Allelopathy and Allelochemicals of Leucaenaleucocephala: Comparison
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Leucaena leucocephala (Lam.) de Wit is native to southern Mexico and Central America and is now naturalized in more than 130 countries. The spread of L. leucocephala is probably due to its multipurpose use such as fodder, timber, paper pulp, shade trees, and soil amendment. However, the species is listed in the world’s 100 worst invasive alien species, and an aggressive colonizer. It forms dense monospecific stands and threatens native plant communities, especially in oceanic islands. Phytotoxic chemical interactions such as allelopathy have been reported to play an important role in the invasion of several invasive plant species.

  • invasive plant
  • allelochemical
  • mimosine
  • phytotoxicity
  • rhizosphere soil

1. Introduction

Leucaena leucocephala (Lam.) de Wit, belonging to Fabaceae, is native to southern Mexico and Central America [1][2]. The species is essentially a tropical species with poor cold tolerance, situated at a latitude between 30 degrees north and south of the equator. It grows well where an annual precipitation is between 650 mm and 3000 mm with dry seasons up to 4–6 months, and an average annual temperature is between 25 °C and 30 °C [3][4][5]. Three subspecies of L. leucocephala are recognized; ssp. leucocephala is shrubby and highly branched up to 5 m in height, ssp. glabrate is a large trunk with poorly branched up to 20 m in height, and ssp. ixtahuacana is medium-sized and grows up to 10 m in height with many branches [1][2][6]. The species has alternate and bipinnate leaves with 4–9 pairs of pinnae per leaf, and 13–21 pairs of leaflets per pinnae (Figure 1). The leaves show nyctinasty in the evening [7]. It is an evergreen but facultatively deciduous species under stress conditions such as low temperature and severe dryness [1][2]. L. leucocephala is a fast-growing species, capable of reaching reproductive maturity within 12 months, and 4 months under ideal condition [8][9]. Flower heads actively grow young shoots of 12–21 diameter, and bear 100–180 flowers per head. One flower head generates 5–20 pods. Pods are 11–19 cm long 15–21 mm wide and contain 8–18 seeds per pod (Figure 1). The species flowers all year-round and produces abundant seeds, mostly by self-fertility [2][6].
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Figure 1.
Leucaena leucocephala
. (
A
) Leaf, (
B
) Flower head, (
C
) Flower, (
D
) Pod. Photos were taken in Yoron Island, Japan by Kato-Noguchi.
L. leucocephala was carried from Central America, probably as livestock fodder, to the Philippines, Guam, and West-Pacific islands between the 16th and 18th century [3][10]. The species was also introduced to plantations in Indonesia, Papua New Guinea, Malaysia, and other counties of Southeast Asia. It was then taken to Hawaii, Australia, India, East West Africa, and Caribbean islands during the 19th century [3][11]. The distribution of the species has already expanded throughout the tropic and subtropics [1][2].
One of the reasons of the spread of L. leucocephala is probably due to its beneficial traits. The species is recognized as a high quality and nourishing fodder tress in the tropics and subtropics. It is used for feedstuff for ruminants (cattle, water buffalos, and goats) and non-ruminants (rabbit, chickens, and fishes) [3][12]. The leaves of the species contain high levels of protein (22–28% of the dry weight) with essential amino acids such as phenylalanine, leucine, isoleucine, and histidine, and several minerals such as calcium and phosphorus [13][14][15]. It contains carbohydrates up to 20% of the dry weight [14]. The species is also used for paper pulp and timber. The wood is strong and medium density, and suitable for carpentry materials. Its caloric value as fuelwood is about 4600 calories per kg, and its biochar improves soil property of crop fields [16][17][18][19].
L. leucocephala works as shade trees in several plantations such as coffee, tea, and cacao. It also acts as a shelterbelt for a variety of crops [20][21][22]. The species is a possible candidate for the restoring vegetation covering slops, watersheds, and degraded lands to reduce erosion, and to recover vegetation [23][24][25]. In addition, its leaves and young pods are used as vegetables by local people in Central America and South Asia. Brown, red, and black dyes are extracted from its pods, leaves, and bark in Mexico. The roots and bark of the species are also used for a folk remedy, and the roots are used to get an abortion [3][26]. Thus, L. leucocephala is widely recognized as a multipurpose plant species.

2. Allelopathy

Allelopathy is chemical interaction among plants and caused by allelochemicals [27], which are produced in plants and released into the vicinity of the plants including rhizosphere soil either by root exudation, decomposition of plant litter and residues, and rainfall leachates and volatilization from the plant parts [28][29][30].

2.1. Plant Extract

Allelopathic activity of the extracts of leaves, seeds, bark, and aerial parts of L. leucocephala on crops and weeds were determined since allelochemicals are synthesized and accumulated in certain plant parts [27][28][29][30]. Aqueous extracts of the leaves of L. leucocephala suppressed the radicle growth of Lactuca sativa L. and Oryza sativa L. seedlings [31], and the seedling growth of Ischaemum rugosum Saisb and Vigna radiata (L.) R. Wilczek [32]. Its aqueous leaf and seed extracts showed the inhibitory activity on the germination and seedling growth of three weed species, Ageratum conyzoides L. Tridax procumbens L., and Emilia sonchifolia (L.) DC. Ex Wight [33]. Aqueous leaf, seed, and bark extracts of L. leucocephala inhibited the germination, growth, and crop yield of Zea mays L. under pot culture conditions [34].

2.2. Leachate

For the simulation of rainfall conditions, plant tissues were soaked in water, and its supernatant was used as leaches from the tissues by rainfall [35][36][37][38][39]. The senescent leaves of L. leucocephala was soaked in water for 48 h, and its supernatant showed inhibitory activity on the germination and growth of Raphanus sativus L. [37]. The soaking water of L. leucocephala leaves also enhanced electrolyte leakage from the leaf cells of Eichhornia crassipes (Martius) Solms. and increased the activities of catalase and ascorbate peroxidase in the leaves [38].

2.3. Plant Litter and Residue

Leaf litter of L. leucocephala was mixed with soil, and the seeds of a woody plant, Albiza procera (Roxb.) Benth., and crop plants, Vigna unguiculata (L.) Walp., Cicer arietinum L. and Cajanus cajan (L.) Millsp. were sown into the mixture. The treatments resulted in the suppression of the germination and growth of these test plant species [39]. Soil mixture with decomposing leaves of L. leucocephala increased the mortality of five tree species, Alnus formosana (Burkill) Makino, Acacia confusa Marr., Liquidambar formosana Hance, Casuarina glauca Sieber, and Mimosa pudica L. [31]. Aqueous extracts of L. leucocephala litter, which accumulated on the forest floors, showed the suppression of the germination and radicle growth of Lolium multiflorum Lam. [31], and Ageratum conyzoides L. Tridax procumbens L., and Emilia sonchifolia (L.) DC. ex Wight [40]. Leaf mulch of L. leucocephala covered on soil surface or mixed with soil inhibited the germination and growth of Vigna unguiculata (L.) Walp., and the root nodulation of V. unguiculate [41]. Those observations indicate that leaf litter and residues of L. leucocephala may contain certain allelochemicals, and some of them may be liberated into the soil during their decomposition processes.

2.4. Rhizosphere Soil and Root Exudate

The seeds of Ageratum conyzoides L., Tridax procumbens L., and Emilia sonchifolia (L.) DC. ex Wight were sown into the soil collected from L. leucocephala infested areas. The treatments resulted in the suppression of the germination and growth of those plant species [40]. Rhizosphere soil of L. leucocephala also inhibited the germination and growth of Vigna radiata (L.) R.Wilczek and Glycine max L. [42]. Aqueous extracts of the soil of the forest floors under L. leucocephala trees showed the inhibition of the radicle growth of Lactuca sativa L. [31]. In addition, root exudates from L. leucocephala showed the suppression of the germination and growth of Ageratum conyzoides L., Tridax procumbens L., and Emilia sonchifolia (L.) DC. ex Wight [40]. Those observations suggest that rhizosphere soil of L. leucocephala may contain certain allelochemicals, which may be supplied through root exudation, decomposition of plant litter and residues, and rainfall leachates.

3. Allelochemical

Phenolic acids, flavonoids, and mimosine were isolated and identified from L. leucocephala as its allelopathic agents (Figure 2).
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Figure 23. Allelochemicals identified in L. leucocephala. (1) p-hydroxybenzoic acid, (2) protocatechuic acid, (3) vanillic acid, (4) gallic acid, (5) p-hydroxyphenylacetic acid, (6) p-hydroxycinnamic acid, (7) caffeic acid, (8) ferulic acid, (9) epicatechin, (10) epigallocatechin, (11) gallocatechin, (12) quercetin, (13) mimosine.

3.1. Phenolic Acid

Phenolic acids such as p-hydroxybenzoic acid (1), protocatechuic acid (2), vanillic acid (3), gallic acid (4), p-hydroxyphenylacetic acid (5), p-hydroxycinnamic acid (6), caffeic acid (7), and ferulic acid (8) were identified in the leaves of L. leucocephala. Total concentrations of those phenolic acids in young leaves were 2-fold greater than those in mature leaves [31]. The concentration of total phenolic compounds in L. leucocephala plants was estimated to be 1.3 to 2.8 mg g−1 of dry weight of the plants [43]. Phenolic acids have been found in a wide range of plants, plant residues, and soils, and their involvement has been often mentioned in the allelopathy of those plant species [44][45].

3.2. Flavonoid

Flavonoids such as epicatechin (9), epigallocatechin (10), and gallocatechin (11) were identified in L. leucocephala roots. Those compounds inhibited the nitrification process, which is an important step in the nitrogen cycle in soil [46]. Quercetin (12) and other 16 flavonoids were identified in L. leucocephala leaves, and some of them showed antioxidant activity [47]. L. leucocephala was reported to contain condensed tannins, which may contribute towards the plant resistance to pathogens and insects. [48][49][50].

3.3. Mimosine

Mimosine (13); L-mimosine, synonym; leucenol) is a non-protein amino acid. It was first isolated from Mimosa pudica L [51], and found in some other species of the genus, Mimosa and Leucaena, including L. leucocephala [52][53][54]. Mimosine possesses a wide range of pharmacological and biological properties, such as anti-tumor, apoptotic, anti-inflammation, anti-viral, and cell cycle blocking effects [55]. It also possesses the inhibitory activity on the germination and growth of several plant species [31][56][57]. Therefore, mimosine is possibly involved in the allelopathy of L. leucocephala.

4. Conclusions

Although the economic value of L. leucocephala is widely recognized, the species is listed in the world’s 100 worst invasive alien species. It is an aggressive colonizer and forms dense monospecific stands. It interferes the regeneration and replacement of native plant species in its dominant forests. The species richness in L. leucocephala invaded forests was lower than that in its uninvaded forests, and seedling establishment of native plant species under L. leucocephala invaded areas was also low. Sunlight intensity and other conditions of the forest floors between L. leucocephala forests and native forests were not apparent. In addition, plant extracts, leachates, root exudates, plant litter and residues, and rhizosphere soil of L. leucocephala showed the enhancement of the mortality and suppression of the germination and growth of several plant species including weeds and woody plants. Those observations suggest that L. leucocephala is allelopathic and contains allelochemicals which affect the plant mortality, germination, and growth, and some of the allelochemicals may be released into the vicinity of L. leucocephala, including its rhizosphere soil. L. leucocephala produces a large amount of mimosine and accumulates it in almost all parts of the plants. Mimosine showed growth inhibitory activity against several plant species including some shrubs and another invasive plant species. Mimosine blocked cell division of protoplasts from Petunia hybrida between G1 and S phases, and disturbed some enzyme activities such as peroxidase, catalase, and IAA oxidase. In addition, several phenolic acids and flavonoids were identified in L. leucocephala. However, the concentrations of mimosine, phenolic acids, and flavonoids in the rhizosphere soil and vicinity of L. leucocephala have not yet been reported. The information is essential to evaluate the contribution of mimosine, phenolic acids, and flavonoids to the allelopathy of L. leucocephala.

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