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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Proteomic profiling uncovered the cytosolic superoxide dismutase BsSOD1 associated with plant defence in the herbal orchid Bletilla striata

Bao-Wei Lu A , Feng-Xia An https://orcid.org/0000-0002-7242-7156 A E , Liang-Jing Cao B , Yong-Jian Yang A , Peng-Ming Liu A , Xuan Wang B , Bao-Liang Yang A , Yu-Lei Zhang B C , Yan-Feng Ding D and Jun Liu https://orcid.org/0000-0003-1338-523X B E
+ Author Affiliations
- Author Affiliations

A School of Chinese Medicine, Bozhou University, Bozhou, 236800, China.

B National Key Facility for Crop Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, 100081, China.

C Wanbei Pharmaceutical Co. of Bozhou City Co. Ltd, Bozhou, 236800, China.

D Laha Town Health Center, Qiqihar, 161342, China.

E Corresponding authors. Email: an_fengxia@163.com; liujun@caas.cn

Functional Plant Biology 47(10) 937-944 https://doi.org/10.1071/FP19345
Submitted: 2 December 2019  Accepted: 29 April 2020   Published: 26 June 2020

Abstract

The herbal orchid Bletilla striata (Thunb.) Rchb.f. has a long cultivation history and has been widely used in medicines and cosmetics. The fungal infection leaf blight (LB) seriously threatens B. striata cultivation. Here, we systemically collected wild B. striata accessions and isolated the accessions with strong resistance against LB. We carried out proteomic profiling analysis of LB-resistant and LB-susceptible accessions, and identified a large number of differentially expressed proteins with significant gene ontology enrichment for ‘oxidoreductase activity.’ Of the proteins identified in the reactive oxygen species signalling pathway, the protein abundance of the Cu–Zn superoxide dismutase BsSOD1 and its gene expression level were higher in LB-resistant accessions than in LB-susceptible lines. Transient expression of the dismutase fused with yellow fluorescent protein determined that its subcellular localisation is in the cytoplasm. Our study provides new insights into the molecular markers associated with fungal infection in B. striata.

Additional keywords: disease resistance, leaf blight, protoplast transformation.


References

Bart R, Chern M, Park CJ, Bartley L, Ronald PC (2006) A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods 2, 13
A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts.Crossref | GoogleScholarGoogle Scholar | 16808845PubMed |

Ching SL (2012) Glyoxylate reductase isoform 1 is localized in the cytosol and not peroxisomes in plant cells. Journal of Integrative Plant Biology 54, 152–168.
Glyoxylate reductase isoform 1 is localized in the cytosol and not peroxisomes in plant cells.Crossref | GoogleScholarGoogle Scholar | 22309191PubMed |

Edlich W, Lorenz G, Lyr H, Nega E, Pommer EH (1989) New aspects on the infection mechanism of Botrytis cinerea Pers. Netherlands Journal of Plant Pathology 95, 53–62.
New aspects on the infection mechanism of Botrytis cinerea Pers.Crossref | GoogleScholarGoogle Scholar |

Elad Y (1997) Responses of plants to infection by Botrytis cinerea and novel means involved in reducing their susceptibility to infection. Biological Reviews of the Cambridge Philosophical Society 72, 381–422.
Responses of plants to infection by Botrytis cinerea and novel means involved in reducing their susceptibility to infection.Crossref | GoogleScholarGoogle Scholar |

Gou M, Hua J (2012) Complex regulation of an R gene SNC1 revealed by autoimmune mutants. Plant Signaling & Behavior 7, 213–216.
Complex regulation of an R gene SNC1 revealed by autoimmune mutants.Crossref | GoogleScholarGoogle Scholar |

Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Current Biology 10, 751–757.
The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 10898976PubMed |

Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. The Plant Journal 74, 840–851.
Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23480361PubMed |

Han J, Pan Y, Wang X, Zhang Y, Ma Z (2016) Antisense expression of Gossypium barbadense UGD6 in Arabidopsis thaliana significantly alters cell wall composition. Science China. Life Sciences 59, 213–218.
Antisense expression of Gossypium barbadense UGD6 in Arabidopsis thaliana significantly alters cell wall composition.Crossref | GoogleScholarGoogle Scholar | 26810898PubMed |

Hussain A, Yun BW, Kim JH, Gupta KJ, Hyung NI, Loake GJ (2019) Novel and conserved functions of S-nitrosoglutathione reductase (GSNOR) in tomato. Journal of Experimental Botany 70, 4877–4886.
Novel and conserved functions of S-nitrosoglutathione reductase (GSNOR) in tomato.Crossref | GoogleScholarGoogle Scholar | 31089684PubMed |

Jung WJ, Park RD, Mabood F, Souleimanov A, Smith DL (2011) Effects of Pseudomonas aureofaciens 63–28 on defense responses in soybean plants infected by Rhizoctonia solani. Journal of Microbiology and Biotechnology 21, 379–386.
Effects of Pseudomonas aureofaciens 63–28 on defense responses in soybean plants infected by Rhizoctonia solani.Crossref | GoogleScholarGoogle Scholar | 21532321PubMed |

Kuzniak E, Skłodowska M (2004) The effect of Botrytis cinerea infection on the antioxidant profile of mitochondria from tomato leaves. Journal of Experimental Botany 55, 605–612.
The effect of Botrytis cinerea infection on the antioxidant profile of mitochondria from tomato leaves.Crossref | GoogleScholarGoogle Scholar | 14966215PubMed |

Li Z, Han X, Song X, Zhang Y, Jiang J, Han Q, Liu M, Qiao G, Zhuo R (2017) Overexpressing the Sedum alfredii Cu/Zn superoxide dismutase increased resistance to oxidative stress in transgenic Arabidopsis. Frontiers in Plant Science 8, 1010
Overexpressing the Sedum alfredii Cu/Zn superoxide dismutase increased resistance to oxidative stress in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28659953PubMed |

Li Y, Cao XL, Zhu Y, Yang XM, Zhang KN, Xiao ZY, Wang H, Zhao JH, Zhang LL, Li GB, Zheng YP, Fan J, Wang J, Chen XQ, Wu XJ, Zhao JQ, Dong OX, Chen XW, Chern M, Wang WM (2019) Osa-miR398b boosts H2O2 production and rice blast disease-resistance via multiple superoxide dismutases. New Phytologist 222, 1507–1522.
Osa-miR398b boosts H2O2 production and rice blast disease-resistance via multiple superoxide dismutases.Crossref | GoogleScholarGoogle Scholar | 30632163PubMed |

Lightfoot DJ, McGrann GR, Able AJ (2017) The role of a cytosolic superoxide dismutase in barley–pathogen interactions. Molecular Plant Pathology 18, 323–335.
The role of a cytosolic superoxide dismutase in barley–pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 26992055PubMed |

Lin YF, Chen YY, Hsiao YY, Shen CY, Hsu JL, Yeh CM, Mitsuda N, Ohme-Takagi M, Liu ZJ, Tsai WC (2016) Genome-wide identification and characterization of TCP genes involved in ovule development of Phalaenopsis equestris. Journal of Experimental Botany 67, 5051–5066.
Genome-wide identification and characterization of TCP genes involved in ovule development of Phalaenopsis equestris.Crossref | GoogleScholarGoogle Scholar | 27543606PubMed |

Lisitsa AV, Petushkova NA, Levitsky LI, Zgoda VG, Larina OV, Kisrieva YS, Frankevich VE, Gamidov SI (2019) Comparative analysis of the performance of Mascot and IdentiPy algorithms on a benchmark dataset obtained by tandem mass spectrometry analysis of testicular biopsies. Molecular Biology 53, 147–155.
Comparative analysis of the performance of Mascot and IdentiPy algorithms on a benchmark dataset obtained by tandem mass spectrometry analysis of testicular biopsies.Crossref | GoogleScholarGoogle Scholar |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method. Methods 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT method.Crossref | GoogleScholarGoogle Scholar | 11846609PubMed |

Lu H, Higgins VJ (1999) The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum. Physiological and Molecular Plant Pathology 54, 131–143.
The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum.Crossref | GoogleScholarGoogle Scholar |

McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymatic function for erythrocuprein (hemocuprein). The Journal of Biological Chemistry 244, 6049–6055.

Morita H, Koyama K, Sugimoto Y, Kobayashi Ji (2005) Antimitotic activity and reversal of breast cancer resistance protein-mediated drug resistance by stilbenoids from Bletilla striata. Bioorganic & Medicinal Chemistry Letters 15, 1051–1054.

Ogoshi A (1987) Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kühn. Annual Review of Phytopathology 25, 125–143.
Ecology and pathogenicity of anastomosis and intraspecific groups of Rhizoctonia solani Kühn.Crossref | GoogleScholarGoogle Scholar |

Okubara PA, Dickman MB, Blechl AE (2014) Molecular and genetic aspects of controlling the soilborne necrotrophic pathogens Rhizoctonia and Pythium. Plant Science 228, 61–70.
Molecular and genetic aspects of controlling the soilborne necrotrophic pathogens Rhizoctonia and Pythium.Crossref | GoogleScholarGoogle Scholar | 25438786PubMed |

Paranidharan V, Palaniswami A, Vidhyasekaran P, Velazhahan R (2005) A host-specific toxin of Rhizoctonia solani triggers superoxide dismutase (SOD) activity in rice. Archives of Phytopathology and Plant Protection 38, 151–157.
A host-specific toxin of Rhizoctonia solani triggers superoxide dismutase (SOD) activity in rice.Crossref | GoogleScholarGoogle Scholar |

Peng Q, Li M, Xue F, Liu H (2014) Structure and immunobiological activity of a new polysaccharide from Bletilla striata. Carbohydrate Polymers 107, 119–123.
Structure and immunobiological activity of a new polysaccharide from Bletilla striata.Crossref | GoogleScholarGoogle Scholar | 24702926PubMed |

Qian CD, Jiang F-S, Yu H-S, Shen Y, Fu Y-H, Cheng D-Q, Gan L-S, Ding Z-S (2015) Antibacterial biphenanthrenes from the fibrous roots of Bletilla striata. Journal of Natural Products 78, 939
Antibacterial biphenanthrenes from the fibrous roots of Bletilla striata.Crossref | GoogleScholarGoogle Scholar | 25760525PubMed |

Sayers EW, Cavanaugh M, Clark K, Ostell J, Pruitt KD, Karsch-Mizrachi I (2019) GenBank. Nucleic Acids Research 48, D84–D86.
GenBank.Crossref | GoogleScholarGoogle Scholar |

Smith CM, Clement SL (2012) Molecular bases of plant resistance to arthropods. Annual Review of Entomology 57, 309–328.
Molecular bases of plant resistance to arthropods.Crossref | GoogleScholarGoogle Scholar | 21910639PubMed |

Sunkar R, Kapoor A, Zhu J-K (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. The Plant Cell 18, 2051–2065.
Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance.Crossref | GoogleScholarGoogle Scholar | 16861386PubMed |

Sutherland MW (1991) The generation of oxygen radicals during host plant response to infection. Physiological and Molecular Plant Pathology 39, 79–93.
The generation of oxygen radicals during host plant response to infection.Crossref | GoogleScholarGoogle Scholar |

Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M (2014) Shotgun proteomics of plant plasma membrane and microdomain proteins using nano-LC-MS/MS. Methods in Molecular Biology (Clifton, N.J.) 1072, 481–498.
Shotgun proteomics of plant plasma membrane and microdomain proteins using nano-LC-MS/MS.Crossref | GoogleScholarGoogle Scholar |

Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research 45, W122–W129.
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update.Crossref | GoogleScholarGoogle Scholar | 28472432PubMed |

Tzeng DD, Devay JE (1993) Role of oxygen radicals in plant disease development. Advances in Plant Pathology 10, 1–33.

Vera-Estrella R, Blumwald E, Higgins VJ (1993) Non-specific glycopeptide elicitors of Cladosporium fulvum: evidence for involvement of active oxygen species in elicitor-induced effects on tomato cell suspensions. Physiological and Molecular Plant Pathology 42, 9–22.
Non-specific glycopeptide elicitors of Cladosporium fulvum: evidence for involvement of active oxygen species in elicitor-induced effects on tomato cell suspensions.Crossref | GoogleScholarGoogle Scholar |

Wang M, Zhao X, Xiao Z, Yin X, Xing T, Xia G (2016) A wheat superoxide dismutase gene TaSOD2 enhances salt resistance through modulating redox homeostasis by promoting NADPH oxidase activity. Plant Molecular Biology 91, 115–130.
A wheat superoxide dismutase gene TaSOD2 enhances salt resistance through modulating redox homeostasis by promoting NADPH oxidase activity.Crossref | GoogleScholarGoogle Scholar | 26869262PubMed |

Wu J, Zhu J, Wang L, Wang S (2017) Genome-wide association study identifies NBS-LRR-encoding genes related with anthracnose and common bacterial blight in the common bean. Frontiers in Plant Science 8, 1398
Genome-wide association study identifies NBS-LRR-encoding genes related with anthracnose and common bacterial blight in the common bean.Crossref | GoogleScholarGoogle Scholar | 28848595PubMed |

Xing Y, Cao Q, Zhang Q, Qin L, Jia W, Zhang J (2013) MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis. Plant & Cell Physiology 54, 1217–1227.
MKK5 regulates high light-induced gene expression of Cu/Zn superoxide dismutase 1 and 2 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Xu C, Wang Y, Yu Y, Duan J, Liao Z, Xiong G, Meng X, Liu G, Qian Q, Li J (2012) Degradation of MONOCULM 1 by APC/CTAD1 regulates rice tillering. Nature Communications 3, 750
Degradation of MONOCULM 1 by APC/CTAD1 regulates rice tillering.Crossref | GoogleScholarGoogle Scholar | 22434193PubMed |

Xu D, Chen H, Aci M, Pan Y, Shangguan Y, Ma J, Li L, Qian G, Wang Q (2018) De novo assembly, characterization and development of EST-SSRs from Bletilla striata transcriptomes profiled throughout the whole growing period. PLoS One 13, e0205954
De novo assembly, characterization and development of EST-SSRs from Bletilla striata transcriptomes profiled throughout the whole growing period.Crossref | GoogleScholarGoogle Scholar | 30365506PubMed |