Plants as the Extended Phenotype of Endophytes—The Actual Source of Bioactive Compounds
Abstract
:1. Introduction
2. Are Endophytes Crucial for Plant Existence?
3. The Actual Source of Plant Bioactive Molecules
4. Molecular Background of Host-Specific Compounds Synthesis
5. Co-Evolution of Plant and Its Endophytes
6. Future Prospects
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Microorganisms | Living Conditions/Specifics |
---|---|
Rhizospheric | soil in close proximity to roots and its exudates |
Rhizoplanic | surface of plant roots |
Phyllospheric (=epiphytes) | surface of aerial parts of a plant |
Endophytic (=endophytes) | inside plant tissues without causing any apparent harm to plant host |
Obligate | living inside a plant during their entire lifespan |
Facultative | optionally living inside of a plant |
Systemic (true) | strictly symbiotic, non-pathogenic at any stage of its lifespan |
Non-systemic (transient) | live asymptomatically within plant for a part of their lifespan, can turn into pathogen when plant host is stressed or resource-limited |
Competent | successfully colonize plant, can alter its physiology and be selectively favored |
Opportunistic | occasionally enter a plant and benefit from its internal environment |
Passenger | enter a plant accidently in the absence of selective forces for efficient root colonization |
Compound | Properties | Endophyte | Plant Host | Amount Produced by Endophyte Ex Planta | Reference |
---|---|---|---|---|---|
Fungi | |||||
Aconitine | Analgesic, anti-inflammatory, anti-tumor | Cladosporium cladosporioides XJ-A C03 | Aconitum leucostomum | 236.4 µg/g 1 | [108] |
Alternariol | Cytotoxic | Alternaria sp. | Polygonum senegalense | ND | [109] |
Andrographolide | Anti-inflammatory, antineoplastic, anti-platelet aggregation | Colletotrichum sp. (AP-4, AP-12) | Andrographis paniculata | 30.089 ± 0.992 mg/g 1 (AP-4), 28.617 ± 0.641 mg/g 1 (AP-12) | [110] |
Asarone | Anticonvulsant, GABA modulator | Penicillium pinophilum | Alloteropsis cimicina | ND | [111] |
Asiaticoside | Antioxidant, anti-inflammatory, antirheumatic | Colletotrichum gloeosporioides | Centella asiactica | 62.29 ± 3.36 µg/100 mL 2 | [112] |
Azadirachtin | Hepatoprotective, insecticide | Eupenicillium parvum | Azadirachta indica | 0.4 µg/100 g 1; 43 µg/L 2 | [113] |
Cajaninstilbene acid | Analgesic, antioxidant, anti-inflammatory, hypoglycemic, neuroprotective | Fusarium proliferatum | Cajanus cajan | 100.5 ± 9.4 µg/g 1; 504.8 ± 20.1 µg/mL 2 | [114] |
Camptothecin | Anticancer (inhibition of DNA topoisomerase I), potential antineoplastic agent | Fusarium solani (MTCC 9667, 9668) | Apodytes dimidiata | 37 µg/100 g 1; 53 µg/100 g 1 | [86] |
Fusarium solani | Camptotheca acuminata | 150 ± 20 µg/L 2 | [88] | ||
Alternaria alstroemeriae (NCIM1408) | Nothapodytes nimmoniana | 426.7 ± 33.6 µg/g 1 | [115] | ||
Alternaria burnsii (NCIM1409) | 403.3 ± 41.6 µg/g 1 | ||||
Fusarium sp. | 2.17 µg/100 mg 1 | [89] | |||
Capsaicin | Analgesic | Alternaria alternata | Capsicum annuum | 8.30 µg/L 2 | [116] |
Colchicine | Anti-gout, anti-inflammatory | Diaporthe perseae | Glorosa superba | 55.25 uµg/g 1 | [117] |
Deoxypodophyllotoxin | Precursor for podophyllotoxin, anticancer | Aspergillus fumigatus | Juniperus communis | 4 ± 2 µg/100 g 1; 3 ± 2 µg/L 2 | [118] |
Dendrobine | Anti-cataract, anti-influenza A virus, and anti-tumor, promising therapeutical effects on Alzheimer’s disease | Trichoderma longibrachiatum MD33 | Dendrobium nobile | ND | [119] |
Digoxin | Anti-arrhythmia drug, cardiotonic drug | Unidentified | Digitalis lanata | ND | [120] |
Diosgenin | Anticancer, antiatherogenic, antineoplastic, and antiviral agent | Aspergillus flavus | Dioscorea zingiberensis | ND | [121] |
Curvularia lunata | |||||
Fusarium sp. | |||||
Paecilomyces sp. | Paris podophylla | ND | [122] | ||
Emodin | Antioxidant, anti-inflammatory, antimicrobial, hepatoprotective, precursor to hypericin | Epicoccum nigrum | Hypericum perforatum | 87.7 µg/mL 3 | [123] |
Thielavia subthermophilia | 113 ± 1 µg/100 g 1 | [124] | |||
Forskolin | Antihypertensive, anti-HIV, platelet aggregation inhibitor | Rhizactonia bataticola | Coleus forskoholii | 0.5 mg 2 | [125] |
Gentiopicrin | Antifungal, antihistamine, anti-inflammatory | Unidentified (QJ18) | Gentiana macrophylla | ND | [126] |
Ginsenoside Rg3 | Antioxidant, antidiabetic, antineoplastic agent, apoptosis inducer | Chaetomium sp. | Panax ginseng | 5.60 ± 1.17 mg/g 1 | [92] |
Gymnemagenin | Antidiabetic, antiviral | Penicillium oxalicum | Gymnema sylvestre | ND | [127] |
Huperzine A | Neuroprotective, treatment of Alzheimer’s disease | Acremonium sp. | Huperzia serrata | 8.32 µg/L 2 | [128] |
Shiraia sp. Slf14 | 327.8 µg/L 2 | [129] | |||
Hypericin | Antidepressant, anti-inflammatory, antineoplastic, immunostimulating | Epicoccum nigrum | Hypericum perforatum | 117.1 µg/mL 3 | [123] |
Thielavia subthermophilia | 35 ± 2 µg/100 g 1 | [124,130] | |||
Imperialine-3β-D-glucoside | Anti-tumor | Fusarium redolens 6WBY3 | Fritillaria unibracteata | 18.8 µg/L 2 | [131] |
Loline alkaloids | Insecticidal | Neotyphodium uncinatum | Lolium pratense | 700 mg/L 2 | [132] |
Kaempferol | Antioxidant, antibacterial | Mucor fragilis | Sinopodophyllum hexandrum | ND | [96] |
Myrtucommulones | Anti-oxidant, anti-inflammatory, anti-tumor | Neofusicoccum australe | Myrtus communis | 0.2 mg/L 2 | [133] |
Nigranoic acid | Anti-neoplastic agent, HIV-1 reverse transcriptase inhibitor | Umbelopsis dimorphia | Kadsura angustifolia | ND | [134] |
Peiminine | Anticancer, anti-inflammatory | Fusarium sp. | Fritillaria unibracteata | 0.021 mg/L 2; 0.0054 mg/g 1 | [135] |
Peimisine | Anticancer, anti-inflammatory, angiotensin-converting enzyme (ACE) inhibitor | Fusarium sp. | Fritillaria unibracteata | 0.09 mg/L2; 0.0023 mg/g 1 | [135] |
Fusarium redolens 6WBY3 | 16.0 µg/L 2 | [131] | |||
Piperine | Antioxidant, anti-inflammatory, antimycobacterial, insecticidial, increasing bioavailability of drugs | Colletotrichum gloeosporioides | Piper nigrum | ND | [136] |
Periconia sp. | Piper longum | 750 mg 3 | [137] | ||
Podophyllotoxin (PTOX) | Antimitotic, anti-tumor, precursor for anticancer drugs, e.g., etoposide and teniposide | Fusarium sp. (WB5121) | Dysosma versipellis | 277 µg/g 1 | [97] |
Fusarium oxysporum | Juniper recurva | 28 µg/g 1 | [98] | ||
Fusarium solani | Podophyllum hexandrum | 29.16 ± 0.57 µg/g 1 | [95] | ||
Phialocephaa fortinii | Podophyllum peltatum | 189 µg/L 2 | [99] | ||
Trametes hirsuta | Podophyllum hexandrum | 31 µg/g 1 | [91] | ||
Mucor fragilis | Sinopodophyllum hexandrum | 49.3 µg/g 1 | [96] | ||
Quercetin monoglycosides | Antioxidant, stimulating bacterial enzymatic activity | Nigrospora oryzae | Loranthus micranthus | ND | [138] |
Quinidine | Antiarrhythmic, antimalarial | Diaporthe spp. (CLS-3) | Cinchona ledgeriana | 82.5 µg/L 2 | [139] |
Resveratrol | Antioxidant, anti-inflammatory, antimutagen, antiviral, phytoestrogenic | Alternaria sp. MG1 | Vitis vinifera | 353 µg/L 2 | [103] |
Arcopilus aureus | 89.1 µg/mL 2 | [101] | |||
Botryosphaeria sp. | 37.3 µg/mL 2 | ||||
Nigrospora sp. | 25.2 µg/mL 2 | ||||
Aspergillus stellifer AB4 | 300 µg/L 2 | [104] | |||
Fusarium equiseti | 52.3 µg/mL 2 | [100] | |||
Quambalaria cyanescens | 40 mg/L 2 | [102] | |||
Rhein | Anticancer, anti-inflammatory, antimicrobial, hemostatic | Fusarium solani | Rheum palmatum | 5.672 mg/L 2 | [140] |
Saikosaponin d | Anti-inflammatory, anti-tumor, immunomodulatory | Fusarium acuminatum | Bupleurum scorzonerifolium | 2.40 µg/mL 2 | [141] |
Fusarium oxysporum | 2.17 µg/mL 2 | ||||
Salidroside | Adaptogenic, antioxidant, antidepressant, anti-inflammatory, neuroprotective | Phialocephala fortinii (Rac56) | Rhodiola angusta | 2.339 ± 0.1093 mg/mL 2 | [142] |
Salvianolic acid C | Anticancer, antioxidant, treatment of cardiovascular and cerebrovascular diseases | Phoma glomerata D14 | Salvia miliorrhiza | 0.054 µg/mL 2; 47.67 ± 0.04 µg/g 3 | [143] |
Saponin | Anti-inflammatory, antimicrobial, anti-ulcer, haemolytic, hepatoprotective | Fusarium sp. (Pg27) | Panax ginseng | 0.181 mg/mL 2 | [144] |
Silybin A and B, isosilybin A | Anti-tumor, hepatoprotective | Aspergillus iizukae | Silybum marianum | 0.13–0.22 µg/g 3 | [145] |
Sipeimine | Anti-tumor, antitussive | Unidentified (Fu7) | Fritillaria ussuriensis | ND | [146] |
Solamargine | Antidiabetogenic, cytotoxic | Aspergillus flavus | Solanum nigrum | 250–300 µg/L2 | [147] |
Tanshinone I and IIA | Anti-inflammatory, anticoronaviral, anticancer | Trichoderma atroviride D16 | Salvia miliorrhiza | 1.119 ± 0.008 µg/g 1 (I); 3.049 ± 0.001 µg/g 1 (IIA) | [148] |
Taxol (paclitaxel) | Chemotherapy drug | Annulohypoxylon sp. MUS1 | Taxus wallichiana | 282.05 µg/L 2 | [149] |
Aspergillus fumigatus | Taxus sp. | 1.60 g/L 2 | [150] | ||
Seimatoantlerium nepalense | Taxus wallichiana | ND | [151] | ||
Seimatoantlerium tepuisense | Venezuelan guyana | 250–350 ng/L 2 | [152] | ||
Taxomyces andreanae | Taxus brevifolia | 24–50 ng/L 2 | [77] | ||
Tyrosol | Antioxidant, cardioprotective | Phialocephala fortinii (Rac56) | Rhodiola angusta | 2.002 ± 0.0009 mg/mL 2 | [142] |
Vinblastine | Antineoplastic, anti-tumor | Curvularia verruculosa | Catharanthus roseus | 182 µg/L 2 | [105] |
Fusarium oxysporum | 76 µg/L 2 | [25] | |||
Fusarium solani | ND | [107] | |||
Talaromyces radicus | 70 µg/L 2 | [153] | |||
Vincamine | Antihypertensive, vasodilator | Geomyces sp. | Nerium indicum | 1.279 mg/L 2 | [154] |
Unidentified (Vm-J2) | Vinca minor | 0.1 mg/L 2 | [155] | ||
Vincristine | Chemotherapy drug | Eutypella sp. | Catharanthus roseus | 53 ± 5.0 µg/L 2 | [106] |
Fusarium oxysporum | 67 µg/L 2 | [25] | |||
Fusarium solani | ND | [107] | |||
Viniferin | Anti-inflammatory, anticancer, anti-angiogenic, antimicrobial, anthelminthic | Aspergillus stellifer AB4 | Vitis vinifera | 324 µg/L 2 | [104] |
Withanolide | Antioxidant, anti-inflammatory, antistress, cardioprotective, neuroprotective | Taleromyces pinophilus | Withania somnifera | 360 mg/L 2 | [156] |
Bacteria | |||||
Achillin | Anti-inflammatory, antihypertensive, vasorelaxant | Microbacterium maritypicum | Ephedra foliata | ND | [157] |
Berberine | Analgesic, anti-inflammatory, antimicrobial, hypolipidemic | Kytococcus schroeteri | Ephedra foliata | ND | [157] |
Paenibacillus polymyxa | |||||
Camptothecin | Anticancer (inhibition of DNA topoisomerase I), potential antineoplastic agent | Bacillus cereus ChST | Miquelia dentata | 1.177 µg/mL 2 | [90] |
Bacillus subtilis PXJ-5 | 1.554 µg/mL 2 | ||||
Bacillus subtilis | Pyrenacantha angustifolia | 0.18 µg/mL 2 | [158] | ||
Kytococcus schroeteri | Ephedra foliata | ND | [157] | ||
Daunorubicin | Antibiotic, antineoplastic, anticancer | Paenibacillus polymyxa | Ephedra foliata | ND | [157] |
Dendrobine analogs | Anti-cataract, and anti-influenza A virus, anti-tumor, promising therapeutical effects for Alzheimer’s disease | Pseudomonas proteogens CHA0 | Dendrobium sp. | ND | [159] |
Diosgenin | Anticancer, antiatherogenic, antineoplastic, and antiviral agent | Bacillus sp. | Trigonella foenum-graceum | 527.83 µg/L 2 | [160] |
Bacillus cereus | 156.33 µg/L 2 | ||||
Galanthamine | Treatment of Alzheimer’s disease | Paenibacillus lautus | Leucojum aestivum | 37.51 µg/g 1 | [161] |
Burkholderia graminis | Narcissus tazetta | 37.8 µg/L 2 | [162] | ||
Bacillus thuringiensis | 61.0 µg/L 2 | ||||
Ginsenoside Rg3 | Antioxidant, antidiabetic, antineoplastic agent, apoptosis inducer | Burkholderia sp. | Panax ginseng | ND | [93] |
Agrobacterium sp. (PDA-2) | 62.20 mg/L 2 | [94] | |||
Harmine | Anti-inflammatory, anti-tumor, hallucinogen | Microbacterium maritypicum | Ephedra foliata | ND | [157] |
Ligustrazine | Anti-inflammatory, nootropic | Bacillus subtilis | Ligusticum chuanxiong | 1.0268 mg/L 2 | [163] |
Lycorine | Anticancer | Paenibacillus lautus | Leucojum aestivum | 37.51 µg/g 1 | [163] |
Maytansine | Antimicrobial, antineoplastic | Unidentified | Putterlickia retrospinosa | ND | [164] |
Putterlickia verrucosa | |||||
Myricetin | Antioxidant, anti-inflammatory, antithrombotic, antidiabetic, neuroprotective | Microbacterium maritypicum | Ephedra foliata | ND | [157] |
Oxylipins | Antibiotic | Bacillus sp. | Alternanthera brasiliana | ND | [165] |
Taxol (paclitaxel) | Chemotherapy drug | Kitasatospora sp. | Taxus baccata | ND | [166] |
Sanguinarine | Antibiotic, anticancer | Paenibacillus polymyxa | Ephedra foliata | ND | [157] |
Vindoline | Antimitotic, precursor for vinblastine | Microbacterium sp. | Catharanthus roseus | 82 ug/L 2 | [167] |
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Rutkowska, N.; Drożdżyński, P.; Ryngajłło, M.; Marchut-Mikołajczyk, O. Plants as the Extended Phenotype of Endophytes—The Actual Source of Bioactive Compounds. Int. J. Mol. Sci. 2023, 24, 10096. https://doi.org/10.3390/ijms241210096
Rutkowska N, Drożdżyński P, Ryngajłło M, Marchut-Mikołajczyk O. Plants as the Extended Phenotype of Endophytes—The Actual Source of Bioactive Compounds. International Journal of Molecular Sciences. 2023; 24(12):10096. https://doi.org/10.3390/ijms241210096
Chicago/Turabian StyleRutkowska, Natalia, Piotr Drożdżyński, Małgorzata Ryngajłło, and Olga Marchut-Mikołajczyk. 2023. "Plants as the Extended Phenotype of Endophytes—The Actual Source of Bioactive Compounds" International Journal of Molecular Sciences 24, no. 12: 10096. https://doi.org/10.3390/ijms241210096