Skip to main content
SpringerLink
Log in

Defensive capabilities of contrasting sorghum genotypes against Atherigona soccata (Rondani) infestation

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Plants are equipped with a wide range of defensive mechanisms such as morphophysiological, biochemical, molecular, and hormonal signaling for protecting against insect-pest infestation. The infestation of a devastating pest shoot fly [Atherigona soccata (Rodani)] at seedling stage causes huge loss of sorghum crop productivity. In morphophysiological screening ICSV700, ICSV705, and IS18551 have been categorized as resistant, PSC-4 moderately resistant, SL-44 and SWARNA as susceptible. The present study focused on the role of defensive gene expression and its products viz: superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), polyphenol oxidase (PPO), phenyl alanine ammonia lyase (PAL), responsive enzymes, and metabolites restoring redox status in sorghum plants against shoot fly infestation. In both leaf and stem tissue of sorghum genotypes, shoot fly infestation induced SOD, APX, DHAR, GR, PAL, and PPO activities while CAT activity was significantly declined at 15 and 21 days after emergence (DAE). IS18551 with resistant behavior showed upregulation of SOD, GR, APX, and DHAR along with accumulation of ascorbate, glutathione enhancing redox status of the plant during shoot fly infestation at later stage of infestation. While SWARNA with susceptible response exhibited enhanced activity of phenylpropanoid pathway enzymes PAL and PPO which in turn increased the levels of secondary metabolites like o-dihydroxyphenol and other phenols deterring the insect to attack the plant. The qRT-PCR data predicted that stress-responsive genes were initially unregulated in SWARNA; however, at 21 DAE, multifold higher expression of SOD, CAT, APX, and PPO (24.8-, 37.2-, 21.7-, and 17.9-fold respectively) in 1S18551 indicates the resistance behavior of this genotype against insect infestation owing to sustainable development capability.

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

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article (and its additional files). Requests for material should be made to the corresponding author.

References

  • Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid- a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8:613

    Article  PubMed  PubMed Central  Google Scholar 

  • Andersen EJ, Ali S, Byamukama E, Yen Y, Nepal MP (2018) Disease resistance mechanisms in plants. Genes 9:339

    Article  CAS  PubMed Central  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, The Netherlands, pp 227–287

    Google Scholar 

  • Atkison NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63(10):3523–3544

    Article  CAS  Google Scholar 

  • Becana M, Aparicio-Tejo P, Irigoyen JJ, Sanchez-Diaz M (1986) Some enzymes of hydrogen peroxide metabolism in leaves and root nodules of Medicago sativa. Plant Physiol 82:1169–1171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belete T (2018) Defense mechanisms of plants to insect pests: from morphological to biochemical approach. Trends Appl Sci Res 2(2): 555584.

  • Berner M, Krug D, Bihlmaier C, Vente A, Muller R, Bechthold A (2006) Genes and enzymes involved in caffeic acid biosynthesis in the actinomycete Saccharothrix espanaensis. J Bacteriol 188:2666–2673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berner JM, Westhuizen AJ (2010) The selective induction of the phenylalanine ammonia-lyase pathway in the resistance response of wheat to the russian wheat aphid. Cereal Res Commun 38(4):506–513

    Article  CAS  Google Scholar 

  • Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  PubMed  Google Scholar 

  • Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nat 181:1199–2000

    Article  CAS  Google Scholar 

  • Chamarthi SK, Sharma HC, Sahrawat KL, Narasu LM, Dhillon MK (2010) Physico-chemical mechanisms of resistance to shoot fly, Atherigona soccata in sorghum, Sorghum bicolor. J Appl Entomol 135:446–455

    Article  Google Scholar 

  • Chance B, Maehly AC (1955) Assay of catalases and peroxidases. Meth Enzymol 2:764–775

    Article  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  CAS  PubMed  Google Scholar 

  • Chu B, Zhang S, Wang L, Zhu XZ, Luo JY, Wang CY, Lu LM, Cui JJ (2017) Genetic regulation of defence responses in cotton to insect herbivores. AoB PLANTS https://academic.oup.com/aobpla

  • Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Dordrecht, pp 253–270

    Chapter  Google Scholar 

  • Cooper WC, Jia L, Goggin FL (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. Chem Ecol 30:2527–2542

    Article  CAS  Google Scholar 

  • Czerniewicz P, Sytykiewicz H, Durak R, Borowiak-Sobkowiak B, Chrzanowski G (2017) Role of phenolic compounds during antioxidative responses of winter triticale to aphid and beetle attack. Plant Physiol and Biochem 118:529–540

    Article  CAS  Google Scholar 

  • Dale JW, Schantz M (2003) From genes to genomes. Concepts and applications of DNA technology. 3rd ed. John Wiley and Sons Ltd., The Atrium, Southern Gate, Chichester, West Sussex, England. 143–161

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

    Google Scholar 

  • Dubey NK, Goel R, Ranjan A, Idris A, Singh SK, Bag SK, Chandrashekar K, Pandey KD, Singh PK, Sawant SV (2013) Comparative transcriptome analysis of Gossypium hirsutum L. in response to sap sucking insects: aphid and whitefly. BMC Genom. 14: 241

  • Faize M, Burgos L, Faize L, Piqueras A, Nicolas E, Barba-Espin G, Clemente-Moreno MJ, Alcobendas R, Artlip T, Hernandez JA (2011) Involvement of cytosolic ascorbate peroxidase and Cu/Zn-superoxide dismutase for improved tolerance against drought stress. J Exp Bot 62:2599–2613

    Article  CAS  PubMed  Google Scholar 

  • Ghanta S, Chattopadhyay S (2011) Glutathione as a signaling molecule Another challenge to pathogens. Plant Signal Behav 6:783–788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol and Biochem 48:909–930

    Article  CAS  Google Scholar 

  • Gorthy S, Narasu L, Gaddameedi A, Sharma HC, Kotla A, Deshpande SP, Are AK (2017) Introgression of shoot Fly (Atherigona soccata L. Moench) resistance QTLs into elite post-rainy season Sorghum varieties using marker assisted backcrossing (MABC). Front Plant Sci 8:1494

  • Hasanuzzaman M, Borhannuddin Bhuyan MHM, Anee TI, Parvin K, Nahar K, Mahmud JL, Fujita M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants (Basel) 8(9):384

    Article  CAS  Google Scholar 

  • Horvath E, Janda T, Szalai G, Emil Paldi E (2002) In vitro salicylic acid inhibition of catalase activity in maize: differences between the isozymes and a possible role in the induction of chilling tolerance. Plant Sci 163:1129–1135

    Article  CAS  Google Scholar 

  • Inbar M, Doostdar H, Gerling D, Mayer RT (2003) Induction of systemic acquired resistance in cotton by BTH has a negligible effect on phytophagous insects. Entomol Exp Appl 99:65–70

    Article  Google Scholar 

  • Kaur H, Salh PK, Singh B (2017) Role of defense enzymes and phenolics in resistance of wheat crop (Triticum aestivum L.) towards aphid complex. Int J Plant Sci 12:304–311

    CAS  Google Scholar 

  • Kaur R, Gupta AK, Taggar GK (2014) Role of catalase, H2O2 and phenolics in resistance if pigeonpea toward Helicoverpa armigera (Hubner). Acta Physiol Plant 36:1513–1527

    Article  CAS  Google Scholar 

  • Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Infestation of potato (Solanum tuberosum L.) by the peach-potato aphid (Myzus persicae Sulzer) alters cellular redox status and is influenced by ascorbate. Plant Cell Environ 35:430–440

    Article  CAS  PubMed  Google Scholar 

  • Kovalikova Z, Kubes J, Skalicky M, Kuchtickova N, Maskova L, Tuma J, Vachova P, Hejnak V (2019) Changes in content of polyphenols and ascorbic acid in leaves of white cabbage after pest infestation. Molecules 24:2622

    Article  CAS  PubMed Central  Google Scholar 

  • Kumar AA, Reddy BVS, Sharma HC, Ramaiah B (2008) Shoot fly (Atherigona soccata) resistance in improved grain sorghum hybrids. E J SAT Agric Res 6:1–4

    Google Scholar 

  • Kumari A, Goyal M, Kumar R, Sohu RS (2021) Morphophysiological and biochemical attributes influence intra-genotypic preference of shoot fly [Atherigona soccata (Rondani)] among sorghum genotypes. Protoplasma 258:87–102

    Article  PubMed  Google Scholar 

  • Law MY, Charles SA, Halliwell B (1983) Glutathione and ascorbic acid in spinach (Spinacia oleraceaL.) chloroplasts: The effect of hydrogen peroxide and of paraquat. Biochem J 210:899–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Zhang S, Whitworth RJ, Stuart JJ, Chen MS (2015) Unbalanced activation of glutathione metabolic pathways suggests potential involvement in plant defense against the gall midge Mayetiola destructor in wheat. Sci Rep 5:8092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Huang D, Chen C, Zhu S, Gao J (2019) Regulation of ascorbateglutathione cycle in peaches via nitric oxide treatment during cold storage. Sci Hortic 247:400–406

    Article  CAS  Google Scholar 

  • Maffei ME, Mithöfer A, Boland W (2007) Insects feeding on plants: rapid signals and responses preceding the induction of phytochemical release. Phytochem 68:2946–2959

    Article  CAS  Google Scholar 

  • Mai VC, Drzewieckac K, Jelen H, Narozna D, Sobkowiak RR, Kesy J, Wieczoreka JF, Gabrys B, Morkunas I (2014) Differential induction of Pisum sativum defense signaling molecules in response to pea aphid infestation. Plant Sci 221:1–12

    Article  CAS  PubMed  Google Scholar 

  • Meitei AL, Bhattacharjee M, Dhar S, Chowdhury N, Sharma R, Acharjee S, Sarmah BK (2018) Activity of defense related enzymes and gene expression in pigeon pea (Cajanus cajan) due to feeding of Helicoverpa armigera larvae. Int J Plant Prod 13:231–238

    CAS  Google Scholar 

  • Mittal A, Yadav IS, Arora NK, Boora RS, Mittal M, Kaur P, Erskine W, Chhuneja P, Gill M.I.S., Singh K(2020) RNA-sequencing based gene expression landscape of guava cv. Allahabad Safeda and comparative analysis to colored cultivars. BMC Genom 21: 484.

  • Mohammed R, Are AK, Munghate RS, Bhavanasi RB, Polavarapu KK, Sharma HC (2016) Inheritance of Resistance to Sorghum Shoot Fly, Atherigona soccata in Sorghum, Sorghum bicolor (L.) Moench. Front Plant Sci 7: 543.

  • Nair PM, Vaidyanathan CS (1964) A colorimetric method for determination of pyrocatechol and related substances. Anal Biochem 7:315–321

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nath P, Panday AK, Kumar A, Rai AB, Palanivel H (2017) Biochemical Resistance Traits of Bitter Gourd against Fruit Fly Bactrocera cucurbitae (Coquillett) Infestation. J Agric Sci 9:9752–9760

    Google Scholar 

  • Nazar R, Umar S, Khan NA (2015) Exogenous salicylic acid improves photosynthesis and growth through increase in ascorbate-glutathione metabolism and S assimilation in mustard under salt stress. Plant Signal Behav10: e1003751.

  • Oliveira CM, Ferreira ACS, de Freitas V, Silva AM (2011) Oxidation mechanisms occurring in wines. Food Res Int 44:1115–1126

    Article  CAS  Google Scholar 

  • Padmaja PG, Shwetha BL, Swetha G, Patil JV (2014) Oxidative Enzyme Changes in Sorghum Infested by Shoot Fly. J Insect Sci 14:1–5

    Article  Google Scholar 

  • Padmaja PG, Woodcock CM, Bruce TJA (2010) Electrophysiological and Behavioral Responses of Sorghum Shoot Fly, Atherigona soccata, to Sorghum Volatiles. J Chem Ecol 36:1346–1353

    Article  CAS  PubMed  Google Scholar 

  • Pandey S, Fartyal D, Agarwal A, Shukla T, James D, Kaul T, Negi YK, Arora S, Reddy MK (2017) Abiotic Stress Tolerance in Plants: Myriad Roles of Ascorbate Peroxidase. Front. Plant Sci. https://doi.org/10.3389/fpls.2017.00581

  • Papadopoulou GV, Dam NMV (2017) Mechanisms and ecological implications of plant mediated interactions between belowground and aboveground insect herbivores. " Ecol Res 32: 13–26

  • Rani PU, Jyothsna Y (2010) Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiol Plant 32:695–701

    Article  CAS  Google Scholar 

  • Rolff M, Schottenheim J, Decker H, Tuczek F (2011) Copper-O2 reactivity of tyrosinase models towards external monophenolic substrates: Molecular mechanism and comparison with the enzyme. R Soc Chem 40:4077–4098

    Article  CAS  Google Scholar 

  • Rossatto T, do Amaral MN, Benitez LC, Vighi IL, Braga EJB, de Magalhaes Junior AM, Maia MAC, da Silva Pinto L (2017) Gene expression and activity of antioxidant enzymes in rice plants, cv. BRS AG, under saline stress. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-017-0467-2.

  • Sanabria NM, Huang JC, Dubery IA (2010) Self/nonself perception in plants in innate immunity and defense. Landes Biosci 1:40–54

    Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shivashankar S, Sumathi M, Krishnakumar NK, Rao VK (2014) Role of phenolic acids and enzymes of phenylpropanoid pathway in resistance of chayote fruit (Sechium edule) against infestation by melon fly. Bactrocera Cucurbitae, Annals of Applied Biology 16:420–433

    Google Scholar 

  • Singla P, Bhardwaj RD, Kaur S, Kaur J (2019) Stripe rust induced defence mechanisms in the leaves of contrasting barley genotypes (Hordeum vulgare L.) at the seedling stage. Protoplasma https://doi.org/10.1007/s00709-019-01428-5.

  • Sinha (1972) Colorometricassay of catalase. Anal Biochem 47: 389-394

  • Sonalkar VU, Pagire KS, Gulhane AR, Ghorade RB (2018) Management of shoot fly, atherigona soccata (Diptera: Muscidae) in Kharif Sorghum in Vidarbha. Int J Curr Microbiol Appl Sci 7:2192–2206

    Article  CAS  Google Scholar 

  • Soto PE (1974) Ovipositional preference and antibiosis in relation to resistance to sorghum shoot fly. J Econ Entomol 67:265–267

    Article  CAS  PubMed  Google Scholar 

  • Stout MJ, Workman KV, Bostock RM, Duffey SS (1998) Stimulation and attenuation of induced resistance by elicitors and inhibitors of chemical induction in tomato (Lycopersicon esculentum) foliage. Entomol Exp Appl 86:267–279

    Article  CAS  Google Scholar 

  • Sytykiewicz H (2014) Differential expression of superoxide dismutase genes in aphid-stressed maize (Zea mays L.) seedlings. Plos One 9: e94847

  • Sytykiewicz H (2016) Expression PATTERNS OF GENES INVOLVED IN ASCORBATE-GLUTATHIONE CYCLE IN APHID-INFESTED MAIze (Zea mays L.) Seedlings. Int J Mol Sci 17: 268

  • Taranto F, Pasqualone A, Mangini G, Tripodi P, Miazzi MM, Pavan S, Montemurro C (2017) Polyphenol oxidases in crops: biochemical, physiological and genetic aspects. Int J Mol Sci 18:377

    Article  CAS  PubMed Central  Google Scholar 

  • Teixeira FK, Menezes-Benavente L, Galvao VC, Pinheiro M (2005) Multigene families encode the major en zymes of antioxidant metabolism in Eucalyptus grandis L. Genet Mol Biol 28:529–538

    Article  CAS  Google Scholar 

  • Torres MA (2010) ROS in biotic interactions. Plant Cell Physiol 138:414–429

    Article  CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  PubMed  PubMed Central  Google Scholar 

  • Yendrek CR, Koester RP, Ainsworth EAA (2015) Comparative analysis of transcriptomic, biochemical, and physiological responses to elevated ozone identifies species-specific mechanisms of resilience in legume crops. J Exp Bot 66:7101–7112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zauberman G, Ronen R, Akerman M, Weksler A, Rot I, Fuchs Y (1991) Post-harvest retention of the red colour of litchi fruit pericarp. Sci Hortic 47:89–97

    Article  CAS  Google Scholar 

  • Zavala JA, Patankar AG, Gase K, Hui D, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134:1181–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu-Salzman K, Luthe DS, Felton GW (2008) Arthropod-inducible proteins: broad-spectrum defenses against multiple herbivores. Plant Physiol 146:852–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the International Crop Research Institute for the Semi-Arid Tropics (ICRISAT) Patancheru, Telangana and Department of Plant Breeding and Genetics, Punjab Agricultural University, Ludhiana, for providing study material.

Author information

Authors and Affiliations

  1. Department of Biochemistry, Punjab Agricultural University, Ludhiana, 141004, India

    Archana Kumari

  2. Department of Plant Breeding, and Genetics, Punjab Agricultural University, Ludhiana, 141004, India

    Meenakshi Goyal

  3. School of Agricultural Biotechnology, Punjab Agricultural University, Ludhiana, 141004, India

    Amandeep Mittal

  4. Department of Vegetable Crops, Punjab Agricultural University, Ludhiana, 141004, India

    Ravinder Kumar

Authors
  1. Archana Kumari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Meenakshi Goyal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amandeep Mittal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ravinder Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Archana Kumari.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Handling Editor: Peter Nick

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 650 kb)

Supplementary file2 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumari, A., Goyal, M., Mittal, A. et al. Defensive capabilities of contrasting sorghum genotypes against Atherigona soccata (Rondani) infestation. Protoplasma 259, 809–822 (2022). https://doi.org/10.1007/s00709-021-01703-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-021-01703-4

Keywords

Search

Navigation