Phytotoxic Substances Involved in Teak Allelopathy and Agroforestry

: Teak ( Tectona grandis L.f.) is one of the most valuable timber species, and is cultivated in agroforestry systems in many countries across the tropical and subtropical regions of the world. The species is also one of the most essential trees in home gardens in South Asia due to its wood quality and medicinal value in folk remedies. It is a deciduous tree species, and the amount of litter that falls from teak trees is huge. The decomposition rate of the litter is relatively fast in tropical humid conditions. The interactions between teak and weeds, or crops, under the teak trees have been evaluated in terms of allelopathy. Evidence of allelopathy is documented in the literature over the decades. The leachate and extracts of teak leaves suppress the germination and growth of several other plant species. Phytotoxic substances, such as phenolics, benzofurans, quinones, terpens, apocarotenoids and phenylpropanoids, in the teak leaves, were isolated and identiﬁed. Some phytotoxic substances may be released into the soil under teak trees from leaf leachate and the decomposition of the litters, which accumulate by annual leaf fall and can affect the germination and growth of undergrowth plant species as allelopathic substances. The allelopathy of teak is potentially useful for weed management options in agroforestry and other agriculture systems to reduce commercial herbicide dependency. It was also reported that agroforestry systems with teak enhance income through the production of crops and woods, and provide energy efﬁciency for crop cultivation.


Introduction
Teak (Tectona grandis L.f.), belonging to the family of Lamiaceae, is a large deciduous tree up to 40 m in height. The leaves are ovate (40 cm long, 20 cm wide) and hairy on the lower surface. It has small, fragrant white flowers attached in panicles at the end of its branches. Teak is one of the most valuable timber species because of its beautiful appearance and durable property [1,2]. Although native to South and Southeast Asia, the significant economic potential of teak wood led the species to be introduced into the agroforestry systems of many countries across tropical Asia, Africa and Central and South America [3][4][5][6][7].
Home gardens in tropical and subtropical countries surround residences of local inhabitants, and create small forest-like structures. They are considered to be the traditional agroforestry systems characterized by complexity of the structure and multiple functions. Home gardens consist of various kinds of tree species, with crops, livestock, poultry and fishes-those species have been selected by local inhabitants for their preference, productivity and sociocultural aspects. Home gardens provide various food and goods, including commodities such as animal products, fruits, vegetables, folk medicine, ornamentals, fodder, timber and fuel [8][9][10][11][12][13]. Teak is one of the most essential trees in home gardens in South Asia, because it is a very precious wood species and important in folk remedies [8,14,15]. Hot water extracts of teak barks are applied for the treatment of bronchitis, biliousness, hyperacidity, diabetes, dysentery, and leprosy. Water extracts of teak leaves are used in pruritus, stomatitis, ulcers and wounds. Hot water extracts of teak roots are applied for anuria treatments. Oil extracts of the flowers are useful for scabies and hair growth. It has also been used as an important plant in Ayurvedic treatments [2,16].
Evidence of the pharmacological properties of teak plants has been accumulated over the past decades. Ethanol extracts of teak leaves have shown significant wound healing activity [17]. Ethanol extracts of teak roots have hyperglycemic activity [18]. Ethanol extracts of teak barks show anti-inflammatory and analgesic potentials [19]. Petroleum ether extracts of teak seeds have hair growth activity [20]. Many compounds with pharmacological activities were also isolated from various parts of teak plants [2,16,21].
Some plants have shown excellent weed control abilities as soil additives and/or in intercropping, due to their characteristics of allelopathy [22,23]. Plants produce hundreds of secondary metabolites. Some of those compounds are released into the surrounding environments through root exudation, volatilization, leaching and decomposition of the plants. Those compounds with allelopathic activity are able to inhibit the growth and germination of neighboring plant species [24][25][26]. Therefore, allelopathy of plants is potentially useful for weed management options in several agriculture settings, including agroforestry systems, for the reduction of commercial herbicide dependency [27,28]. Many phytotoxic substances with allelopathic activity in teak have already been isolated and characterized. However, there has been no review article about the phytotoxic substances involved in teak allelopathy. Thus, this review provides a short overview of allelopathic properties and phytotoxic substances which have allelopathic activities of teak, and discusses the importance of allelopathy for agroforestry systems.

Ecological Impact of Teak
The effects of teak on biodiversity, and its allelopathic effects, are discussed in this section. Teak plantations have replaced a significant proportion of natural forests in the tropical and subtropical regions in the world, and have, subsequently, affected the biodiversity of those forests [29][30][31][32]. The population and diversity of the understory vegetation of the 10-year-old teak plantation were reported to be significantly less than those of native rehabilitated forests nearby, although sunlight intensity on the forest floor was not different between them [4]. Weed diversity under teak trees was also lower than that under the trees of Albizzia procera (Roxb.) Benth., Aleurites fordii (Hemsl.) Airy Shaw, Arceca cantechu L., Azadiratcha indica A.Juss., Gmelina arborea Roxb., and Toona ciliata M.Roem. [33]. There were also more understory plant species outside of the teak canopy than under its own canopy [34].
The shade produced by large teak leaves may partially explain this phenomenon. The allelopathic characteristics of teak may also be one of the reasons to reduce the population and diversity of undergrowth plant species of teak forests. Several phytotoxic substances were identified in teak leaves [2,16,21,35]. Teak leaves drop to the forest floor through annual defoliation, and the phytotoxic substances in the leaves may be common in the forest soil due to the decomposition process of the leaves. Those substances may affect the growth of undergrowth plant species. Therefore, many researchers have focused on evaluating the allelopathic potential of the leaves, as teak is a deciduous tree species [2,16,21,35]. In addition, the amount of fallen leaf litter is significant [36].

Allelopathic Property of Teak
The allelopathic activity of leachate, leaves, and extracts of teak are discussed in this section.

Leachate
Teak leaves were soaked in water for 24 h and the soaking water was applied as leaf leachate. The soaking water suppressed the germination and growth of cowpea (Vigna unguiculata (L.) Walp.), Momordica charantia L. and eggplant (Solanum melongena L.) in Petri dish and pot culture conditions [37]. Leaf litter under teak trees was mixed with washed sand and the mixture was percolated with water. The water from the mixture also suppressed the germination and seedling growth of Cicer arietinum L. [38]. Those results suggest that some phytotoxic substances may be released from teak leaves by water as leaf leachate.

Effects of Teak Leaves
Teak leaves were used as mulch for the cultivation of turmeric (Curcuma longa L.) for six months, and the treatments resulted in significantly lower yield of turmeric rhizome [15]. Powder (100 g/7.2 m 2 ) of fallen teak leaves was applied on a field of wheat (Triticum aestivum L.), and weed emergence on the field was monitored. The dominant weed species in the field were Cyndon dactylon (L.) Pers., Echinochloa colona (L.) Link, Cyperus rotundus L., Cyperus difformis L., Amaranthus viridis L., Chenopodium album L. and Melilotus alba L. At 21 days after the powder application, a 45% reduction in weed population was observed. However, the treatment did not affect the growth of wheat [39]. Those observations indicate that some phytotoxic substances were released from teak leaves, and suppressed weed eminence and growth.

Extract of Teak Soil
The chemicals in soil under teak trees were extracted with water, and allelopathic activity of the extracts was determined by tomato (Solanum lycopersicum L.). The extracts inhibited the germination and growth of tomato with extract concentration dependently [40,41], which indicated that the soil contained some phytotoxic substances.

Extracts of Teak Leaves
Aqueous extracts of fallen teak leaves inhibited the seedling growth and protein contents of Vigna mungo (L.) Happer and Vigna radiata (L.) R.Wilczek [42]. Methanol extracts of fallen leaves of teak reduced the germination of Echinochloa colona L. and Cyperus difformis L. [43]. Methanol extracts of fallen teak leaf powder were applied in a wheat field (10.8 g methanol extract residue/7.2 m 2 ) and weed emergence in the field was monitored. The highest reduction (56%) in weed population was recorded 14 days after treatments. However, the treatment did not affect the growth of wheat [39].
Aqueous extracts of teak roots suppressed the germination and seedling growth of Hibiscus esculentus L. [51]. Inhibitory activity of the extracts of teak leaves, barks and seeds was compared against the growth of maize (Zea mays L.), and leaf extracts showed the greatest inhibitory activity [52]. Those findings described in this section indicated that the extracts of the fallen and fresh teak leaves, roots and barks suppressed the germination and growth of many plant species, both weeds and crops. Those findings also suggested that the leaves, roots and barks may contain some phytotoxic substances, which are extractable with water and/or methanol. Allelopathic activity of the leachate, leaves, and extracts of teak and target plant species, are summarized in Table 1.

Phytotoxic Substances with Allelopathic Activity in Teak
Phytotoxic substances with allelopathic activity identified in teak are discussed in this section. All phytotoxic substances listed in Table 2 and Figure 1 were isolated from fresh teak leaves with water. Naphthotectone (3) inhibited the germination and seedling growth of wheat (Triticum aestivum L.), onion (Allium cepa L.), tomato (Lycopersicon esculentum L.), and lettuce (Lactuca sativa L.) [53]. Rhinocerotinoic acid (8) suppressed the germination and seedling growth of wheat and lettuce [54]. 2-Oxokovalenic acid (9) and 19-hydroxyferruginol (11) inhibited the germination and seedling growth of wheat, onion, lettuce; 3β-hydroxy-7,8-dihydro-β-ionol (15) inhibited the seedling growth of wheat, onion and tomato; and 3β-hydroxy-7,8-dihydro-β-ionone (16) inhibited the seedling growth of wheat, onion, tomato and lettuce [55]. Other compounds listed in Table 2 inhibited the seedling growth of wheat [54][55][56]. Although those compounds were isolated and identified from teak leaves for potential use as a source of natural herbicide model and/or bioactive compounds, the allelopathic effects of those compounds were determined only by crop plants. It may be necessary to determine the activity of those compounds on weed species.  [56] Several phenolics were also identified in teak barks and leaves [39,50,57]. Phenolic compounds have been found in a wide range of plants and soils, and often mentioned as putative allelopathic substances [58,59]. The importance and contribution of those phenolics found in teak are not clear because no information regarding the phytotoxic activity of those compounds for teak allelopathy is available in the literature. However, gallic and ellagic acids were identified in teak leaf extracts [60], and the allelopathic activity of those compounds isolated from other plant sources were reported [61,62]. Therefore, some phenolics in teak plants may contribute to the allelopathy of teak. Phenolic compounds inhibit some enzyme activities and physiological processes, such as plant hormone functions, water balance and mineral uptake, as well as stomatal functions, respiration, and photosynthesis [58,63].
A number of secondary metabolites in many classes have been isolated and identified from various parts of teak plants, such as barks, flowers, fruits, leaves and roots. Those compounds were quinones, terpenes, apocarotenoids, phenolics, flavonoids, saponins, lignans and norlignans [16,64]. Teak wood shows resistance to termite and fungal damages, and napthoquinones and anthraquinones contribute a resistance property [65][66][67][68]. Some other compounds were also related to the pharmacological activities of teak [2,16,21,35,57]. Although those compounds have been associated with the pharmacological effects and property of its wood characteristics, some of those compounds may possess phytotoxic activity. Appl. Sci. 2021, 11, x FOR PEER REVIEW 6 of 11

Teak Allelopathy
A possible release process of phytotoxic substances with allelopathic activity is discussed in this section. In agriculture and forestry systems, phytotoxic substances in plants can be released into the soil, either by the exudates from living plant tissues or by the decomposition of plant residues. Some of those substances have allelopathic effects [25,26,69]. Annual litter fall from teak trees onto forest floors varies, from 1.7 to 6.4 t/ha, which will depend on the tree's age. More than 90% of the litter originates from fallen leaves because teak is a deciduous tree species. About 25% of teak litter on the forest floor decomposes during the initial 60 days after accumulation [70], and 54% of the accumulated litter decomposes in the first six months [36]. Compared with other tropical plant species, such as Paraserianthes falcataria (Mig.) Barmeby & J.W.Grimes and Eucalyputus tereticornis Sm., the decomposition rate of teak litter was faster than that of their litters in tropical humid conditions [71][72][73].
The phytotoxic substances in the leaves may be liberated into forest soil by the decomposition process of the leaves, and act as allelopathic substances. Allelopathic substances are able to inhibit germination, seedling establishment, and plant growth of other plant species [25,26,69]. In fact, a substantial number of phytotoxic substances with allelopathic activity were identified in teak leaves ( Table 2). It was also reported that the soil under teak trees had inhibitory characteristics [40,41]. Therefore, teak trees may be able to inhibit the germination and growth of understory plant species through their allelopathy.

Agroforestry System with Teak
Agroforestry systems and the allelopathy of teak are discussed in this section. Agroforestry systems are characterized by a combination of tree and crop cultivations and have been recognized as a sustainable land use system over conventional agriculture [74]. Trees can provide microclimate conditions suitable for crop production, and contribute a large amount of litter on the soil surface. The litter fall increases organic matter in the soil and decreases soil erosion [75][76][77][78]. However, it is essential to design agroforestry systems with an appropriate selection of tree and crop combinations, and the distribution of resources, such as light, water, nutrients, and space requirements, for those combinations [74,79].
Teak was introduced into the agroforestry systems in many countries in tropical and subtropical regions because of its significant economic potential [3,4,7]. The effects of teak trees on crop productions have been evaluated in several agroforestry systems. Coffee cultivation in agroforestry systems with teak increased organic matter and phosphorus contents in the soil, as well as coffee yield [80]. Crop productions with cultural rotations of upland rice, cotton (Gossypium arboretum L.), cassava (Manihot esculenta Crantz), chilli, and ginger succeeded in teak agroforestry systems [81]. These systems also resulted in good production of peanut (Arachis hypogaea L.), soybean (Glycine max (L.) Merr.) [82], and rice [83]. In addition, teak leaf mulching provided a significantly high rhizome yield of ginger [84]. The reasons for the increases in crop productions were not mentioned clearly; it may be because of the inhibition of the emergence and growth of the competitive weed species [80][81][82]. The selection of crop plant species and development of their production systems with teak are necessary to avoid the phytotoxic effects of teak and enhance crop productivity. Agroforestry systems with teak may be able to integrate the balance of crop production, ecological aspects and sustainability [85]. Teak agroforestry systems are reported to provide 40% of household income through the production of the crops and woods [86], and to increase energy efficiency for crop production [87].

Conclusions
The teak leaf mulch, leachate, and extracts of teak leaves, roots, barks and soil suppressed the germination and growth of several other plant species (Table 1). Phytotoxic substances, such as phenolics, benzofurans, quinones, terpens, apocarotenoids and phenylpropanoids in the teak leaves, were isolated (Table 2). Those observations and findings suggest that teak is allelopathic and contains several phytotoxic substances with allelo-pathic activity. The evidence also shows that some of those phytoxic substances in teak are released into the soil under teak trees through the decomposition process of the litter. Those compounds possibly act as allelopathic substances. Allelopathic substances can inhibit the germination and growth of understory plants, both crops and weeds, in teak systems. Considering the importance of teak in agroforestry systems, the allelopathy of teak is potentially useful for weed management options in agroforestry and other agriculture settings to reduce commercial herbicide dependency for developing sustainable agriculture systems. The agroforestry system with teak may be able to integrate the balance of crop production, ecological aspects, and sustainability. However, the selection of crop plant species and development of their production systems with teak are necessary to avoid phytotoxic effects of teak and enhance crop productivity.