Skip to main content
SpringerLink
Log in

Comparative Study of Susceptible and Tolerant Genotype Reveals Efficient Recovery and Root System Contributes to Heat Stress Tolerance in Rice

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

In changing climate scenario, heat stress caused by increased atmospheric CO2 is a major concern for rice productivity. There is a need to decipher the mechanisms of heat stress susceptibility and tolerance response of rice cultivars considering that high temperature is detrimental to growth and development of rice crop. The present study was designed to understand the heat stress response in heat-susceptible (Vandana) and heat-tolerant (N22) cultivars of rice. Rice seedlings were subjected to short-duration (24 h, SDS) and long-duration (5 days, LDS) heat stress (42 °C/36 °C, day/night). Besides the heat stress, recovery response (REC) of both the cultivars was also studied. Physiological parameters (chlorophyll content and membrane thermostability) and root/shoot length analysis revealed that N22 has better efficiency in recovering from heat stress. In particular, root tissue of N22 showed increased thermotolerance during SDS and LDS when compared with Vandana. In addition to physiological studies, gene expression pattern of 13 genes including heat shock transcription factors and heat shock proteins and 9 microRNAs (miRNAs) was analyzed in root and shoot of both the genotypes during various treatments. Gene and miRNA expression studies showed that root tissue of N22 was more responsive during SDS and LDS, suggesting important function of roots in heat stress tolerance. Further, during recovery, root tissue of both the genotypes showed more significant change in gene expression than shoot which signifies the vital role of plant root system in heat stress recovery response. Very high expression of an unknown iron-sulfur cluster-binding protein OsFd involved in electron transport activity was observed in root tissue of N22 during all the stress treatments. This study shows that better recovery and efficient root system play an important role in heat tolerance trait of N22.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CWIP:

Cell wall integrity protein

SOD:

Superoxide dismutase

SPS:

Sucrose phosphate synthase

SPL:

Squamosa promoter binding protein

NF-Y:

Nuclear transcription factor-Y

ARF:

Auxin response factor

HSP:

Heat shock protein

Hsf:

Heat shock transcription factor

miRNA:

microRNA

References

  • Barrera-Figueroa BE, Wu Z, Liu R (2013) Abiotic stress-associated microRNAs in plants: discovery, expression analysis and evolution. Front Biol 8(2):189–197

    Article  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  • Blum A, Ebercon A (1981) Cell membrane stability as a measure of drought and heat tolerance in wheat. Crop Sci 21:43–47

    Article  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  PubMed  CAS  Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. Amer Soc Plant Physio, Rockville, pp 1158–1249

    Google Scholar 

  • Cao L, Zhao J, Zhan X, Li D, He L, Cheng S (2003) Mapping QTLs for heat tolerance and correlation between heat tolerance and photosynthetic rate in rice. Chin J Rice Sci 17:223–227

    CAS  Google Scholar 

  • Chen L, Ren Y, Zhang Y, Xu J, Sun F, Zhang Z, Wang Y (2012) Genome-wide identification and expression analysis of heat-responsive and novel microRNAs in Populus tomentosa. Gene 504:160–165

    Article  PubMed  CAS  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • García-Valenzuela X, Garcá-Moya E, Rascón-Cruz Q, Herrera-Estrella L, Aguado-Santacruz GA (2005) Chlorophyll accumulation is enhanced by osmotic stress in graminaceous chlorophyllic cells. J Plant Physiol 162(6):650–661

    Article  PubMed  Google Scholar 

  • Gupta SC, Sharma A, Mishra M, Mishra R, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384

    Article  PubMed  CAS  Google Scholar 

  • Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006) Global temperature change. PNAS 103:14288–14293

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Haque M, Hasan M, Rajib M, Hasan M (2009) Identification of cultivable heat tolerant wheat genotypes suitable for Patuakhali district in Bangladesh. J Bangladesh Agril Univ 7(2):241–246

    Google Scholar 

  • Hashimoto H, Kurra-Hotta M, Katoh S (1989) Changes in protein content and in the structure and number of chloroplasts during leaf senescence in rice seedlings. Plant Cell Physiol 30:707–715

    CAS  Google Scholar 

  • Huang B, Liu X (2003) Summer root decline: production and mortality for four cultivars of creeping bent grass. Crop Sci 43:258–265

    Article  Google Scholar 

  • Huang B, Rachmilevitch S, Xu J (2012) Root carbon and protein metabolism associated with heat tolerance. J Exp Bot 63(9):3455–3465

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Jeong DH, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. J Plant Biol 56:187–197

    Article  CAS  Google Scholar 

  • Jeong DH, Park S, Zhai J, Gurazada SG, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jung KH, An G (2012) Application of MapMan and RiceNet drives systematic analyses of the early heat stress transcriptome in rice seedlings. J Plant Biol 55:436–449

    Article  CAS  Google Scholar 

  • Jung KH, Gho HJ, Nguyen MX, Kim SR, An G (2013) Genome-wide expression analysis of HSP70 family genes in rice and identification of a cytosolic HSP70 gene highly induced under heat stress. Funct Integr Genomics 13(3):391–402

    Google Scholar 

  • Kochhar S, Kochhar VK (2005) Expression of antioxidant enzymes and heat shock proteins in relation to combined stress of cadmium and heat in Vigna mungo seedlings. Plant Sci 168:921–929

    Article  CAS  Google Scholar 

  • Kotak S, Larkindale J, Lee U, Von Koskull-doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  PubMed  CAS  Google Scholar 

  • Lei D, Tan L, Liu F, Chen L, Sun C (2013) Identification of heat-sensitive QTL derived from common wild rice (Oryza rufipogon Griff.). Plant Sci 201–202:121–127

    Google Scholar 

  • Liu X, Huang B (2005) Root physiological factors involved in creeping bentgrass response to high soil temperatures. Environ Exp Bot 53:233–245

    Article  Google Scholar 

  • Liu AL, Zou J, Zhang XW, Zhou XY, Wang WF, Xiong XY, Chen LY, Chen XB (2010) Expression profiles of class A rice heat shock transcription factor genes under abiotic stresses. J Plant Biol 53:142–149

    Article  Google Scholar 

  • Lv DK, Bai X, Li Y, Ding XD, Ge Y, Cai H, Ji W, Wu N, Zhu YM (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459(1–2):39–47

    Article  PubMed  CAS  Google Scholar 

  • Mangrauthia SK, Agarwal S, Sailaja B, Madhav MS, Voleti SR (2013) MicroRNAs and their role in salt stress response in plants. In: Ahmad P et al (eds) Salt stress in plants: Signalling, omics and adaptations. Springer, New York, pp 15–46

    Chapter  Google Scholar 

  • Matsui T, Kobayasi K, Yoshimota M, Hasegawa T (2007) Stability of rice pollination in the field under hot and dry conditions in the Riverina region of New South Wales, Australia. Plant Prod Sci 10:57–63

    Article  Google Scholar 

  • McMichael BL, Burke JJ (2002) Temperature effects on root growth. In: Waisel Y, Eshel Y, Kafkafi U (eds) Plant roots: The hidden half, 3rd edn. Marcel Dekker, New York

    Google Scholar 

  • Mohammed AR, Tarpley L (2009) High night temperatures affect rice productivity through altered pollen germination and spikelet fertility. Agric For Meteorol 149:999–1008

    Article  Google Scholar 

  • Nielsen KF (1974) Roots and root temperatures. In: Carson EW (ed) The plant root and its environment. University Press of Virginia, Charlottesville, pp 293–333

    Google Scholar 

  • Poli Y, Basava RK, Panigrahy M, Vinukonda VP, Dokula NR, Voleti SR, Desiraju S, Neelamraju S (2013) Characterization of a Nagina22 rice mutant for heat tolerance and mapping of yield traits. Rice 6:36

    Article  PubMed  Google Scholar 

  • Romero-Aranda R, Soria T, Cuartero J (2001) Tomato plant-water uptake and plant-water relations under saline growth conditions. Plant Sci 160:265–272

    Article  PubMed  CAS  Google Scholar 

  • Sailaja B, Voleti SR, Subrahmanyam D, Sarla N, Vishnu Prasanth V, Bhadana VP, Mangrauthia SK (2014) Prediction and expression analysis of microRNAs associated with heat stress in Oryza sativa. Rice Sci 21:3–12

    Article  Google Scholar 

  • Sarkar NK, Kim YK, Grover A (2013) Co-expression network analysis associated with call of rice seedlings for encountering heat stress. Plant Mol Biol 84(1–2):125–143

    PubMed  Google Scholar 

  • Steel RGD, Torrie JH (1997) Principles and procedures of statistics, 2nd edn. McGraw-Hill Book Co, New York

    Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress regulated micro-RNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Veerasamy M, He YL, Huang B (2007) Leaf senescence and protein metabolism in creeping bent grass exposed to heat stress and treated with cytokinins. J Am Soc Hortic Sci 132:467–472

    CAS  Google Scholar 

  • Vierling E (1991) The role of heat shock proteins in plants. Annu Rev Plant Physiol 42:579–620

    Article  CAS  Google Scholar 

  • Wahid S, Gelani M, Ashraf Foolad MR (2007) Heat tolerance in plants: an overview. Env Exp Bot 61(3):199–223

    Google Scholar 

  • Xin M, Wang Y, Yao Y, Xie C, Peng H, Ni LZ, Sun Q (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123–134

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu Q, Huang B (2000a) Effects of air and soil temperature on carbohydrate metabolism in creeping bentgrass. Crop Sci 40:1368–1374

    Article  Google Scholar 

  • Xu Q, Huang B (2000b) Growth and physiological responses of creeping bent grass to differential shoot and root temperatures. Crop Sci 40:1363–1368

    Article  Google Scholar 

  • Xu Q, Huang B (2001) Lowering soil temperature under supra optimal air temperature improved shoot and root growth in creeping bent grass. Crop Sci 41:1878–1883

    Article  Google Scholar 

  • Yabe N, Takahashi T, Komeda Y (1994) Analysis of tissue-specific expression of Arabidopsis thaliana HSP90-family gene HSP81. Plant Cell Physiol 35:1207–1219

    PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. IRRI, Philippines

    Google Scholar 

  • Yu X, Wang H, Lu Y, Ruiter M, Cariaso M, Prins M, Tunenn AV, He Y (2011) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63(2):1025–1038

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Han C, Liu Z (2009) Absorption spectrum estimating rice chlorophyll concentration: preliminary investigations. J Plant Breed Crop Sci 1:223–229

    CAS  Google Scholar 

  • Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590

    Article  PubMed  CAS  Google Scholar 

  • Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29–39

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61(15):4157–4168

    Article  PubMed  CAS  Google Scholar 

  • Zou J, Liu A, Chen X, Zhou X, Gao G, Wang W, Zhang X (2009) Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J Plant Physiol 166(8):851–861

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are highly thankful to the Project Director, Directorate of Rice Research, for his kind support. Financial support received from the National Initiative on Climate Resilient Agriculture (NICRA) project is acknowledged.

Author information

Authors and Affiliations

  1. Directorate of Rice Research, Hyderabad, Andhra Pradesh, India

    B. Sailaja, V. Vishnu Prasanth, N. Sarla, D. Subrahmanyam, S. R. Voleti, B. C. Viraktamath & Satendra K. Mangrauthia

  2. Centre for Biotechnology, Institute of Science & Technology, Jawaharlal Nehru Technological University, Hyderabad, India

    Nazreen Anjum

Authors
  1. B. Sailaja
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nazreen Anjum
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Vishnu Prasanth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Sarla
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D. Subrahmanyam
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. S. R. Voleti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. B. C. Viraktamath
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Satendra K. Mangrauthia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Satendra K. Mangrauthia.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 34 kb)

ESM 2

(DOC 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sailaja, B., Anjum, N., Vishnu Prasanth, V. et al. Comparative Study of Susceptible and Tolerant Genotype Reveals Efficient Recovery and Root System Contributes to Heat Stress Tolerance in Rice. Plant Mol Biol Rep 32, 1228–1240 (2014). https://doi.org/10.1007/s11105-014-0728-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-014-0728-y

Keywords

Search

Navigation