Physiological and molecular insights into the allelopathic effects on agroecosystems under changing environmental conditions

Abstract

Allelopathy is a natural phenomenon of competing and interfering with other plants or microbial growth by synthesizing and releasing the bioactive compounds of plant or microbial origin known as allelochemicals. This is a sub-discipline of chemical ecology concerned with the effects of bioactive compounds produced by plants or microorganisms on the growth, development and distribution of other plants and microorganisms in natural communities or agricultural systems. Allelochemicals have a direct or indirect harmful effect on one plant by others, especially on the development, survivability, growth, and reproduction of species through the production of chemical inhibitors released into the environment. Cultivation systems that take advantage of allelopathic plants’ stimulatory/inhibitory effects on plant growth and development while avoiding allelopathic autotoxicity is critical for long-term agricultural development. Allelopathy is one element that defines plant relationships and is involved in weed management, crop protection, and microbial contact. Besides, the allelopathic phenomenon has also been reported in the forest ecosystem; however, its presence depends on the forest type and the surrounding environment. In the present article, major aspects addressed are (1) literature review on the impacts of allelopathy in agroecosystems and underpinning the research gaps, (2) chemical, physiological, and ecological mechanisms of allelopathy, (3) genetic manipulations, plant defense, economic benefits, fate, prospects and challenges of allelopathy. The literature search and consolidation efforts in this article shall pave the way for future research on the potential application of allelopathic interactions across various ecosystems.

Introduction

Allelopathy is an inter-species interaction in which one species release chemical compounds into the environment that act as toxins to other species. The name “allelopathy” originated from the Greek terms allelon, which means “of each other,” and pathos, which means “to suffer.” It is characterized by a combination of donor plant-induced biotic and abiotic stressors on recipient plants. Allelopathy is a fundamental scientific concept in chemical ecology. It refers to the impact of plant or microbial chemicals on the growth, production, and dispersal of other plants and microbes in natural communities or agricultural systems (De Albuquerque et al. 2011; Yang et al. 2011).

In the realm of agriculture and forestry, allelopathy holds significant promise as a sustainable solution for various challenges, including weed management, crop protection, and soil health maintenance. Harnessing the allelopathic potential of plants can lead to beneficial outcomes such as weed suppression, enhanced crop productivity, and reduced reliance on synthetic agrochemicals. However, it also presents challenges such as autotoxicity and ecological imbalance, necessitating a nuanced approach to its application (Kostina-Bednarz et al. 2023; Ain et al. 2023).

Contemporary research in weed management underscores the pivotal role of allelopathy as an eco-friendly alternative to conventional herbicides. The diverse benefits offered by allelopathic compounds make them attractive candidates for addressing concerns related to environmental pollution and herbicide resistance (Jabran et al. 2015). Despite the abundance of allelopathic plant species and their chemical compounds, only a fraction has been explored for their potential as bioherbicides, highlighting the untapped reservoir of natural resources awaiting discovery and exploitation (Li et al. 2019).

Establishing ecological, sustainable, and integrated weed control strategies requires using allelopathic cover crops, intercropping, incorporating allelopathic plants to crop rotation, and using the residues as mulch. One of the main challenges to attaining sustainable crop protection in the present era is the limited availability of bioherbicides (Jabran et al. 2015). While allelochemicals offer numerous advantages, their direct use as bioherbicides is constrained by several limitations. Articulating the diverse modes of action for each allelochemical class and understanding the influence of environmental conditions on their efficacy pose challenges. While traditionally, this concept has been studied from a physiological and ecological perspective, recent advances in microbial and molecular biology provide new insights into the emerging trends of allelopathic interactions at the physiological, microbial, and molecular levels (Fig. 1).

Fig. 1.

Sources of allelopathy

Physiological allelopathic interactions elucidate the intricate mechanisms by which allelochemicals modulate various physiological processes in recipient plants. These chemicals can influence seed germination, seedling growth, enzyme activity, and nutrient uptake, thereby shaping plant growth and productivity. Understanding the physiological basis of allelopathy is essential for devising strategies to optimize its beneficial effects while minimizing potential drawbacks (Pan et al. 2023; Shi et al. 2023).

At the microbiological level, allelopathic interactions exert profound effects on soil microbialcommunities, influencing nutrient cycling and ecosystem dynamics. Allelochemicals can modulate microbial activity and diversity, consequently altering nutrient availability and plant–microbe interactions. Moreover, allelopathic interactions may impact symbiotic associations such as mycorrhizal colonization, further influencing plant nutrition and health (Pan et al. 2023; Zhao et al. 2023; Xu et al. 2023).

Molecular allelopathy delves into the intricate signaling pathways and gene expression patterns underlying allelochemical-induced responses in recipient plants. These molecular responses govern stress tolerance, defense mechanisms, and growth regulation, offering insights into the genetic basis of allelopathy. By deciphering the molecular mechanisms of allelochemical production and action, researchers can pave the way for targeted manipulation of allelopathic interactions for agricultural and ecological benefits (Fang et al. 2020; Patni et al. 2023).

Allelopathy represents a multifaceted phenomenon with far-reaching implications for ecological sustainability and agricultural productivity. By elucidating the physiological, microbial, and molecular dimensions of allelopathic interactions, we can unlock its potential as a tool for weed management, crop protection, and soil health enhancement (Zhao et al. 2023; Xu et al. 2023; Pan et al. 2023).

Allelochemical Interactions

Allelopathic effects are primarily determined by the quantity of chemicals released, the chemical and physical characteristics of the soil that affect how long chemicals remain in the environment, the replenishment of allelochemicals, and nearby species (Weiner 2001). Numerous studies have been done on allelopathy, which recently attracted interest due to its potential to explain plant growth restriction in interspecies interactions and influence the plant community (Ortega et al. 2007). For allelopathy to be an ecologically significant mechanism influencing plant development in field conditions, allelochemicals must accumulate, persist at phytotoxic levels, and come into contact with the target plant (Inderjit et al. 2005).

Innumerable studies have been published on the genetic diversity of allelopathy in crop cultivars about allelopathic traits and their potential for creating superior allelopathic traits in weed-suppressing cultivars (Putman and Duke, 1974). Several other crops were tested, including Avena sativa L. (oat), Triticum aestivum L. (wheat), Hordeum vulgare L. (barley), O. sativa (Dilday et al., 1991), Secale cereal L. (rye), and Sorghum Moench spp. (Table 1). The existence of genetic diversity indicates that allelopathic trait is genetically regulated.

Table 1.

Allelopathy reported in various crops and tree species

Allelochemical producing weeds/crops/trees	Allelochemicals	Affected crops	References
Cereals
Rye (Secale cereale)	MBOA, BOA, HMBOA, DIBOA	Ipomoea lacunose, Eleusine indica, Amaranthus palmeri, Chenopodium album, Abutilon theophrasti, Brachiaria plantaginea, Bidenspilosa, Euphorbia heterophylla	Krogh et al. (2006)
Oat (Avena sativa)	Tricin, acacetin and diosmetin syringic acid and syringoside	Digitaria sanguinalis, Eleusine indica, Amaranthus retroflexus, Datura stramonium
Sudangrass (Sorghum sudanense)	p-hydroxybenzoic acid, p-hydroxybenzaldehyde, ethyl-p-hydroxybenzoate, diosmetin and tricin	Broad leaved weeds	Uddin et al. (2014)
Wheat (Triticum aestivum)	DIMBOA, syringic acid, vanillic acid, p-hydroxybenzoic acid, cis-ferulic acid, trans-ferulic acid, trans-p-coumaric acid, cis-p-coumaric acid	Ipomoea lacunose, Eleusine indica, Amaranthus palmeri	Wu et al. (2000)
Legumes
Pea (Pisum sativum)	Macckian, anhydropisatin, and pisatin	Chenopodium album, Amaranthus hybridus, Thlaspi arvense, Taraxacumo_cinale, Stellaria media, Elymus repens, Panicum crus-galli, Setaria glauca
Egyptian clover (Trifolium alexandrinum)		Amaranthus retroflexus, Convolvulus arvensis, Secale cereale, Sinapis arvensis	Maighany et al. (2007)
Sunn hemp (Crotalaria juncea)		Lactuca sativa, Secale cereal, Amaranthus hybridus	Colegate et al. (2012)
Hairy vetch (Viciavillosa)		Amaranthus retroflexus	Ercoli et al. (2007)
Non‐legumes
Forage radish (Raphanus sativus)	Syringic acid, Vanillic, Gallic acid, Gallic acid, Ferulic acid, Caffeic acid	Avenafatua, Hordeum spontaneum	Rasul and Ali (2020)
Field mustard (Brassica campestris)	Benzyl isothiocyanate, allyl isothiocyanate, 3-butenyl isothiocyanate	Sorghum halepense	Petrova et al. (2015)
Rapeseed, canola (Brassica napus)	Glucosinolates, 2-Phenylethyl-isothiocyanate, benzyl isothiocyanate, allyl isothiocyanate, 3-butenyl isothiocyanate	Lolium rigidum Gaudin Sorghum halepense	Petrova et al. (2015)
Field mustard (Brassica rapa)	2-Phenylethyl-isothiocyanate	Sorghum halepense	Petrova et al. (2015)
Sunflower (Helianthus annus)	p-hydroxybenzoic acid, syringic acid, caffeic acid, gallic acid, protocatechuic acid,vanillic acid	Chenopodium album	Rawat et al. (2017) Anjum and Bajwa (2010)
Buckwheat (Fagopyrum esculentum)	Trans-cinnamic acid, trans-cinnamic acid derivatives, benzoic acid derivatives, and flavonoids	Echinochloa crus-galli, Aperaspica-venti., Galium aparine., Vicia hirsute Matricaria inodora Setaria glauca L.	Szwed and Mitrus (2019)
Flax (Linum usitatissimum)	Phenylpropanoids/coniferyl alcohol	Stellaria media
Niger (Guizotia abyssinica)	Coumarin, benzoic acid and cinnamic acid	Oxygonum sinuatum, Gutierrezia sarothrae, Cynodon dactylon	Moraa et al. (2018)
Tree species
Black Walnut (Juglans nigra)	Juglone	Tomato, alfa alfa, strawberry, soybean	Bohm et al. (2006); Jose and Holzmueller (2008)
Eucalyptus spp.	1,8-cineol	Amaranthus retroflexus	Azizi and Fuji (2006)
Tree of heaven (Ailanthus altissima)	Ailanthone	Amaranthus retroflexus, Setaria glauca, Echinochloa crus-galli, Zea mays	Heisey (1996)
Pinus spp.	Terpenes (α-pinene, β-cariofilene and α-humulene), Phenolic compounds (9α,13β-epidioxyabeit-8(14)en-18-oic acid), and Flavonoids (quercetin, catechin, kaempferol, myricetin)	A. sativa, L. minor, F. arundinacea and C. dactylon	Nektarioset al. (2005); Ormeno et al. (2007); Kato-Noguchi et al. (2009)
Robinia pseudoacacia L	Obinetin, myricetin, and quercetin	Solanum lycopersicum L., Lettuce; E. crus-galli, white clover, lettuce, and Chinese cabbage	Pedrol et al. (2018); Bektić et al. (2021)
Mango (Mangifera indica), Poplar (Populus eltoids), Arjun (Terminalia arjuna), Palas (Butea monosperma), Bakaine (Melia azedarach), Acacia mangium, Acacia auriculiformis, Bael (Aegle marmelos), Teak (Tectona grandis), Jackfruit(Artocarpus heterophyllus), Shisham (Dalbergia sissoo)	Caffeic acid, Feru-lic acid; Coumaric acid, Benzoic acid; Vanelic, Chloro-genic; Gallic; Hydroxybenzoic and Cinnamic acid	Black gram, Gram, Pea, Sponge gourd, Mustard, Okra, Brinjal, Chilli, Tomato	Kumari et al. (2016)

Allelochemicals and Mode of Action

Allelochemicals, ubiquitous in plants, are present in various plant parts such as leaves, bark, roots, root exudates, flowers, and fruits. The mechanisms of allelochemical release into the rhizosphere include leaching from leaves and aerial plant parts, volatile emissions, root exudation, and the breakdown of bark and leaf litter (Weir et al. 2004). Upon encountering target plants, allelochemicals exert their effects through diverse biochemical pathways, influencing a wide array of biological processes. These impacts are observed across multiple levels of plant organization, spanning from molecular to ecological scales (Bogatek and Gniazdowska, 2007).

Studies have elucidated that allelochemicals disrupt numerous physiological functions in recipient organisms, emphasizing the importance of understanding their effects on receptor plants and other species. Benzoic acid, cinnamic acid, alkaloids, and terpenoids, among others, released from various plant sources, have been implicated in altering physiological and ecological processes such as germination and seedling growth (Kumar et al. 2015, 2019; Macías et al. 2019).

Within plants, allelochemicals primarily disrupt various physiological processes including phytohormone metabolism, photosynthesis, respiration, ion and water uptake, cell division, cell differentiation, enzyme function, signal transduction, and gene expression (Li et al. 2022). Studies have demonstrated their direct interference with photosynthesis, resulting in decreased CO₂ assimilation rates (Li et al. 2020). This inhibition predominantly affects stomatal behavior, electron transport within the thylakoid, and the carbon reduction cycle (Kumar et al. 2016, 2017). Despite considerable investigation, the precise mechanism responsible for the reduction in carbon assimilation remains elusive. Allelochemicals are recognized for their impact on chlorophyll levels, integral to photosynthetic membranes, achieved through mechanisms such as inhibiting chlorophyll synthesis or promoting chlorophyll breakdown, thereby reducing chlorophyll accumulation in treated plants (Pramaink et al. 2001).

Allelochemicals also influence crop growth by altering many stages of respiration, including oxidative phosphorylation, mitochondrial electron transfer, and ATP enzyme activity. These allelochemicals directly limit ATP synthesis enzyme activity, NADH oxidation, and mitochondrial ATP generation, disrupt plant oxidative phosphorylation, and eventually, respiration is inhibited; reversibly, they can promote respiration by triggering CO₂. It was speculated that respiration was inhibited by corn pollen extract by inhibiting the electron transport chain upstream of cytochrome c and limiting oxygen consumption (Ortega et al. 1988). Rasmussen et al. (1992) also conducted a similar investigation and concluded that the allelochemical sorgoleone (extracted from soybean and corn seedlings) interrupts the electron transport chain in the mitochondria. Furthermore, juglone extracted from the walnut also affects the corn and soybean seedlings (Hejl and Koster 2004).

When plant roots come into contact with allelochemicals, it initiates a cascade of effects that disrupt the uptake of water and ions. This alteration in ion and water uptake triggers changes in crucial membrane proteins like plasma membrane H + -ATPase, vital for maintaining cell turgor and mineral absorption. Consequently, stomatal closure occurs, impacting essential plant processes (Omezzine et al. 2014). Various studies have highlighted the direct impact of root exudates and derivatives of cinnamic and benzoic acids on stomatal behaviour in plants such as cucumber, wheat, tobacco, and sunflower (Yu et al. 2003) (Fig. 2). This alteration in stomatal behavior affects plant productivity, as it directly influences photosynthesis rates and leaf area, with reduced leaf area hindering growth and development.

Fig.2.

Structures of some allelochemicals

The allelopathic interaction, regulated by soil chemical properties and soil microbes, significantly influences crop growth. While allelopathy can indirectly facilitate plant-plant interactions, its indirect impacts through soil microbes may lead to soil sickness and hamper plant development. Nevertheless, rhizosphere soil microbes can also contribute positively to plant allelopathic potential by activating non-toxic versions of allelochemicals, underscoring the complexity of allelopathic interactions in agricultural ecosystems (Mishra et al. 2013; Wu et al. 2015; Kumar et al. 2020a, 2020b).

Allelopathy presents an innovative avenue for sustainable farming practices, aiming to boost crop yields while preserving ecosystem balance. However, modern agricultural methods often prioritize productivity through the widespread use of synthetic chemicals, leading to potential environmental concerns. Despite its promise, allelopathy’s effects on crops vary, with allelochemicals either directly affecting target organisms or being degraded by soil microbes. Distinguishing between direct and indirect effects in the field poses challenges, with indirect impacts often holding greater ecological significance (Kumar et al. 2020a, b).

It’s speculated that allelochemicals may penetrate soil, impacting target plant roots and soil characteristics, influencing rhizospheric interactions and nutrient uptake. Soil microorganisms play a crucial role in transforming these compounds, altering their activity and availability for transport (Zhang et al. 2021).

Allelopathy and Its Impacts on Soil Microbes and Ecosystem Processes

Allelopathy can have a major impact on microbial communities and ecological systems. Allelochemicals produced by plants can affect the distribution and abundance of microbes and the activities of microbes in the environment (Zeng 2014). In addition, allelopathy can lead to changes in the structure of microbial communities, including the production of new microbial species and the loss of existing species. Allelopathy can also affect the cycling of nutrients, as allelochemicals may affect the decomposition of organic matter, the availability of nutrients, and the uptake of nutrients by plants. Ultimately, allelopathy can majorly impact the structure and functioning of entire ecosystems (Xu et al. 2023).

Using allelopathic impacts on crop harvests, farmers can reduce the use of herbicides and related chemical contaminants, and this approach offers appropriate methods for a long-term increase in agricultural production and ecological balance. Researchers are interested in using allelopathy to manage weeds, insect pests, crop diseases, nitrogen management in farms, and the manufacturing of innovative allelochemistry-based insecticides to boost agricultural output and preserve the natural world (Figs. 3 and 4) (Jabran et al. 2015).

Fig. 3.

Microbial and ecological consequences of allelopathy

Fig. 4.

Input and output dynamics of allelochemicals in soil

Phytotoxins, conversely, are substances produced by certain microorganisms that can be highly toxic to plants and are classified as allelochemicals. These toxins are found in various forms, including proteins, peptides, and lipopolysaccharides. Both beneficial and pathogenic microorganisms can produce them but are usually associated with disease-causing microbes. Microbial phytotoxins such as isomycin, tentoxin, biopoloroxin, and herbimycin can affect plants, including stunted growth, lower yields, or even death (Moreno-Robles et al. 2022; Ain et al. 2023; Xu et al. 2023).

Notwithstanding this, they may affect certain plant parts, such as the stems or leaves, and they may also reduce a plant’s ability to resist disease. The mechanisms by which microbial phytotoxins cause their effects have yet to be fully understood. Generally, it is thought that the toxins bind to certain proteins or receptors on the plant’s surface and interfere with normal cellular processes. This can disrupt the plant’s metabolism, resulting in various symptoms depending on the toxin and the tissue affected. To reduce the effects of microbial phytotoxins, various methods have been developed. These include using protective coatings on the plant’s surface to block the toxins, using chemical compounds to neutralize the toxins, and using biological controls such as beneficial microorganisms. Genetic engineering can also make plants more resistant to microbial phytotoxins (Xu et al. 2023; Mehal et al. 2023).

Allelopathy and Ecosystem

Allelochemicals can play a key role in succession, an ecosystem’s long-term, slow evolution. This transformation is crucial for the ecosystem’s health as it contributes to developing a diverse and balanced environment. Allelochemicals’ ability to alter the soil’s composition is one of their main effects on succession. They may encourage the development of particular bacteria and fungi, which may alter the amount of nutrients available in the soil, affect the kinds of plants that can flourish there, and ultimately influence the successional pattern. These substances impact interspecies competition by reducing the rate of species diversification, allowing other species to flourish, and inhibiting the growth of new plants, which slows the rate of succession (Xu et al. 2023; Chou et al. 2023).

The ecosystem can avoid becoming overly stable or uniform by maintaining diversity and complexity. Additionally, allelochemicals can speed up succession by encouraging the spread of particular species (Narwal et al. 2000; Kumar et al. 2022). Empetrum hermaphroditism prevents Pinus sylvestris from regenerating in a way that leads to coniferous forest, contrary to what would typically be the natural climatic vegetation in boreal regions.

Forest fires would avoid this impact, which occurs frequently enough to prevent the slow-growing crowberry shrub from dominating large areas in natural settings. Crowberry bushes have taken over, which is a problem for the development of forests because human activity has decreased the frequency of natural fires and the area that needs to be protected from them to protect wood production. Allelochemical inhibition of ectomycorrhiza-producing fungi, as well as other symbiotic fungi, is another tactic for impacting tree phases in succession that rely on symbiosis (Carvalho et al. 2022; Xu et al. 2023).

Allelochemicals Impact on Invasion and Dominance

Plant-produced allelochemicals significantly impact species invasion and dominance in various ecosystems. These can influence the species’ ability to survive and reproduce in a given environment. Plant allelochemicals can influence herbivore growth and development, as well as inhibit the growth of competing plants. These substances directly impact a species’ ability to invade and dominate an ecosystem. Allelochemicals can facilitate the successful invasion of a new species by inhibiting the growth of competing species, allowing the invader to gain a foothold in the ecosystem (Kato-Noguchi 2022).

In addition to influencing species’ invasion and dominance, allelochemicals affect an ecosystem’s composition and structure. Allelochemicals produced by a successful invader may reduce the ecosystem’s diversity and increase the invader’s dominance. In this way, allelochemicals can significantly impact the overall functioning and stability of an ecosystem. By influencing species’ growth, development, and reproduction, these chemicals can allow one species to outcompete others for resources and gain a foothold in a new environment. Allelochemicals can, therefore, significantly impact how an ecosystem is composed and structured. They have an impact on the invasion process by changing the biotic and abiotic processes in the ecosystem (Uddin et al. 2014). These allelopathic properties can be found in various plant parts, including roots, flowers, shells, mulch, blooms, and leaves. Most allelopathic plants store protective substances in their leaves; when the leaves drop and deteriorate, these poisons may affect nearby plants.

Additionally, some plants release poisons through their roots, which are subsequently ingested by trees and other plants. Prunus laurocerasus, Rhus spp., Rhododendron spp., Sambucus spp., Forsythia spp., and Solidago spp. are common plants exhibiting allelopathic properties. Juglans nigra is an excellent illustration of an invasive species that dominates its surroundings. The tree’s buds, endocarp, and roots possess allelopathic properties, and the soil surrounding the tree contains juglone, a lethal substance (Ochekwu and Uzoma 2020).

Allelopathy and Soil

The release of allelochemicals by plants into the soil initiates chemical interactions referred to as allelopathy, which represents a fascinating ecological occurrence. These substances have the potential to significantly affect nearby plants’ germination, growth, and general health. Many plant species use the complex ecological tactic of allelopathy to create mutualistic relationships or obtain a competitive edge. Allelochemicals like phenolic acids, terpenoids, and alkaloids play a role in this process by either promoting the growth of neighboring allies or suppressing the growth of rival plants. Because the soil acts as a vehicle for the interaction and transfer of various allelochemicals, this dynamic process takes place there (Bachheti et al. 2020; TlakGajger and Dar 2021).

Allelopathy research and its impacts on soil give important insights for agricultural operations, including possibilities for more effective and sustainable weed control, crop management, and ecosystem preservation. A comprehensive grasp of the complex interplay between allelopathy and soil is essential for sustainable agriculture. Using this knowledge, farmers may maximize crop growth, lessen their reliance on synthetic herbicides, and promote a more balanced ecology (Zhan et al. 2022; Xu et al. 2023; Choudhary et al. 2023).

Soil fertility management in agriculture heavily relies on biomass (crop leftovers and other organic wastes) to keep the soil’s level of organic matter high and supply the crops nutrient needs. Depending on the type, quantity, placement depth, and duration of the decomposition process of plant residues, the generation of allelochemicals by volatiles, leaching, and microbial degradation in soil influences crop germination, growth, and yield. The activity of these substances is affected or altered by soil factors, including inorganic and organic content, ion exchange capacity, reactive mineral surfaces, and biotic barriers (Inderjit 2001).

Root exudates and biomass breakdown are the main sources of allelochemicals in agriculture and forestry. These substances are immediately incorporated into the soil, as well as those released as volatiles or leachates during precipitation (rain, snow, fog, mist, dew), which also directly or indirectly enter the soil through a variety of physical, chemical, and microbiological and biodegradation processes in the soil. Most allelochemicals are either lost through runoff or absorbed by the soil’s deeper layers through precipitation or irrigation water. However, not much information is available about these components (Aslam et al. 2017; Scavo et al. 2019).

Allelopathy and Plant Growth

Allelopathy is important in forming plant communities and fostering plants competition in ecosystems. A few allelochemicals have growth-promoting properties that improve plant vigor, seed germination, and overall performance. These substances might improve the recipient plants’ access to nutrients, encourage the growth of their roots, and improve their microenvironment. On the other hand, a lot of allelochemicals have inhibitory effects, which prevent rival plants from growing by interfering with vital physiological functions. These inhibitory allelopathic substances have the ability to impede the germination of seeds, extension of roots, and intake of nutrients, hence aiding in the establishment of plant species dominance within a certain habitat (Kumar et al. 2021a, b, c; Pan et al. 2023; Shan et al. 2023).Positive allelopathic effects can occur when allelochemicals enhance the growth and development of neighboring plants. For example, some allelochemicals released by leguminous plants can stimulate the growth of other plants by increasing nitrogen availability in the soil. Similarly, allelopathic effects can promote seedlings’ germination and early growth by breaking seed dormancy (Zhan et al. 2022; Han et al. 2024).

Conversely, allelochemicals that prevent surrounding plants from growing and developing might have adverse allelopathic consequences. Allelopathy occasionally results in decreased plant development and agricultural output. For instance, black walnut woods can generate allelochemicals that harm other plants, rendering it difficult to cultivate crops next to these trees. Allelopathic effects can be considered a form of biotic stress and an important factor in natural plant community dynamics. These can range from mild to strong, depending on the species of plants involved, the amount of allelochemicals released, and the environment in which the plants are growing (Bishop et al. 2023; Lal and Biswas 2023).

Allelopathy can also influence the competition between plants by inhibiting the growth of competing species, allowing the releasing species to outcompete them. In addition, allelopathy can affect the entire plant community by influencing the recruitment of seeds and seedlings and the success rate of germination. This can lead to changes in the species composition of a plant community. Allelochemicals can also affect the availability of nutrients in the soil and can be used as a form of weed control. They can be released by plants to inhibit the growth of weeds, reducing the need for chemical herbicides. This can be beneficial for both the environment and the agricultural industry (Liu et al. 2022; Lal and Biswas 2023; Chou and Wang 2023).

Overall, allelopathy has the potential to have a significant effect on plant growth. It is an important factor to consider when managing plant communities and can be used to enhance crop production and reduce the need for chemical herbicides. Allelopathic effects on plant growth are complex and depend on various factors, including the concentration and type of allelochemicals, the specific plant species involved, and the growing conditions. Understanding these effects can help farmers and gardeners make informed decisions about managing plant communities and maximizing crop yields (Scavo et al. 2019; Tiwari and Prajapati 2023).

Comprehending and utilizing allelopathy in agriculture can have useful consequences for sustainable crop management. The use of allelopathic cover crops, intercropping, and strategic crop rotation can achieve weed suppression and increased crop yield.Farmers may be able to lessen their dependency on synthetic herbicides by utilizing allelopathic interactions, which would support ecologically sound and environmentally benign farming methods (Mahé et al. 2022; Valiño et al. 2023).

Allelopathy and Plant Physiology

Allelopathic effects can also have significant impacts on plant physiology (Choudhary et al. 2023). They can modify several phases of respiration, such as oxidative phosphorylation, electron transport in mitochondria, ATP enzyme activity, and CO₂ synthesis, which all impact plant development . These substances can impede NADH oxidation by lowering oxygen consumption. They can also block ATP synthesis enzyme activity, decrease ATP production in mitochondria, and interfere with plant oxidative phosphorylation (Dong and Fu 2023). Besides that, they increase CO₂ release, which encourages respiration. Oxygen consumption was decreased by an electron pathway inhibitor provided by a corn pollen extract in ethanol. Upstream of cytochrome c was likely the precise inhibitory location in watermelon (Ortega et al. 1988). By preventing electron transport at the b-c1 complex, sorgoleone similarly reduced the activity of mitochondria isolated from etiolated soybean and corn seedlings (Rasmussen et al. 1992). The mitochondria in the root cells of maize and soybean seedlings are similarly affected by juglone, which disrupts root oxygen absorption (Hejl and Koster 2004). The allelochemical has the following deleterious repercussions on physiological parameters:

• Net CO₂ assimilation rates and respiration electron transfer: Allelopathic compounds can affect the rates of photosynthesis and respiration in neighboring plants, which can impact their overall growth and development. For example, Benzoxazolin-2(3H)-one (BOA) can inhibit photosynthesis, reducing net CO₂ assimilation rates, while others can stimulate respiration electron transfer, leading to increased energy production(Chou and Wang 2023; Motmainna et al. 2023).

• Plant metabolism: Plant metabolism and enzyme activity can be impacted, which can impact how well plants can synthesise and use different molecules. They can increase the production of secondary metabolites like flavonoids, terpenes, and phenolics, strengthening a plant’s defenses against pathogens and herbivores (Shan et al. 2023; Kikraliya et al. 2023).

• Ion transport and water relations: They can also influence how effectively plants absorb and transport vital nutrients and water, as well as increase the permeability of plant cell membranes, which makes it possible for ions and water to enter the plant’s cells more effectively. Other allelochemicals, on the other hand, can reduce water potential and impede ion transport, resulting in decreased nutrient uptake and water stress in plants (Kostina-Bednarz et al. 2023).

Allelochemicals Impact on Water and Nutrient Uptake

Allelochemicals can impact nutrient absorption by altering the availability of nutrients in the soil and influencing the absorption of certain nutrients. They may reduce the availability of nitrogen or other essential nutrients in the soil, or they may influence the absorption of certain nutrients, such as potassium, by altering plant root systems or changing the microbial activity in the soil. They can alter the activity of specific enzymes, which can change how plants absorb nutrients and have both positive and negative effects on nutrient absorption (Scavo et al. 2019; Latif et al. 2022).

The chemicals produced by legumes, such as salicylic, lactic, p-hydroxybenzoic, adipic vanillic, malic, succinic, and glycolic acids from V. faba and P. vulgaris root exudates, can help fix nitrogen in the soil, increasing the amount of nitrogen available for uptake by other plants (Asaduzzaman and Asao 2012; Mondal et al. 2015). Allelochemicals may also adversely affect nutrient absorption by affecting the growth of soil microorganisms that also hinder nutrient supply. For example, a small amount of dibutyl phthalate improves N absorption while decreasing P and K absorption. N, P, and K cannot be absorbed whenever this molecule is present in large quantities. Tomato roots exposed to trace amounts of diphenylamine accumulate more N and K, albeit less P (Scavo et al. 2019; Han et al. 2024).

Allelochemical concentration, the sensitivity of the receiving plants, and the particular chemical properties of the compounds involved are some of the complex interplaying factors that determine how allelochemicals affect water and nutrient uptake. While certain allelochemicals function as inhibitors, impeding these processes, others may function as stimulants, encouraging nearby plants to absorb water and nutrients. Since these interactions can have cascading impacts on nutrient availability, water quality, and overall ecosystem health, understanding these allelopathic interactions is essential to managing aquatic ecosystems (Ain et al. 2023; Motmainna et al. 2023; Han et al. 2024).

Allelopathic Plants and Natural Herbicides

Allelopathic plants, an intriguing aspect of ecological interactions, play a pivotal role in natural weed management through the release of allelochemicals. These compounds, found in plants like black walnut, sunflowers, and specific rice varieties, possess the ability to inhibit the germination and growth of neighboring plants. Similar to other allelopathic plants, sunflowers release compounds that hinder the growth of weeds, which makes them useful in crop rotation schemes. Certain types of rice help suppress weeds by producing substances like momilactone (Serra Serra et al. 2021). These allelopathic qualities can be used to create natural herbicides, which offer a more environmentally friendly option than their synthetic equivalents. These organic herbicides have advantages including biodegradability, reduced detrimental impact on the environment, and conservation of biodiversity. To control allelopathic chemicals specificity and improve application techniques, nevertheless, much thought is required. There is hope for resilient and sustainable weed control techniques in landscape and agriculture by utilizing the potential of allelopathic plants and natural herbicides (Kostina-Bednarz et al. 2023; Berestetskiy 2023).

Among other plant products as herbicides, juglone (allelochemicals) released through roots, leaves, and nuts, from black walnut (Juglans nigra), was found to be effective against redroot pigweed (Amaranthus retroflexus), velvetleaf (Abutilon theophrasti), and barnyard grass (Echinochloa crus-galli) and also influencing the vegetation in their vicinity (Michael et al. 2010). Sorgoleone is another allelochemical that is formed by the root hairs of Sorghum bicolor. It is extruded as oily droplets, accumulates in the soil, and suppresses photosynthesis in seedlings that are still very young. Other significant plant compounds with potential herbicidal action are gallic acid (spurge), phlorizin (apple root), trimethyl xanthene (coffee), dhurrin (sorghum), and cinch (eucalyptus) (Motmainna et al. 2023; Thang et al. 2023).

Forestry/Agroforestry Allelopathic Effects on Crops/Annuals

Forestry and agroforestry practices involve the management and cultivation of trees and shrubs alongside agricultural crops. One significant aspect of these practices is the allelopathic effects they can have on crops and annual plants. Tree species may release allelochemicals through their roots, leaves, or decomposition of organic matter, affecting the growth, development and the productivity of neighboring crops and annuals (Kumari et al. 2016).

Tree species such as Eucalyptus spp., release allelochemicals (1,8-cineol) which can accumulate in the soil and interfere with the growth of Amaranthus retroflexus (Azizi and Fuji 2006). Similarly, Juglans nigra also release allelochemical (Juglone) and affect the growth and productivity of the number of crops for instance tomato, alfa alfa, strawberry and soybean (Bohm et al. 2006; Jose and Holzmueller 2008).

Pinus spp. is releases a allelochemicals in the form of terpenes (α-pinene, β-cariofilene and α-humulene), phenolic compounds (9α,13β-epidioxyabeit-8(14)en-18-oic acid), and flavonoids (quercetin, catechin, kaempferol, myricetin) and affect the growth, germination, nutrient uptake and productivity of A. sativa, L. minor, F. arundinacea and C. dactylon (Nektarios et al. 2005; Ormeno et al. 2007; Kato-Noguchi et al. 2009). Allelopathy poses challenges for farmers and land managers as they must carefully select tree species and manage their spatial arrangement to minimize negative impacts on crop productivity while maximizing the benefits of agroforestry systems.

Allelopathy and Genetic Manipulation

The development of cultivars with allelopathic potential that reduces dependence on chemical herbicides and also ensures less environmental pollution can be one of the potential applications of allelopathy. Genetic variation with respect to allelopathic potential has been reported in several cereal crops and can be utilized in conventional breeding programs to develop varieties with improved allelopathic properties (Jensen et al. 2001).

These existing variations can be utilized in breeding programs and can also act as a source of candidate genes, which can be utilized in gene introgression and genetic manipulation. Although work has been done in the conventional breeding of allelopathic crops, very limited to negligible research is available on genetic manipulation for allelopathic traits. Duke et al. (2001) exhaustively reviewed the scope and application of genetic engineering in developing allelopathic crops. According to the review, the allelopathic potential of any crop can either be increased by the over-expression of key genes involved in the biosynthesis of particular allelochemical or by the introduction of novel gene(s) into a crop through genetic transformation to enable the production of desired allelochemical(s).

This way, crop plants can be imparted more competitive ability over weeds, and farming activities could be made less dependent on chemical herbicides. As shown in Fig. 5, strategies for developing allelopathic crops through molecular interventions may require certain primary steps to be known. Firstly, the particular allelochemical should be characterized, and its proper identification is necessary for deducing its biosynthesis pathway. Secondly, the key enzymes and factors involved during biosynthesis are to be deciphered, and then finally, the respective gene(s) encoding target enzymes and any regulatory sequences like the promoters can be manipulated for over-expression.

Fig. 5.

Showing strategies for the development of allelopathic crops through molecular interventions. Two scenarios are presented: ‘Manipulation of any existing allelopathic trait(s)’ that would begin with identifying and characterizing the potential allelochemical and then proceeding towards identification of proteins and respective gene(s) involve in biosynthesis (steps shown in bold boxes). The dotted boxes outline some of the techniques and approaches that lead to the pathway elucidation and gene identification. Once gene(s) are identified within a plant, overexpression and gene silenced lines can be developed accordingly to manipulate allelochemical production. Another strategy involves ‘Introduction of the new allelopathic trait(s)’ that involves the transformation of allelochemical encoding transgene(s) into host plants (steps outlined in bold boxes) through standard genetic engineering methods (dotted boxes). Additionally, challenges associated with both approaches are presented

Both strategies of allelochemical manipulation, whether through genetic engineering or transgenic approaches, hold promise but pose significant challenges. Structural and functional information about target allelochemical-producing genes is essential for successful genetic modification in candidate crops. However, many allelochemical biosynthesis pathways are poorly understood, involving multiple genes and requiring precise targeting, often to roots, for expression and exudation into the soil. Environmental factors, tissue specificity, and genotypic variation must also be considered during metabolic pathway modification for allelochemical production. Furthermore, the complexity increases when groups of allelochemicals act synergistically, necessitating manipulation of multigene phenomena. Additionally, the introduction of foreign genes into crops must not compromise yield or growth parameters. Although the commercialization of allelopathic crops through genetic modification has yet to be realized, molecular studies in rice and other plants have identified genes contributing to allelopathic potential (Wu et al. 2000; Gealy and Yan 2012; Peng et al. 2014; Hickman et al. 2021).

Detailed analysis of allelopathy phenomena is conducted through genetically modified overexpression or repression lines in model crops like rice, providing valuable candidate genes for genetic improvement programs such as breeding or transgenics (Li et al. 2020). Studies across crop species have identified genes or proteins involved in allelochemical biosynthesis pathways, offering potential for the development of transgenic plants expressing unique allelopathic properties (Song et al. 2008).

For instance, rice exposed to low nitrogen conditions exhibited increased allelopathic activity, with overexpression of genes encoding phenolics biosynthesis and detoxification enzymes like phenylalanine ammonia lyase, O-methyltransferase, triosephosphate isomerase, and cyt-P450. Proteomic analysis revealed induced expression of phenylalanine ammonia lyase, HMG CoA reductase three, and a thioredoxin in rice grown alongside E. crus-galli (barnyard grass weed) (Lin et al. 2004). Additionally, a MYB transcription factor gene in rice has been characterized, influencing the crop’s allelopathic potential (Fang et al. 2020).

The characterized OsMYB57, when expressed in higher amounts under the influence of the VP64 transcription activator, upregulates key genes in the phenylpropanoid pathway, elevates L-phenylalanine contents, and enhances rice plants’ inhibitory action against barnyard grass (Zhao et al. 2015). Comparative studies between allelopathic rice PI312777 and non-allelopathic rice Lemont revealed higher expression levels of OsMAPK11 and OsPAL2,3 proteins in the allelopathic variety. These findings shed light on rice allelopathy behavior and suggest avenues for enhancing allelopathic traits through genetic manipulation.

Additionally, studies on the biosynthetic pathways of momilactone B, a potent weed-suppressing allelochemical in rice, have identified key genes via reverse genetics gene-knockout approaches (Xu et al. 2012). Furthermore, a differential gene expression analysis between alleopathic (PI312777) and non-allelopathic (Lemont) rice varieties exposed to barnyard grass root exudates highlighted the involvement of genes in shikimate and acetic acid metabolic pathways, with significant differential expression observed in both rice accessions (Zhang et al. 2019).

Transgenic lines of allelopathic rice PI312777, with varied expression levels of the OsPAL2-1 gene, exhibited differential phenolic acid exudation, influencing the growth of rhizosphere myxobacteria and demonstrating allelopathic effects on barnyard grass. Overexpression of OsPAL2-1 led to higher phenolic acid release, particularly ferulic acid, stimulating chemotactic activity in myxobacteria and triggering the production of various allelochemicals (Li et al. 2020).

Similarly, transgenic tobacco plants expressing caffeine biosynthesis genes showed significant caffeine production, offering potential insect pest inhibition. These developments underscore the importance of genetically modified lines in elucidating allelopathic gene functions and paving the way for future advancements in allelopathic transgenic crops. Once functionally characterized, these candidate genes could be introduced into non-allelopathic species to study their phenotypic effects (Yang et al. 2004).

In sorghum, the cloning of the SOR1 gene involved in sorgoleone biosynthesis and the identification of allelopathic trait quantitative trait loci (QTLs) offer insights into the biosynthetic pathways of sorgoleone. Additionally, studies on regulatory compounds like methyl jasmonate and jasmonic acid in sorghum allelochemical biosynthesis gene expression regulation, along with structural and functional genomics studies in garlic, further contribute to understanding allelopathic mechanisms (Cheng et al. 2016; Shehzad and Okuno 2020).

The advancements in next-generation sequencing (NGS) technology have revolutionized gene discovery and trait analysis in plant genomes, facilitating the generation of comprehensive genomic datasets and enabling the study of intricate mechanisms underlying crop and allelopathy and plant-plant interactions. High-throughput NGS platforms offer valuable functional insights into the genetic basis of allelopathy in crops and weeds, providing a foundation for transgenic approaches to introduce weed-suppressive traits into non-allelopathic crops (Peng et al. 2014).

However, the complexity of this process necessitates a thorough understanding before practical implementation. Successful transformation requires the precise regulation and localization of multiple gene cassettes, along with addressing socio-political concerns surrounding genetically modified crops expressing foreign genes. Rigorous assessments of weediness, ecological impact, and resistance to allelochemicals are imperative for the responsible development and commercialization of transgenic allelopathic crops, highlighting the importance of comprehensive risk assessment before widespread adoption (Duke et al. 2001; Bertin et al. 2008).

Future Prospects and Challenges

Recent advancements in research methodologies, biotechnological manipulation, field management techniques, and technical instrumentation have significantly expanded our understanding of allelopathy. There is a growing focus on disease resistance, defense mechanisms, and chemical signaling among plants. Understanding allelochemical actions in soil holds promise for improving weed and pest control in agroecosystems, with recent in-silico analyses uncovering potential fungicidal properties in certain proteins from Prosopis cineria. Using allelopathic processes efficiently helps govern agroecosystems, with current objectives being on crop selection, breeding techniques, and the use of allelopathic substances as bioherbicides.

Allelopathy offers potential applications in controlling nutrient soil dynamics, enhancing plant nutrient utilization, and mitigating heavy metal toxicity. Despite these promising prospects, many aspects of these interactions remain poorly understood. Investigating the impact of soil physical and chemical characteristics, particularly soil texture and structure, on allelochemical phytotoxicity presents a significant challenge. Understanding the complex plant-microorganism interactions in the rhizosphere is crucial for elucidating aboveground chemical communication and physiological processes. While hundreds of allelochemicals have been identified in root exudates, further research is needed to elucidate their transport mechanisms across plasma membranes and to monitor the genes involved in breeding programs.

Future studies should focus on deciphering the mode of action of allelochemicals and formulating them into commercial weed control products. Given the complexity and heterogeneity of soil systems, interdisciplinary collaboration among agronomy, ecology, plant physiology, and soil chemistry is essential. Integrating allelopathy into herbicide studies, plant breeding, and crop production has the potential to revolutionize our understanding of crop-environment interactions and enhance agricultural and forest sustainability.

Conclusion

The allelopathic effects on agroecosystems in a changing environment are complex and multifaceted. The physiological and molecular insights into these effects have revealed a range of mechanisms that can be used to improve crop productivity and reduce the negative impacts of allelopathy. These include using allelochemicals to reduce competition between plants, manipulating plant hormones to increase crop yield, and using physiological and molecular approaches to modify the expression of allelochemicals. Furthermore, its importance in nature is now widely recognized. Even though plant-plant interference problems have shown to be a substantial hurdle to understanding how allelopathy works, allelopathy research has grown in scale and diversity in recent years. Moreover, as environmental changes are undergoing, allelopathy research is gaining traction, and the physiological and ecological mechanisms of allelopathy are increasingly being elucidated. This article has focused on understanding allelopathy’s molecular, physiological, and ecological consequences.

Declarations

Conflict of interest

The authors declare no conflict of interest.