CoChat
Sign Up
Cited by 66Plant-Microbe Interactions and ImmunityPowdery Mildew Fungal DiseasesInsect-Plant Interactions and Control

The DOI matches its Crossref record.

The Epiphytic Fungus Pseudozyma aphidis Induces Jasmonic Acid- and Salicylic Acid/Nonexpressor of PR1-Independent Local and Systemic Resistance

Open access
Buxdorf, Kobi, Rahat, Ido, Gafni, Aviva, Levy, Maggie·2013·Plant Physiology
DOI 10.1104/pp.112.212969PMC PMC3613472
Open this paper in CoChat — free account

Abstract

Pseudozyma spp. are yeast-like fungi, classified in the Ustilaginales, which are mostly epiphytic or saprophytic and are not pathogenic to plants. Several Pseudozyma species have been reported to exhibit biological activity against powdery mildews. However, previous studies have reported that Pseudozyma aphidis, which can colonize plant surfaces, is not associated with the ‎‎collapse of powdery ‎mildew colonies. In this report, we describe a novel P. aphidis strain and study its interactions with its plant host and the plant pathogen Botrytis cinerea. This isolate was found to secrete extracellular metabolites that inhibit various fungal pathogens in vitro and significantly reduce B. cinerea infection in vivo. Moreover, P. aphidis sensitized Arabidopsis (Arabidopsis thaliana) plants’ defense machinery via local and systemic induction of PATHOGENESIS-RELATED1 (PR1) and PLANT DEFENSIN1.2 (PDF1.2) expression. P. aphidis also reduced B. cinerea infection, locally and systemically, in Arabidopsis mutants impaired in jasmonic acid (JA) or salicylic acid (SA) signaling. Thus, in addition to direct inhibition, P. aphidis may inhibit B. cinerea infection via induced resistance in a manner independent of SA, JA, and Nonexpressor of PR1 (NPR1). P. aphidis primed the plant defense machinery and induced stronger activation of PDF1.2 after B. cinerea infection. Finally, P. aphidis fully or partially reconstituted PR1 and PDF1.2 expression in npr1-1 mutant and in plants with the SA hydroxylase NahG transgene, but not in a jasmonate resistant1-1 mutant, after B. cinerea infection, suggesting that P. aphidis can bypass the SA/NPR1, but not JA, pathway to activate PR genes. Thus, either partial gene activation is sufficient to induce resistance, or the resistance is not directed solely through PR1 and PDF1.2 but probably through other pathogen-resistance genes or pathways as well.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1104/pp.112.212969

Cites

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Biocontrol yeasts can elicit systemic resistance of plants against a broad range of pathogens.

    “Biocontrol yeasts can elicit systemic resistance of plants against a broad range of pathogens (Supplementary Table 1) (Barda et al. 2015; Buxdorf et al. 2013a, b; Lee et al. 2017; Liu et al. 2016)”

    From Biocontrol yeasts: mechanisms and applications (2019) · cites this paper as Buxdorf et al. 2013a, b

    The Abstract and Discussion report that the yeast-like biocontrol fungus Pseudozyma aphidis induced systemic resistance to Botrytis cinerea in Arabidopsis. The Abstract also reports inhibition of various fungal pathogens in vitro, but it does not show systemic resistance against that broader range. The copy provides no page numbers for these passages. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

No references could be resolved yet.

Research works printed but not linked: 69

  1. Alfano, 2007, Systemic modulation of gene expression in tomato by Trichoderma hamatum 382, Phytopathology, 97, 429, 10.1094/PHYTO-97-4-0429 · DOI
  2. Allen, 2004, Effect of foliar disease on the epiphytic yeast communities of creeping bentgrass and tall fescue, Can J Microbiol, 50, 853, 10.1139/w04-073 · DOI
  3. Avis, 2001, Specificity and mode of action of the antifungal fatty acid cis-9-heptadecenoic acid produced by Pseudozyma flocculosa., Appl Environ Microbiol, 67, 956, 10.1128/AEM.67.2.956-960.2001 · DOI
  4. Avis, 2002, Mechanisms and means of detection of biocontrol activity of Pseudozyma yeasts against plant-pathogenic fungi, FEMS Yeast Res, 2, 5
  5. Avis, 2001, Molecular and physiological analysis of the powdery mildew antagonist Pseudozyma flocculosa and related fungi, Phytopathology, 91, 249, 10.1094/PHYTO.2001.91.3.249 · DOI
  6. Bashi, 1977, Environmental factors limiting growth of Sporobolomyces roseus, an antagonist of Cochliobolus sativus, on wheat leaves, Trans Br Mycol Soc, 68, 17, 10.1016/S0007-1536(77)80146-0 · DOI
  7. Beckers, 2006, Fine-Tuning Plant Defence Signalling: Salicylate versus Jasmonate, Plant Biol (Stuttg), 8, 1, 10.1055/s-2005-872705 · DOI
  8. Begerow, 2000, Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences, Mycol Res, 104, 53, 10.1017/S0953756299001161 · DOI
  9. Bélanger, 1994, Commercial-scale control of rose powdery mildew with a fungal antagonist, Plant Dis, 78, 420, 10.1094/PD-78-0420 · DOI
  10. Benyagoub, 1996, Influence of a subinhibitory dose of antifungal fatty acids from Sporothrix flocculosa on cellular lipid composition in fungi, Lipids, 31, 1077, 10.1007/BF02522465 · DOI
  11. Bleve, 2006, Isolation of epiphytic yeasts with potential for biocontrol of Aspergillus carbonarius and A. niger on grape, Int J Food Microbiol, 108, 204, 10.1016/j.ijfoodmicro.2005.12.004 · DOI
  12. Boekhout, 1995, Pseudozyma Bandoni emend. Boekhout, a genus for yeast-like anamorphs of Ustilaginales., J Gen Appl Microbiol, 41, 359, 10.2323/jgam.41.359 · DOI
  13. Broekaert, 2006, The role of ethylene in host-pathogen interactions, Annu Rev Phytopathol, 44, 393, 10.1146/annurev.phyto.44.070505.143440 · DOI
  14. Cao, 1994, Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance, Plant Cell, 6, 1583, 10.2307/3869945 · DOI
  15. Chalutz, 1990, Postharvest biocontrol of green and blue mold and sour rot of citrus fruit by Debaryomyces hansenii., Plant Dis, 74, 134, 10.1094/PD-74-0134 · DOI
  16. Conn, 2008, Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana., Mol Plant Microbe Interact, 21, 208, 10.1094/MPMI-21-2-0208 · DOI
  17. Cook, 1997, Attachment microbes antagonistic against Botrytis cinerea—biological control and scanning electron microscope studies in vivo, Ann Appl Biol, 131, 503, 10.1111/j.1744-7348.1997.tb05177.x · DOI
  18. Czechowski, 2005, Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis, Plant Physiol, 139, 5, 10.1104/pp.105.063743 · DOI
  19. Després, 2000, The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors, Plant Cell, 12, 279, 10.1105/tpc.12.2.279 · DOI
  20. Dik, 1991, Consumption of aphid honeydew, a wheat yield reduction factor, by phyllosphere yeasts under field conditions, Eur J Plant Pathol, 97, 209
  21. Dik, 1992, Influence of climatic and nutritional factors on yeast population dynamics in the phyllosphere of wheat, Microb Ecol, 23, 41, 10.1007/BF00165906 · DOI
  22. Dik, 1998, Comparison of three biological control agents against cucumber powdery mildew (Sphaerotheca fuliginea) in semi-commercial-scale glasshouse trials, Eur J Plant Pathol, 104, 413, 10.1023/A:1008025416672 · DOI
  23. Dong, 2004, NPR1, all things considered, Curr Opin Plant Biol, 7, 547, 10.1016/j.pbi.2004.07.005 · DOI
  24. Durrant, 2004, Systemic acquired resistance, Annu Rev Phytopathol, 42, 185, 10.1146/annurev.phyto.42.040803.140421 · DOI · Paper page
  25. Fan, 2002, In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis, Plant Cell, 14, 1377, 10.1105/tpc.001628 · DOI
  26. Fernández, 2012, Yeast and yeast-like fungi associated with dry indehiscent fruits of Nothofagus nervosa in Patagonia, Argentina, FEMS Microbiol Ecol, 80, 179, 10.1111/j.1574-6941.2011.01287.x · DOI
  27. Filonow, 1996, Biological Control of Botrytis cinerea in apple by yeasts from various habitats and their putative mechanisms of antagonism, Biol Control, 7, 212, 10.1006/bcon.1996.0086 · DOI
  28. Fokkema, 1979, Manipulation of yeasts on field-grown wheat leaves and their antagonistic effect on Cochliobolus sativus and Septoria nodorum., Trans Br Mycol Soc, 72, 19, 10.1016/S0007-1536(79)80003-0 · DOI
  29. Fokkema, 1975, The buffering capacity of the natural mycoflora of rye leaves to infection by Cochliobolus sativus and its susceptibility to benomyl, Neth J Plant Pathol, 81, 176, 10.1007/BF01976329 · DOI
  30. Gaffney, 1993, Requirement of salicylic Acid for the induction of systemic acquired resistance, Science, 261, 754, 10.1126/science.261.5122.754 · DOI
  31. Glazebrook, 2005, Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens, Annu Rev Phytopathol, 43, 205, 10.1146/annurev.phyto.43.040204.135923 · DOI
  32. Grant, 2006, Systemic immunity, Curr Opin Plant Biol, 9, 414, 10.1016/j.pbi.2006.05.013 · DOI
  33. Haas, 2005, Biological control of soil-borne pathogens by fluorescent pseudomonads, Nat Rev Microbiol, 3, 307, 10.1038/nrmicro1129 · DOI
  34. Hajlaoui, 1991, Comparative effects of temperature and humidity on the activity of three potential antagonists of rose powdery mildew, Neth J Plant Pathol, 97, 203, 10.1007/BF01989818 · DOI
  35. Hajlaoui, 1993, Antagonism of the yeast-like phylloplane fungus Sporothrix flocculosa against Erysiphe graminis var tritici., Biocontrol Sci Technol, 3, 427, 10.1080/09583159309355297 · DOI
  36. Hajlaoui, 1994, Antifungal activity of extracellular metabolites produced by Sporothrix flocculosa., Biocontrol Sci Technol, 4, 229, 10.1080/09583159409355331 · DOI
  37. Hammami, 2011, Ecological basis of the interaction between Pseudozyma flocculosa and powdery mildew fungi, Appl Environ Microbiol, 77, 926, 10.1128/AEM.01255-10 · DOI
  38. Heil, 2002, Induced systemic resistance (ISR) against pathogens in the context of induced plant defences, Ann Bot (Lond), 89, 503, 10.1093/aob/mcf076 · DOI
  39. Henninger, 1975, [Pichia lindnerii sp. n., a new methanol assimilating yeast from soil], Arch Microbiol, 105, 47, 10.1007/BF00447111 · DOI
  40. Hossain, 2007, The plant growth-promoting fungus Penicillium simplicissimum GP17-2 induces resistance in Arabidopsis thaliana by activation of multiple defense signals, Plant Cell Physiol, 48, 1724, 10.1093/pcp/pcm144 · DOI
  41. Jarvis, 1989, Factors affecting antagonism of cucumber powdery mildew by Stephanoascus flocculosus and S. rugulosus., Mycol Res, 92, 162, 10.1016/S0953-7562(89)80006-1 · DOI
  42. Kinkema, 2000, Nuclear localization of NPR1 is required for activation of PR gene expression, Plant Cell, 12, 2339, 10.1105/tpc.12.12.2339 · DOI
  43. Korolev, 2008, The role of phytohormones in basal resistance and Trichoderma-induced systemic resistance to Botrytis cinerea in Arabidopsis thaliana., BioControl, 53, 667, 10.1007/s10526-007-9103-3 · DOI
  44. Levy, 2011, Pseudozyma aphidis as a biocontrol agent against various plant pathogens, Patent Cooperation Treaty Patent Publication No, WO 2011/151819
  45. Loake, 2007, Salicylic acid in plant defence—the players and protagonists, Curr Opin Plant Biol, 10, 466, 10.1016/j.pbi.2007.08.008 · DOI
  46. Mou, 2003, Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes, Cell, 113, 935, 10.1016/S0092-8674(03)00429-X · DOI
  47. Paz, 2007, Antagonistic effects of the endophytic fungus Meira geulakonigii on the citrus rust mite Phyllocoptruta oleivora., J Appl Microbiol, 103, 2570, 10.1111/j.1365-2672.2007.03512.x · DOI
  48. Penninckx, 1996, Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway, Plant Cell, 8, 2309
  49. Penninckx, 1998, Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis, Plant Cell, 10, 2103, 10.1105/tpc.10.12.2103 · DOI
  50. Perfect, 1999, Colletotrichum: A model genus for studies on pathology and fungal-plant interactions, Fungal Genet Biol, 27, 186, 10.1006/fgbi.1999.1143 · DOI · Paper page
  51. Pusey, 2009, Epiphytic bacteria and yeasts on apple blossoms and their potential as antagonists of Erwinia amylovora., Phytopathology, 99, 571, 10.1094/PHYTO-99-5-0571 · DOI · Paper page
  52. Raacke, 2006, Yeast increases resistance in Arabidopsis against Pseudomonas syringae and Botrytis cinerea by salicylic acid-dependent as well as -independent mechanisms, Mol Plant Microbe Interact, 19, 1138, 10.1094/MPMI-19-1138 · DOI
  53. Rau, 2005, Formation and analysis of mannosylerythritol lipids secreted by Pseudozyma aphidis., Appl Microbiol Biotechnol, 66, 551, 10.1007/s00253-004-1672-9 · DOI
  54. Robiglio, 2011, Yeast biocontrol of fungal spoilage of pears stored at low temperature, Int J Food Microbiol, 147, 211, 10.1016/j.ijfoodmicro.2011.04.007 · DOI
  55. Shoresh, 2010, Induced systemic resistance and plant responses to fungal biocontrol agents, Annu Rev Phytopathol, 48, 21, 10.1146/annurev-phyto-073009-114450 · DOI
  56. Shoresh, 2005, Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203, Phytopathology, 95, 76, 10.1094/PHYTO-95-0076 · DOI
  57. Somssich, 2003, Closing another gap in the plant SAR puzzle, Cell, 113, 815, 10.1016/S0092-8674(03)00473-2 · DOI
  58. Spoel, 2003, NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol, Plant Cell, 15, 760, 10.1105/tpc.009159 · DOI
  59. Starmer, 1987, The ecological role of killer yeasts in natural communities of yeasts, Can J Microbiol, 33, 783, 10.1139/m87-134 · DOI
  60. Staswick, 1992, Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant, Proc Natl Acad Sci USA, 89, 6837, 10.1073/pnas.89.15.6837 · DOI
  61. Stein, 2008, Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1, Plant Cell Physiol, 49, 1747, 10.1093/pcp/pcn147 · DOI
  62. Thomma, 1998, Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens, Proc Natl Acad Sci USA, 95, 15107, 10.1073/pnas.95.25.15107 · DOI
  63. Tucci, 2011, The beneficial effect of Trichoderma spp. on tomato is modulated by the plant genotype, Mol Plant Pathol, 12, 341, 10.1111/j.1364-3703.2010.00674.x · DOI
  64. Urquhart, 2002, Hydrolytic enzymes and antifungal compounds produced by Tilletiopsis species, phyllosphere yeasts that are antagonists of powdery mildew fungi, Can J Microbiol, 48, 219, 10.1139/w02-008 · DOI
  65. van Loon, 2006, Significance of inducible defense-related proteins in infected plants, Annu Rev Phytopathol, 44, 135, 10.1146/annurev.phyto.44.070505.143425 · DOI
  66. Wang, 2005, Induction of protein secretory pathway is required for systemic acquired resistance, Science, 308, 1036, 10.1126/science.1108791 · DOI
  67. Yaffe, 2012, LogSpin: a simple, economical and fast method for RNA isolation from infected or healthy plants and other eukaryotic tissues, BMC Res Notes, 5, 45, 10.1186/1756-0500-5-45 · DOI
  68. Zhang, 1999, Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene, Proc Natl Acad Sci USA, 96, 6523, 10.1073/pnas.96.11.6523 · DOI
  69. Zhou, 2000, NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid, Mol Plant Microbe Interact, 13, 191, 10.1094/MPMI.2000.13.2.191 · DOI

Cited by

Sorted by citations

Metadata

Authors
Buxdorf, K., Rahat, I., Gafni, A., & Levy, M.
Affiliations
Hebrew University of Jerusalem (IL)
ORCID
Levy, Maggie
Venue
Plant Physiology
Publisher
Oxford University Press (OUP)
Published
2013-02-06
Volume
161
Issue
4
Pages
2014-2022
ISSN
  • 0032-0889 (ISSN-L)
  • 1532-2548
DOI
10.1104/pp.112.212969
PMC
PMC3613472
OpenAlex
W2041038630
Cited by
66
References
0
Citations by year
2026: 4 · 2025: 4 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 9 · 2020: 7 · 2019: 4 · 2018: 4 · 2017: 6 · 2016: 4 · 2015: 4 · 2014: 6 · 2013: 1
FWCI
6.03
Type
journal article
Language
en
Open access
Licence
academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations
  • PLANT PHYSIOLOGY (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Powdery Mildew Fungal Diseases
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Keywords
Pseudozyma aphidis, Botrytis cinerea, induced systemic resistance, jasmonic acid signaling, salicylic acid signaling, NPR1, PDF1.2, plant defense priming, epiphytic fungi, Arabidopsis thaliana, powdery mildew, plant-fungal interactions
MeSH terms
Basidiomycota, Cyclopentanes, Mutation, Pest Control, Biological, Plant Diseases, Arabidopsis, Plant Leaves, Solanum lycopersicum, Salicylic Acid, Botrytis, Arabidopsis Proteins, Oxylipins, Microbial Interactions, Disease Resistance

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review