Skip to main content
SpringerLink
Log in

Genome-wide mining of respiratory burst homologs and its expression in response to biotic and abiotic stresses in Triticum aestivum

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Background

Membrane-bound NADPH oxidases (Nicotinamide adenine ainucleotide phosphate oxidase) also called respiratory burst oxidase homologs (Rboh) play an essential role in ROS production under normal as well as environmental stress conditions in plants.

Objective

To identify and study respiratory burst homologs (Rboh) from the wheat genome as well as characterize their role in various biological and molecular processes along with expression in response to biotic and abiotic stresses.

Methods

The Rboh homologs in the wheat genome were predicted based on data processing, alignment of sequences and phylogenetic analysis of sequences in numerous plant species and wheat. The conserved motifs were known followed by domain design study. The 3-D structure prediction and similarity modeling were administered for NADPH enzyme domain. Gene ontology and a functional study were done in addition to expression analysis of Triticum aestivum respiratory burst oxidase (TaRboh) gene family in response to biotic as well as abiotic stress.

Results

Phylogenetic analysis of Rboh gene family members among seven plant species including wheat, classified the family into four subfamilies. Rboh genes are mainly involved in various biological processes such as Response to oxidative stress, Superoxide anion generation, Hydrogen peroxide biosynthetic process. Among the molecular functions, calcium ion binding, peroxidase activity, oxidoreductase activity, superoxide-generating NADPH oxidase activity are essential. Enzyme annotation of the family and superfamily revealed that it encodes to five structural clusters and coding to enzymes NAD(P)H oxidase (H2O2-forming) (EC:1.6.3.1), Ferric-chelate reductase (NADH) (EC: 1.16.1.7), Peroxidase (EC: 1.11.1.7), Ribose-phosphate diphosphokinase (EC: 2.7.6.1). The enzymes contain six membrane-spanning domains, two hemes, and conserved motifs associated with NADPH, EF-hand and FAD binding. The outcomes additionally reflect a distinct role of this enzyme in different molecular functions which are responsible for the stress signaling. Further, the transcripts of TaRboh found expressed in various plant parts such as stem, leaves, spike, seed, and roots. We also observed expression of these gene family members under drought/combination of drought + heat and important wheat pathogens such as Puccinia striformis, Blumeria graminis f.sp. tritici, Fusarium graminiarum, F. pseudograminiarum, and Zymoseptoria tritici.

Conclusions

The investigation demonstrated that identified respiratory burst homologs (Rboh) in T. aestivum were involved in pathogen activated ROS production and have regulatory functions in cell death and defense responses.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Aguirre J, Ríos-Momberg M, Hewitt D, Hansberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13:111–118

    Article  CAS  PubMed  Google Scholar 

  • Amicucci E, Gaschler K, Ward JM (1999) NADPH oxidase genes from tomato (Lycopersicon esculentum) and curly-leaf pond-weed (Potamogeton crispus). Plant Biol 1:524–528

    Article  CAS  Google Scholar 

  • Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20:1390–1406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asano T, Hayashi N, Kobayashi M, Aoki N, Miyao A, Mitsuhara I, Ichikawa H, Komatsu S, Hirochika H, Kikuchi S, Ohsugi R (2012) A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance. Plant J 69:26–36

    Article  CAS  PubMed  Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    Article  CAS  PubMed  Google Scholar 

  • Barna B, Fodor J, Pogany M, Kiraly Z (2003) Role of reactive oxygen species and antioxidants in plant disease resistance. Pest Manag Sci 59:459–464

    Article  CAS  PubMed  Google Scholar 

  • Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245–313

    Article  CAS  PubMed  Google Scholar 

  • Castrignanò T, De Meo PD, Cozzetto D, Talamo IG, Tramontano A (2006) The PMDB Protein Model Database. Nucleic Acids Res 34:D306–D309

    Article  CAS  PubMed  Google Scholar 

  • Chang YL, Li WY, Miao H, Yang SQ, Li R, Wang X, Chen KM (2016) Comprehensive genomic analysis and expression profiling of the NOX gene families under abiotic stresses and hormones in plants. Genome Biol Evol 8:791–810

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaouch S, Queval G, Noctor G (2012) AtRbohF is a crucial modulator of defense-associated metabolism and a key factor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis. Plant J 69:613–627

    Article  CAS  PubMed  Google Scholar 

  • Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511–1519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, Bennett M, Mansfield J, Zipfel C, Hamann T (2011) Cell wall damage-induced lignin biosynthesis is regulated by a ROS-and jasmonic acid-dependent process in Arabidopsis thaliana. Plant Physiol 156:1364–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dmochowska-Boguta M, Nadolska-Orczyk A, Orczyk W (2013) Roles of peroxidases and NADPH oxidases in the oxidative response of wheat (Triticum aestivum) to brown rust (Puccinia triticina) infection. Plant Pathol 62:993–1002

    Article  CAS  Google Scholar 

  • Fiser A, Sali A (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol 374:461–491

    Article  CAS  PubMed  Google Scholar 

  • Geiszt M (2006) NADPH oxidases: new kids on the block. Cardiovasc Res 71:289–299

    Article  CAS  PubMed  Google Scholar 

  • Joshi AK, Mishra B, Chatrath R, Ortiz-Ferrara G, Singh RP (2007) Wheat improvement in India: present status, emerging challenges, and future prospects. Euphytica 157:431–446

    Article  Google Scholar 

  • Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S (2014) Ca2 + -activated reactive oxygen species production by Arabidopsis RbohH, and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Király L, Hafez YM, Fodor J, Király Z (2008) Suppression of tobacco mosaic virus-induced hypersensitive-type narcotization in tobacco at high temperature is associated with down regulation of NADPH oxidase and superoxide and stimulation of dehydro ascorbate reductase. J Gen Virol 89:799–808

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Künstler A, Bacsó R, Albert R, Barna B, Király Z, Hafez YM, Király L (2018) Superoxide (O2¯) accumulation contributes to symptomless (type I) nonhost resistance of plants to biotrophic pathogens. Plant Physiol Biochem 128:115–125

    Article  CAS  PubMed  Google Scholar 

  • Kuntal BK, Aparoy P, Reddanna P (2010) EasyModeller: a graphical interface to MODELLER. BMC Res Notes. 3:226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance Annu Rev Plant Biol 48:251–275

    Article  CAS  Google Scholar 

  • Laskowski RA (2001) PDBsum: summaries and analyses of PDB structures. Nucleic Acids Res 29:221–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Bork P (2017) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46(D1):D493–D496

    Article  CAS  PubMed Central  Google Scholar 

  • Lightfoot DJ, Boettcher A, Little A, Shirley N, Able AJ (2008) Identification and characterization of barley (Hordeum vulgare) respiratory burst oxidase homolog family members. Funct Plant Biol 35:347–359

    Article  CAS  Google Scholar 

  • Liu P, Li RL, Zhang L, Wang QL, Niehaus K, Baluška F, Šamaj J, Lin JX (2009) Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 60:303–313

    Article  CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M (2016) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marino D, Andrio E, Danchin EG, Oger E, Gucciardo S, Lambert A, Puppo A, Pauly N (2011) A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytol 189:580–592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    Article  CAS  PubMed  Google Scholar 

  • Maruta T, Inoue T, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2011) Arabidopsis NADPH oxidases, AtrbohD and AtrbohF, are essential for jasmonic acid-induced expression of genes regulated by MYC2 transcription factor. Plant Sci 180:655–660

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Mittler R (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal 2:45–46

    Google Scholar 

  • Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2 + regulates reactive oxygen species production and pH during mechano-sensing in Arabidopsis roots. Plant Cell 21:2341–2356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller K, Carstens AC, Linkies A, Torres MA, Leubner-Metzger G (2009) The NADPH-oxidase AtrbohB plays a role in Arabidopsis seed after-ripening. New Phytol 184:885–897

    Article  CAS  PubMed  Google Scholar 

  • Nestler J, Liu S, Wen TJ, Paschold A, Marcon C, Tang HM, Li D, Li L, Meeley RB, Sakai H, Bruce W (2014) Roothairless5, which functions in maize (Zea mays L) root hair initiation and elongation encodes a monocot-specific NADPH oxidase. Plant J 79:729–740

    Article  CAS  PubMed  Google Scholar 

  • Pearce S, Vazquez-Gross H, Herin SY, Hane D, Wang Y, Gu YQ, Dubcovsky J (2015) WheatExp: an RNA-seq expression database for polyploid wheat. BMC Plant Biol 15:299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penfield S, Li Y, Gilday AD, Graham S, Graham IA (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18:1887–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Potocký M, Jones MA, Bezvoda R, Smirnoff N, Zárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174:742–751

    Article  CAS  PubMed  Google Scholar 

  • Ramírez-González RH, Borrill P, Lang D, Harrington SA, Brinton J, Venturini L, Davey M, Jacobs J, Ex F, Pasha A, Khedikar Y, Robinson SJ, Cory AT, Florio T, Concia L, Juery C, Schoonbeek H, Steuernagel B, Xiang D, Ridout CJ, Chalhoub B, Mayer KFX, Benhamed M, Latrasse D, Bendahmane A, Wulff BBH, Appels R, Tiwari V, Datla R, Choulet F, Pozniak CJ, Provart NJ, Sharpe AG, Paux E, Spannagl M, Bräutigam A, Uauy C, International Wheat Genome Sequencing Consortium (2018) The transcriptional landscape of polyploid wheat. Science 361(6403):6089. https://doi.org/10.1126/scienceaar6089

    Article  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Supek F, Bošnjak M, Škunca N, Šmuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS One 6:e21800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki N, Rivero RM, Shulaev V, Blumwald E, Mittler R (2014) Abiotic and biotic stress combinations. New Phytol 203:32–43

    Article  PubMed  Google Scholar 

  • Takeda S, Gapper C, Kaya H, Bell E, Kuchitsu K, Dolan L (2008) Local positive feedback regulation determines cell shape in root hair cells. Science 319:1241–1244

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91 (phox) homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522

    Article  CAS  PubMed  Google Scholar 

  • Wang GF, Li WQ, Li WY, Wu GL, Zhou CY, Chen KM (2013) Characterization of rice NADPH oxidase genes and their expression under various environmental conditions. Int J Mol Sci 14:9440–9458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Zhang MM, Wang YJ, Gao YT, Li R, Wang GF, Chen KM (2016) The plasma membrane NADPH oxidase OsRbohA plays a crucial role in developmental regulation and drought-stress response in rice. Physiol Plant 156:421–443

    Article  CAS  PubMed  Google Scholar 

  • Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamoto K (2007) Regulation of rice NADPH oxidase by binding of RacGTPase to its N-terminal extension. Plant Cell 19:4022–4034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie YJ, Xu S, Han B, Wu MZ, Yuan XX, Han Y, Shen WB (2011) Evidence of Arabidopsis salt acclimation induced by up-regulation of HY1 and the regulatory role of RbohD-derived reactive oxygen species synthesis. Plant J 66:280–292

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa NK, Tsutsumi N, Yoshioka H, Nakazono M (2017) An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell 29:775–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshie Y, Goto K, Takai R, Iwano M, Takayama S, Isogai A, Che FS (2005) Function of the rice gp91phox homologs OsrbohA and OsrbohE genes in ROS dependent plant immune responses. Plant Biotechnol 22:127–135

    Article  CAS  Google Scholar 

  • Yoshioka H, Sugie K, Park HJ, Maeda H, Tsuda N, Kawakita K, Doke N (2001) Induction of plant gp91 phox homolog by fungal cell wall, arachidonic acid, and salicylic acid in potato. Mol Plant Microbe Interact 14:725–736

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka H, Numata N, Nakajima K (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15:706–718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshioka H, Mase K, Yoshioka M, Kobayashi M, Asai S (2011) Regulatory mechanisms of nitric oxide and reactive oxygen species generation and their role in plant immunity. Nitric Oxide 25:216–221

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are grateful to CIMMYT for providing the necessary financial support through CRP WHEAT. SN and SS acknowledge the award of an INSPIRE fellowship (IF 150037 & IF 150234) by the Indian government’s Department of Science and Technology.

Author information

Author notes

  1. Sudhir Navathe

    Present address: Agharkar Research Institute, G. G. Agarkar Road, Pune, 411004, India

Authors and Affiliations

  1. Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, Banaras Hindu University, Varanasi, UP, 221005, India

    Sudhir Navathe, Ramesh Chand & Vinod Kumar Mishra

  2. Department of Molecular and Human Genetics, Institute of Sciences, Banaras Hindu University, Varanasi, UP, 221005, India

    Sakshi Singh

  3. Centre for Bioinformatics, School of Biotechnology, Institute of Sciences, Banaras Hindu University, Varanasi, 221005, UP, India

    Vinay Kumar Singh

  4. International Maize and Wheat Improvement Center (CIMMYT), G-2, B-Block, NASC Complex, DPS Marg, New Delhi, 110012, India

    Arun Kumar Joshi

  5. Borlaug Institute for South Asia (BISA), G-2, B-Block, NASC Complex, DPS Marg, New Delhi, 110012, India

    Arun Kumar Joshi

Authors
  1. Sudhir Navathe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sakshi Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vinay Kumar Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ramesh Chand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vinod Kumar Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arun Kumar Joshi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

SN, planned experiments with help of RC, VKM and AKJ; SN, carried out data mining and analysis of the data aided by SS and VKS. SN wrote a manuscript with the help of the other authors. All of the authors have read and approved the final draft.

Corresponding author

Correspondence to Ramesh Chand.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This research does not perform any experiment on human and animals. Data used in this work were collected from open sources, and all in vitro data were generated at the Banaras Hindu University-Varanasi, India. Hence, the authors declare that there is no compliance with ethical standards.

Additional information

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 material 1 (PPTX 1663 kb)

Supplementary material 2 (DOCX 53 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Navathe, S., Singh, S., Singh, V.K. et al. Genome-wide mining of respiratory burst homologs and its expression in response to biotic and abiotic stresses in Triticum aestivum. Genes Genom 41, 1027–1043 (2019). https://doi.org/10.1007/s13258-019-00821-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-019-00821-x

Keywords

Search

Navigation