Abstract
This study was undertaken to investigate the effect of biostimulants such as spermidine (1 mM, 2 mM), indole-3-acetic acid (10–3 M, 10–5 M), brassinolide (1 mg/L, 2 mg/L) and boron (50 mg/L, 100 mg/L) on protecting rice plants from heat-induced damage. Two rice genotypes, Nagina 22 (heat tolerant) and Manu Ratna (heat susceptible), primed with biostimulant solution were germinated, 14-day-old seedlings were further foliar sprayed with respective treatment solutions prior to the induction of heat stress (42 °C, 48 h). Heat stress-induced fatal damages to non-biostimulant-treated rice seedlings, whereas biostimulant-treated ones were protected from heat stress-induced damages, marked by lower levels of malondialdehyde (MDA), H2O2 coupled with increased levels of seedling vigour index (SVI), chlorophyll and proline contents. Results showed that 1 mM spermidine (Spd) and 10–5 M indole-3-acetic acid (IAA)-treated rice seedlings showed increased heat tolerance and were evaluated for its effect at reproductive stage stress in a pot culture study. At the panicle initiation stage, plants were pretreated with 1 mM Spd and 10–5 M IAA followed by the induction of heat stress, kee** it in a temperature-controlled polyhouse (42.1 °C, till the time of harvest). Spd- and IAA-pretreated heat-exposed plants exhibited yield improvement over control by altering physiological, biochemical and molecular mechanisms. Therefore, we conclude from our results that foliar IAA or Spd applications can be regarded as an agronomic strategy for mitigating the adverse effects of heat stress conditions on rice plants.
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Abbreviations
- Spd:
-
Spermidine
- IAA:
-
Indole-3-acetic acid
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- CAT:
-
Catalase
- MDA:
-
Malondialdehyde
- CMSI:
-
Cell membrane stability index
- SVI:
-
Seedling vigor index
- HT:
-
High temperature
- Pro:
-
Proline
- Chl:
-
Chlorophyll
- B:
-
Boron
References
Abdel Latef AAH, Tahjib-Ul-Arif M, Rhaman MS (2021) Exogenous auxin-mediated salt stress alleviation in faba bean (Vicia faba L.). Agron 11(3):547–568
Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria 1. Crop Sci 13(6):630–633
Aebi H (1974) Catalase. Methods of enzymatic analysis. Elsevier, NY, pp 673–684
Amrutha V, Shanija S, Beena R, Sarada S, Sajitha RT, Roy S, Manju RV, Viji MM (2021a) High temperature induced changes in quality and yield parameters of tomato (Solanum lycopersicum L) and similarity coefficients among genotypes using SSR markers. Heliyon. https://doi.org/10.1016/j.heliyon.2021.e05988
Amrutha V, Shanija S, Beena R, Nithya N, Jaslam MPK, Soni KB, Viji MM (2021b) Population structure analysis and marker trait association in selected set of Indian tomato (Solanum lycopersicum L.) varieties under high temperature condition. Gen Resour Crop Evol. https://doi.org/10.1007/s10722-021-01216-2
Arnon DT (1949) Copper enzymes in isolated chloroplast polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15
Aryadeep R, Supratim B, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or sermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328
Baker HG, Baker I (1979) Starch in angiosperm pollen grains and its evolutionary significance. Am J of Bot 66(5):591–600
Basra SMA, Farooq M, Tabassum R, Ahmad N (2005) Physiological and biochemical aspects of seed vigor enhancement treatments in fine rice (Oryza sativa L.). Seed Sci and Technol 33:623–628
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Beena R (2013) Research paradigm and inference of studies on high temperature stress in rice (Oryza sativa L.). Adv Plant Physiol 14:497–511
Beena R, Vighneswaran V, Sindumole P, Narayankutty MC, Voleti SR (2018) Impact of high temperature stress during reproductive and grain filling stage in rice. Oryza, an Int J on Rice 55(1):126–133
Beena R, Veena V, Jaslam MPK, Nithya N, Adarsh VS (2021) Germplasm innovation for high-temperature tolerance from traditional rice accessions of Kerala using genetic variability, genetic advance, path coefficient analysis and principal component analysis. J of Crop Sci and Biotechnol 24:555–556
Calderón-Páez SE, Cueto-Niño YA, Sánchez-Reinoso AD, Garces-Varon G, Chávez-Arias CC, Restrepo-Díaz H (2021) Foliar boron compounds applications mitigate heat stress caused by high daytime temperatures in rice (Oryza sativa L.) Boron mitigates heat stress in rice. J Plant Nutr 44(17):2414–2527
Camejo D, Jiménez A, Alarcón JJ, Torres W, Gómez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Funct Plant Biol 33(2):177–187
Castorina G, Consonni G (2020) The role of brassinosteroids in controlling plant height in Poaceae: a genet perspective. Int J Mol Sci 21:1191
Chen Q, Dai X, De-Paoli H, Cheng Y, Takebayashi Y, Kasahara H, Kamiya Y, Zhao Y (2014) Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant and Cell Physiol 55(6):1072–1079
Chen M, Fu Y, Mou Q, An J, Zhu X, Ahmed T, Zhang S, Basit F, Hu J, Guan Y (2021) Spermidine induces expression of stress associated proteins (SAPs) genes and protects rice seed from heat stress-induced damage during grain-filling. Antioxidants 10(10):1544
Crawford B, Yanofsky MF (2011) Half-filled promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Dev 138:2999–3009
Dai AH, Nie YX, Yu B, Li Q, Lu LY, Bai JG (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10
Das S, Mohanty S, Dash D, Muduli KC (2019) Enhancement of growth and seed yield of rice (Oryza sativa L.) through foliar spray of osmoprotectants under high temperature stress. Indian J of Tradit Knowl 19(1):92–100
Diao Q, Song Y, Qi H (2015) Exogenous spermidine enhances chilling tolerance of tomato (Solanum lycopersicum L.) seedlings via involvement in polyamines metabolism and physiological parameter levels. Acta Physiol Plant 37:1–15
Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J of Plant Physiol 165(15):1620–1635
Eklund DM, Staldal V, Valsecchi I (2010) The Arabidopsis thaliana STYLISH1 protein acts as a transcriptional activator regulating auxin biosynthesis. Plant Cell 22:349–363
Fu G, Feng B, Zhang C, Yang Y, Yang X, Chen T, Zhao X, Zhang X, ** Q, Tao L (2016) Heat stress is more damaging to superior spikelets than inferiors of rice (Oryza sativa L.) due to their different organ temperatures. Front Plant Sci 7:1637
Fu Y, Gu Q, Dong Q, Zhang Z, Lin C, Hu W, Pan R, Guan Y, Hu J (2019) Spermidine enhances heat tolerance of rice seeds by modulating endogenous starch and polyamine metabolism. Molecules 24(7):1395
Gadallah MAA (1999) Effects of proline and glycinebetaine on Vicia faba responses to salt stress. Biol Plant 42(2):249–257
García-Hernández EDR, López GIC (2005) Structural cell wall proteins from five pollen species and their relationship with boron. Brazilian J Plant Physiol 17:375–381
Guangwu Z, Xuwen J (2014) Roles of gibberellin and auxin in promoting seed germination and seedling vigor in Pinus massoniana. Forest Sci 60(2):367–373
Guru T, Kunta RT, Rao P (2016) Improving pollen viability and stigma receptivity by boron application as a physiological approach for high yields in rice. Bioscan 11(1):79–83
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Holá D, Benešová M, Honnerová J, Hnilička F, Rothová O, Kočová M, Hniličková H (2010) The evaluation of photosynthetic parameters in maize inbred lines subjected to water deficiency: can these parameters be used for the prediction of performance of hybrid progeny? Photosynth 48(4):545–558
Hozain MD, Abdelmageed H, Lee J, Kang M, Fokar M, Allen RD, Holaday AS (2012) Expression of AtSAP5 in cotton up-regulates putative stress-responsive genes and improves the tolerance to rapidly develo** water deficit and moderate heat stress. J of Plant Physiol 169(13):1261–1270
IPCC, Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M (2021) Climate change 2021: The Phys sci basis contribution of working group I to the sixth assess. Rep. of the intergovernmental panel on clim. change.
Jagadish SVK, Cairns J, Lafitte R, Wheeler TR, PriceAH and Craufurd PQ, (2010) Genetic analysis of heat tolerance at anthesis in rice. Crop Sci 50:1633–1641
Jagadish SVK, Septiningsih EM, Kohli A, Thomson MJ, Ye C, Redona E, Kumar A, Gregorio GB, Wassmann R, Ismail AM, Singh RK (2012) Genetic advances in adapting rice to a rapidly changing climate. J Agron Crop Sci 198(5):360–373
Janni M, Gullì M, Maestri E, Marmiroli M, Valliyodan B, Nguyen HT, Marmiroli N, Foyer C (2020) Molecular and genetic bases of heat stress responses in crop plants and breeding for increased resilience and productivity. J Exp Bot 71:3780–3802
Kang M, Fokar M, Abdelmageed H, Allen RD (2011) Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity. Plant Mol Biol 75(4–5):451–466
Kim JI, Baek D, Park HC (2013) Overexpression of Arabidopsis YUCCA6 in potato results in high-auxin developmental phenotypes and enhanced resistance to water deficit. Mol Plant 6:337–349
Kono Y (1978) Generation of superoxide radicals during auto-oxidation of hydroxyl-amine hydrochloride an assay for SOD. Arch Biochem Biophys 186:189–195
Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiol Plant 34(1):75–86
Kusano T, Berberich T, Tateda C, Takahashi Y (2008) Polyamines: essential factors for growth and survival. Plant 228(3):367–381
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
Matsui T, Omasa K (2002) Rice (Oryza sativa L.) cultivars tolerant to high temperature at flowering: anther characteristics. Ann of Bot 89(6):683–687
Matthes MS, Best NB, Robil JM, Malcomber S, Gallavotti A, McSteen P (2019) Auxin EvoDevo: conservation and diversification of genes regulating auxin biosynthesis, transport, and signaling. Mol Plant 12(3):298–320
Mittler R, Finka A, Goloubinoff P (2012) How do plants feel the heat? Trends Biochem Sci 37:118–125
Mostofa MG, Yoshida N, Fujita MJ (2014) Spermidine pretreatment enhances heat tolerance in rice seedlings through modulating antioxidative and glyoxalase systems. Plant Growth Regul 73:31–44
Muhammad F, Shahzad M, Basra H (2008) Seed priming with polyamines improves the germination and early seedling growth in fine rice. J New Seeds 9:145–155
Nayyar H, Kaur R, Kaur S, Singh RS (2014) γ-aminobutyric acid (GABA) imparts partial protection from heat stress injury to rice seedlings by improving leaf turgor and upregulating osmoprotectants and antioxidants. J Plant Growth Regul 33:408–419
Niu Y, **ang Y (2018) An overview of biomembrane functions in plant responses to high-temperature stress. Front Plant Sci 9:915
Ogweno JO, Song XS, Shi K, Hu WH, Mao WH, Zhou YH, Yu JQ, Nogués S (2008) Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Reg 27(1):49–57
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
Prasanth VV, Babu MS, Basava RK, Tripura VGN, Venkata SK, Mangrauthia SR, Voleti S, Neelamraju, (2017) Trait and marker associations in Oryza nivara and O. rufipogon derived rice lines under two different heat stress conditions. Front Plant Sci 8:1819
Pravallika K, Arunkumar C, Vijayakumar A, Beena R, Jayalekshmi VG (2020) Effect of high temperature stress on seed filling and nutritional quality of rice (Oryza sativa L.). J Crop Weed 16(2):18–23
Quintero-Calderon EH, Sanchez-Reinoso AD, Chavez-Arias CC, Garces-Varon G, Restrepo-Diaz H (2021) Rice seedlings showed a higher heat tolerance through the foliar application of biostimulants. Notulae Bot Hortic Agrobot Cluj-Napoca 49(1):12120–12120
Raghunath MP, Beena R (2021) Manipulation of flowering time to mitigate high temperature stress in rice (Oryza sativa L.). Indian J Agric Res 1:4
Raghunath M, Beena R, Mohan V, Viji M, Manju R, Stephen R (2021) High temperature stress mitigation in rice (Oryza sativa L.): Foliar application of plant growth regulators and nutrients. J Crop Weed 17(1):34–47
Rizzardi K, Landberg K, Nilsson L, Ljung K, Larsson AS (2011) TFL2/LHP1 is involved in auxin biosynthesis through positive regulation of YUCCA genes. Plant J 65:897–906
Sailaja B, Subrahmanyam D, Neelamraju S, Vishnukiran T, Rao YV, Vijayalakshmi P, Voleti SR, Bhadana VP, Mangrauthia SK (2015) Integrated physiological, biochemical, and molecular analysis identifies important traits and mechanisms associated with differential response of rice genotypes to elevated temperature. Front Plant Sci 6:1044
Sairam RK, Deshmukh PS, Shukla DS (1997) Tolerance of drought and temperature stress in relation to increased antioxidant enzyme activity in wheat. J Agron Crop Sci 178(3):171–178
Savchenko GE, Klyuchareva EA, Abramchik LM, Serdyuchenko EV (2002) Effect of periodic heat shock on the inner membrane system of etioplasts. Russian J Plant Physiol 49(3):349–359
Sharma L, Dalal M, Verma RK, Kumar SV, Yadav SK, Pushkar S, Kushwaha SR, Bhowmik A, Chinnusamy V (2018) Auxin protects spikelet fertility and grain yield under drought and heat stresses in rice. Environ and Exp Bot 150:9–24
Sohlberg JJ, Myrenas M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E (2006) STY1 regulates auxin homeostasis cts apical-basal patterning of the Arabidopsis gynoecium. Plant J 47:112–123
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 45:911–921
Thussagunpanit J, Jutamanee K, Kaveeta L, Chai-arree W, Pankean P, Suksamrarn A (2013) Effects of brassinosteroid and ecdysone analogue on pollen germination of rice under heat stress. J Pestic Sci 38:105–111
Trigueros M, Navarrete-Gomez M, Sato S, Christensen SK, Pelaz S, Weigel D, Yanofsky MF, Ferrandiz C (2009) The NGATHA genes direct style development in the Arabidopsis gynoecium. Plant Cell 21:1394–1409
Vaishali M, Marcus C, Chibucos Vipaporn P, Paul F, Morris, (2012) Kinetic and phylogenetic analysis of plant polyamine uptake transporters. Funct Plant Biol 236(4):1261–1273
Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 zinc-finger (s) in rice and their phylogenetic relationship with Arabidopsis. Mol Genet Genomics 276(6):565–575
Xu J, Henry A, Sreenivasulu N (2020) Rice yield formation under high day and night temperatures—a prerequisite to ensure future food security. Plant Cell Environ 43:1595–1608
Yin CC, Ma B, Wang W, **ong Q, Zhao H, Chen SY, Zhang JS (2016) RNA extraction and preparation in rice (Oryza sativa). Curr Protocols in Plant Biol 1(2):411–418
Yu CW, Murphy TM, Lin CH (2003) Hydrogen peroxide-induces chilling tolerance in mung beans mediated through ABA independent glutathione accumulation. Funct Plant Biol 30:955–963
Zhang C, Bai MY, Chong K (2014) Brassinosteroid-mediated regulation of agronomic traits in rice. Plant Cell Rep 33:683–696
Zhang C, Li G, Chen T, Feng B, Fu W, Yan J, Islam MR, ** Q, Tao L, Fu G (2018) Heat stress induces spikelet sterility in rice at anthesis through inhibition of pollen tube elongation interfering with auxin homeostasis in pollinated pistils. Rice 11(1):1–12
Zhao Y (2011) Auxin biosynthesis: a simple two-step pathway converts tryptophan to indole-3-acetic acid in plants. Mol Plant 5:334–338
Zhao Q, Zhou L, Liu J, Cao Z, Du X, Huang F, Pan G, Cheng F (2018) Involvement of CAT in the detoxification of HT-induced ROS burst in rice anther and its relation to pollen fertility. Plant Cell Rep 37:741–757
Zhou R, Hu Q, Pu Q, Chen M, Zhu X, Gao C, Zhou G, Liu L, Wang Z, Yang J, Zhang J (2020) Spermidine enhanced free polyamine levels and expression of polyamine biosynthesis enzyme gene in rice spikelets under heat tolerance before heading. Sci Rep 10(1):1–9
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The authors thank Kerala Agricultural University for providing all the facilities.
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by (Lakshmi G.), (Dr.Beena R.), (Dr.Soni K.B..), (Dr.Viji, M.M.) and Dr.Uday Chand Jha). The first draft of the manuscript was written by (Lakshmi G.) and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Lakshmi, G., Beena, R., Soni, K.B. et al. Exogenously applied plant growth regulator protects rice from heat-induced damage by modulating plant defense mechanism. J. Crop Sci. Biotechnol. 26, 63–75 (2023). https://doi.org/10.1007/s12892-022-00162-4
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DOI: https://doi.org/10.1007/s12892-022-00162-4