Phanerochaete chrysosporium strain B-22, a nematophagous fungus parasitizing Meloidogyne incognita
Autoři:
Bin Du aff001; Yumei Xu aff001; Hailong Dong aff001; Yan Li aff002; Jianming Wang aff001
Působiště autorů:
College of Agriculture, Shanxi Agricultural University, Taigu, Shanxi, China
aff001; Department of Horticulture, Taiyuan University, Taiyuan, Shanxi, China
aff002
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0216688
Souhrn
The root-knot nematode Meloidogyne incognita has a wide host range and it is one of the most economically important crop parasites worldwide. Biological control has been a good approach for reducing M. incognita infection, for which many nematophagous fungi are reportedly applicable. However, the controlling effects of Phanerochaete chrysosporium strain B-22 are still unclear. In the present study we characterized the parasitism of this strain on M. incognita eggs, second-stage juveniles (J2), and adult females. The highest corrected mortality was 71.9% at 3 × 108 colony forming units (CFU) mL-1 and the estimated median lethal concentration of the fungus was 0.96 × 108 CFU mL-1. Two days after treatment with Phanerochaete chrysosporium strain B-22 eggshells were dissolved. A strong lethal effect was noted against J2, as the fungal spores developed in their body walls, germinated, and the resulting hyphae crossed the juvenile cuticle to dissolve it, thereby causing shrinkage and deformation of the juvenile body wall. The spores and hyphae also attacked adult females, causing the shrinkage and dissolution of their bodies and leakage of contents after five days. Greenhouse experiments revealed that different concentrations of the fungal spores effectively controlled M. incognita. In the roots, the highest inhibition rate for adult females, juveniles, egg mass, and gall index was 84.61%, 78.91%, 84.25%, and 79.48%, respectively. The highest juvenile inhibition rate was 89.18% in the soil. Phanerochaete chrysosporium strain B-22 also improved tomato plant growth, therefore being safe for tomato plants while effectively parasitizing M. incognita. This strain is thus a promising biocontrol agent against M. incognita.
Klíčová slova:
Death rates – Fungal spores – Fungi – Nematode infections – Parasitic diseases – Parasitism – Plant growth and development – Tomatoes
Zdroje
1. Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature biotechnology. 2008;26(8):909–15. doi: 10.1038/nbt.1482 18660804.
2. Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, et al. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular plant pathology. 2013;14(9):946–61. doi: 10.1111/mpp.12057 23809086.
3. Ding X, Shields J, Allen R, Hussey RS. Molecular cloning and characterisation of a venom allergen AG5-like cDNA from Meloidogyne incognita. International Journal for Parasitology. 2000;30(1):77–81. doi: 10.1016/s0020-7519(99)00165-4 10675748
4. Aocheng C, Meixia G, Dongdong Y, Liangang M, Qiuxia W, Yuan L, et al. Evaluation of sulfuryl fluoride as a soil fumigant in China. Pest Management Science. 2014;70(2):219–27. doi: 10.1002/ps.3535 23512505
5. Trudgill Blok. Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathologia Mediterranea. 2001:39: 53–77. doi: 10.1371/journal.pone.0050875.g001
6. Sasser, Eisenback, Carter, Triantaphyllou. The international Meloidogyne project—its goals and accomplishments. Annu Rev Phytopathol 1983: 21: 271–88. doi: 10.1146/annurev.py.21.090183.001415
7. Huang WK, Sun JH, Cui JK, Wang GF, Kong LA, Peng H, et al. Efficacy evaluation of fungus Syncephalastrum racemosum and nematicide avermectin against the root-knot nematode Meloidogyne incognita on cucumber. Plos One. 2014;9(2):e89717. doi: 10.1371/journal.pone.0089717 24586982
8. Abo-Korah MS. Biological Control of Root-Knot Nematode, Meloidogyne javanica Infecting Ground Cherry, Using Two Nematophagous and Mychorrhizal Fungi. Egyptian Journal of Biological Pest Control. 2017;27(1), 2017, 111–115.
9. Marin MV, Santos LS, Gaion LA, Rabelo HO, Franco CA, Diniz GMM, et al. Selection of resistant rootstocks to Meloidogyne enterolobii and M. incognita for okra (Abelmoschus esculentus L. Moench). Chilean journal of agricultural research. 2017;77(1):57–64. doi: 10.4067/s0718-58392017000100007
10. Mantelin S, Bellafiore S, Kyndt T. Meloidogyne graminicola: a major threat to rice agriculture. Mol Plant Pathol. 2017;18(1):3–15. doi: 10.1111/mpp.12394 26950515.
11. Chen J, Abawi GS, Zuckerman BM. Suppression of Meloidogyne hapla and Its Damage to Lettuce Grown in a Mineral Soil Amended with Chitin and Biocontrol Organisms. Journal of Nematology. 1999;31(4S):719–25. 19270942
12. Ismail AE. Growing Jatropha Curcas and Jatropha Gossypiifolia as a Interculture with Sunflower for Control of Meloidogyne Javanica in Egypt. International Journal of Sustainable Agricultural Research. 2014;1(2):39–44.
13. Okada H, Araki M, Tsukiboshi T, Harada H. Characteristics of Tylencholaimus parvus (Nematoda:Dorylaimida) as a fungivorus nematode. Nematology. 2005;7(6):843–9. doi: 10.1163/156854105776186424
14. Verdejo-Lucas S, Ornat C, Sorribas FJ, Stchiegel A. Species of Root-knot Nematodes and Fungal Egg Parasites Recovered from Vegetables in Almería and Barcelona, Spain. Journal of Nematology. 2002;34(4):405–8. 19265964
15. Ashraf MS, Khan TA. Effect of opportunistic fungi on the life cycle of the root-knot nematode (Meloidogyne javanica) on brinjal. Archives of Phytopathology and Plant Protection. 2005;38(3):227–33. doi: 10.1080/03235400500094498
16. Trifonova Z, Karadjova J, Georgieva T. Fungal parasites of the root-knot nematodes Meloidogyne spp. in southern Bulgaria. Estonian Journal of Ecology. 2009;58(1):47–52. doi: 10.3176/eco.2009.1.05
17. Siddiqui ZA, Akhtar MS. Effects of antagonistic fungi, plant growth-promoting rhizobacteria, and arbuscular mycorrhizal fungi alone and in combination on the reproduction of Meloidogyne incognita and growth of tomato. Journal of General Plant Pathology. 2009;75(2):144. doi: 10.1007/s10327-009-0154-4
18. Goswami J, Pandey RK, Tewari JP, Goswami BK. Management of root knot nematode on tomato through application of fungal antagonists, Acremonium strictum and Trichoderma harzianum. Journal of Environmental Science & Health Part B. 2008;43(3):237–40. doi: 10.1080/03601230701771164 18368544
19. Vianene NM, Abawi GS. Hirsutella rhossiliensisand Verticillium chlamydosporium as Biocontrol Agents of the Root-knot Nematode Meloidogyne hapla on Lettuce. Journal of Nematology. 2000;32(1):85. 19270953
20. Anastasiadis IA, Giannakou IO, Prophetou-Athanasiadou DA, Gowen SR. The combined effect of the application of a biocontrol agent Paecilomyces lilacinus, with various practices for the control of root-knot nematodes. Crop Protection. 2008;27(3):352–61. doi: 10.1016/j.cropro.2007.06.008
21. Li J, Zou C, Xu J, Ji X, Niu X, Yang J, et al. Molecular Mechanisms of Nematode-Nematophagous Microbe Interactions: Basis for Biological Control of Plant-Parasitic Nematodes. Annual Review of Phytopathology. 2015;53(1):67–95. doi: 10.1146/annurev-phyto-080614-120336 25938277
22. Zeng G-M, Chen A-W, Chen G-Q, Hu X-J, Guan S, Shang C, et al. Responses of Phanerochaete chrysosporium to Toxic Pollutants: Physiological Flux, Oxidative Stress, and Detoxification. Environmental Science & Technology. 2012;46(14):7818–25. doi: 10.1021/es301006j 22703191
23. Zeng G-M, Huang D, Huang G, Hu T, Jiang X, Feng C, et al. Composting of lead-contaminated solid waste with inocula of white-rot fungus. Bioresource Technology. 2007;98(2):320–6. doi: 10.1016/j.biortech.2006.01.001 16495049
24. Ray A, Ayoubi-Canaan P, Hartson SD, Prade R, Mort AJ. Phanerochaete chrysosporium produces a diverse array of extracellular enzymes when grown on sorghum. Applied Microbiology and Biotechnology. 2012;93(5):2075–89. doi: 10.1007/s00253-012-3907-5 22290653
25. Kersten P, Cullen D. Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal genetics and biology: FG & B. 2007;44(2):77–87. doi: 10.1016/j.fgb.2006.07.007 16971147.
26. Xu SX, Zhang SM, You XY, Jia XC, Wu K. Degradation of soil phenolic acids by Phanerochaete chrysosporium under continuous cropping of cucumber. Ying Yong Sheng Tai Xue Bao. 2008;19(11):2480–4. 19238850
27. Li P, Chen J, Li Y, Zhang K, Wang H. Possible mechanisms of control of Fusarium wilt of cut chrysanthemum by Phanerochaete chrysosporium in continuous cropping fields: A case study. Scientific reports. 2017;7(1):15994. doi: 10.1038/s41598-017-16125-7 29167484; PubMed Central PMCID: PMC5700048.
28. Barron GL, Thorn RG. Destruction of nematodes by species of Pleurotus. Canadian Journal of Botany. 1987; 65:774–8. doi: 10.1139/b87-103
29. Satou T, Kaneko K, Li W, Koike K. The toxin produced by pleurotus ostreatus reduces the head size of nematodes. Biological & pharmaceutical bulletin. 2008;31(4):574–6. doi: 10.1248/bpb.31.574 18379043.
30. Iijima N, Yoshino H, Ten LC, Ando A, Watanabe K, Nagata Y. Two genes encoding fruit body lectins of Pleurotus cornucopiae: sequence similarity with the lectin of a nematode-trapping fungus. Bioscience, biotechnology, and biochemistry. 2002;66(10):2083–9. doi: 10.1271/bbb.66.2083 12450118.
31. Eisenback JD. Detailed morphology and anatomy of second-stage juveniles, males, and females of the genus Meloidogyne (root-knot nematodes). In: Sasser JN, Carter CC, editors. An advanced treatise on meloidogyne. vol. 1: Biology and control. Raleigh, NC: North Carolina State University Graphics. 95–112.1985.
32. Hussey RS, Barker KR. A comparison of methods of collecting inocula of Meloidogyne species, including a new technique. Plant Dis Report. 1973; 57:1025–8.
33. Burdsall HH, JR., ESLYN WE. A new Phanerochochaete with a Chrysosporium imperfect state. Mycotaxon. 1974;1(2):123–33.
34. Mittal N, Saxena G, Mukerji KG. Integrated control of root-knot disease in three crop plants using chitin and Paecilomyces lilacinus. Crop Protection. 1995;14(8):647–51.
35. Zhang SW, Liu J, Xu BL, Gu LJ, Xue YY. Parasitic and lethal effects of Trichoderma longibrachiatum on Heterodera avenae: microscopic observation and bioassay. Ying Yong Sheng Tai Xue Bao. 2013;24(10):2955–60. 24483093.
36. Schwartz HT. A protocol describing pharynx counts and a review of other assays of apoptotic cell death in the nematode worm Caenorhabditis elegans. Nature protocols. 2007;2(3):705–14. doi: 10.1038/nprot.2007.93 17406633.
37. Dong H, Zhou X-G, Wang J, Xu Y, Lu P. Myrothecium verrucaria strain X-16, a novel parasitic fungus to Meloidogyne hapla. Biological Control. 2015;83:7–12. doi: 10.1016/j.biocontrol.2014.12.016
38. Yan XN, Sikora RA, Zheng JW. Potential use of cucumber (Cucumis sativus L.) endophytic fungi as seed treatment agents against root-knot nematode Meloidogyne incognita. Journal of Zhejiang University Science B. 2011;12(3):219–25. doi: 10.1631/jzus.B1000165 21370507; PubMed Central PMCID: PMC3048937.
39. Castillo, Nico, Azcón-Aguilar. Protection of olive planting stocks against parasitism of root-knot nematodes by arbuscular mycorrhizal fungi. Plant Pathology. 2006;55: 705–13. doi: 10.1111/j.1365-3059.2006.01400.x
40. Sharon E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels GJ, et al. Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. European Journal of Plant Pathology. 2007;118(3):247–58. doi: 10.1007/s10658-007-9140-x
41. Bird DM, Kaloshian I. Are roots special? Nematodes have their say. Physiological and Molecular Plant Pathology. 2003;62(2):115–23. doi: 10.1016/s0885-5765(03)00045-6
42. Affokpon A, Coyne DL, Htay CC, Agbèdè RD, Lawouin L, Coosemans J. Biocontrol potential of native Trichoderma isolates against root-knot nematodes in West African vegetable production systems. Soil Biology and Biochemistry. 2011;43(3):600–8. doi: 10.1016/j.soilbio.2010.11.029
43. Thorn RG, Barron GL. Carnivorous mushrooms. Science. 1984;224:76–8. doi: 10.1126/science.224.4644.76 17783527
44. Tan Q, Chen G, Zeng G, Chen A, Guan S, Li Z, et al. Physiological fluxes and antioxidative enzymes activities of immobilized Phanerochaete chrysosporium loaded with TiO2 nanoparticles after exposure to toxic pollutants in solution. Chemosphere. 2015; 128:21–7. doi: 10.1016/j.chemosphere.2014.12.088 25638529.
45. Kadri T, Rouissi T, Kaur Brar S, Cledon M, Sarma S, Verma M. Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: A review. Journal of environmental sciences. 2017; 51:52–74. doi: 10.1016/j.jes.2016.08.023 28115152.
46. Su Y, Xian H, Shi S, Zhang C, Manik SM, Mao J, et al. Biodegradation of lignin and nicotine with white rot fungi for the delignification and detoxification of tobacco stalk. BMC biotechnology. 2016;16(1):81. doi: 10.1186/s12896-016-0311-8 27871279; PubMed Central PMCID: PMC5117543.
47. Hu L, Zeng G, Chen G, Dong H, Liu Y, Wan J, et al. Treatment of landfill leachate using immobilized Phanerochaete chrysosporium loaded with nitrogen-doped TiO (2) nanoparticles. Journal of hazardous materials. 2016; 301:106–18. doi: 10.1016/j.jhazmat.2015.08.060 26355412.
48. Herve V, Ketter E, Pierrat JC, Gelhaye E, Frey-Klett P. Impact of Phanerochaete chrysosporium on the Functional Diversity of Bacterial Communities Associated with Decaying Wood. PLoS One. 2016;11(1): e0147100. doi: 10.1371/journal.pone.0147100 26824755; PubMed Central PMCID: PMC4732817.
49. Wei B-Q, Xue Q-Y, Wei L-H, Niu D-D, Liu H-X, Chen L-F, et al. A novel screening strategy to identify biocontrol fungi using protease production or chitinase activity against Meloidogyne root-knot nematodes. Biocontrol Science and Technology. 2009;19(8):859–70. doi: 10.1080/09583150903165636
50. Yang J, Huang X, Tian B, Wang M, Niu Q, Zhang K. Isolation and characterization of a serine protease from the nematophagous fungus, Lecanicillium psalliotae, displaying nematicidal activity. Biotechnology letters. 2005;27(15):1123–8. doi: 10.1007/s10529-005-8461-0 16132863.
51. Thorn G, Tsuneda A. Interactions between Pleurotus species, nematodes, and bacteria on agar and in wood. Transactions of the Mycological Society of Japan. 1993;34:449–64.
52. Kwok OCH, Plattner, Weisleder, Wicklow D. A nematicidal toxin from Pleurotus ostreatus NRRL 3526. Journal of Chemical Ecology. 1992;18(2):127–37. doi: 10.1007/BF00993748 24254904
53. Marlin M, Wolf A, Alomran M, Carta L, Newcombe G. Nematophagous Pleurotus Species Consume Some Nematode Species but Are Themselves Consumed by Others. Forests. 2019;10(5):404. doi: 10.3390/f10050404
Článek vyšel v časopise
PLOS One
2020 Číslo 1
- Tisícileté topoly, mokří psi, stárnoucí kočky a ospalé octomilky – „jednohubky“ z výzkumu 2024/41
- Jaké jsou aktuální trendy v léčbě karcinomu slinivky?
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Menstruační krev má značný diagnostický potenciál, mimo jiné u diabetu
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
Nejčtenější v tomto čísle
- Severity of misophonia symptoms is associated with worse cognitive control when exposed to misophonia trigger sounds
- Chemical analysis of snus products from the United States and northern Europe
- Calcium dobesilate reduces VEGF signaling by interfering with heparan sulfate binding site and protects from vascular complications in diabetic mice
- Effect of Lactobacillus acidophilus D2/CSL (CECT 4529) supplementation in drinking water on chicken crop and caeca microbiome
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy