Skip to main content

Advertisement

SpringerLink
Log in

Comparative Analysis of the Expression of Resistance-Related Genes Respond to the Diversity Foliar Pathogens of Pseudostellaria heterophylla

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

The foliar disease, which is the primary complex disease of Pseudostellaria heterophylla, can be caused by multiple co-infecting pathogens, resulting in a significant reduction in yield. However, there is a lack of research on the relationship between co-infection of various pathogens and the response of resistance-related genes in P. heterophylla. Through the use of 18S rDNA sequencing and pathogenicity testing, it has been determined that Fusarium oxysporum, Alternaria alternata, Arcopilus aureus, Botrytis cinerea, Nemania diffusa, Whalleya microplaca, and Cladosporium cladosporioides are co-infecting pathogens responsible for foliar diseases in P. heterophylla. Furthermore, the qRT-PCR analysis revealed that F. oxysporum, A. alternata, B. cinerea, A. aureus, N. diffusa, Schizophyllum commune, C. cladosporioides, and Coprinellus xanthothrix upregulated ten, two, three, four, seven, thirteen, five, one, and six resistance-related genes, respectively. These findings suggest that a total of 22 resistance-related genes were implicated in the response to diverse fungi, and the magnitude and frequency of induction of resistance-related genes varied considerably among the different fungi. The aforementioned gene associated with resistance was found to be implicated in the response to multiple fungi, including PhPRP1, PhBDRN15, PhBDRN11, and PhBDRN3, which were found to be involved in the resistance response to nine, five, four, and four fungi, respectively. The findings indicate that the PhPRP1, PhBDRN15, PhBDRN11, and PhBDRN3 genes exhibit a broad-spectrum resistance to various fungi. Furthermore, the avirulence fungi C. xanthothrix, which is known to affect P. heterophylla, was found to prime a wide range of resistance responses in P. heterophylla, thereby enhancing its disease resistance. This study provided insight into the management strategies for foliar diseases of P. heterophylla and new genetic materials for disease-resistant breeding.

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

Similar content being viewed by others

References

  1. Zhao Y-P, Lin S, Chu L, Gao J, Azeem S, Lin W (2016) Insight into structure dynamics of soil microbiota mediated by the richness of replanted Pseudostellaria heterophylla. Sci Rep 6:26175–26183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Pang W, Lin S, Dai Q, Zhang H, Hu J (2011) Antitussive activity of Pseudostellaria heterophylla (Miq.) Pax extracts and improvement in lung function via adjustment of multi-cytokine levels. Molecules 16:3360–3370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Hu DJ, Shakerian F, Zhao J, Li SP (2019) Chemistry, pharmacology and analysis of Pseudostellaria heterophylla: a mini-review. Chin Med 14:21

    Article  PubMed  PubMed Central  Google Scholar 

  4. Wu L, Xiao Z, Li M, Wang J, Yang B, Chen J, Tong Q, Lin WJPD (2019) First report of Sclerotium rolfsii var. delphinii causing Southern Wilt of Pseudostellaria heterophylla in China. Plant Dis 103:1419

    Article  Google Scholar 

  5. Yuan Q-S, Wang X, Wang L, Ou X, Jiang W, Kang C, Guo L, Zhou T (2021) First report of Arcopilus aureus causing leaf black spot disease of Pseudostellaria heterophylla in China. Plant Dis 105:4168

    Article  Google Scholar 

  6. He J, Liang S, Zhang G-J, Zhao Z, Li Z (2021) Pathogen identification and screening of fungicides against Pseudostellaria heterophylla (Miq.) Pax leaf spot. J South Agric 52:2124–2132

    CAS  Google Scholar 

  7. Kuang Y, Wang Z, Abah F, Hu H, Bao J (2020) Long-read genome sequence resource of Ascochyta versabilis causing leaf spot disease in Pseudostellaria heterophylla. Mol Plant-Microbe Interactions 33:1438

    Article  CAS  Google Scholar 

  8. Pinto PM, Ricardo CP (1995) Lupinus albus L. pathogenesis-related proteins that show similarity to PR-10 proteins. Plant Physiol 109:1345–1351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Tellis M, Mathur M, Gurjar G, Kadoo N, Gupta V (2017) Identification and functionality prediction of pathogenesis-related protein 1 from legume family. Proteins 85:2066–2080

    Article  CAS  PubMed  Google Scholar 

  10. Boccardo NA, Segretin ME, Hernandez I, Mirkin FG, Chacón O, Lopez Y, Borrás-Hidalgo O, Bravo-Almonacid FF (2019) Expression of pathogenesis-related proteins in transplastomic tobacco plants confers resistance to filamentous pathogens under field trials. Sci Rep 9:2791

    Article  PubMed  PubMed Central  Google Scholar 

  11. Caruso C, Caporale C, Chilosi G, Vacca F, Bertini L, Magro P, Poerio E, Buonocore V (1996) Structural and antifungal properties of a pathogenesis-related protein from wheat kernel. J Protein Chem 15:35–44

    Article  CAS  PubMed  Google Scholar 

  12. Steiner B, Schieszl K, Litwicka E, Kurz H, Lemmens M, Jia H, Muehlbauer G, Buerstmayr HJT, Genetics A (2008) Differential gene expression of related wheat lines with contrasting levels of head blight resistance after Fusarium graminearum inoculation. Theor Appl Genet 36:267–269

    CAS  Google Scholar 

  13. Hou M, Xu W, Hui B, Liu Y, Li L, Liu L, Liu B, Liu GJPCR (2012) Characteristic expression of rice pathogenesis-related proteins in rice leaves during interactions with Xanthomonas oryzae pv. oryzae. Plant Cell Rep 31:895–904

    Article  CAS  PubMed  Google Scholar 

  14. Larran S, Perelló A, Simón MR, Moreno V (2002) Isolation and analysis of endophytic microorganisms in wheat (Triticum aestivum L.) leaves. World J Microbiol Biotechnol 18:683–686

    Article  CAS  Google Scholar 

  15. Gong A, Zhou T, Xiao C, Jiang W, Zhou Y, Zhang J, Liang Q, Yang C, Zheng W, Zhang C (2019) Association between dipsacus saponin VI level and diversity of endophytic fungi in roots of Dipsacus asperoides. World J Microbiol Biotechnol 35:1–4. https://doi.org/10.1007/s11274-019-2616-y

    Article  CAS  Google Scholar 

  16. Deepika YS, Mahadevakumar S, Amruthesh KN, Lakshmidevi N (2020) A new collar rot disease of cowpea (Vigna unguiculata) caused by Aplosporella hesperidica in India. Lett Appl Microbiol 71:154–163

    Article  CAS  PubMed  Google Scholar 

  17. Cooke BM, Jones DG, Kaye B (2006) Disease assessment and yield loss. Springer, Amsterdam

    Book  Google Scholar 

  18. Ogata-Gutiérrez K, Chumpitaz-Segovia C, Lirio-Paredes J, Finetti-Sialer MM, Zúñiga-Dávila D (2017) Characterization and potential of plant growth promoting rhizobacteria isolated from native Andean crops. World J Microbiol Biotechnol 33:203

    Article  PubMed  Google Scholar 

  19. Omar NH, Mohd M, Mohamed Nor NMI, Zakaria L (2018) Characterization and pathogenicity of Fusarium species associated with leaf spot of mango (Mangifera indica L.). Microb Pathog 114:362–368

    Article  PubMed  Google Scholar 

  20. Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  21. Abbas MF, Rafiq M, Al-Sadi AM, Alfarraj S, Alharbi SA, Arif M, Ansari MJ (2021) Molecular characterization of leaf spot caused by Alternaria alternata on buttonwood (Conocarpus erectus L.) and determination of pathogenicity by a novel disease rating scale. PLoS ONE 16:e0251471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Riquelme D, Aravena Z, Valdés-Gómez H, Latorre BA, Díaz GA, Zoffoli JP (2021) Characterization of Botrytis cinerea and B. prunorum from healthy floral structures and decayed “hayward” kiwifruit during post-harvest storage. Plant Dis 105:2129–2140

    Article  CAS  PubMed  Google Scholar 

  23. Nam MH, Park MS, Kim HS, Kim TI, Kim HG (2015) Cladosporium cladosporioides and C. tenuissimum cause blossom blight in strawberry in Korea. Mycobiology 43:354–359

    Article  PubMed  PubMed Central  Google Scholar 

  24. Rahman MZ, Ahmad K, Siddiqui Y, Saad N, Hun TG, Mohd Hata E, Rashed O, Hossain MI, Kutawa AB (2021) First report of Fusarium wilt disease on watermelon caused by Fusarium oxysporum f. sp. niveum (FON) in Malaysia. Plant Dis 105(12):4169

    Article  Google Scholar 

  25. Badalyan SM (2018) Morphological characteristics of monokaryotic and dikaryotic collections of three medicinal Coprinellus species (Agaricomycetes). Int J Med Mushrooms 20:665–676

    Article  PubMed  Google Scholar 

  26. Pi YH, Long SH, Wu YP, Liu LL, Lin Y, Long Q, Kang JC, Kang YQ, Chang CR, Shen XC, Wijayawardene NN, Zhang X, Li QR (2021) A taxonomic study of Nemania from China, with six new species. MycoKeys 83:39–67

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kamei K, Unno H, Ito J, Nishimura K, Miyaji M (1999) Analysis of the cases in which Schizophyllum commune was isolated. Nihon Ishinkin Gakkai zasshi = Jpn J Med Mycol 40:175–181

    Article  CAS  Google Scholar 

  28. He X (2013) Atlas of edible and medicinal fungi in Sichuan basin. Science Press of China, Beijing

    Google Scholar 

  29. Din HM, Rashed O, Ahmad K (2020) Prevalence of fusarium wilt disease of cucumber (Cucumis sativus Linn) in Peninsular Malaysia caused by Fusarium oxysporum and F. solani. Trop Life Sci Res 31:29–45

    Article  PubMed  PubMed Central  Google Scholar 

  30. Kuruppu PU (1999) First report of Fusarium oxysporum causing a leaf twisting disease on Allium cepa var. ascalonicum in Sri Lanka. Plant Dis 83:695

    Article  CAS  PubMed  Google Scholar 

  31. Praveen B, Nagaraja A, Kumar MKP, Pramesh D, Buella PP (2020) First report of Alternaria alternata causing leaf blight on little millet (Panicum sumatrense) in India. Plant Dis 105:1202

    Article  Google Scholar 

  32. Shafique MS, Amrao L, Saeed S, Ahmed MZ, Abdullah A (2020) Occurrence of leaf spot caused by alternaria alternata on eggplant (Solanum melongena) in Pakistan. Plant Dis 105:1224

    Article  Google Scholar 

  33. Ahmadu T, Ahmad K, Ismail SI, Rashed O, Asib N, Omar D (2021) Antifungal efficacy of Moringa oleifera leaf and seed extracts against Botrytis cinerea causing gray mold disease of tomato (Solanum lycopersicum L.). Braz J Biol 81:1007–1022

    Article  CAS  PubMed  Google Scholar 

  34. Zhou Y, Tang Q, Wu M, Mou D, Liu H, Wang S, Zhang C, Ding L, Luo J (2018) Comparative transcriptomics provides novel insights into the mechanisms of selenium tolerance in the hyperaccumulator plant Cardamine hupingshanensis. Sci Rep 8:2789

    Article  PubMed  PubMed Central  Google Scholar 

  35. Dai YC (2005) First report of sapwood rot of peach caused by Schizophyllum commune in China. Plant Dis 89:778–778

    Article  CAS  PubMed  Google Scholar 

  36. Mukhtar I, Ashraf HJ, Khokhar I, Huang Q, Chen B, Xie B (2020) First report of cladosporium blossom blight caused by Cladosporium cladosporioides on Calliandra haematocephala in China. Plant Dis 105:1570

    Article  Google Scholar 

  37. Kumarihamy M, Ferreira D, Croom EM Jr, Sahu R, Tekwani BL, Duke SO, Khan S, Techen N, Nanayakkara NPD (2019) Antiplasmodial and cytotoxic cytochalasins from an endophytic fungus, Nemania sp. UM10M, isolated from a diseased Torreya taxifolia leaf. Molecules (Basel, Switzerland) 24:777

    Article  PubMed  Google Scholar 

  38. Mahmood T, Hein GL, Jensen SG (1998) Mixed infection of hard red winter wheat with high plains virus and wheat streak mosaic virus from wheat curl mites in Nebraska. Plant Dis 82:311–315

    Article  CAS  PubMed  Google Scholar 

  39. Marchetto KM, Power AG (2018) Coinfection timing drives host population dynamics through changes in virulence. Am Nat 191:173–183

    Article  PubMed  Google Scholar 

  40. Rottstock T, Joshi J, Kummer V, Fischer M (2014) Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95:1907–1917

    Article  PubMed  Google Scholar 

  41. Syller J (2012) Facilitative and antagonistic interactions between plant viruses in mixed infections. Mol Plant Pathol 13:204–216

    Article  PubMed  Google Scholar 

  42. Barrett LG, Zala M, Mikaberidze A, Alassimone J, Ahmad M, McDonald BA, Sánchez-Vallet A (2021) Mixed infections alter transmission potential in a fungal plant pathogen. Environ Microbiol 23:2315–2330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Liu J, Liu X, Dai L, Wang G (2007) Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J Genetics Genomics 34:765–776

    Article  Google Scholar 

  44. Kesarwani M, Yoo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144:336–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Li S, Lin D, Zhang Y, Deng M, Chen Y, Lv B, Li B, Lei Y, Wang Y, Zhao L, Liang Y, Liu J, Chen K, Liu Z, Xiao J, Qiu JL, Gao C (2022) Genome-edited powdery mildew resistance in wheat without growth penalties. Nature 602:455–460

    Article  CAS  PubMed  Google Scholar 

  46. Cai L, Zhang W, Jia H, Feng H, Wei X, Chen H, Wang D, Xue Y, Sun X (2020) Plant-derived compounds: a potential source of drugs against tobacco mosaic virus. Pestic Biochem Physiol 169:104589

    Article  CAS  PubMed  Google Scholar 

  47. Wang J, Wang HY, Xia XM, Li PP, Wang KY (2013) Inhibitory effect of sulfated lentinan and lentinan against tobacco mosaic virus (TMV) in tobacco seedlings. Int J Biol Macromol 61:264–269

    Article  CAS  PubMed  Google Scholar 

  48. Zhang Z, Wang H, Wang K, Jiang L, Wang D (2017) Use of lentinan to control sharp eyespot of wheat, and the mechanism involved. J Agric Food Chem 65:10891–10898

    Article  CAS  PubMed  Google Scholar 

  49. De Vega D, Holden N, Hedley PE, Morris J, Luna E, Newton A (2021) Chitosan primes plant defence mechanisms against Botrytis cinerea, including expression of Avr9/Cf-9 rapidly elicited genes. Plant Cell Environ 44:290–303

    Article  PubMed  Google Scholar 

  50. El Hadrami A, Adam LR, El Hadrami I, Daayf F (2010) Chitosan in plant protection. Mar Drugs 8:968–987

    Article  PubMed  PubMed Central  Google Scholar 

  51. Lopez-Moya F, Martin-Urdiroz M, Oses-Ruiz M, Were VM, Fricker MD, Littlejohn G, Lopez-Llorca LV, Talbot NJ (2021) Chitosan inhibits septin-mediated plant infection by the rice blast fungus Magnaporthe oryzae in a protein kinase C and Nox1 NADPH oxidase-dependent manner. New Phytol 230:1578–1593

    Article  CAS  PubMed  Google Scholar 

  52. Suarez-Fernandez M, Marhuenda-Egea FC, Lopez-Moya F, Arnao MB, Cabrera-Escribano F, Nueda MJ, Gunsé B, Lopez-Llorca LV (2020) Chitosan induces plant hormones and defenses in tomato root exudates. Front Plant Sci 11:572087

    Article  PubMed  PubMed Central  Google Scholar 

  53. García YH, Zamora OR, Troncoso-Rojas R, Tiznado-Hernández ME, Báez-Flores ME, Carvajal-Millan E, Rascón-Chu A (2021) Toward understanding the molecular recognition of fungal chitin and activation of the plant defense mechanism in horticultural crops. Molecules 26:6513

    Article  PubMed  PubMed Central  Google Scholar 

  54. Gong BQ, Wang FZ, Li JF (2020) Hide-and-seek: chitin-triggered plant immunity and fungal counterstrategies. Trends Plant Sci 25:805–816

    Article  CAS  PubMed  Google Scholar 

  55. Parada RY, Egusa M, Aklog YF, Miura C, Ifuku S, Kaminaka H (2018) Optimization of nanofibrillation degree of chitin for induction of plant disease resistance: elicitor activity and systemic resistance induced by chitin nanofiber in cabbage and strawberry. Int J Biol Macromol 118:2185–2192

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Ability Establishment of Sustainable Use for Valuable Chinese Medicine Resources [Grant Number 2060302], the National Technical System of Traditional Chinese Medicine Industry [grant number CARS-21], Guizhou Provincial Program on Commercialization of Scientific and Technological Archievements [Qian Ke He Cheng Guo (2021) Yi Ban 136], the High-level Innovative Talents of Guizhou Province of China [Qian Ke He Platform and Talent (2018)5638-2], Innovation Group Major Research Projects [Qian Jiao He KY Zi (2018)022], Guizhou Provincial Major Scientific and Technological Program [Qian Ke He Zhi Cheng (2022) Yi Ban 136], Guizhou Provincial Basic Research Program (Natural Science) [Qian Ke He Ji Chu -ZK (2023) Yi Ban 415], Scientific and technological innovation project of China Academy of Chinese Medical Sciences (CI2021B013), Young Scientific and technological Talents Development Project of Education Department of Guizhou Province [Qian Jiao He KY Zi (2022)265], and Guizhou Postgraduate Research Fund [Qian Jiao He YJSCXJH(2020)159]. We thank Guizhou Jincaohai Medicinal Materials Development Co., LTD for providing help with sampling.

Author information

Author notes

  1. Xiao-Ai Wang and Yanping Gao have equal work in this paper.

Authors and Affiliations

  1. Resource Institute for Chinese & Ethnic Materia Medica, Guizhou University of Traditional Chinese Medicine, Guiyang, 550025, China

    Xiao-Ai Wang, Yanping Gao, Weike Jiang, Lu Wang, Hui Wang, Xiaohong Ou, Yang Yang, Honglin Wu, Tao Zhou & Qing-Song Yuan

  2. National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, Beijing, 100700, China

    Lanping Guo & Qing-Song Yuan

Authors
  1. Xiao-Ai Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yanping Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weike Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaohong Ou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Honglin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lanping Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Tao Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Qing-Song Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

QSY, XAW, TZ, LPG, and WKJ designed the research and wrote the manuscript. XAW, LW, HW, and HLW performed the experiments. YPG, QSY, YY, and XHO analyzed the data. All the authors participated in the discussion and approved the manuscript as submitted.

Corresponding authors

Correspondence to Tao Zhou or Qing-Song Yuan.

Ethics declarations

Competing Interests

The authors declare that they have no known competing financial interests.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 35 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, XA., Gao, Y., Jiang, W. et al. Comparative Analysis of the Expression of Resistance-Related Genes Respond to the Diversity Foliar Pathogens of Pseudostellaria heterophylla. Curr Microbiol 80, 298 (2023). https://doi.org/10.1007/s00284-023-03410-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03410-0

Search

Navigation