddy KR, Reddy VR (2011) High-temperature effects on rice growth, yield, and grain quality. Adv Agron 111:87–206

    CAS  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Gu W, Li J, Li C, Xie T, Qu D, Meng Y, Li C, Wei S (2018) Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones. Plant Physiol Biochem 129:35–55

    CAS  PubMed  Google Scholar 

  • Liu HP, Dong BH, Zhang YY, Liu ZP, Liu YL (2004) Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings. Plant Sci 166:1261–1267

    CAS  Google Scholar 

  • Liu JH, Wang W, Wu H, Gong X, Moriguchi T (2015) Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci 6:827

    PubMed  PubMed Central  Google Scholar 

  • Lyman NB, Jagadish SVK, Nalley LL, Dixon BL, Siebenmorgen T (2013) Neglecting rice milling yield and quality underestimates economic losses from high-temperature stress. PLoS ONE 8:e72157

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum L.). Plant Biol 13:1–6

    CAS  PubMed  Google Scholar 

  • Milla MAR, Maurer A, Huete AR, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathways. The Plant J 36:602–615

    Google Scholar 

  • Minocha R, Majumdar R, Minocha SC (2014) Polyamines and abiotic stress in plants: a complex relationship. Front Plant Sci 5:175–175

    PubMed  PubMed Central  Google Scholar 

  • Ouyang J, Song C, Chen D (2017) Research progress on heat-tolerance mechanism and transports of polyamines in plant. Mol Plant Breed 15:3286–3294

    Google Scholar 

  • Pál M, Szalai G, Janda T (2015) Speculation: Polyamines are important in abiotic stress signaling. Plant Sci 237:16–23

    PubMed  Google Scholar 

  • Powell NJ, Ravash X, Edlington R, Rudy JD (2012) Yield stability for cereals in a changing climate. Funct Plant Biol 39:539–552

    PubMed  Google Scholar 

  • Prasad PVV, Boote KJ, Allen LH Jr, 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 Crops Res 95:398–411

    Google Scholar 

  • Sarsu F (2018) Screening protocols for heat tolerance in rice at the seedling and reproductiv stages, In: Pre-field screening protocols for heat-tolerant mutants in rice. Springer, Cham, pp 9–24. https://doi.org/10.1007/978-3-319-77338-4_2

    Google Scholar 

  • Schleussner CF, Deryng D, Müller C, Elliott J, Saeed F, Folberth C, Liu W, Wang X, Pugh TAM, Thiery W, Seneviratne SI, Rogelj J (2018) Crop productivity changes in 1.5 °C and 2 °C worlds under climate sensitivity uncertainty. Environ Res Lett 13:064007

    Google Scholar 

  • Sharma P, Dubey RS (2004) Ascorbate peroxidase from rice seedlings: properties of enzyme isoforms, effects of stresses and protective roles of osmolytes. Plant Sci 167:541–550

    CAS  Google Scholar 

  • Shi W, Yin X, Struik PC, Solis C, Xie F, Schmidt RC, Huang M, Zou Y, Ye C, Jagadish SVK (2017) High day- and night-time temperatures affect grain growth dynamics in contrasting rice genotypes. J Exp Bot 68:5233–5245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi WM, Muramoto Y, Ueda A, Takabe T (2001) Cloning of peroxisomal ascorbate peroxidase gene from barley and enhanced thermotolerance by overexpressing in Arabidopsis thaliana. Gene 273:23–27

    CAS  PubMed  Google Scholar 

  • Sinclair TR, Allen LH, Drake GM (1995) Temperature gradient chambers for research on global environment change: II. Design for plot studies. Biotronics: reports of Biotron Institute. Kyushu Univ 24:99–108

    Google Scholar 

  • Singh MP (2015) Role of putrescine in growth, development and abiotic stress tolerance of rice (Oryza sativa L.) (Doctoral dissertation, Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi)

  • Szymańska R, Ślesak I, Orzechowska A, Kruk J (2017) Physiological and biochemical responses to high light and temperature stress in plants. Environ Exp Bot 139:165–177

    Google Scholar 

  • Tang S, Zhang H, Li L, Liu X, Chen L, Chen W, Ding Y (2018) Exogenous spermidine enhances the photosynthetic and antioxidant capacity of rice under heat stress during early grain-filling period. Funct Plant Biol 45(9):911–921

    CAS  PubMed  Google Scholar 

  • 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. Agril For Meteorol 170:206–215

    Google Scholar 

  • Tian J, Wang LP, Yang YJ, Sun J, Guo SR (2012) Exogenous spermidine alleviates the oxidative damage in cucumber seedlings subjected to high temperatures. J Am Soc Hort Sci 137:11–19

    CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354

    CAS  PubMed  Google Scholar 

  • Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199–223

    Google Scholar 

  • Yoshida S, Satake T, Mackill DS (1981) High-temperature stress in rice [study conducted at IRRI, Philippines]. IRRI Research Paper Series (Philippines)

  • Zaman-Allah MJ, David M, Vadez V (2011) Chickpea genotypes contrasting for seed yield under terminal drought stress in the field differ for traits related to the control of water use. Funct Plant Biol 38:270–281

    PubMed  Google Scholar 

  • Zhang CX, Fu GF, Yang XQ, Yang YJ, Zhao X, Chen TT, Zhang XF, Jin QY, Tao LX (2016) Heat stress effects are stronger on spikelets than on flag leaves in rice due to differences in dissipation capacity. J Agron Crop Sci 202:394–408

    CAS  Google Scholar 

Download references

Acknowledgement

Authors thank to S.R.Voleti and P.R.Rao, IIRR, Rajendranagar, Hyderabad Telangana, 500030, India for providing seed material under ACRIP project,

Funding

Authors acknowledge the financial grant received from Indian Council of Agricultural Research (ICAR), New Delhi, India through National Innovations on Climate Resilient Agriculture (NICRA-IARI) Project Grant No.12–115. RNB acknowledges the financial support from DST Fast Track Young Scientist Grant (YSS/2015/000523) 2015–2019.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Madan Pal.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests related to publication of this paper.

Additional information

Communicated by J. Huang.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PPTX 4930 kb)

Supplementary file2 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karwa, S., Bahuguna, R.N., Chaturvedi, A.K. et al. Phenotyping and characterization of heat stress tolerance at reproductive stage in rice (Oryza sativa L.). Acta Physiol Plant 42, 29 (2020). https://doi.org/10.1007/s11738-020-3016-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-020-3016-5

Keywords

Navigation