Skip to main content
Log in

Differences in immunity between pathogen-resistant and -susceptible yam cultivars reveal insights into disease prevention underlying ethylene supplementation

  • Original Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Leaf necrosis induced by fungal pathogens is one of the most devastating diseases of yam. The objectives of this study were to examine the production of defensive phytohormones and perform a comparative transcriptome analysis between two yam cultivars with different resistance levels against Botrytis cinerea inoculation. After inoculation with B. cinerea, the endogenous ethylene level was found to have accumulated to a higher level in the MH1 resistant cultivar. Meanwhile, expression profiles identified differential defense regulation of ethylene pathway in MH1 (versus susceptible cv. MH3) in response to B. cinerea. A number of ethylene-synthesis and -responsive genes were expressed at higher levels in MH1 than in MH3 after inoculation. Furthermore, ethylene supplementation in MH3 plants by ethephon spraying indeed enhanced the resistance against B. cinerea and Colletotrichum alatae, and elevated the expression of DaEIN2 and DaERF96. Our work improves understanding of defense mechanism and highlights the function of ethylene potentially utilized for yam protection against diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Similar content being viewed by others

Abbreviations

B. cinerea :

Botrytis cinerea

Chl:

Chlorophyll

EIL:

Ethylene-insensitive 3 like

ERF:

Ethylene-responsive transcription factor

ET:

Ethylene

JA:

Jasmonic acid

MH:

Minghuai

RPKM:

Reads per kilobase per million mapped reads

SA:

Salicylic acid

References

  • Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot 53:2039–2055

    CAS  PubMed  Google Scholar 

  • Amorim A, Lidiane L, da Fonseca dos Santos R, Pacifico Bezerra Neto J, Guida-Santos M, Crovella S, Maria Benko-Iseppon A (2017) Transcription factors involved in plant resistance to pathogens. Curr Protein Pept Sci 18:335–351

    CAS  PubMed  Google Scholar 

  • Broekgaarden C, Caarls L, Vos IA, Pieterse CM, Van Wees SC (2015) Ethylene: traffic controller on hormonal crossroads to defense. Plant Physiol 169:2371–2379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 18:756

    CAS  PubMed  Google Scholar 

  • Catinot J, Huang JB, Huang PY, Tseng MY, Chen YL, Gu SY, Lo WS, Wang LC, Chen YR, Zimmerli L (2015) ETHYLENE RESPONSE FACTOR 96 positively regulates A rabidopsis resistance to necrotrophic pathogens by direct binding to GCC elements of jasmonate- and ethylene-responsive defence genes. Plant Cell Environ 38:2721–2734

    CAS  PubMed  Google Scholar 

  • Chen L, Zhang L, Yu D (2010) Wounding-induced WRKY8 is involved in basal defense in Arabidopsis. MolPlant–Microbe Interact 23:558–565

    CAS  Google Scholar 

  • Chen Z, Lu H-H, Hua S, Lin K-H, Chen N, Zhang Y, Chen S-P (2019) Cloning and overexpression of the ascorbate peroxidase gene from the yam (Dioscorea alata) enhances chilling and flood tolerance in transgenic Arabidopsis. J Plant Res 132:1–10

    Google Scholar 

  • Cole RD, Anderson GL, Williams PL (2004) The nematode Caenorhabditis elegans as a model of organophosphate-induced mammalian neurotoxicity. Toxicol Appl Pharmacol 194:248–256

    CAS  PubMed  Google Scholar 

  • Cooper DC (2012) Mobile image ratiometry for the detection of Botrytis cinerea (Gray Mold). Nat Preced 6989:1

    Google Scholar 

  • Demir S, ÇELİKEL FG (2019) Effects of plant growth regulators on the plant height and quantitative properties of Narcissus tazetta. Turk J Agric For 43(1):105–114

    CAS  Google Scholar 

  • Duan X, Cai C, Yang Y, Chen F, Sang Z, Ma L (2019) Fall ethephon application enhances the freezing tolerance of Magnolia wufengensis during overwintering. Forests 10:868

    Google Scholar 

  • Egesi C, Onyeka T, Asiedu R (2007) Severity of anthracnose and virus diseases of water yam (Dioscorea alata L.) in Nigeria I: effects of yam genotype and date of planting. Crop Prot 26:1259–1265

    Google Scholar 

  • El-Kazzaz M, Sommer N, Kader A (1983) Ethylene effects on in vitro and in vivo growth of certain postharvest fruit-infecting fungi. Phytopathology 73:998–1001

    CAS  Google Scholar 

  • Gao H, Xia X, An L, Xin X, Liang Y (2017) Reversion of hyperhydricity in pink (Dianthus chinensis L.) plantlets by AgNO3 and its associated mechanism during in vitro culture. Plant Sci 254:1–11

    CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    CAS  PubMed  Google Scholar 

  • Hua L, Yong C, Zhanquan Z, Boqiang L, Guozheng Q, Shiping T (2018) Pathogenic mechanisms and control strategies of Botrytis cinerea causing post-harvest decay in fruits and vegetables. Food Qual Saf 2(3):111–119

    CAS  Google Scholar 

  • Huang P-Y, Catinot J, Zimmerli L (2015) Ethylene response factors in Arabidopsis immunity. J Exp Bot 67:1231–1241

    PubMed  Google Scholar 

  • Ijato JY (2019) Fungal pathogens of yam (Dioscorea rotundata Poir) and their bio-control. Life Sci J 16(9):92–94. https://doi.org/10.7537/marslsj160919.11

    Article  Google Scholar 

  • Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol 15:431–437

    CAS  PubMed  Google Scholar 

  • Li T, Zhang J, Tang J, Liu Z, Li Y, Chen J, Zou L (2020a) Combined use of Trichoderma atroviride CCTCCSBW0199 and brassinolide to control Botrytis cinerea infection in tomato. Plant Dis. https://doi.org/10.1094/PDIS-07-19-1568-RE

    Article  PubMed  Google Scholar 

  • Li Z, Liu H, Ding Z, Yan J, Yu H, Pan R, Hu J, Guan Y, Hua J (2020b) Low temperature enhances plant immunity via salicylic acid pathway genes that are repressed by ethylene. Plant Physiol 182:626–639

    CAS  PubMed  Google Scholar 

  • Lin HF, Xiong J, Zhou HM, Chen CM, Lin FZ, Xu XM, Oelmüller R, Xu WF, Yeh K-W (2019) Growth promotion and disease resistance induced in anthurium colonized by the beneficial root endophyte Piriformospora indica. BMC Plant Biol 19(1):40

    PubMed  PubMed Central  Google Scholar 

  • Liu X, Inoue H, Hayashi N, Jiang C-J, Takatsuji H (2016) CC-NBS-LRR-type R proteins for rice blast commonly interact with specific WRKY transcription factors. Plant Mol Biol Rep 34:533–537

    CAS  Google Scholar 

  • Ma J, Lin F, Qin W, Wang P (2004) Differential response of four cyanobacterial and green algal species to triazophos, fentin acetate, and ethephon. Bull Environ Contam Toxicol 73:890–897

    CAS  PubMed  Google Scholar 

  • Massee G (1908) Fungi exotici: VIII. Bull Miscel Inf 216–219

  • Minocha R, Martinez G, Lyons B, Long S (2009) Development of a standardized methodology for quantifying total chlorophyll and carotenoids from foliage of hardwood and conifer tree species. Can J For Res 39:849–861

    CAS  Google Scholar 

  • Mutlu A, Öktem A (2017) Effect of different ethephon doses to plant height, lodging and grain yield of durum wheat (Triticum durum L.). Mediterr Agric Sci 30:53–58

    Google Scholar 

  • Okigbo RN (2003) Mycoflora of tuber surface of white yam (Dioscorea rotundata Poir) and postharvest control of pathogens with Bacillus subtilis. Mycopathologia 156(2):81–85

    PubMed  Google Scholar 

  • Polycarp D, Afoakwa E, Budu A, Otoo E (2012) Characterization of chemical composition and anti-nutritional factors in seven species within the Ghanaian yam (Dioscorea) germplasm. Intern Food Res J19:985–992

    Google Scholar 

  • Popoola AR, Adedibu BO, Ganiyu SA (2013) Rapid assessment of resistance of tissue-cultured water yam (Dioscorea alata) and white guinea yam (Dioscorea rotundata) to anthracnose (Colletotrichum gloeosporioides Penz.). Arch Phytopathol Plant Prot 46:663–669

    CAS  Google Scholar 

  • Saltveit ME (1999) Effect of ethylene on quality of fresh fruits and vegetables. Postha Biol Technol 15:279–292

    CAS  Google Scholar 

  • Shuai Z, Shixiong L, Taixin Y (2013) Co-toxicity and effect of mixtures of difenoconazole and pyraclostrobin against Colletotrichum gloeosporioides on yam. Plant Prot 39::160–163

    Google Scholar 

  • Soares ACF, Sousa CS, Garrido MS, Perez JO, Almeida NS (2006) Soil streptomycetes with in vitro activity against the yam pathogens Curvularia eragrostides and Colletotrichum gloeosporioides. Braz J Microbiol 37(4):456–461

    Google Scholar 

  • Song S, Huang H, Gao H, Wang J, Wu D, Liu X, Yang S, Zhai Q, Li C, Qi T (2014) Interaction between MYC2 and ETHYLENE INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant Cell 26:263–279

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soto-Suárez M, Baldrich P, Weigel D, Rubio-Somoza I, San Segundo B (2017) The Arabidopsis miR396 mediates pathogen-associated molecular pattern-triggered immune responses against fungal pathogens. Sci Rep 7:44898

    PubMed  PubMed Central  Google Scholar 

  • Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathogen 2:e123

    Google Scholar 

  • Wild M, Davière J-M, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24:3307–3319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winch J, Newhook F, Jackson G, Cole J (1984) Studies of Colletotrichum gloeosporioides disease on yam, Dioscorea alata, in Solomon Islands. Plant Pathol 33:467–477

    Google Scholar 

  • Windram O, Madhou P, McHattie S, Hill C, Hickman R, Cooke E, Jenkins DJ, Penfold CA, Baxter L, Breeze E (2012) Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:3530–3557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xing X, Li X, Zhang M (2017) Transcriptome analysis of resistant and susceptible tobacco (Nicotiana tabacum) in response to root-knot nematode Meloidogyne incognita infection. Biochem Biophy Res Commun 482:1114–1121

    CAS  Google Scholar 

  • Yang Y-X, Ahammed J, Wu G, Fan C, Zhou SY Y-H (2015) Crosstalk among jasmonate, salicylate and ethylene signaling pathways in plant disease and immune responses. Curr Protein Pept Sci 16:450–461

    CAS  PubMed  Google Scholar 

  • Yoosukyingsataporn S, Detpiratmongkol S (2019) Effects of ethephon on growth and yield of sweet sorghum (Sorghum bicolor L. Moench) at different growth stages. Iran J Plant Physiol 10(1):2987–2887

    Google Scholar 

  • Zhang X, Zhu Z, An F, Hao D, Li P, Song J, Yi C, Guo H (2014) Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell 26:1105–1117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Wei T, Yin KQ, Chen Z, Gu H, Qu LJ, Qin G (2012) Arabidopsis RAP2. 2 plays an important role in plant resistance to Botrytis cinerea and ethylene responses. New Phytol 195:450–460

    CAS  PubMed  Google Scholar 

  • Zheng H, Dong L, Han X, Jin H, Yin C, Han Y, Li B, Qin H, Zhang J, Shen Q, Zhang K, Wang D (2020) The TuMYB46L-TuACO3 module regulates ethylene biosynthesis in einkorn wheat defense to powdery mildew. New Phytol 225:2526–2541

    CAS  PubMed  Google Scholar 

  • Zhu X, Zhu J-K (2013) Double repression in jasmonate-mediated plant defense. Mol Cell 50:459–460

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Fujian Provincial Department of Science and Technology, China (Grants 2018N0069 and 2019N0045). We really appreciate to Dr. D. Chamberlin for English polishing, Dr. C.P. Cheng for providing B. cinerea, and Y. Cao for providing C. alatae.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by SH, ZC, LL, YZ, JY, and S-PC. The first draft of the manuscript was written by K-HL and S-PC and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Shi-Peng Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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 file1 (PDF 548 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hua, S., Chen, Z., Li, L. et al. Differences in immunity between pathogen-resistant and -susceptible yam cultivars reveal insights into disease prevention underlying ethylene supplementation. J. Plant Biochem. Biotechnol. 30, 254–264 (2021). https://doi.org/10.1007/s13562-020-00582-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-020-00582-9

Keywords

Navigation