Secondary metabolites of six Siberian and Crimean Armillaria species and their in vitro phytotoxicity to pine, larch and poplar

doi:10.3832/ifor3840-014

Secondary metabolites of six Siberian and Crimean Armillaria species and their in vitro phytotoxicity to pine, larch and poplar

Tatyana V Antipova⁽¹⁾ , Valentina P Zhelifonova⁽¹⁾, Yulia A Litovka^(2-3), Igor N Pavlov^(2-3), Boris P Baskunov⁽¹⁾, Zhanna A Kokh^(2-4), Polina V Makolova^(2-3), Anton A Timofeev⁽²⁾, Anatoly G Kozlovsky⁽¹⁾

iForest - Biogeosciences and Forestry, Volume 15, Issue 1, Pages 38-46 (2022)
doi: https://doi.org/10.3832/ifor3840-014
Published: Feb 04, 2022 - Copyright © 2022 SISEF

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Basidiomycetes Armillaria infect deciduous, coniferous and fruit trees, causing enormous economic damage. The role of secondary metabolites (tricyclic sesquiterpene aryl esters - melleolides) in the life cycle and pathogenesis of Armillaria is under active investigation. To date, not all species of Armillaria have been tested for the biosynthesis of melleolides. We investigated the secondary metabolite profiles of six root-pathogenic species of the genus Armillaria (A. borealis Marxmüller & Korhonen, A. cepistipes Velenovský, A. gallica Marxm, A. mellea (Vahl) P. Kummer, A. sinapina Bérubé & Dessur, A. ostoyae (Romagn.) Herink) distributed in Siberia (South Krasnoyarsk Krai, Republic of Tyva, Republic of Khakassia, Taimyr Peninsula), Russian Far East (Sikhote-Alin) and Crimea (Krymsky National Park, Chatyr-Dag Mountain Lower Plateau). A total of 15 compounds were identified in the metabolome profile. Two compounds (melleolide D and melledonal C) are synthesized by all investigated strains irrespective of their geographic location and host plant. The maximum spectrum of melleolides (7-8 compounds) was found in isolates of A. borealis, A. gallica, A. sinapina, A. ostoyae. In submerged culture, the maximum accumulation of melleolides varied from 2 up to 239 mg l^-1. A mixture of melleolide D and melledonal C (1:1) synthesized by the most productive strain A. mellea Cr2-17 was first found to have a phytotoxic action on the growth parameters of the callus culture Populus balsamifera and 10-day-old conifer seedlings. A 0.5% concentration of melleolides caused a credible decrease of P. balsamifera callus raw biomass; a decrease of the viability of Larix sibirica and, which is especially significant, Pinus sylvestris seedlings; inhibition of stem and root growth processes; dechromation of foliage; loss of turgor. The occurrence of a broad range of melleolides in the metabolome profile and two common compounds in all investigated strains, with a phytotoxic action at their sufficiently high concentration, enables considering the synthesis of melleolides by Armillaria fungi as one of the possible mechanisms of their pathogenicity efficiently realized in strains characterized by overproduction of melleolides under natural conditions.

Keywords

Melleolides, Metabolome, Armillaria fungi, Phytotoxicity, Callus, Coniferous Plants

Authors’ address

(1)

0000-0002-4860-2647
0000-0001-9213-9584
0000-0002-0342-2431

GK Skryabin Institute of Biochemistry and Physiology of Microorganisms, FRC Pushchino Centre for Biological Research, Russian Academy of Sciences, 5 Prosp. Nauki, Pushchino, Moscow Region, 142290 (Russia)

(2)

0000-0001-5343-7896
0000-0001-7312-0933
0000-0003-4016-7596

VN Sukachev Institute of Forest, FRC KSC, Siberian Branch, Russian Academy of Sciences, 50 Akademgorodok Str., Bld 28, Krasnoyarsk, 660036 (Russia)

(3)

0000-0001-5343-7896
0000-0001-7312-0933

FSBEIHE MF Reshetnev Siberian State University of Science and Technology, 82 Prosp. Mira, Krasnoyarsk, 660037 (Russia)

(4)

0000-0003-4016-7596
FSBEIHE Krasnoyarsk State Agrarian University, 90 Prosp. Mira, Krasnoyarsk, 660049 (Russia)

Corresponding author

Tatyana V Antipova
tatantip@rambler.ru

Citation

Antipova TV, Zhelifonova VP, Litovka YA, Pavlov IN, Baskunov BP, Kokh ZA, Makolova PV, Timofeev AA, Kozlovsky AG (2022). Secondary metabolites of six Siberian and Crimean Armillaria species and their in vitro phytotoxicity to pine, larch and poplar. iForest 15: 38-46. - doi: 10.3832/ifor3840-014

Academic Editor

Alberto Santini

Paper history

Received: Apr 06, 2021
Accepted: Dec 02, 2021

First online: Feb 04, 2022
Publication Date: Feb 28, 2022
Publication Time: 2.13 months

Open Access

This article is distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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List of the papers citing this article based on CrossRef Cited-by.

(1)

Alves E, Lucas GC, Pozza EA, Alves De M C (2012)
Scanning electron microscopy for fungal sample examination. In: “Laboratory Protocols in Fungal Biology: Current Methods in Fungal Biology” (Gupta VK, Tuohy MG, Ayyachamy M, Turner KM, O’Donovan A eds). Springer New York, New York, USA, pp. 133-150.
CrossRef | Gscholar

(2)

Baumgartner K, Coetzee MP, Hoffmeister D (2011)
Secrets of the subterranean pathosystem of Armillaria. Molecular Plant Pathology 12 (6): 515-534.
CrossRef | Gscholar

(3)

Bohnert D, Nutzmann H-W, Schroeckh V, Horn F, Dahse H-M, Brakhage AA, Hoffmeister D (2014)
Cytotoxic and antifungal activities of melleolide antibiotics follow dissimilar structure-activity relationships. Phytochemistry 105: 101-108.
CrossRef | Gscholar

(4)

Bukhalo AS (1988)
Higher edible basidiomycetes in pure culture. Naukova Dumka, Kiev, Ukraine, pp. 144. [in Russian]
Gscholar

(5)

Butenko RG (1999)
Biology of higher plant cells in vitro and biotechnologies on their basis (study guide). FBK-Press, Moscow, Russia, pp. 160. [in Russian]
Gscholar

(6)

Cardillo R, Nasini G (1986)
Structures of melleolides B-D, three antibacterial sesquiterpenoids from Armillaria mellea. Phytochemistry 25 (2): 471-474.
CrossRef | Gscholar

(7)

Chen YJ, Chen CC, Huang HL (2016)
Induction of apoptosis by Armillaria mellea constituent armillarikin in human hepatocellular carcinoma. OncoTargets and Therapy 9: 4773-4783.
CrossRef | Gscholar

(8)

Coetzee MPA, Wingfield BD, Wingfield MJ (2018)
Armillaria root-rot pathogens: species boundaries and global distribution. Pathogens 7 (4): 83.
CrossRef | Gscholar

(9)

Dorfer M, Gressler M, Hoffmeister D (2019a)
Diversity and bioactivity of Armillaria sesquiterpene aryl ester natural products. Mycological Progress 18: 1027-1037.
CrossRef | Gscholar

(10)

Dorfer M, Heine D, Konig S, Gore S, Werz O, Hertweck C, Gressler M, Hoffmeister D (2019b)
Melleolides impact fungal translation via elongation factor 2. Organic and Biomolecular Chemistry 17: 4906-4916.
CrossRef | Gscholar

(11)

Endress R (1994)
Plant cell biotechnology. Springer-Verlag, Berlin, Heidelberg, Germany, pp. 353.
CrossRef | Gscholar

(12)

Guillaumin JJ, Mohammed C, Courtecuisse N AR, Gregory SC, Holdenrieder O, Intini M, Lung B, Marxmüller H, Morrison D, Rishbeth J, Termorshuizen AJ, Tirro A, Van Dam B (1993)
Geographical distribution and ecology of the Armillaria species in western Europe. Forest Pathology 23 (6-7): 321-341.
CrossRef | Gscholar

(13)

Kalinin FL, Sarnatskaya VV, Polishchuk VE (1980)
Tissue culture methods in plant physiology and biochemistry. Naukova Dumka, Kiev, Ukraine, pp. 488. [in Russian]
Gscholar

(14)

Kobori H, Sekiya A, Suzuki T, Choi J, Hirai H, Kawagishi H (2015)
Bioactive sesquiterpene aryl esters from the culture broth of Armillaria sp. Journal of Natural Products 78 (1): 163-167.
CrossRef | Gscholar

(15)

Korhonen K, Hintikka V (1980)
Simple isolation and inoculation methods for fungal cultures. Karstenia 20: 19-22.
CrossRef | Gscholar

(16)

Maloy OC (1974)
Benomyl-malt agar for the purification of cultures of wood decay fungi. Plant Disease Reporter 58: 902-904.
Gscholar

(17)

Marçais B, Bréda N (2006)
Role of an opportunistic pathogen in the decline of stressed oak trees. Journal of Ecology 94: 1214-1223.
CrossRef | Gscholar

(18)

Misiek M, Hoffmeister D (2012)
Sesquiterpene aryl ester natural products in North American Armillaria species. Mycological Progress 11 (1): 7-15.
CrossRef | Gscholar

(19)

Momose I, Sekizava R, Hosokawa N, Iinuma H, Matsui S, Nakamura H, Naganawa H, Hamada M, Takeuchi T (2000)
Melleolides K, L and M, new melleolides from Armillariella mellea. Journal of Antibiotics 53 (2): 137-143.
CrossRef | Gscholar

(20)

Morrison DJ, Pellow KW (2002)
Variation in virulence among isolates of Armillaria ostoyae. Forest Pathology 32: 99-107.
CrossRef | Gscholar

(21)

Pavlov IN, Litovka Y, Litvinova EA, Timofeev AA, Pashenova NV, Safronova IE, Kulakov SS, Mulyava VV, Mulyava VE (2017)
Armillaria borealis Marxm. and Korhonen: distribution, phytopathogenicity and morphological and cultural features. AgroEko-Info 29 (3): 18.
Online | Gscholar

(22)

Peipp H, Sonnenbichler J (1992)
Occurrence of antibiotic compounds in cultures of Armillaria ostoyae growing in the presence of an antagonistic fungus or host plant cells. Biological Chemistry Hoppe-Seyler 373 (2): 675-684.
CrossRef | Gscholar

(23)

Prospero S, Holdenrieder O, Rigling D (2004)
Comparison of the virulence of Armillaria cepistipes and Armillaria ostoyae on four Norway spruce provenances. Forest Pathology 34: 1-14.
CrossRef | Gscholar

(24)

Tiidema A, Truve E (2004)
Efficient regeneration of fertile barley plants from callus cultures of several Nordic cultivars. Hereditas 140: 171-176.
CrossRef | Gscholar

(25)

Tsyrenov VZ (2003)
Basics of biotechnology: cultivation of isolated plant cells and tissues (study guide). ESSTU, Ulan-Ude, Russia, pp. 58. [in Russian]
Gscholar

(26)

White TJ, Bruns T, Lee S, Taylor J (1990)
Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: “PCR protocols: A guide to Methods and Applications”, (Innis N, Gelfand D, Sninsky J, White T eds). Academic Press, New York, USA, pp. 315-322.
CrossRef | Gscholar

(27)

Whitney RD, Myren DT, Britnell WE (1978)
Comparison of malt agar with malt plus orthophenylphenol for isolating Armillaria mellea and other fungi from conifer roots. Canadian Journal of Forest Research 8: 348-351.
CrossRef | Gscholar

(28)

Zhelifonova VP, Antipova TV, Litvinova EA, Baskunov BP, Litovka Y, Pavlov IN, Kozlovsky AG (2019)
Biosynthesis of protoilludene sesquiterpene aryl esters by siberian strains of the genus Armillaria fungi. Applied Biochemistry and Microbiology 55 (3): 277-283.
CrossRef | Gscholar

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