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Constitutive H2O2 is involved in sorghum defense against aphids

  • Yutao ShaoEmail author
  • Mingxin Guo
  • Xianfeng He
  • Qingxin Fan
  • Zhenjie Wang
  • Jin Jia
  • Jiangbo Guo
Original Article
  • 17 Downloads

Abstract

Reactive oxygen species (ROS) play a major role in plant defense against pathogens, but the evidence for their role in defense against insects is still limited. In this study, HN16 and its mutated line (asm1) were used as research objects, and the potential role of H2O2 in sorghum against aphid was examined. Constitutive H2O2 was considered the main factor associated with increased aphid tolerance, although aphid feeding also induced an increase in the H2O2 concentration. By studying ROS scavenging enzymes, it was found that APX and GPX were closely related, but SOD, POX and CAT were not involved in RMES1-mediated resistance. DEGs involved in the detoxification of ROS in HN16 worked through different means. Analysis of three DEGs encoding APX and GPX revealed that although the expression changes of SbAPx1 were consistent and those of SbGPx1 and SbGPx2 were inconsistent with enzyme activity, they all played an important role in RMES1-mediated resistance to aphids.

Keywords

Antioxidant enzymes Melanaphis sacchari Reactive oxygen species 

Abbreviations

APX

Ascorbate peroxidase

ANOVA

One-way analysis of variance

CAT

Catalase

DEG

Differentially expressed gene

F3H

Flavanone-3-hydroxylases

GPX

Glutathione peroxidase

Grx

Glutaredoxins

GST

Glutathione S-transferases

H2O2

Hydrogen peroxide

POX

Peroxidase

ROS

Reactive oxygen species

SOD

Superoxide dismutase

Trx

Thioredoxins

Notes

Acknowledgements

This study was supported by grants from the National Natural Science Foundation of China (31660396), the Natural Science Foundation of Inner Mongolia (2016MS0308), the Innovation Fund (Excellent Youth Science Fund) of Inner Mongolia University of Science and Technology (2017YQL09) and the Innovation Fund for College Students of Inner Mongolia University of Science and Technology (2015016).

Authors’ contributions

YS, JJ and JG contributed to the experimental design and writing of this manuscript. MG, XH and QF contributed to the performance of experiments. ZW contributed to the data analysis.

References

  1. Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35–45CrossRefGoogle Scholar
  2. Almagro L, Gómez Ros LV, Belchi-Navarro S, Bru R, Ros Barceló A, Pedreño MA (2008) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390CrossRefGoogle Scholar
  3. Anjum NA, Gill SS, Gill R, Hasanuzzaman M, Duarte AC, Pereira E et al (2014) Metal/metalloid stress tolerance in plants: role of ascorbate, its redox couple, and associated enzymes. Protoplasma 251:1265–1283CrossRefGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399CrossRefGoogle Scholar
  5. Barna B, Fodor J, Harrach BD, Pogány M, Király Z (2012) The janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol Biochem 59:37CrossRefGoogle Scholar
  6. Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201CrossRefGoogle Scholar
  7. Bellincampi D, Dipierro N, Salvi G, Cervone F, De Lorenzo G (2000) Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol 122:1379–1386CrossRefGoogle Scholar
  8. Camejo D, Guzmán-Cedeño Á, Moreno A (2016) Reactive oxygen species, essential molecules, during plant-pathogen interactions. Plant Physiol Biochem 103:10–23CrossRefGoogle Scholar
  9. Chen MS (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114CrossRefGoogle Scholar
  10. Coppola V, Coppola M, Rocco M, Digilio MC, D’Ambrosio C, Renzone G et al (2013) Transcriptomic and proteomic analysis of a compatible tomato-aphid interaction reveals a predominant salicylic acid-dependent plant response. BMC Genom 14:515–532CrossRefGoogle Scholar
  11. 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.  https://doi.org/10.3389/fenvs.2014.00053 CrossRefGoogle Scholar
  12. Dixon DP, Skipsey M, Edwards R (2010) Roles for glutathione transferases in plant secondary metabolism. Phytochemistry 71:338–350CrossRefGoogle Scholar
  13. Foyer CH, Noctor G (2013) Redox signaling in plants. Antioxid Redox Signal 18:2087–2090CrossRefGoogle Scholar
  14. Fu JY (2014) Cloning of a new glutathione peroxidase gene from tea plant (Camellia sinensis) and expression analysis under biotic and abiotic stresses. Bot Stud 55:7.  https://doi.org/10.1186/1999-3110-55-7 CrossRefGoogle Scholar
  15. Gao F, Chen J, Ma T, Li H, Wang N, Li Z et al (2014) The glutathione peroxidase gene family in Thellungiella salsuginea: genome-wide identification, classification, and gene and protein expression analysis under stress conditions. Int J Mol Sci 15:3319–3335CrossRefGoogle Scholar
  16. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  17. Gill RS, Gupta AK, Taggar GK, Taggar MS (2010) Role of oxidative enzymes in plant defenses against insect herbivory. Acta Phytopathol Entomol Hung 45:277–290CrossRefGoogle Scholar
  18. Giovanini MP, Puthoff DP, Nemacheck JA, Mittapalli O, Saltzmann KD, Ohm HW, Shukle RH, Williams CE (2006) Gene-for-gene defense of wheat against the hessian fly lacks a classical oxidative burst. Mol Plant-Microbe Interact 19:1023–1033CrossRefGoogle Scholar
  19. Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124:21–29CrossRefGoogle Scholar
  20. Gulsen O, Eickhoff T, Heng-Moss T, Shearman R, Baxendale F, Sarath G et al (2010) Characterization of peroxidase changes in resistant and susceptible warm season turf grasses challenged by Blissus occiduus. Arthropod Plant Interact 4:45–55CrossRefGoogle Scholar
  21. Gutsche A, Heng-Moss T, Sarath G, Twigg P, Xia Y, Lu G et al (2009) Gene expression profiling of tolerant barley in response to Diuraphis noxia (Hemiptera: Aphididae) feeding. Bull Entomol Res 99:163–173CrossRefGoogle Scholar
  22. Han Y, Wang Y, Bi JL, Yang XQ, Huang Y, Zhao X, Hu Y, Cai QN (2009) Constitutive and induced activities of defense-related enzymes in aphid-resistant and aphid-susceptible cultivars of wheat. J Chem Ecol 35:176–182CrossRefGoogle Scholar
  23. Heng-Moss T, Sarath G, Baxendale F, Novak D, Bose S, Ni X, Quisenberry S (2004) Characterization of oxidative enzyme changes in buffalograsses challenged by Blissus occiduus. J Econ Entomol 97:1086–1095CrossRefGoogle Scholar
  24. Hernández JA, Jimenez A, Mullineaux PM, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defense. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  25. Hossain MA, Bhattacharjee S, Armin SM, Qian P, Xin W, Li HY et al (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci 6:420.  https://doi.org/10.3389/fpls.2015.00420 Google Scholar
  26. Inupakutika MA, Sengupta S, Devireddy AR, Azad RK, Mittler R (2016) The evolution of reactive oxygen species metabolism. J Exp Bot 67:5933–5943CrossRefGoogle Scholar
  27. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago, pp 1–319CrossRefGoogle Scholar
  28. Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837Google Scholar
  29. Kiani M, Szczepaniec A (2018) Effects of sugarcane aphid herbivory on transcriptional responses of resistant and susceptible sorghum. BMC Genom.  https://doi.org/10.1186/s12864-018-5095-x Google Scholar
  30. Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203CrossRefGoogle Scholar
  31. Kuzniak E, Sklodowska M (2004) Fungal pathogen-induced changes in the antioxidant systems of leaf peroxisomes from infected tomato plants. Planta 222:192–200CrossRefGoogle Scholar
  32. Lazzarotto F, Teixeira FK, Rosa SB, Dunand C, Fernandes CL, et al (2011) Ascorbate peroxidase-related (APx-R) is a new heme-containing protein functionally associated with ascorbate peroxidase but evolutionarily divergent. New Phytologist 191:234–250CrossRefGoogle Scholar
  33. Lehmann S, Serrano M, L’Haridon F, Tjamos SE, Metraux JP (2015) Reactive oxygen species and plant resistance to fungal pathogens. Phytochem 112:54–62CrossRefGoogle Scholar
  34. Liu X, Williams CE, Nemacheck JA, Wang H, Subramanyam S, Zheng C, Chen M-S (2010) Reactive oxygen species are involved in plant defense against a gall midge. Plant Physiol 152:985–999CrossRefGoogle Scholar
  35. Liu SH, Ju JF, Xia GM (2014) Identification of the flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase genes from Antarctic moss and their regulation during abiotic stress. Gene 543:145–152CrossRefGoogle Scholar
  36. 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 25:402–408CrossRefGoogle Scholar
  37. Mai VC, Bednarski W, Borowiak-Sobkowiak B, Wilkaniec B, Samardakiewicz S, Morkunas I (2013) Oxidative stress in pea seedling leaves in response to Acyrthosiphon pisum infestation. Phytochemistry 93:49–62CrossRefGoogle Scholar
  38. Meyer Y, Belin C, Delorme-Hinoux V, Reichheld JP, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160CrossRefGoogle Scholar
  39. Mittler R (2016) ROS are good. Trends Plant Sci 22:11–19CrossRefGoogle Scholar
  40. Moloi MJ, vander Westhuizen A (2006) The reactive oxygen species are involved in resistance responses of wheat to the russian wheat aphid. J Plant Physiol 163:1118–1125CrossRefGoogle Scholar
  41. Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:596–604CrossRefGoogle Scholar
  42. Ozyigit II, Ertugrul F, Recep V, Kurtoglu KY, Ibrahim K et al (2016) Identification and comparative analysis of H2O2-scavenging enzymes (ascorbate peroxidase and glutathione peroxidase) in selected plants employing bioinformatics approaches. Front Plant Sci 7:301.  https://doi.org/10.3389/fpls.2016.00301 CrossRefGoogle Scholar
  43. Petrov VD, VanBreusegem F (2012) Hydrogen peroxide-a central hub for information flow in plant cells. AoB Plants.  https://doi.org/10.1093/aobpla/pls014 Google Scholar
  44. Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ Exp Bot 99:141–149CrossRefGoogle Scholar
  45. Simonovicova M, Tamás L, Huttová J, Mistrík I (2004) Effect of aluminium on oxidative stress related enzymes activities in barley roots. Biol Plant 48:261–266CrossRefGoogle Scholar
  46. Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16CrossRefGoogle Scholar
  47. Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Intl J Mol Sci 16:13561–13578CrossRefGoogle Scholar
  48. Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270CrossRefGoogle Scholar
  49. Thakur M, Sohal BS (2013) Role of elicitors in inducing resistance in plants against pathogen infection: a review. ISRN Biochem 2:1–10CrossRefGoogle Scholar
  50. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J 11:1187–1194CrossRefGoogle Scholar
  51. Vorwerk S, Somerville S, Somerville C (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci 9:203–209CrossRefGoogle Scholar
  52. Wang FM, Zhao SM, Han YH, Shao YT, Dong ZY, Gao Y, Zhang KP, Liu X, Li DW, Chang JH, Wang DW (2013) Efficient and fine mapping of RMES1 conferring resistance to sorghum aphid Melanaphis sacchari. Mol Breed 31:777–784CrossRefGoogle Scholar
  53. Yang Y, Han C, Liu Q, Lin B, Wang J (2008) Effect of drought and low light on growth and enzymatic antioxidant system of Picea asperata seedlings. Acta Physiol Plant 30:433–440CrossRefGoogle Scholar
  54. Zhang CN, Wu JX, Dai W, Chen L (2005) Activities of some isoenzymes in the leaves of Brassica oleracea seedlings infested by peach aphid (Myzus persicae). Acta Bot Boreal-Occident Sin 25:1566–1569Google Scholar

Copyright information

© Botanical Society of Sao Paulo 2019

Authors and Affiliations

  1. 1.School of Life Science and TechnologyInner Mongolia University of Science and TechnologyBaotouPeople’s Republic of China

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