Skip to main content
SpringerLink
Log in

Cotton Chitinase Gene GhChi6 Improves the Arabidopsis Defense Response to Aphid Attack

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

Abstract

Despite the involvement of many members of the chitinase family in the plant immune system, the exact functions of most chitinases remain poorly understood, especially in plant defense responses to phytophagous insects. Here, the gene GhChi6, which encodes a chitinase protein in Gossypium hirsutum, was shown to be induced by cotton aphid feeding and mechanical wounding. Overexpression of GhChi6 in Arabidopsis plants improved their defense response to aphids. The activities of chitinase and PPO in GhChi6 transgenic Arabidopsis plants were higher than those in wild-type plants. Callose deposition in leaves from GhChi6 transgenic Arabidopsis plants was clearly increased compared with wild-type plants. The levels of AtEDS1, AtPAD4, and AtEDS5 in the SA signaling pathway were higher in GhChi6 transgenic Arabidopsis Line4 than those in wild-type plants, while the expression levels of AtLOX2 in the JA signaling pathway and AtEIN2 in the ethylene signaling pathway were lower in GhChi6 transgenic Arabidopsis Line4 than those in wild-type plants. These results collectively showed that the cotton chitinase gene GhChi6 modulated the plant defense response to aphid attack, which may help guide strategies for improving cotton aphid prevention.

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
Fig. 8

Similar content being viewed by others

Abbreviations

qPCR:

Quantitative real-time polymerase chain reaction

ORF:

Open reading frame

MS:

Murashige and Skoog

PCR:

Polymerase chain reaction

PAL:

Phenylalanine ammonialyase

PPO:

Polyphenol oxidase

SOD:

Superoxide dismutase

SA:

Salicylic acid

JA:

Jasmonic acid

Bt:

Bacillus thuringiensis

References

  • Asrorov AM, Matušíková I, Gálová Z, Gregorová Z, Mészáros P, Dalimova S, Salikhov S (2017) The family of chitinases in cotton G. raimondii. J Microbiol Biotechnol Food Sci 6:1284–1289

    CAS  Google Scholar 

  • Boller T, Gehri A, Mauch F, Vögeli U (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157:22–31

    Article  CAS  PubMed  Google Scholar 

  • Cao B, Bao W, Wuriyanghan H (2017) Silencing of target chitinase genes via oral delivery of dsRNA caused lethal phenotypic effects in Mythimna separata (Lepidoptera: Noctuidae). Appl Biochem Biotech 181:860–866

    Article  CAS  Google Scholar 

  • Chen J, Piao Y, Liu Y, Li X, Piao Z (2018) Genome-wide identification and expression analysis of chitinase gene family in Brassica rapa reveals its role in clubroot resistance. Plant Sci 270:257–267

    Article  CAS  PubMed  Google Scholar 

  • Cheng GW, Breen PJ (1991) Activity of phenylalanine ammonia-lyase (PAL) and concentrations of anthocyanins and phenolics in developing strawberry fruit. J Am Soc Hortic Sci 116:865–869

    Article  CAS  Google Scholar 

  • Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31–40

    Article  CAS  PubMed  Google Scholar 

  • Davis JM, Wu H, Cooke JEK, Reed JM, Luce KS, Michler CH (2002) Pathogen challenge, salicylic acid, and jasmonic acid regulate expression of chitinase gene homologs in pine. Mol Plant-Microbe Interact 15:380–387

    Article  CAS  PubMed  Google Scholar 

  • Du B, Zhang WL, Liu BF, Hu J, Wei Z, Shi ZY, He RF, Zhu LL, Chen RZ, Han B, He GC (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106:22163–22168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giannopolitis CN, Ries S (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 5:309–314

    Article  Google Scholar 

  • Hedrick SA, Bell JN, Boller T, Lamb CJ (1998) Chitinase cDNA cloning and mRNA induction by fungal elicitor, wounding, and infection. Plant Physiol 86:182–186

    Article  Google Scholar 

  • Hermans C, Porco S, Verbruggen N, Bush DR (2010) Chitinase-like protein CTL1 plays a role in altering root system architecture in response to multiple environmental conditions. Plant Physiol 152:904–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Wang J, Du Z, Zhang C, Li L, Xu Z (2013) Enhanced resistance to stripe rust disease in transgenic wheat expressing the rice chitinase gene RC24. Transgenic Res 22:939–947

    Article  CAS  PubMed  Google Scholar 

  • Jannoey P, Channei D (2015) Synthesized nanochitosan induced rice chitinase isozyme expression; application in brown planthopper (BPH) control. NU Int J Sci 12:25–37

    Google Scholar 

  • Kar M, Mishra D (1976) Catalase, peroxidase, and polyphenoloxidase activities during rice leaf senescence. Plant Physiol 57:315–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashyap P, Deswal R (2017) A novel class I Chitinase from Hippophae rhamnoides: indications for participating in ICE-CBF cold stress signaling pathway. Plant Sci 259:62–70

    Article  CAS  PubMed  Google Scholar 

  • Kasprzewska ANNA (2003) Plant chitinases-regulation and function. Cell Mol Biol Lett 8:809–824

    CAS  PubMed  Google Scholar 

  • Kitajima S, Kamei K, Taketani S, Yamaguchi M, Kawai F, Komatsu A, Inukai Y (2010) Two chitinase-like proteins abundantly accumulated in latex of mulberry show insecticidal activity. BMC Biochem 11:1–76

    Article  CAS  Google Scholar 

  • Lawrence SD, Novak NG (2006) Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol Lett 28:593–599

    Article  CAS  PubMed  Google Scholar 

  • Lin W, Anuratha CS, Datta K, Potrykus I, Muthukrishnan S, Datta SK (1995) Genetic engineering of rice for resistance to sheath blight. Nat Biotechnol 13:686–691

    Article  CAS  Google Scholar 

  • Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Mol Plant-Microbe Interact 24:183–193

    Article  CAS  PubMed  Google Scholar 

  • Mahanil S, Attajarusit J, Stout MJ, Thipyapong P (2008) Overexpression of tomato polyphenol oxidase increases resistance to common cutworm. Plant Sci 174:456–466

    Article  CAS  Google Scholar 

  • Martos S, Spanò D, Agustí N, Poschenrieder C, Pintus F, Mole L, Medda R (2017) A chitinase from Euphorbia characias latex is a novel and powerful plant-based pesticide against Drosophila suzukii. Ann Appl Biol 171:252–263

    Article  CAS  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 49:69–76

    Article  CAS  Google Scholar 

  • Mészáros P, Rybanský Ľ, Spieß N, Socha P, Kuna R, Libantová J, MoravčíkováBeáta J, Hauptvogel P, Matušíková I (2014) Plant chitinase responses to different metal-type stresses reveal specificity. Plant Cell Rep 33:1789–1799

    Article  PubMed  CAS  Google Scholar 

  • Moravčíková J, Ujvariová N, Žur I, Gálová Z, Gregorová Z, Zimová M, Eva Boszorádová I, Matušíková MI (2017) Chitinase activities in wheat and its relative species. Agric 63:14–22

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 5:473–497

    Article  Google Scholar 

  • Naessens E, Dubreuil G, Giordanengo P, Baron OL, Minet-Kebdani N, Keller H, Coustau C (2015) A secreted MIF cytokine enables aphid feeding and represses plant immune responses. Curr Biol 25:1898–1903

    Article  CAS  PubMed  Google Scholar 

  • Neuhaus JM, Fritig B, Linthorst HJM, Meins F, Mikkelsen JD, Ryals J (1996) A revised nomenclature for chitinase genes. Plant Mol Biol Rep 14:102–104

    Article  CAS  Google Scholar 

  • Nowak H, Komor E (2010a) How aphids decide what is good for them: experiments to test aphid feeding behaviour on Tanacetum vulgare (L.) using different nitrogen regimes. Oecologia 163:973–984

    Article  PubMed  Google Scholar 

  • Nowak H, Komor E (2010b) How aphids decide what is good for them: experiments to test aphid feeding behaviour on Tanacetum vulgare (L.) using divergent different nitrogen regimes. Oecologia 163:973–984

    Article  PubMed  Google Scholar 

  • Passarinho PA, Van Hengel AJ, Fransz PF, de Vries SC (2001) Expression pattern of the Arabidopsis thaliana AtEP3/AtchitIV endochitinase gene. Planta 212:556–567

    Article  CAS  PubMed  Google Scholar 

  • Pegadaraju V, Knepper C, Reese J (2005) Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem feeding green peach aphid. Plant Physiol 139:1927–1934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Punja ZK, Zhang YY (1993) Plant chitinases and their roles in resistance to fungal diseases. J Nematol 25:526–540

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rajendran L, Ramanathan A, Durairaj C, Samiyappan R (2011) Endophytic Bacillus subtilis enriched with chitin offer induced systemic resistance in cotton against aphid infestation. Arch Phytopathol Plant Prot 14:1375–1389

    Article  CAS  Google Scholar 

  • Rajesh T, Maruthasalam S, Kalpana K, Poovannan K, Kumar KK, Kokiladevi E, Sudhakar D, Samiyappan R, Balasubramanian P (2016) Stability of sheath blight resistance in transgenic ASD16 rice lines expressing a rice chi11 gene encoding chitinase. Biol Plant 60:749–756

    Article  CAS  Google Scholar 

  • Su Y, Xu L, Wang S, Wang Z, Yang Y, Chen Y, Que Y (2015) Identification, phylogeny, and transcript of chitinase family genes in sugarcane. Sci Rep 5:1–1510768

    Google Scholar 

  • Takakura Y, Ito T, Saito H, Inoue T, Komari T, Kuwata S (2000) Flower-predominant expression of a gene encoding a novel class I chitinase in rice (Oryza sativa L.). Plant Mol Biol 42:883–897

    Article  CAS  PubMed  Google Scholar 

  • van der Holst PP, Schlaman HR (2001) Proteins involved in the production and perception of oligosaccharides in relation to plant and animal development. Curr Opin Struc Biol 11:608–616

    Article  Google Scholar 

  • Wang J, Constabel CP (2004) Polyphenol oxidase overexpression in transgenic Populus enhances resistance to herbivory by forest tent caterpillar (Malacosoma disstria). Planta 220:87–96

    Article  CAS  PubMed  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 

  • Xu J, Xu J, Xu X, Tian L, Wang G, Zhang X, Zhang X, Wang X, Guo W (2016) Discovery and identification of candidate genes from the chitinase gene family for Verticillium dahliae resistance in cotton. Sci Rep 6:1–1229022

    Article  CAS  Google Scholar 

  • Zeng XF, Li L, Li JR, Zhao DG (2016) Constitutive expression of McCHIT1–PAT enhances resistance to rice blast and herbicide, but does not affect grain yield in transgenic glutinous rice. Biotechnol Appl Biochem 63:77–85

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Fan J, Sun J, Francis F, Chen J (2016) Salicylic acid confers enhanced resistance to Glomerella leaf spot in apple. Plant Physiol Biochem 106:64–72

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Fan J, Sun J, Francis F, Chen J (2017) Transcriptome analysis of the salivary glands of the grain aphid, Sitobion avenae. Sci Rep 7:1–14

    Article  CAS  Google Scholar 

  • Zhang JM, Ma LF, Li W, Zhang J, Li DD, Li XB (2014) Cotton TCTP1 gene encoding a translationally controlled tumor protein participates in plant response and tolerance to aphids. Plant Cell Tissue Organ 117:145–156

    Article  CAS  Google Scholar 

  • Zhao KJ, Chye ML (1999) Methyl jasmonate induces expression of a novel Brassica juncea chitinase with two chitin-binding domains. Plant Mol Biol 40:1009–1018

    Article  CAS  PubMed  Google Scholar 

  • Züst T, Agrawal AA (2016) Mechanisms and evolution of plant resistance to aphids. Nat Plants 2:1–915206

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 31471783).

Author information

Author notes

  1. Xiao Zhong and Pei Feng contributed equally to this work and should be considered as co-first authors.

Authors and Affiliations

  1. Institute of Entomology, College of Agriculture, Yangtze University, Jingzhou, 434025, China

    Xiao Zhong, Pei Feng, Qiqi Ma, Yi Zhang & Jianmin Zhang

  2. College of Life Sciences, Yangtze University, Jingzhou, 434025, China

    Yazhen Yang

Authors
  1. Xiao Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pei Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qiqi Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yazhen Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianmin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZJM and YYZ conceived and designed the research. ZX, FP, MQQ, YS, and SQ performed the experiments. ZJM, WXP, and YYZ analyzed the data and wrote the manuscript.

Corresponding author

Correspondence to Jianmin Zhang.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights

Our study has no research involved human participants or animals.

Additional information

Publisher’s Note

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

Key message

GhChi6 overexpression in Arabidopsis could improve Arabidopsis defensive response to aphids. The activities of chitinase, polyphenol oxidase, and the callose deposits in Ghchi6 transgenic Arabidopsis were higher than that in wild type. Ghchi6 may modulate plant defensive response to aphids through SA signal pathway.

Electronic Supplementary Material

Table S1

primer sequences (XLS 68 kb)

File S1

Cotton chitinase ESTs (DOC 62 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhong, X., Feng, P., Ma, Q. et al. Cotton Chitinase Gene GhChi6 Improves the Arabidopsis Defense Response to Aphid Attack. Plant Mol Biol Rep 39, 251–261 (2021). https://doi.org/10.1007/s11105-020-01248-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-020-01248-5

Keywords

Search

Navigation