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

Integrated transcriptome and proteome analyses unravel a series of early defence responses in Sarcandra glabra against Colletotrichum gloeosporioides

Ni Jiang A B , Birun Lin A C * , Lisha Song B , Guiyu Tan B , Zhanjiang Zhang B and Kai Yu https://orcid.org/0000-0001-5338-3437 D E *
+ Author Affiliations
- Author Affiliations

A College of Agriculture, Guangxi University, Nanning 530004, China.

B Guangxi Botanical Garden of Medicinal Plants, Nanning 530023, China.

C Guangdong Key Laboratory of High Technology for Plant Protection, Institute of Plant Protection, Guangdong Academy of Agricultural Sciences, Guangzhou 510640, China.

D College of Animal Science and Technology, Guangxi University, Nanning 530004, China.

E Department of Omics Technology, Nanning Current Science Biotechnology Co., Ltd., Nanning 530005, China.

* Correspondence to: linbr@126.com, bioneer@foxmail.com

Handling Editor: Calum Wilson

Functional Plant Biology 50(12) 1047-1061 https://doi.org/10.1071/FP23084
Submitted: 8 April 2023  Accepted: 20 September 2023  Published: 10 October 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Anthracnose caused by Colletotrichum gloeosporioides critically threatens the growth and commercial cultivation of Sarcandra glabra. However, the defence responses and underlying mechanisms remain unclear. Herein, we aimed to investigate the molecular reprogramming in S. glabra leaves infected with C. gloeosporioides. Leaf tissues at 0, 24 and 48 h post-inoculation (hpi) were analysed by combining RNA sequencing and Tandem Mass Tag-based liquid chromatography with tandem mass spectrometry. In total, 18 441 and 25 691 differentially expressed genes were identified at 24 and 48 hpi compared to 0 hpi (uninoculated control), respectively. In addition, 1240 and 1570 differentially abundant proteins were discovered at 24 and 48 hpi compared to 0 hpi, respectively. Correlation analysis revealed that transcription and translation levels were highly consistent regarding repeatability and expression. Analyses using databases KEGG and iPATH revealed tricitric acid cycle, glycolysis/gluconeogenesis and phenylpropanoid biosynthesis were induced, whereas photosynthesis and tryptophan were suppressed. Enzymatic activity assay results were consistent with the upregulation of defence-related enzymes including superoxide dismutases, catalases, peroxidases and chitinases. The transcriptome expression results were additionally validated by quantitative real-time polymerase chain reaction analyses. This study provides insights into the molecular reprogramming in S. glabra leaves during infection, which lay a foundation for investigating the mechanisms of host-Colletotrichum interactions and breeding disease-resistant plants.

Keywords: antioxidant enzyme, Colletotrichum gloeosporioides, correlation analysis, defence mechanism, photosynthesis, proteome, Sarcandra glabra, transcriptome.

References

Adhikari TB, Aryal R, Redpath LE, Van den Broeck L, Ashrafi H, Philbrick AN, Jacobs RL, Sozzani R, Louws FJ (2022) RNA-Seq and gene regulatory network analyses uncover candidate genes in the early defense to two Hemibiotrophic colletorichum spp. in strawberry. Frontiers in Genetics 12, 805771.
| Crossref | Google Scholar | PubMed |

Allan AC, Hellens RP, Laing WA (2008) MYB transcription factors that colour our fruit. Trends in Plant Science 13, 99-102.
| Crossref | Google Scholar | PubMed |

Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant, Cell & Environment 33, 1597-1613.
| Crossref | Google Scholar | PubMed |

Chen F, Fu Q, Pu L, Zhang P, Huang Y, Hou Z, Xu Z, Chen D, Huang F, Deng T, Liang X, Lu Y, Zhang M (2018) Integrated analysis of quantitative proteome and transcriptional profiles reveals the dynamic function of maternally expressed proteins after parthenogenetic activation of buffalo oocyte. Molecular & Cellular Proteomics 17, 1875-1891.
| Crossref | Google Scholar | PubMed |

Chinese Pharmacopoeia Commission (2015) ‘Pharmacopoeia of the People’s Republic of China. Vol. 1.’ (Chemical Industry Press: Beijing, China)

Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676.
| Crossref | Google Scholar | PubMed |

Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology 13, 414-430.
| Crossref | Google Scholar | PubMed |

Ebrahim S, Kalidindi U, Singh B (2011) Pathogenesis related (PR) proteins in plant defense mechanism. In ‘Science against microbial pathogens: communicating current research and technological advances’. (Ed. A Mendez-Vilas) pp. 1043–1054. (Formatex Research Center: Badajoz, Spain)

Fan J, Chen C, Yu Q, Brlansky RH, Li Z-G, Gmitter FG, Jr (2011) Comparative iTRAQ proteome and transcriptome analyses of sweet orange infected by “Candidatus Liberibacter asiaticus”. Physiologia Plantarum 143, 235-245.
| Crossref | Google Scholar | PubMed |

Fang X, Chen W, Xin Y, Zhang H, Yan C, Yu H, Liu H, Xiao W, Wang S, Zheng G, Liu H, Jin L, Ma H, Ruan S (2012) Proteomic analysis of strawberry leaves infected with Colletotrichum fragariae. Journal of Proteomics 75, 4074-4090.
| Crossref | Google Scholar | PubMed |

Fang H, Liu X, Dong Y, Feng S, Zhou R, Wang C, Ma X, Liu J, Yang KQ (2021) Transcriptome and proteome analysis of walnut (Juglans regia L.) fruit in response to infection by Colletotrichum gloeosporioides. BMC Plant Biology 21, 249.
| Crossref | Google Scholar | PubMed |

Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155, 2-18.
| Crossref | Google Scholar | PubMed |

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644-652.
| Crossref | Google Scholar | PubMed |

Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cellular Microbiology 6, 201-211.
| Crossref | Google Scholar | PubMed |

Hu Y, Zhong S, Zhang M, Liang Y, Gong G, Chang X, Tan F, Yang H, Qiu X, Luo L, Luo P (2020) Potential role of photosynthesis in the regulation of reactive oxygen species and defence responses to Blumeria graminis f. sp. tritici in wheat. International Journal of Molecular Sciences 21, 5767.
| Crossref | Google Scholar | PubMed |

Jacob P, Hirt H, Bendahmane A (2017) The heat-shock protein/chaperone network and multiple stress resistance. Plant Biotechnology Journal 15, 405-414.
| Crossref | Google Scholar | PubMed |

Jiang N, Tang MQ, Lan ZZ, Huang YC, Lin Y, Bai LH (2012) Influences of anthracnose on the quality of Sarcandra glabra and pathogen identification. Plant Protection 38, 83-88.
| Google Scholar |

Jiang N, Lin B, Song L, Tan G, Zhang ZJ, Wei SG (2021a) First report of Corynespora cassicola causing black spot on Sarcandra glabra in China. Plant Disease 105(11), 3754.
| Crossref | Google Scholar | PubMed |

Jiang L, Wu P, Yang L, Liu C, Guo P, Wang H, Wang S, Xu F, Zhuang Q, Tong X, Liu P, Luo L (2021b) Transcriptomics and metabolomics reveal the induction of flavonoid biosynthesis pathway in the interaction of Stylosanthes-Colletotrichum gloeosporioides. Genomics 113, 2702-2716.
| Crossref | Google Scholar | PubMed |

Jin L, Guan X, Liu W, Zhang X, Yan W, Yao W, Gao X (2012) Characterization and antioxidant activity of a polysaccharide extracted from Sarcandra glabra. Carbohydrate Polymers 90, 524-532.
| Crossref | Google Scholar | PubMed |

Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proceedings of the National Academy of Sciences of the United States of America 103, 11086-11091.
| Crossref | Google Scholar | PubMed |

Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28, 27-30.
| Crossref | Google Scholar | PubMed |

Ksiazkiewicz M, Rychel-Bielska S, Plewinski P, Bielski W, Nuc M, Kozak B, Krajewski P, Jedryczka M (2022) A successful defense of the narrow-leafed lupin against anthracnose involves quick and orchestrated reprogramming of oxidation–reduction, photosynthesis and pathogenesis-related genes. Scientific Reports 12, 8164.
| Crossref | Google Scholar | PubMed |

Lei L, Hong YY, Nie XY, Xiao SG, Yi TY (2021) First report of Athelia rolfsii causing southern blight on Sarcandra glabra in China. Plant Disease 105, 4152.
| Crossref | Google Scholar | PubMed |

Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323.
| Crossref | Google Scholar | PubMed |

Li H, Wang Z, Sun X, Pan C, Gao X, Liu W (2019a) Chemical and rheological properties of proteoglycans from Sarcandra glabra (Thunb.) Nakai. International Journal of Biological Macromolecules 132, 641-650.
| Crossref | Google Scholar | PubMed |

Li T, Fan P, Yun Z, Jiang G, Zhang Z, Jiang Y (2019b) β-aminobutyric acid priming acquisition and defense response of mango fruit to Colletotrichum gloeosporioides infection based on quantitative proteomics. Cells 8, 1029.
| Crossref | Google Scholar | PubMed |

Li DD, Li LJ, Xiao YF, Wang Q (2022) Research progress in chemical constituents and pharmacological activities of Caoshanhu. Chinese Traditional Patent Medicine 44, 2924-2928.
| Google Scholar |

Liu W, Zheng Y, Zhang Z, Yao W, Gao X (2014) Hypoglycemic, hypolipidemic and antioxidant effects of Sarcandra glabra polysaccharide in type 2 diabetic mice. Food Function 5, 2850-2860.
| Crossref | Google Scholar | PubMed |

Liu J, Li X, Lin J, Li Y, Wang T, Jiang Q, Chen D (2016) Sarcandra glabra (Caoshanhu) protects mesenchymal stem cells from oxidative stress: a bioevaluation and mechanistic chemistry. BMC Complementary and Alternative Medicine 16, 423.
| Crossref | Google Scholar | PubMed |

Liu W, Lu W, Chai Y, Liu Y, Yao W, Gao X (2017) Preliminary structural characterization and hypoglycemic effects of an acidic polysaccharide SERP1 from the residue of Sarcandra glabra. Carbohydrate Polymers 176, 140-151.
| Crossref | Google Scholar | PubMed |

Liu W, Gong X, Luo J, Jiang L, Lu W, Pan C, Yao W, Gao X, Tian H (2021) A purified acidic polysaccharide from Sarcandra glabra as vaccine adjuvant to enhance anti-tumor effect of cancer vaccine. Carbohydrate Polymers 263, 117967.
| Crossref | Google Scholar | PubMed |

Lorenc-Kukula K, Jafra S, Oszmianski J, Szopa J (2005) Ectopic expression of anthocyanin 5-o-glucosyltransferase in potato tuber causes increased resistance to bacteria. Journal of Agricultural and Food Chemistry 53, 272-281.
| Crossref | Google Scholar | PubMed |

Mehmood N, Yuan Y, Ali M, Ali M, Iftikhar J, Cheng C, Lyu M, Wu B (2021) Early transcriptional response of terpenoid metabolism to Colletotrichum gloeosporioides in a resistant wild strawberry Fragaria nilgerrensis. Phytochemistry 181, 112590.
| Crossref | Google Scholar | PubMed |

Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33, 453-467.
| Crossref | Google Scholar | PubMed |

Miranda VdJ, Porto WF, Fernandes GdR, Pogue R, Nolasco DO, Araujo ACG, Cota LV, Freitas CG, Dias SC, Franco OL (2017) Comparative transcriptomic analysis indicates genes associated with local and systemic resistance to Colletotrichum graminicola in maize. Scientific Reports 7, 2483.
| Crossref | Google Scholar | PubMed |

Moura HFN, Vasconcelos IM, Souza CEA, Silva FDA, Moreno FBMB, Lobo MDP, Monteiro-Moreira ACO, Moura AA, Costa JH, Oliveira JTA (2014) Proteomics changes during the incompatible interaction between cowpea and Colletotrichum gloeosporioides (Penz.) Penz and Sacc. Plant Science 217–218, 158-175.
| Crossref | Google Scholar | PubMed |

Pang SH (2008) ‘Applied Yao medicine.’ (Guangxi Technology Press: Nanning, China)

Peng X, Yuan Y, Zhang S, Zhou X (2021) First report of anthracnose on Camellia japonica caused by Colletotrichum siamense in Zhejiang province, China. Plant Disease 106(2), 768.
| Crossref | Google Scholar | PubMed |

Punja ZK, Zhang YY (1993) Plant chitinases and their roles in resistance to fungal diseases. Journal of Nematology 25, 526-540.
| Google Scholar | PubMed |

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101-1108.
| Crossref | Google Scholar | PubMed |

Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012, 1-26.
| Crossref | Google Scholar |

Silva FDA, Vasconcelos IM, Saraiva KDC, Costa JH, Fernandes CF, Oliveira JTA (2019) The expression of the genes involved in redox metabolism and hydrogen peroxide balance is associated with the resistance of cowpea [Vigna unguiculata (L.) Walp.] to the hemibiotrophic fungus Colletotrichum gloeosporioides. Journal of Plant Physiology 233, 73-83.
| Crossref | Google Scholar | PubMed |

Song L, Jiang N, Wei S, Lan Z, Pan L (2020) Isolation, screening, and identification of actinomycetes with antifungal and enzyme activity assays against Colletotrichum dematium of Sarcandra glabra. Mycobiology 48, 37-43.
| Crossref | Google Scholar | PubMed |

Sun X, Zhao Q, Si Y, Li K, Zhu J, Gao X, Liu W (2020) Bioactive structural basis of proteoglycans from Sarcandra glabra based on spectrum-effect relationship. Journal of Ethnopharmacology 259, 112941.
| Crossref | Google Scholar | PubMed |

Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiology 141, 373-378.
| Crossref | Google Scholar | PubMed |

Voll LM, Horst RJ, Voitsik A-M, Zajic D, Samans B, Pons-Kuhnemann J, Doehlemann G, Munch S, Wahl R, Molitor A, Hofmann J, Schmiedl A, Waller F, Deising HB, Kahmann R, Kamper J, Kogel K-H, Sonnewald U (2011) Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming. Frontiers in Plant Science 2, 39.
| Crossref | Google Scholar | PubMed |

Wang F, Zhang F, Chen M, Liu Z, Zhang Z, Fu J, Ma Y (2017) Comparative transcriptomics reveals differential gene expression related to Colletotrichum gloeosporioides resistance in the octoploid strawberry. Frontiers in Plant Science 8, 779.
| Crossref | Google Scholar | PubMed |

Wang J, Li D, Peng Y, Cai M, Liang Z, Yuan Z, Du X, Wang J, Schnable PS, Gu R, Li L (2022) The anthocyanin accumulation related ZmBZ1, facilitates seedling salinity stress tolerance via ROS scavenging. International Journal of Molecular Sciences 23, 16123.
| Crossref | Google Scholar |

Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research 39, W316-W322.
| Crossref | Google Scholar | PubMed |

Yang H, Luo P (2021) Changes in photosynthesis could provide important insight into the interaction between wheat and fungal pathogens. International Journal of Molecular Sciences 22, 8865.
| Crossref | Google Scholar | PubMed |

Zeng Y, Liu J, Zhang Q, Qin X, Li Z, Sun G, Jin S (2021) The traditional uses, phytochemistry and pharmacology of Sarcandra glabra (Thunb.) Nakai, a Chinese herb with potential for development: review. Frontiers in Pharmacology 12, 652926.
| Crossref | Google Scholar | PubMed |

Zhang Z, Liu W, Zheng Y, Jin L, Yao W, Gao X (2014) SGP-2, an acidic polysaccharide from Sarcandra glabra, inhibits proliferation and migration of human osteosarcoma cells. Food Function 5, 167-175.
| Crossref | Google Scholar | PubMed |

Zhang L, Huang X, He C, Zhang Q-Y, Zou X, Duan K, Gao Q (2018) Novel fungal pathogenicity and leaf defense strategies are revealed by simultaneous transcriptome analysis of Colletotrichum fructicola and strawberry infected by this Fungus. Frontiers in Plant Science 9, 434.
| Crossref | Google Scholar | PubMed |

Zhang GJ, Chen XR, Ding HX, Liang S, Li Z (2021) First report of Pestalotiopsis lushanensis causing brown leaf spot on Sarcandra glabra in China. Plant Disease 105(4), 1219.
| Crossref | Google Scholar | PubMed |

Zhou H, Liang J, Lv D, Hu Y, Zhu Y, Si J, Wu S (2013) Characterization of phenolics of Sarcandra glabra by non-targeted high-performance liquid chromatography fingerprinting and following targeted electrospray ionisation tandem mass spectrometry/time-of-flight mass spectrometry analyses. Food Chemistry 138, 2390-2398.
| Crossref | Google Scholar | PubMed |