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Review

Patents on Endophytic Fungi for Agriculture and Bio- and Phytoremediation Applications

by
Humberto E. Ortega
1,2,
Daniel Torres-Mendoza
1,3 and
Luis Cubilla-Rios
1,*
1
Laboratory of Tropical Bioorganic Chemistry, Faculty of Natural, Exact Sciences and Technology, University of Panama, Panama 0824, Panama
2
Department of Organic Chemistry, Faculty of Natural, Exact Sciences and Technology, University of Panama, Panama 0824, Panama
3
Vicerrectoría de Investigación y Postgrado, University of Panama, Panama 0824, Panama
*
Author to whom correspondence should be addressed.
Microorganisms 2020, 8(8), 1237; https://doi.org/10.3390/microorganisms8081237
Submission received: 7 June 2020 / Revised: 3 July 2020 / Accepted: 7 July 2020 / Published: 14 August 2020
(This article belongs to the Section Microbial Biotechnology)
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Abstract

:
Plant endophytic fungi spend all or part of their lives inside host tissues without causing disease symptoms. They can colonize the plant to protect against predators, pathogens and abiotic stresses generated by drought, salinity, high concentrations of heavy metals, UV radiation and temperature fluctuations. They can also promote plant growth through the biosynthesis of phytohormones and nutrient acquisition. In recent years, the study of endophytic fungi for biological control of plant diseases and pests has been intensified to try to reduce the ecological and public health impacts due the use of chemicals and the emergence of fungicide resistance. In this review, we examine 185 patents related to endophytic fungi (from January 1988 to December 2019) and discuss their applicability for abiotic stress tolerance and growth promotion of plants, as agents for biocontrol of herbivores and plant pathogens and bio- and phytoremediation applications.

Graphical Abstract

1. Introduction

An endophytic fungus is any organism inhabiting plant organs that, at certain point in its lifetime, can colonize tissues without causing apparent harm [1]. Endophytic fungi have been a proven source of secondary metabolites with potential uses as anticancer, antibiotics, antivirals, anti-inflammatories, antioxidants, neuroprotective agents, insecticides and antifungals, and have multiple applications in biotechnological developments in pharmaceutical, agriculture, cosmetic, food industry and environmental processes [2]. In the last decades, studies of endophytic fungi have resulted in a number of patents linked to the production of biologically active secondary metabolites and in biotransformation processes [3].
Moreover, interaction between fungi and their hosts drives changes in the host metabolism, altering the response to environmental stress and predator attack. Additionally, this interaction leads to the production of secondary metabolites by both the fungi and the host, which further enhance the capability to respond to the environment [4,5,6,7].
The use of endophytic fungi for environmental applications such as growth promotion, relief of abiotic stress, biocontrol of pest and plant pathogens and bio/phytoremediation has gained important attention in recent years due to the concern about global climate change and contamination in soils and natural sources that increases stress in crops, limiting and reducing the production [8,9,10,11]. Furthermore, basic and applied research has been conducted to develop processes, methodologies and technologies that resulted in a considerable number of patents with new proposals to overcome some of these challenges. Therefore, in this review, we cover patents on endophytic fungi applications related to (a) abiotic stress tolerance and growth promotion of plants; (b) biocontrol of herbivores and plant pathogens; (c) bio- or phytoremediation.
The highlighted topics in each of the patents, cited here, could inspire other researchers to take their investigation to the next level and contribute to overcome, in a more efficient way, some of the principal challenges of humanity today.

2. Materials and Methods

The present review was conducted mainly through searches in the Scifinder® and Google Patents databases. The search was initially conducted in Scifinder® using the terms “endophytic fungi” and “patents” covering the period from 1988 to 2019. 12,315 references were found. After removing duplicates (those describing the same patent/endophyte), we selected those related to the aim of this review, resulting in 185 documents. The patents covered in this study are described in five tables below.

3. Results

The description and analysis of patents was divided, considering the main objective of each one, into four sections; those associated to: (Section 3.1) abiotic stress tolerance and growth promotion of plants; (Section 3.2) biocontrol of herbivores and plant pathogens, and (Section 3.3) bio- and phytoremediation applications; (Section 3.4) patents where the endophyte has multiple applications. The information in tables describe the fungi, the host plant where they were isolated, and the main application of the patent. All endophytes, listed in the tables, have beneficial effects on plants, even though some of them could be considered as pathogens in previous reports.

3.1. Abiotic Stress Tolerance and Growth Promotion of Plants

The principal abiotic stress factors in plants include drought, salinity, high heavy metal concentrations, UV radiation and temperature fluctuations [12]. Abiotic stress affects the cellular pathways of plants, resulting in negative changes to their physiology and morphology [12]. Endophytic fungi have been shown to help their host plant to overcome abiotic stress and promote plant growth through the biosynthesis of phytohormones (indole-3-acetic-acid, gibberellins, cytokinins, ethylene, acetoin, 2, 3-butanediol) and nutrient absorption and uptake [12,13,14].
Plant endophytic fungi have been patented based on their ability to improve the following in plants: (a) root and seed development; (b) nutrient uptake or absorption; (c) photosynthesis promotion; (d) growth of biomass; (e) increase chlorophyll content; and (f) abiotic stress resistance. Numerous genera have been used for such purposes, including Acremonium, Alternaria, Aspergillus, Chaetomium, Fusarium, Penicillium, and others (Table 1 and Table 2). A specific area of application for which endophytic fungi have been widely used is in the growth promotion of medicinal plants; this includes such species as Acanthopanax senticosus [15], Salvia miltiorrhiza [16], Rumex gmelinii Turcz [17], Acacia confusa [18], Coix lacryma-jobi [19], Cynanchum acuminata [20], Huperzia serrata [21], Anoectochilus roxburghii [22], Arnebia sp. [23], Saussurea sp. [24], Rhizoma bletillae [25], Salvia miltiorrhiza [26,27], and Eucalyptus sp. [28,29,30]. Additionally, some endophytic fungi have been patented due to their capability to promote the growth of crop plants such as corn, tomato, soybean, rice, wheat, potato, and barley [31,32,33,34,35,36,37] as well as other useful plants such as Casuarina equisetifolia [38,39,40,41], fir [42,43,44,45], Aleurites montana [46,47,48,49,50,51], Dendrobium sp. [52,53,54], tobacco [55,56,57,58], Schima superba [59,60,61], Bletilla striata [62,63], and Paphiopedilum sp. [64].

3.2. Biocontrol of Herbivores and Plant Pathogens

Crop plant diseases represent a major threat in agriculture [101]. The number of chemicals that can be effectively used to control pathogens has been reduced due to the emergence of fungicide resistance along with an increased awareness of the negative associated ecological and public health impacts [101]. Due to these problems, study of the biological control of plant diseases with endophytes has intensified in recent years [101]. Endophytes have been shown to protect their hosts against diseases, reducing infection levels and inhibiting the growth of pathogens [102,103]. The proposed mechanisms used by endophytes are the production of antimicrobial and structural compounds, niche competition, and the induction of plant immunity [104].
Several patents describe the biocontrol of herbivores and plant pathogens using endophytic fungi (Table 3). Species of the genus Acremonium have been described to control Verticillium wilt [105]; Argentine stem weevil (Listronotus bonariensis) [106]; plant diseases caused by banana root nematode and different pathogenic microbes such as Bipolaris oryzae, Colletotrichum falcatum, Colletotrichum gloeosporioides, Corynespora cassiicola, Corynespora sp., Drechslera sp., Fusarium oxysporum, Gloeosporium musarum, and Magnaporthe grisea [107]; and to prevent fescue toxicosis [108]. Species of Alternaria can control the growth of different pathogens such as Rhizoctonia solani, Fusarium oxysporum, Botrytis cinerea, Phytophthora capsici, Pseudomonas aeruginosa, Proteus hauseri, and Plasmopara viticola [109,110,111,112,113,114,115]. Members of the genus Aspergillus have been applied to limit the growth of nematodes in soil [116]; the plant pathogenic fungi Sclerotinia sclerotiorum, Rhizoctonia solani, and Thanatephorus cucumeris [52,117,118]; as well as grass fungi [119]. Several strains of the genus Chaetomium have been reported to enhance plant disease resistance in Anoectochilus roxburghii cultivation [16], to control different plant pathogenic fungi [120,121,122], to inhibit Erwinia causing soft rot and Ralstonia solanacearum causing bacterial wilt [123], to inhibit anthracnose apple pathogens [124], in the preparation of an anti-plant pathogen fermentation liquid broth [125], and in the production of chaetoglobosin A with antagonistic activity against Exserohilum turcicum, Coniothyrium diplodiella, and Rhizopus stolonifer [126]. Species of Fusarium can prevent and treat black spot and fungal diseases in Panax notoginseng [127,128], control five plant pathogenic fungi (Fusarium oxysporum, Cytospora mandshurica, Colletotrichum gloeosporioides, Venturia pyrina, and Fusarium graminearum) [129], and control rice blast disease [130,131] and bacterial wilt of ginger [132]. Species of Neotyphodium can decrease the mildewing rate of Elymus sibiricus seeds at the germination stage [133] and improve fungicide and pest resistance in plants [134,135]. Species of Penicillium can restrain the effects of Panax notoginseng anthracnose, root rot [136,137,138], and Alternaria panax [139]; control different harmful pathogenic fungi [140,141] and litchi downy blight [142]; and prevent plant diseases such as Sclerotinia rot of colza and tobacco blackleg [53]. Species of Rhexocercosporidium can control the fungal pathogens Colletotrichum gloeosporioides, Fusarium solani, and Alternaria panax Whetzel on Panax notoginseng [143,144,145].
Endophytic fungi of different genera such as Beauveria, Cladosporium, Metarhizium, Muscodor, Trichoderma, and others have also been described in patents to control pests or different plant diseases (Table 3).

3.3. Bio- and Phytoremediation

Bioremediation is a process that uses microorganisms, plants or enzymes to detoxify contamination in natural sources. In phytoremediation, plants and their own metabolic system can extract toxic chemicals from water, soil and air. This chemicals or contaminants include metals and metalloid pollutants, carcinogenic agents, industrial organic waste material, inorganic pesticides and herbicides, chlorinated products, excess nutrients and radionuclides [10,11,192].
Endophytic fungi have the capability to degrade small and large organic compounds by enzymatic reactions, decompose environmental contaminants, and improve the soil microenvironment [193]. They can also increase the ability of host plants to remove contaminants from soil, water, sediment, and air [194], and to modulate morphological and physiological functions in the host plant improving its resistance to metals and providing different detoxification routes such as extracellular scavenging and complexation, compartmentalization and volatilization [14,195]. Figure 1 shows different bioremediation techniques involving endophytic fungi.
Some patents describe the use of endophytic fungi for bioremediation and phytoremediation (Table 4). Strains of the genus Fusarium have been reported to induce phytoremediation in heavy metal-contaminated soil [196], repair uranium-polluted water bodies [197], and decontaminate and decompose human and animal waste [198]. Additionally, the endophytic fungi Y2R14 and RWDL4-1 can be used to treat wastewater polluted by cadmium [199]. Heavy metals such as mercury, cadmium, arsenic, chromium, and lead are toxic at low concentrations. They can be accumulated in the ecosystem inside living organisms and are capable of entering the food chain [200]. The functions of several organs of the human body can be affected by heavy metals, and some of these substances can cause cancer by long-term exposure [200]. Uranium is a radioactive substance and is also harmful for the environment and human beings [197]. The use of microorganisms to repair large areas of farmland pollution can reduce costs, the use of large amounts of chemicals, and secondary pollution [196].
Species of Phomopsis and Xylaria have been reported to degrade the herbicide MCPA (2-methyl-4-chlorophenoxyacetic acid) in water and soil [201,202]. Additionally, several genera of fungi can be used to produce high-laccase content for soil bioremediation [203].

3.4. Patents that Claim Multiple Applications

A small number of patents comprised more than one possible application (Table 5); this is the case of the applications for Neotyphodium uncinatum to induce insect resistant and drought tolerance in plants [204]; Phoma sp. can improve salt stress resistance, promote the growth and increase biomass in crop plants such as wheat and rice [205]; Clonostachys rosea promotes plant growth, stress resistance and reduces dependency on chemical pesticides [206,207]; Fusarium sp. stimulates plant growth and reduces heavy metal absorption in tobacco [208], and Rhizoctonia sp. fosters plant growth and stress resistance in Anoectochilus roxburghii [22].
We found two patents, whose applications implicated the use a plural number of fungi (genus/species); one of them claims the capability to increase biomass and promote biotic and abiotic stress resistance in cereal crops [37], the other claims to improve dry shoot weight, mean dry grain weight and suppression of seed-borne in cereal crops [35].

4. Discussion

In the present review, we highlight a wide number of endophytic fungi that have been patented for developing processes, methodologies, or new techniques in applications that include but are not restricted to (a) alternatives to overcome biotic and abiotic stress and to reduce the use of chemicals associated with environmental toxicity in agricultural practices, (b) the degradation of harmful compounds, and (c) improvement in the ability of plants to remove contaminants from soil, water, and air. Abiotic stress tolerance and growth promotion of plants, and biocontrol of herbivores and plant pathogens, were the most patentable applications of endophytic fungi with 88 and 90 patents, respectively; concerning bio- and phytoremediation, 7 patents were recorded for the period 1988–2019 (Figure 2). The most representative genera of these applications belong to Alternaria, Aspergillus, Chaetomium, Fusarium, Penicillium and Muscodor.
Studies of endophytic fungi ecology have allowed the understanding of the multiple interactions they develop with their host, other endophytes, as well with herbivores and pathogens that put the host under abiotic stress. Nonetheless, it is evident that one individual or group of endophytes can be used for mitigation stresses from different origins. Due to the concerns about global climate change and its implications in food security, there are an increased interest to develop applications for the use of endophytic fungi in abiotic stress tolerance and growth promotion of important food crops [209], as well as the use for biocontrol of herbivores and plant pathogens. This increment can be noted since 2011 as shown in Figure 3. The loss of growing areas due to contamination and the recovery of spaces contaminated by heavy metals, organic and inorganic compounds will lead the focus of research on endophytic fungi for bio- and phytoremediation applications.
Considering the abundance of endophytic fungi under study, the development of patentable applications like those reviewed here, and other applications still unexplored like fungal pigments [210], has become a prominent research area for this class of microorganisms.

Future Perspectives

The use of endophytic fungi to improve the nutrients absorption in plants can change the optimum usage of organic and inorganic fertilizers [211]. The capability of endophytic fungi to increase biotic and abiotic stress tolerance in plant hosts is an unexplored area for agricultural purposes; the control of pests and diseases under climate change conditions [211]; studies in fungal species related to develop resistance to changes in their environment could lead their application in food production in limited resources areas and as an important alternative for crop production for human sustainability. Many endophytes are now often recognized as symbionts with unique and intimate interactions with the plant host [10]. The genetic engineering of fungi is an easier process than in plants. The genetic modification of endophytic fungi with useful genes could contribute, with new traits, to the inoculation of plants [212].
The use of endophytic fungi on remediation of contaminated ecosystems is an interesting prospect for further studies. Fungi that could increase the capacity of CO2 absorption by plants, degradation and biotransformation of waste, enhance food production without altering its quality or those that provided drought resistance/nutrient absorption capability to plant species related to human or animal feeding could be areas of significance to develop new applications and patents. The investigations applied in these fields are forwarded by the advance in the techniques used for the characterization of endophytic fungi and also by the technological advances in analytical techniques for carrying out studies of chemical processes at the cellular level.

Supplementary Materials

The following are available online at https://www.mdpi.com/2076-2607/8/8/1237/s1, Table S1: List of patens grounded in the use of several endophytic fungi to develop applications.

Author Contributions

H.E.O. and D.T.-M. performed the data search and organized and analyzed the data, visualized and wrote the manuscript; L.C.-R. conceptualized, visualized, supervised, wrote and reviewed the manuscript. All authors read and approved the final manuscript.

Funding

This project was supported by the National System of Research (SNI) and the National Secretariat for Science and Technology of Panama (SENACYT).

Acknowledgments

The authors want to thank University of Sao Paulo, Brazil, for granted access to “Portal de Periodicos CAPES/MEC” and to Phyllis D. Coley for critical review of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Microorganisms 08 01237 g001 550
Figure 1. Bio- and phytoremediation approaches involving endophytic fungi.
Figure 1. Bio- and phytoremediation approaches involving endophytic fungi.
Microorganisms 08 01237 g001
Microorganisms 08 01237 g002 550
Figure 2. Total number of patents for area of application in the period 1988 to 2019.
Figure 2. Total number of patents for area of application in the period 1988 to 2019.
Microorganisms 08 01237 g002
Microorganisms 08 01237 g003 550
Figure 3. Patents of endophytic fungi for agricultural purposes and bio/phytoremediation registered from 1988 to 2019.
Figure 3. Patents of endophytic fungi for agricultural purposes and bio/phytoremediation registered from 1988 to 2019.
Microorganisms 08 01237 g003
Table
Table 1. Endophytic fungi applied to enhance the abiotic stress tolerance of plants.
Table 1. Endophytic fungi applied to enhance the abiotic stress tolerance of plants.
Patent No.EndophyteHost 1Patent ApplicationRef.
CN104762216AArthrinium sp.Salicornia bigeloviiPlant anti-salt stress.[65]
WO2004000017A2Curvularia sp.Dichanthelium languinosumConferring stress tolerance to inoculated plants (monocots and dicots).[66]
WO2009012480A2Fusarium sp.Leymus mollisConferring stress tolerance to inoculated plants (monocots and dicots).[67]
CN105296359ALecanicillium sp.TobaccoReducing the absorption of heavy metals in tobacco.[58]
CN101314760ANeotyphodium chisosumFestuca arundinaceaImproving the stress tolerance to drought and diseases.[68]
CN104004665APapulospora sp.Fir rootsRelieving phosphorus stress in fir.[43]
CN105002099AParaconiothyrium cyclothyrioidesMyricaria rootReducing heavy metal pollution in plants.[69]
CN101974437APenicillium sp.EucalyptusRelieving aluminum toxicity in Eucalyptus.[30]
CN102002463APenicillium sp.Eucalyptus roots, stems, and leavesImproving the cold resistance of Eucalyptus.[28]
CN103865806APhialophora oryzaeNot disclosedReducing the absorption of heavy metals in tobacco[57]
CN107926549APiriformospora indicaNot disclosedImproving the resistance of plants to the herbicide bensulfuron-methyl.[70]
CN103834578APyrenochaeta sp.TobaccoPromoting plant growth and reducing the heavy metal content in tobacco.[55]
CN105316240ARhizopycnis sp.TobaccoReducing the absorption of heavy metals in tobacco.[56]
US20150366217A1Group of several fungi 2Roots of Triticum turgidum L.Improving seed vitality, biotic and abiotic stress resistance, and plant health and yield under both stressed and unstressed environmental conditions.[71]
1 Some patents just provided a common name for the host organism. 2 A list of the group of fungi is in Table S1.
Table
Table 2. Endophytic fungi applied for the growth promotion of plants.
Table 2. Endophytic fungi applied for the growth promotion of plants.
Patent No.EndophyteHost 1Patent ApplicationRef.
CN105907648AAcremonium sp.Panax notoginsengRoot and seed development of different plants including Radix Ginseng, Oryza sativa L., Semen Maydis, Semen Tritici aestivi, Rhizoma Paridis, Rhizoma Solani tuberosi, etc.[34]
CN108513990AAlternaria alternataAcanthopanax senticosusSeedling-stage growth of A. senticosus.[15]
CN104911108AAlternaria sp.Hippophae sp.Drought resistance on turf grass.[72]
CN104818218AAlternaria sp.Aleurites montanaPhosphorus uptake in A. montana.[47]
CN102086439AAlternaria tenuissimaPanax ginsengGrowth of corn plant.[31]
CN103173362AAspergillus sp.Casuarina sp. rhizospherePhotosynthesis in C. equisetifolia.[38]
CN103173361AAspergillus sp.Casuarina sp. rhizosphereNutrient element absorption in Casuarina.[39]
CN103173364AAspergillus sp.Casuarina sp. rhizosphereCasuarina biomass growth.[41]
CN110343619ABotryosphaeria sp.Root of Schima superbaSchima superba seedling height and ground diameter under a low-phosphorus environment.[61]
CN109456902AByssochlamys spectabilisRhizoma bletillaeThe growth of R. bletillae.[25]
CN106929436ACercosporella Sacc.Rumex gmelini TurczGrowth in R. gmelinii Turcz.[17]
CN106801014AChaetomium globosumSalvia miltiorrhizaRadix root biomass, plant height, crown diameter in S. miltiorrhiza.[73]
CN109628322AChaetomium nigricolorBletilla striataThe growth of B. striata.[62]
CN110438011ACladosporium tenuissimumSalvia miltiorrhizaSynthesis of effective components (tanshinone and salvianolic acid substances) in the root system of Salvia miltiorrhiza.[26]
CN104630073AClaviceps sp.Dendrobium officinaleGrowth and yield in D. officinale.[74]
CN104004664AColletotrichum sp.Abies sp. rootsPhotosynthesis of cedar.[45]
CN106085872AColletotrichum sp./Fusarium sp.Acacia sp.Nutrient absorption in A. confusa.[18]
CN104805019AConiothyrium sp.Aleurites sp.Nutrient element absorption in wood oil tree.[75]
CN104004666ACylindrocarpon sp.fir plantGrowth of fir.[42]
CN110250210ADarksidea sp.Stipa capillata rootRooting and growth of maize.[36]
CN109504611ADiaporthe spectabilisBletilla striataGrowth of B. striata.[63]
CN103733829AEmericella foeniculicolaSalvia miltiorrhizaeGrowth of S. miltiorrhizae.[76]
CN105624047AEpichloë bromicolaCoix lacryma-jobiGrowth of Coix lacryma-jobi, Arabidopsis thaliana and other graminaceous plants.[19]
CN105861334AFilobasidium sp.Acacia sp.Taiwan Acacia biomass.[77]
CN105861335AFilobasidium sp.Acacia sp.Nutrient element absorption in Taiwan Acacia in a low-phosphorous environment.[78]
CN106085873AFilobasidium sp./Penicillium sp.Acacia sp.Phosphorous uptake in A. confusa under a low-phosphorus environment.[79]
CN107432135AFusarium redolensNot disclosedGermination of Cynanchum acuminata seeds.[20]
CN103173360AFusarium sp.Casuarina equisetifoliaChlorophyll content of C. equisetifolia.[80]
CN110257259AFusarium sp.Schima superba stemsPhotosynthesis of Schima superba.[59]
CN103114044AHeterodera oryzaericePlant growth regulation and/or plant pathogenicity.[81]
CN103798293AHypha sp.Salvia miltiorrhizaThe growth and improvement of S. miltiorrhiza hairy root tanshinone content.[82]
CN1961631AMycocentrospora sp./Leptodontidium sp.Saussurea involucrataSaussurea sp. growth.[24]
CN104593274ANectria sp.Dendrobium officinaleYield in Dendrobium artificial planting.[83]
US20130104263A1Neotyphodium sp.perennial ryegrassBeneficial properties (phenotype) for plant.[84]
CN104004667APaecilomyces sp.Not disclosedPhosphorus absorption in fir.[44]
CN106010984APenicillium sp.Acacia confusaPlant biomass growth of Taiwan Acacia plant under low-phosphorus environment.[85]
CN101974438APenicillium sp.EucalyptusPhosphorus absorption in Eucalyptus.[29]
CN104818219APenicillium sp.Aleurites montanaRoot growth of A. montana in a low-phosphorous environment.[51]
CN104789481APenicillium sp.Aleurites montanaGrowth and photosynthesis enhancement of A. montana in a low-phosphorus environment.[48]
CN104762219APenicillium sp.Aleurites montanaBiomass growth of A. montana in a low-phosphorus environment.[49]
CN110257258APenicillium sp.Schima superba leavesPhosphorus absorption of Schima superba.[60]
WO2016210238A1Penicillium sp.Not disclosedCultivation of agricultural plants, such as soybean and maize.[33]
CN104818217APestalotia sp.Not disclosedBiomass growth of A. montana.[50]
CN105886405APestalotiopsis sp.Dendrobium officinaleGrowth of D. officinale and change in metabolic components.[54]
CN107988087APezicula ericaewild blueberry rootGrowth effects.[86]
CN109706084APhoma herbarumSalvia miltiorrhizaGrowth of Salvia miltiorrhiza and synthesis of tanshinone compounds.[27]
CN104593273APhyllachora sp.Dendrobium officinaleDendrobium yield.[87]
CN103173363APhyllosticta sp.Casuarina sp.Photosynthesis of C. equisetifolia.[40]
ES2500790A1Pochonia chlamydosporiaNot disclosedFlowering and fruiting and increased yield in crops such as tomatoes.[32]
WO2016038234A1Pochonia chlamydosporiaMeloidogyne spp.Culture yield and reduction in flowering and fructification times.[88]
CN105039172APythium sp.Huperzia serrataImproved transplant survival rate of H. serrate.[21]
CN108041078ARhizopycnis sp.tobaccoRice growth.[89]
WO2019113255A1Serendipita vermifera ssp. besciiAustralian orchidEnhancement of plant performance in combination with phosphite as a phosphorous source.[90]
CN105420119ASchizophyllum communeGinsengHost tissue culture hairy root biomass and ingredients of ginseng saponins.[91]
CN104774771AThermomyces sp.Not disclosedPhotosynthesis of A. montana under a low-phosphorus environment.[46]
CN107046965ATrichoderma sp.Anoectochilus formosanusSeedling adaptation cultivation.[92]
CN104745482ATrichoderma sp.Arnebia euchromaGrowth of Arnebia hairy roots and improved shikonin component content in hairy roots.[23]
CN105969672ATrichoderma sp. Fusarium sp.Acacia sp.Increase in the height and ground diameter of A. confusa seedlings.[93]
CN110408551ATulasnella calosporaRoots of PaphiopedilumGrowth of aseptic seedlings of Paphiopedilum.[64]
CN102876584AXylaria striataOryza meyerianaPlant growth.[94]
CN107460133AZasmidium sp.mangroveGrowth and development of D. officinale.[95]
WO2016179047A1Group of fungiNot disclosedAgronomic traits in plants.[96]
CZ306950B6Group of fungiMiscanthus sp.Growth, especially of graminaceous and Miscanthus plants.[97]
WO2017134664A1Acremonium sclerotigenum/Sarocladium implicatumSet of grass relatives of wheatNutrient uptake.[98]
US20150373993A1Group of several 2 fungiA diverse type of wild relatives or ancestral landraces of maize, wheat, rice, and other seedsAgronomic traits.[99]
WO2018102733A1Group of several 2 fungiAgricultural plantsModulation of the nutritional quality traits in seeds[100]
1 Some patents just provided a common name for the host organism. 2 A list of the group of fungi is in Table S1.
Table
Table 3. Endophytic fungi applied as biocontrol agents of herbivores and plant pathogens.
Table 3. Endophytic fungi applied as biocontrol agents of herbivores and plant pathogens.
Patent No.EndophyteHost 1Patent ApplicationRef.
CN103897992AAcremonium alternatumcottonVerticillium wilt.[105]
US93951A0Acremonium coenophialumNot disclosedFescue toxicosis.[108]
AU639084B2Acremonium loliiFrench perennial ryegrass ecotypeArgentine stem weevil (Listronotus bonariensis) by production of compound peramine.[106]
CN101235355AAcremonium strictumBrachiaria brizanthaBanana root-knot nematode and different pathogenic microbes.[107]
WO2012174585A1Acremonium sp.Brachiaria/UrochloaFungal plant diseases.[146]
CN108192832AAcrocalymma sp.Sinomenium acutumPlant diseases caused by pathogenic bacteria.[147]
CN108085259AArcopilus aureusDendrobium sp.The plant pathogenic fungus Botrytis cinerea.[148]
CN102204570AAlternaria alternataCinnamomum camphoraRhizoctonia solani, Fusarium oxysporum, and Botrytis cinerea.[111]
CN102191184AAlternaria alternataCinnamomum camphoraPlant pathogenic fungi such as Rhizoctonia solani, Fusarium oxysporum, and Botrytis cinerea.[110]
CN110373331AAlternaria alternataHuperzia serrataGray mold of crops.[115]
ES2696982A1Alternaria alternata and Fusarium acuminatumArtemisia thuscula and Austrian ArtemisiaPlant pathogenic fungi with the production of antifungal compounds.[114]
CN103232942AAlternaria sp.Spiraea sp.The plant pathogenic fungus Phytophthora capsici.[112]
CN106520572AAlternaria maliToona sinensisThe pathogens Pseudomonas aeruginosa or Proteus hauseri.[113]
WO2008007251A2Alternaria alternataNot disclosedPlasmopara viticola.[109]
CN108441426AAspergillus nigerAquatic plantPlant parasitic nematodes in soil.[116]
CN104560735AAspergillus oryzaeTephrosia purpureaPlant pathogenic fungi such as Sclerotinia rot of colza and tobacco black shank disease.[52]
CN102191185AAspergillus restrictusAllium sativumPlant pathogenic fungi such as Rhizoctonia solani and Thanatephorus cucumeris.[117]
CN109504610AAspergillus sp.EpiphyteThe pathogenic fungus rhizoctonia solani.[118]
CN108342328AAspergillus versicolorseaweedGrass fungi.[119]
US8709399B2Beauveria bassianamaize stem borer Busseola fuscaHerbivorous insects and/or plant pathogens.[149]
CN105462892ABurkholderia sp.Sophora tonkinensisPanax notoginseng black spot.[150]
CN105838613AChaetomium globosumCajanus cajanFungal plant diseases with the production of flavipin.[151]
CN107475123AChaetomium globosumAnoectochilus roxburghiiPlant disease in Anoectochilus roxburghii cultivation.[16]
CN102742605AChaetomium globosumGinkgo bilobaPlant pathogenic fungi.[122]
CN102690759AChaetomium globosumSolidago canadensisPlant pathogenic fungi propagation[121]
CN101280320AChaetomium globosumNot disclosedPlant fungal diseases with the production of antibiotic substances[120]
CN106754396AChaetomium globosumToona sinensisErwinia and Ralstonia solanacearum[123]
CN104877919AChaetomium globosumPhellopterus littoralisAnthracnose pathogens of apples and certain inhibitory actions against other plant pathogens[124]
CN103255065AChaetomium globosumCamptotheca acuminataPlant pathogens with broth culture of the endophytic fungi[125]
CN102754652AChaetomium globosumGinkgo bilobaExserohilum turcicum, Coniothyrium diplodiella, and Rhizopus stolonifer[126]
CN105368720AChaetomium sp.Healthy cotton plantCotton Verticillium wilt.[152]
CN109749938ACladosporium tenuissimumHealthy Panax notoginsengPanax notoginseng rot.[153]
CN110172408AClonostachys roseaPodophyllum hexandrumDiseases and pests of Podophyllum hexandrum.[154]
CN110272829AColletotrichum boninenseHuperzia serrataSclerotinia sclerotiorum of crops.[155]
WO2014136070A1EpichloëElymus mutabilisPests on Secale spp. plants.[156]
CN105483022AFusarium solaniSophora tonkinensisPanax notoginseng black spot.[127]
CN105483021AFusarium solaniSophora tonkinensisPanax notoginseng fungal diseases.[128]
CN103194490AFusarium solaniGinkgo bilobaFive plant pathogenic fungi.[129]
CN105087386AFusarium sp.Yinchuan Phragmites communisRice blast disease.[130]
CN108624527AFusarium sp.Ginkgo sp.Bacterial wilt in ginger.[132]
CN110558337AFusarium oxysporumGinkgo bilobaRice blast disease.[131]
CN102174416AFusella sp.Angelica sinensisPlant pathogenic bacteria.[157]
WO2016034751A1Guignardia mangiferaePersea indicaPhytopathogens and plant pests.[158]
WO2013081448A2Hendersonia sp.Not disclosedBasal stem rot disease and Ganoderma disease in oil palms.[159]
CN109536390AHypoxylon sp. novMidvein of citrus leavesCitrus black spot disease.[160]
CN103642704ALeptosphaeria sp.cottonCotton Verticillium wilt.[161]
CN103289906AMetarhizium sp.Gentiana manshuricaG. manshurica leaf blight.[162]
CN110229758AMortierella elongataAtractylodes macrocephalaAtractylodes macrocephala root rot.[163]
CN101691541AMuscodor sp.Not disclosedPathogenic fungi.[164]
US20040141955A1Muscodor albus and Muscodor roseusNot disclosedOrganisms such as microbes, insects, and nematodes with volatile compounds.[165]
WO2002082898A1Muscodor albus and Muscodor roseusNot disclosedPlant pathogens, bacteria, nematodes, and insects with volatile antibiotics.[166]
WO2010115156A2Muscodor strobeliiNot disclosedPests and pathogenic microbes, including Ganoderma boninense.[167]
WO2004034785A2Muscodor vitigenusPaullinia paullinioidesInsects with the production of repellents by a novel endophytic fungus.[168]
CN106893678AMyrothecium verrucariagrapesGrape gray mold.[169]
CN104774768ANectria haematococcaFritillaria wabuensisBacteria such as S. aureus and P. aeruginosa and pathogenic fungi.[170]
CN106538108ANeotyphodium sp.gramineous plantsMildewing rate of Elymus sibiricus seeds in the germination stage.[133]
WO2007021200A1Neotyphodium sp.Not disclosedPlant pathogenic fungi.[134]
CA2319847CNeotyphodium sp.Festuca arundinaceaPests and reduce ergopeptine alkaloid levels.[135]
CN102191186ANigrospora oryzaeAllium sativumPlant pathogenic fungi such as Rhizoctonia solani, Colletotrichum lindemuthianum, and Botrytis cinerea.[171]
CN104789482ANigrospora sp.Magnolia officinalisWheat disease.[172]
CN110178857APaecilomyces variotiiHippophae rhamnoidesPlant virus. Induces plant endogenous salicylic acid accumulation and enhances the plant RNA silencing efficiency.[173]
CN105462854APenicillium citrinumSophora tonkinensisPanax notoginseng anthracnose.[136]
CN105462850APenicillium citrinumSophora tonkinensisPanax notoginseng root rot.[137]
CN105462855APenicillium citrinumSophora tonkinensis GagnepAlternaria panax.[139]
CN104531543APenicillium griseofulvumTephrosia purpureaPlant diseases such as Sclerotinia rot of colza, tobacco blackleg, and others with a fermentation product.[53]
CN105255742APenicillium sp.Malus hupehensisHarmful pathogens such as Fusarium solani, F. proliferatum, F. moniliforme, and F. oxysporum.[140]
CN108546651APenicillium sp.Kandelia candelPlant pathogenic fungi such as Fusarium graminearum, Phytophthora sojae, and Colletotrichum musae with a fermentation product.[141]
CN109112069APenicillium sp.Panax notoginseng rootPanax notoginseng root rot.[138]
CN103773699APenicillium purpurogenumLitchiLitchi downy blight.[142]
CN103627643APenicillium simplicissimumHealthy cotton plantCotton Verticillium wilt.[174]
CN104161049APestalotiopsis uvicolaArtemisia japonicaKiwifruit Sclerotinia sclerotiorum, Phytophthora capsici, and other plant pathogenic fungi with a fermentation product.[175]
CN110511878APezicula neosporulosaFirThe pathogenic fungus Fusarium oxysporum.[176]
CN109769535APhialophora oryzaeWild rice rootBacterial blight of rice.[177]
CN102154116APhomopsis wenchengensisNot disclosedPlant pathogenic fungi by antifungal compounds.[178]
CN105462853ARhexocercosporidium sp.Sophora tonkinensisColletotrichum gloeosporioides on Panax notoginseng.[143]
CN105462851ARhexocercosporidium sp.Sophora tonkinensisFusarium solani on Panax notoginseng.[144]
CN105462848ARhexocercosporidium sp.Sophora tonkinensisAlternaria panax Whetzel on Panax notoginseng.[145]
CN102234618ARhizopus and TrichodermaNot disclosedSoft rot disease of the orchid family Dendrobium plants.[179]
CN110452290ASarocladium brachiariaeBrachiaria brizanthaPlant disease and pests.[180]
CN110468057ASeimatosporium sp.Rosa multifloraTobacco powdery mildew caused by Erysiphe cichoracearum.[181]
CN106167767ASchizothecium sp.Not disclosedBanana wilt.[182]
CN110558336ASpirillum roseumNot disclosedLettuce sclerotinia rot.[183]
CN103834580ATalaromyces flavusNot disclosedCotton Verticillium wilt[184]
CN106119134ATalaromyces flavusNot disclosedFruit rot[185]
CN109593658ATalaromyces sp.Fructus corniFungal diseases of wheat[186]
CN105211105ATrichothecium roseumstrawberriesPowdery mildew of wheat[187]
US20120108425A1Trichoderma atroviridehealthy tea leavesFoliar disease in tea plantations caused by Cercospora theae[188]
CN108179115AZopfiella sp.Chrysanthemum morifoliumPlant pathogens such as Fusarium moniliforme, F. oxysporum, Curvularia lunata, and Pythium[189]
WO2018119419A1Group of several 2 fungicottonNematodes, aphids, flea hopper, lygus bug, stink bug, soy looper, cabbage looper, or fungi[190]
US9469836B2Not disclosedPinus strobusPests in Pinus strobus[191]
1 Some patents just provided a common name for the host organism. 2 A list of the group of fungi is in Table S1.
Table
Table 4. Endophytic fungi applied in bioremediation and phytoremediation.
Table 4. Endophytic fungi applied in bioremediation and phytoremediation.
Patent No.EndophyteHost 1Patent ApplicationRef.
CN105733958AFusarium oxysporumNot disclosedPhytoremediation of heavy metal-contaminated soil[196]
CN106340337AFusarium sp.mangroveRepair of uranium-polluted water body[197]
WO2005116272A2Fusarium culmorum and Muscodor albusNot disclosedDecontamination and decomposition of human and animal waste[198]
CN106947697APhomopsis sp.Not disclosedDegradation of the herbicide MCPA (2-methyl-4-chlorophenoxyacetic acid) in water or soil[201]
CN107177511AXylaria sp.Not disclosedDegradation of the herbicide MCPA in water and soil[202]
CN107900098AGroup of several fungi 2Not disclosedProduction and application of a high-laccase content soil remediation agent[203]
CN108751424ANot disclosedwild soybeanTreatment of wastewater polluted by the heavy metal cadmium[199]
1 Some patents just provided a common name for the host organism. 2 A list of the group of fungi is in Table S1.
Table
Table 5. Patents that claim multiple applications.
Table 5. Patents that claim multiple applications.
Patent No.EndophyteHost 1Patent ApplicationRef.
WO2000062600A1Neotyphodium uncinatummeadow fescueImport desired traits: include no adverse effects on herbivore, insect resistance, drought tolerance and improved persistence in the plants.[204]
CN104293681APhoma sp.Not disclosedImproving salt stress resistance in rice and wheat.
Promotion of growth in rice seedling, delaying salt damage of wheat in saline and alkaline land.
Increasing biomass accumulation in wheat.		[205]
US20160007613A1Clonostachys roseaNot disclosedPromotion of plant vigor, health, growth, yield, and resistance to competitive stress.[206]
WO2007107000A1Clonostachys roseaNot disclosedEnhanced plant vigor, health, growth, yield, reducing environmental stress and reduction of dependency on chemical pesticides for pest control.[207]
CN103849572AFusarium sp.Not disclosedPromoting plant growth and reduction of heavy metal absorption in tobacco.[208]
CN101953261ARhizoctonia sp.Anoectochilus roxburghiiGrowth of A. roxburghii, improved the reproductive rate, survival rate and stress resistance.[22]
WO2019115582A1Group of several fungi 2Hordeum murinumIncreased yield and biomass in cereal crops, and promotes biotic and abiotic stress resistance in cereal crops[37]
WO2016030535A1Group of several fungi2Hordeum murinum subsp. murinumImproving dry shoot weight, mean dry grain weight and suppression of seed-borne infection in a cereal crop.[35]
1 Some patents just provided a common name for the host organism. 2 A list of the group of fungi is in Table S1.

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MDPI and ACS Style

Ortega, H.E.; Torres-Mendoza, D.; Cubilla-Rios, L. Patents on Endophytic Fungi for Agriculture and Bio- and Phytoremediation Applications. Microorganisms 2020, 8, 1237. https://doi.org/10.3390/microorganisms8081237

AMA Style

Ortega HE, Torres-Mendoza D, Cubilla-Rios L. Patents on Endophytic Fungi for Agriculture and Bio- and Phytoremediation Applications. Microorganisms. 2020; 8(8):1237. https://doi.org/10.3390/microorganisms8081237

Chicago/Turabian Style

Ortega, Humberto E., Daniel Torres-Mendoza, and Luis Cubilla-Rios. 2020. "Patents on Endophytic Fungi for Agriculture and Bio- and Phytoremediation Applications" Microorganisms 8, no. 8: 1237. https://doi.org/10.3390/microorganisms8081237

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