Natural compounds: an effective and eco-friendly strategies for controlling and combating plant pathogens

Abstract

Currently, the management of phytopathogenic agents is an ongoing challenge globally, as they cause major damage in agricultural plantations. However, the use of synthetic pesticides currently in use has negative effects on the environment and on the living organisms that develop their life cycle in these habitats. For this reason, research in the last decade has led to the identification and exploitation of natural compounds with important antifungal properties as natural alternatives to combat and control pathogens. This review is based on the description of plant extracts, essential oils and natural compounds with important anti-fungal properties. However, their direct application to plants is difficult, because their adhesion and persistence in environmental conditions does not allow this fact. The current challenge is to develop formulations based on natural compounds that retain their properties over time in order to be applied to agricultural crops.

Full text

Received: 08 Nov 2022. Received in revised form: 20 Mar 2023. Accepted: 22 Mar 2023. Published online: 29 Mar 2023.
From Volume 49, Issue 1, 2021, Notulae Botanicae Horti Agrobotanici Cluj-Napoca journal uses article numbers in place of the
traditional method of continuous pagination through the volume. The journal will continue to appear quarterly, as before, with four
annual numbers.
Din A et al. (2023)
Notulae Botanicae Horti Agrobotanici Cluj-Napoca
Volume 51, Issue 1, Article number 12991
DOI:10.15835/nbha51112991
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Natural compounds: an effective and eco
Natural compounds: an effective and ecoNatural compounds: an effective and eco
Natural compounds: an effective and eco-
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-friendly strategies for
friendly strategies for friendly strategies for
friendly strategies for
controlling and combating plant pathogens
controlling and combating plant pathogenscontrolling and combating plant pathogens
controlling and combating plant pathogens
Alin DIN
1,2
*, Ion MITREA
1
, Rodi MITREA
1
1
University of Craiova, Faculty of Horticulture, 13 A.I. Cuza Street, Craiova, Dolj, Romania; din.alin96@yahoo.com (*corresponding
author); mitreaion@yahoo.com; rodimitrea@yahoo.com
2
National Research and Development Institute for Biotechnology in Horticulture Stefanesti Arges, Romania
Abstract
AbstractAbstract
Abstract
Currently, the management of phytopathogenic agents is an ongoing challenge globally, as they cause
major damage in agricultural plantations. However, the use of synthetic pesticides currently in use has negative
effects on the environment and on the living organisms that develop their life cycle in these habitats. For this
reason, research in the last decade has led to the identification and exploitation of natural compounds with
important antifungal properties as natural alternatives to combat and control pathogens. This review is based
on the description of plant extracts, essential oils and natural compounds with important anti-fungal
properties. However, their direct application to plants is difficult, because their adhesion and persistence in
environmental conditions does not allow this fact. The current challenge is to develop formulations based on
natural compounds that retain their properties over time in order to be applied to agricultural crops.
Keywords:
Keywords:Keywords:
Keywords: essential oils; natural compounds; plant protection; phytopathogens; plant extract
Introduction
IntroductionIntroduction
Introduction
Phytopathogenic fungi represents infectious agents of plants, producing changes in different stages of
plant development, even after harvesting during storage. There are numerous fungal species that cause serious
damage to agricultural products, because they affect the quality of fruits and vegetables (nutritional values,
organoleptic characteristics, etc.). More than 25% of cereals (wheat, corn, rice, etc.) are contaminated in most
cases by fungi belonging to the genera Fusarium and Aspergillus, which are indirectly responsible for the
production of alphatoxin B1, which is toxic and highly carcinogenic, as well as more than 300 fungal
metabolites, which can generate metabolic disorders or even poisoning. (Satish et al., 2007; Díaz-Dellavalle et
al., 2011; Lee et al., 2007). In the study by Stracquadanio et al. (2021), it was shown that natural extracts
obtained from Trichoderma asperellum and Trichoderma atroviride applied to tomatoes, wheat and maize,
reduced the production of ochratoxin A. In addition, the extracts reduced the production of mycotoxins in a
dose-dependent manner and with a long-lasting effect.
Plants are a rich source of different chemical compounds such as: alkaloids, flavones and flavonoids,
phenols, terpenes, tannins or quinones. Produced as secondary metabolites, they can constitute up to 30% of
the dry mass of plants, having an essential role in their protection against pathogens, abiotic stress factors, but
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Din A et al. (2023). Not Bot Horti Agrobo 51(1):12991
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also against herbivores. Due to their specific properties, plants have been used since ancient times for medicinal
purposes, but also as food additives. Nowadays, the recognition of the chemical structure and functions of
certain plant compounds allows us to extract and isolate them for use as ingredients in the cosmetic, food,
pharmaceutical, industries etc. There is also great interest in their application as biopesticides, fungicides and
insecticides to protect crop plants (Mazid et al., 2011; Bhagat et al., 2014).
The use of phytopreparations but also of essential oils represents the true means of perspective for the
biological protection of plants, having numerous advantages, such as: the use of these preparations has
demonstrated an effective impact on phytopathogens, the extraction is not complicated and long-lasting, does
not pose a danger to the environment and people, they decompose quickly in agrocenosis, also proving an
increased efficiency (Zarins et al., 2009). Studying of the effectiveness of plant extracts led to the premise that
they can be used as alternative bioformulations to the currently used synthetic fungicides, due to their
antifungal activities, the low level of toxicity for humans and the environment, but also biodegradation. (Du
Plooy et al., 2009; Tripathi and Dubey, 2004).
Plant extracts and essential oils
Plant extracts and essential oilsPlant extracts and essential oils
Plant extracts and essential oils
Algae extracts have been shown to be a possible substitute for synthetic pesticides, as demonstrated by
the study of Jiménez et al. (2011) who evaluated the antifungal potential of extracts from the brown alga
Lessonia trabeculata and observed that it reduced tomato leaf lesions following Botrytis cinerea infection. They
also observed that aqueous and ethanolic extracts of the red alga Gracillaria chilensis inhibited the growth of
Phytophthora cinnamomi. In addition, there are numerous studies that refer to the antifungal activity of brown
algae extracts against fungal species, Cladosporium herbarum, Botrytis cinerea, Cladosporium herbarum,
Phialophora cinerescens, Phoma tracheiphila, Sclerotinia sclerotiorum, Sclerotium rolfsii and Verticillium dahliae
being just a few species of fungi pathogens that showed sensitivity to algae extracts obtained from species
belonging to the Phaeophyceae class (Fenical and Sims, 1973; Moreau et al., 1988; Belattmania et al., 2016;
Esserti et al., 2017; Mohamed and Saber, 2019; Vicente et al., 2021). So, it was found that the potential of the
activities presented by the metabolites produced by seaweed is strongly influenced by both the environment
and the biological factors (Khaleafa et al., 1975; Ballantine et al., 1987; Robles-Centeno et al., 1996; Kumar et
al., 2000; Jiménez et al., 2011; Vicente et al., 2021). Ashwani et al. (2011) observed high efficacy of aqueous
extracts of Cannabis sativa, Parthenium hysterophorus, Urtica dioica, Polystichum squarrosum and Adiantum
venustum against five phytopathogens of high economic importance namely Alternaria solani on tomatoes,
Alternaria zinnia on Zinnia sp., Curvularia lunata on corn, Rhizoctonia solani on potatoes and Fusarium
oxysporum on tomatoes. Notable results were also obtained by Al-Rahmah et al. (2013) who evaluated the
antifungal potential of natural extracts obtained from Lantana camara, Salvadora persica, Thymus vulgaris,
Zingiber officinale and Ziziphus spina on phytopathogens found in tomatoes: Fusarium oxysporum, Pythium
aphanidermatum and Rhizoctonia solani. The extracts of Salvadora persica, Thymus vulgaris and Zingiber
officinale showed a good fungistatic action on the previously mentioned phytopathogenic fungi.
The antifungal properties of the extracts obtained from Ricinus communis and Chromolaena odorata
were tested by Nahunnaro and Bayaso (2012) against the fungus Alternaria solani, the results obtained being
encouraging in the biological control of this phytopathogen. Thyme essential oil is also known for its antifungal
effects, which is why Wu et al. (2011) tested the potential against the phytopathogen Alternaria alternata, the
inhibition percentage being over 60% at the concentration of 500 µL/L. Askarne et al. (2012) evaluated the
antifungal activity of 50 plant species collected in different regions of southern Morocco. Thus, it was
demonstrated that Anvillea radiata and Thymus leptobotrys completely inhibited the mycelial growth of the
pathogenic fungus Penicillium italicum at concentrations of 10%. Promising results were also obtained by Şesan

Din A et al. (2023). Not Bot Horti Agrobo 51(1):12991
3
et al. (2015) who evaluated the antifungal potential of natural extracts obtained from Achillea millefolium,
Allium sativum, Artemisia dracunculus 'Sativa', Hyssopus officinalis, Mentha sp., Rosmarinus officinalis, Satureja
hortensis, Tagetes patula, Valeriana officinalis. The extracts were used in three different concentrations namely
5%, 10% and 20%. The highest efficacy (100%) against the phytopathogen Botrytis cinerea was demonstrated
by the extract obtained from Hyssopus officinalis, at all three concentrations used, followed by the extract from
Satureja hortensis. The extract obtained from Allium sativum and Mentha sp. it is observed that they are
effective only at high concentration, 10% and 20% respectively. However, the study by Shalini et al. (2019)
suggest that neem oil and aqueous extracts obtained from Allium sativum, Leucas martinicensis and Zingiber
officinale can be used to control the phytopathogen Diplocarpon rosae. However, the neem oil tested on the
affected plants showed a phytotoxic effect compared to the other extracts used. The inhibitory effect of Salvia
officinalis extract was tested against the fungus Phakopsora pachyrhizi that produces Asian rust, one of the most
important diseases of soybean crops. The fungus is very aggressive causing significant damage to farmers,
chemical control is not exactly easy. From the studies carried out, a potential substitute for classic pesticides can
be considered the extract from Salvia officinalis that was studied by Borges et al. (2013), they observed a
germination percentage below 15%. In 2010, Schuster et al. (2010) used extract obtained from the species
Glycyrrhiza glabra against six plant pathogens, Phytophthora infestans, Pseudoperonospora cubensis, Podosphaera
xanthii, Blumeria graminis, Uromyces appendiculatus and Botrytis cinerea. The previous study shows that three
of the six phytopathogens, Phytophthora infestans, Pseudoperonospora cubensis and Uromyces appendiculatus,
showed increased sensitivity using the 5% concentration of the extract.
Keeping pace with the activity of antifungal extracts, a number of five extracts obtained from Artemisia
absinthium, Rumex obtusifolius, Taraxacum officinale, Plantago lanceolata and Malva sylvestris were tested as
natural alternatives in the control and combat of phytopathogenic fungi Alternaria alternata, Penicillium
expansum and Mucor piriformis. The percentage of inhibition for all tested extracts being over 60% on the three
tested phytopathogens (Parveen et al., 2014). Moreover, Capsicum extract shows important antifungal
properties against the pathogenic fungus Colletorichum gloeosporioides. (Mihaescu and Neagu Frăsin, 2020).
The efficacy of garlic (Allium sativum) extract against the phytopathogen Fulvia fulva was reported by
Ting-Ting et al. (2011) where it was demonstrated that at the concentration of 80 mg/mL
-1
the percentage of
inhibition is 100%. According to the study conducted by Ramaiah and Garampalli (2015), the extracts
obtained from the species Solanum indicum, Azadirachta indica and Oxalis latifolia demonstrated increased
efficacy against the phytopathogen Fusarium oxysporum f. sp. lycopersici, their inhibition percentage being over
70% of the colony diameter.
The essential oils of Rosmarinus officinalis and Thymbra spicata were tested against the phytopathogen
Monilinia fructigena and the potential for use of both essential oils was shown to be high. However, Thymbra
spicata essential oil at a concentration of 2 μl and demonstrated 100% efficacy, while Rosmarinus officinalis
essential oil at a concentration of 16 μl was shown to completely inhibit mycelial development (Yilar and Bayar,
2018).
In addition, Cymbopogon citratus oil at a concentration of 500 ppm has been shown to completely
inhibit sporulation and germ tube generation of the fungal species Colletotrichum coccodes, Botritys cinerea,
Rhizopus stolonifer and Cladosporium herbarum. (Trösken et al., 2004; Jiménez-Reyes et al., 2019). In contrast,
according to the study by Chang et al. (2008) the oil of Calocedrus macrolepisa var. formosana showed an
important antifungal activity, up to 65% against Pestalotiopsis funerea and 52% against the phytopathogen
Fusarium solani. Antifungal activity of Xanthium strumarium essential oil was demonstrated by Sharifi-Rad et
al. (2015), where it was found to reduce mycelial growth of the phytopathogenic species Aspergillus niger by up
to 34%. Another oil with properties to prevent and fight against the pathogen Botrytis cinerea is ginger.
(Tripathi et al., 2008; JIménez-Reyesa et al., 2019).

Din A et al. (2023). Not Bot Horti Agrobo 51(1):12991
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Major groups of natural compounds with antifungal
Major groups of natural compounds with antifungalMajor groups of natural compounds with antifungal
Major groups of natural compounds with antifungal
potential
potentialpotential
potential
Phenolic compounds
In recent years a number of studies have been reported on the antifungal potential of phenolic
compounds obtained from natural sources. The positions and number of hydroxyl groups in the phenolic group
are believed to be closely related to their toxicity relationship against microorganisms. Thus, the mechanisms
considered to be responsible for the toxicity of phenols against microorganisms include enzymatic inhibition
by oxidized compounds, possibly by reaction with sulfhydryl groups or by nonspecific interactions with
proteins. Among the polyphenols, flavan-3-ols, flavonols and tannins have received the most attention due to
their broad spectrum and greater antimicrobial activity compared to other polyphenols, as well as the fact that
most of them are able to suppress a number of microbial virulence factors (such as: inhibition of biofilm
formation, reduction of host ligand adhesion and neutralization of bacterial toxins) showing synergy with
antibiotics (Daglia, 2012). Antibacterial properties of phenolics may also be due to iron deficiency or hydrogen
bonding with vital proteins such as microbial enzymes (Sanhueza et al., 2014; Kabir et al., 2015).
Flavones are phenolic structures whose chemical structure contains a carbonyl and a 3-hydroxyl group.
Thus, the amentoflavones obtained from Selaginella tamariscina demonstrated an important antifungal action
against the phytopathogen Aspergillus flavus (40 µg/100 µl), a fact demonstrated by Jun Jung et al. (2006). A
series of four compounds, eupomatenoid-3, eupomatenoid-5, conocarpan and orientin, from Piper solmsianum
showed antifungal activity against all tested dermatophytes (Aspergillus flavus, Aspergillus fumigatus, Aspergillus
niger, Aspergillus niger, Microsporum cani, Microsporum gypseum, Trichophyton mentagrophytes, Trichophyton
rubrum, Epidermophyton flocosum, Cryptococcus neoformans, Candida albicans, Candida tropicalis) with values
in the range of 2.0-60.0 mg/ml (De Campos et al., 2005).
The mechanism by which phenolic compounds act focuses on altering the cytoplasmic membrane,
causing cell lysis, and can directly inhibit cellular proteins. These mechanisms are what allow the inhibition of
microorganisms (Abad et al., 2007; Martínez, 2012). For example, a large number of polyphenols extracted
from the leaves of Rhus muelleri inhibit the growth of the fungus Fusarium oxysporum having a diverse
phylogenetic complex (Jasso De Rodríguez et al., 2015). Mendoza et al. (2011) demonstrated that the flavonoid
5,7-dihydroxy-3,8-dimethoxyflavone, extracted from Pseudognaphalium robustum, reduced mycelial growth
and partial spore germination of the fungus Botrytis cinerea.
Stilbenes, especially resveratrol and its derivatives, have become famous for their positive effects on a
wide range of medical conditions, as indicated by a large number of published studies. A less investigated area
of research is their antimicrobial properties. Thus, the research of Caruso et al. (2011) performed on the
phytopathogenic fungus Botrytis cinerea highlighted both the antifungal effect of resveratrol and its potential
to inhibit the development of conidia. The demonstrated optimal concentration, according to Adrian et al.
(1997) being between 60-140 μg/mL. Also, against dermatophytes such as Trichophyton mentagrophytes,
Trichophyton tonsurans, Trichophyton rubrum, Epidermophyton floccosum and Microsporum gypseum, the
inhibitory activity of resveratrol has been shown to be between values of 25-50 μg/mL (Chan, 2002).
Terpenoid compounds
Terpenes are a large class of aromatic chemicals present in a wide variety of plants, foods and essential
oils, and their purpose is to protect plants against fungi, bacteria and animal pests. In general, essential oils have
a high concentration of terpenes and sesquiterpenes (Abad et al., 2007; Martínez, 2012). The antifungal
activity of carrot oil was tested against the pathogen Alternaria alternata, the inhibition percentage was 65% of
the colony diameter. The main esters found in carrot essential oil are sesquiterpenes such as carotol (Abad et
al., 2007). Canelo (Drimys winteri) essential oil contains varying amounts of polygodial and drimenol (Muñoz-

Din A et al. (2023). Not Bot Horti Agrobo 51(1):12991
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Concha et al., 2007). These terpenes have important antifungal properties against the fungus Gaeumannomyces
graminis (Monsálvez et al., 2010).
Thyme is well known for its antifungal effects, thanks to the thymol found in its oil. Shcherbakova L. et
al. (2021) through their studies showed that thymol has a remarkable antifungal action. Also, Zhang et al.
(2016) reported the antifungal efficiency of pure monoterpenes such as: β-citronellol, carvacrol, citral, eugenol,
geraniol and thymol against wood white rot fungi: Trametes hirsuta, Schizophyllum commune and Pycnoporus
sanguineus. Notable results were also obtained by Xie et al. (2017) who confirmed antifungal properties of
essential oils from Origanum vulgare, Cymbopogon citratus, Thymus vulgaris, Pelargonium graveolens,
Cinnamomum zeylanicum and Eugenia caryophyllata against the wood-decomposing fungi Trametes hirsuta
and Laetiporus sulphurous where the following compounds were highlighted: carvacrol, citron, citronellol,
cinnamic aldehyde, eugenol and thymol. The studies carried out by Sempere-Ferre et al. (2021) on two
pathogens Botryotinia fuckeliana and Rhizoctonia solani highlighted the antifungal effects of some natural
compounds (eugenol, carvacrol, thymol and cinnamic aldehyde).
The first report regarding the production of volatile antibiotics was reported by Strobel et al. (2007)
who succeeded in isolating the compounds: 2-methylbutanoic acid, 3-methylbutanoic acid, 2-methyl-2-
butenal, 3-methyl-3-butene-1-OL, guaiol, 1-octene-3-ethyl, formamide , N-(1-methylpropyl), derivatives of
azulene and naphthalene, caryophyllene, phenylethyl alcohol and propanoic acid, from Muscodor albus species
(Xylariaceae family), an endophyte of Guazuma ulmifolia species (a Sterculiaceae plant collected from the
tropical forest-western Ecuador). These compounds were tested against some pathogens of high economic
importance, namely: Botrytis cinerea, Mycosphaerella fijiensis, Pythium ultimum, Phytophthora cinnamomi,
demonstrating their effectiveness by inhibiting the development of the mycelium of the fungi. Also, subsequent
reports showed that Muscodor albus was also found on other host plant types such as Myristica fragrans,
Terminalia prostrata, Cinnamomum zeylanicum and Ginkgo biloba (Worapong et al., 2001; Ezra and Strobel,
2003; Atmosukarto et al., 2005; Lacey and Naven, 2006; Strobel et al., 2007; Banerjee et al., 2010; Alpha et al.,
2015). Diterpenoids, sclareol and 13-epi-sclareol isolated from the resinous extract of Pseudognaphalium
cheiranthifolium, can inhibit the mycelial growth of the phytopathogenic fungus Botrytis cinerea, being able to
be used as a natural control strategy (Mendoza et al., 2015).
Alkaloid compounds
Alkaloids are chemical substances with a wide range of biological activities, usually present in species of
the Solanaceae family. Thus, hyoscyamine isolated from the medicinal plant Hyoscyamus muticus has been
shown to inhibit the growth of several species, including Fusarium dimerum, Fusarium nivale and Fusarium
oxysporum. (Abdel et al., 2009). The study conducted by Soumya and Bindu (2012) highlighted the antifungal
potential of capsaicin isolated from the species Capsicum frutescens, the tests being performed on four species
of fungi, namely Aspergillus flavus, Aspergillus niger, Penicillium sp. and Rhizopus sp. Regarding the effectiveness
of capsaicin, it was also studied by Buitimea-Cantúa et al. (2018) on the phytopathogen Aspergillus parasiticus,
the inhibitory percentage being set at 50%. The research of Slusarenko et al. (2008) demonstrated the
effectiveness of allicin obtained from garlic extract against the fungus Alternaria sp. Similar results were
obtained by Mihaescu et al. (2021) who showed that allicin in vitro exhibits a remarkable fungicidal effect
against the fungus Alternaria solani. Singh et al. (2007) demonstrated that alosecurinin or phyllocrysin isolated
from the root of Phyllanthus amarus, completely inhibits the germination of spores of phytopathogenic fungi
Curvularia sp., Curvularia lunata, Collectotrichum sp., Colletotrichum musae and Heterosporium sp.

Din A et al. (2023). Not Bot Horti Agrobo 51(1):12991
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Conclusions
ConclusionsConclusions
Conclusions
The need of the modern era is to obtain pathogen-free and high-productivity crops to meet global food
requirements. Because of this, the use of plant extracts has emerged as a natural alternative to synthetic
fungicides for controlling and combating phytopathogenic fungi. However, research for the identification and
characterization of new compounds with antifungal potential is still a challenge, being the main current
approaches in the discovery and development of new biopesticides. Also, following the bibliographic study, we
could observe that natural extracts and essential oils from plants present active compounds with important
effective antifungal properties. Finally, it could be observed that the phenolic structures represent real starting
points for the development of new biopesticides due to the effectiveness they have demonstrated. Another class
of compounds that have demonstrated their effectiveness is that of terpenoids, of which the best known are:
carvacrol, citral, eugenol, geraniol and thymol, specialized studies confirming their antifungal potential.
Authors’ Contributions
Authors’ ContributionsAuthors’ Contributions
Authors’ Contributions
Conceptualization: AD and RM; Writing - original draft, review and editing: AD, IM and RM;
Supervision and validation: AD, IM and RM.
All authors read and approved the final manuscript
Ethical approval
Ethical approvalEthical approval
Ethical approval (for researches involving animals or humans)
Not applicable.
Acknowledgements
AcknowledgementsAcknowledgements
Acknowledgements
This research received no specific grant from any funding agency in the public, commercial, or not-for-
profit sectors.
Conflict of
Conflict of Conflict of
Conflict of Interests
InterestsInterests
Interests
The authors declare that there are no conflicts of interest related to this article.
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