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Giant leucaena (Leucaena leucocephala subsp. glabrata):
a versatile tree-legume for sustainable agroforestry
Ahmed Bageel .Michael D. H. Honda .James T. Carrillo .Dulal Borthakur
Received: 22 June 2018 / Accepted: 11 April 2019 / Published online: 30 April 2019
ÓSpringer Nature B.V. 2019
Abstract Leucaena leucocephala (leucaena) is one
of the 22 Leucaena species that originated in Central
America. There are two major subspecies of leucaena,
L. leucocephala subsp. glabrata (giant leucaena) and
L. leucocephala subsp. leucocephala (common leu-
caena). Giant leucaena is a medium size fast-growing
tree important for agroforestry while common leu-
caena is a small bushy shrub that is considered to be an
invasive weed. Giant leucaena can be grown as a
woody tree of up to *20 m in height or maintained as
a bushy fodder legume by repeated harvest of its
foliage several times a year. Giant leucaena grown for
fodder can produce forage dry mater yield of up to
34 Mg ha
-1
year
-1
. High forage yield together with
high protein content makes leucaena an ideal fodder
legume for the tropical and subtropical regions of the
world. Although mimosine present in the leucaena
foliage has toxicity, it should not be a big concern
because ruminants can be successfully inoculated with
the mimosine-metabolizing rumen bacterium
Synergistis jonesii. Alternatively, mimosine present
in the leucaena foliage can be removed easily and
inexpensively through simple processing. Giant leu-
caena cultivars are generally free from diseases and
are highly tolerant to drought. Although infestation by
psyllids may be a problem, a number of psyllid-
resistant cultivars of giant leucaena have been devel-
oped through interspecies hybridization. The wood of
giant leucaena can be used for timber, paper pulp, or
biofuel production. Leucaena foliage and wood may
serve as raw materials for development of new
industry for production of phytochemicals such as
mimosine, tannins and anthocyanins, wood products,
and high-protein animal feed for farm animals in the
future.
Keywords Giant leucaena Fodder tree legume
Mimosine Psyllid resistance Drought tolerance
Agroforestry
Introduction
Leucaena leucocephala (leucaena) is a nitrogen-fixing
tree-legume suitable for sustainable agroforestry sys-
tems. Leucaena grows successfully in a wide range of
tropical and subtropical areas of the world where
minimum daily temperatures are above 15 °C, includ-
ing Central and South America, Africa, southern states
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s10457-019-00392-6) con-
tains supplementary material, which is available to authorized
users.
A. Bageel M. D. H. Honda J. T. Carrillo
D. Borthakur (&)
Department of Molecular Biosciences and
Bioengineering, University of Hawaii at Manoa, 1955
East-West Road, Honolulu, HI 96822, USA
e-mail: dulal@hawaii.edu
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Agroforest Syst (2020) 94:251–268
https://doi.org/10.1007/s10457-019-00392-6(0123456789().,-volV)(0123456789().,-volV)
of USA, Australia, the Philippines, Thailand, Indone-
sia, South-East Asia, and the Pacific Islands. There are
two major types of leucaena: giant leucaena that can
grow as large trees with a height of up to 20 m and
common leucaena that grows as a shrubby and
invasive weed (Fig. 1). Interestingly, giant leucaena
can also be grown and maintained as a shrubby and
high-yielding nutritious fodder for farm animals. The
aim of this review is to provide a comprehensive
discussion on the genetics, characteristics, cultivation
practices, utilities, improved varieties, and uses of
leucaena.
Genetics
The genus Leucaena belongs to Mimoseae tribe,
subfamily Mimosoideae in the Leguminosae family.
There are twenty-two identified Leucaena species;
most of them are diploid having 52 or 56 chromo-
somes (x = 26 or x = 28). The different Leucaena
species and their characteristics are briefly described
in supplementary Table S1. There are also five
tetraploid species (2n = 4x): L. leucocephala, L.
diversfolia, L. pallida, L. confertiflora, and L.involu-
crata. Among these, L. leucocephala,L. pallida, and
L.involucrata are known to be allotetraploids, while L.
diversifolia and L. confertiflora are considered to be
autotetraploids. L. leucocephala is an allotetraploid,
which evolved through natural hybridization between
L. pulverulenta and L. lanceolate (Pan and Brewbaker
1988). The distribution of the Leucaena species is
presented in supplementary Table S2.
Giant leucaena versus common leucaena
L. leucocephala subsp. glabrata, also, known as giant
leucaena, has glabrous leaflets (Hughes 1998a). In
subsp. glabrata, some leaflets contain fine ciliate hairs
along their margins towards the petiolule, and sparse
hairs may be found on the rachis (SA Harris, personal
communication). The natural populations of sub-
species glabrata are widely distributed in Tehuantepec
Fig. 1 Giant and common leucaena. aGiant leucaena trees at
the Waimanalo Research Station, University of Hawaii;
bcommon leucaena plants growing on a barren land in Hawaii
Kai, Honolulu showing its seediness characteristic; and cgiant
leucaena plants maintained as a bush shrub through repeated
harvest of the foliage every few months
123
252 Agroforest Syst (2020) 94:251–268
and northern Veracruz, Mexico (Za
´rate 1999). Sub-
species glabrata includes two different types, Peru and
Salvador, which originated in Peru and El Salvador
regions of South and Central America, respectively.
The trees of both Peru and Salvador types are tall and
high yielding, but they differ in branching behavior
and vigor. The Peru type branches low down on the
trunk while the Salvador type branches sparingly at the
base. Generally, the Salvador type is more vigorous
and matures earlier than the Peru type. The Peru type
cultivars are generally more suitable and productive as
forage than the Salvador type (Zarate 1984). K8, K28,
K29, K67, and K72 are examples of ‘Salvador type’
cultivars, while K5, Cunningham, and Peru are
examples of Peru-type cultivars of giant leucaena.
Because it is a multipurpose tree with various appli-
cations in industry, agriculture, and agroforestry, L.
leucocephala subsp. glabrata is the most important
and most studied among all Leucaena species.
Because of its high productivity and worldwide
success during the 1970s and early 1980s, giant
leucaena was once called a ‘miracle tree’ (Shelton and
Brewbaker 1994). It grows successfully in a wide
range of tropical environments, and shows high
tolerance to various environmental stresses including
drought, infection by microbial pathogens, and insect
pests. Although giant leucaena naturally grows as
medium-sized tall trees, it can be also maintained as
dwarf shrubs for fodder by repeated harvest of the
foliage several times a year. The natural populations of
subspecies glabrata are distributed in Mexico, Tehuan-
tepec and northern Veracruz (Walton 2003).
L. leucocephala subsp. leucocephala, also known
as common leucaena, in general, has smaller leaflets,
leaves and pods than subsp. glabrata. Shoots, leaves
and pods of common leucaena are sparsely pubescent
with very fine soft hairs. Its major differentiating
characteristics with giant leucaena are summarized in
Table 1. Common leucaena has a much shorter
vegetative growth stage in comparison to giant
leucaena. Compared to the tall and big size of giant
leucaena, common leucaena is a small bushy shrub
that forms a lot of seeds, because of which it can
spread easily and is considered invasive. It is an
aggressive colonizer of ruderal sites, disturbed and
degraded habitats, and occasionally agricultural lands.
In Hawaii, it is classified amongst the 12 worst pests
out of 86 serious alien invaders (Cronk and Fuller
1995). The name ‘‘koa haole’’ is generally used to
describe common leucaena, which originated in
Southern Mexico or Guatemala (Wheeler and Brew-
baker 1988). Morphological observations and limited
isozyme studies in Hawaii did not reveal much
variations among the populations of common leucaena
suggesting that common leucaena is made up of a
single genotype (Sun 1996; Brewbaker 2016). The
subspecies leucocephala has the same distribution
path as glabrata, which includes Mexico, Tehuantepec
and northern Veracruz (Walton 2003).
Leucaena germplasm and cultivars
Two major leucaena improvement programs based on
systematic germplasm collection and evaluation
started independently in two locations, one at the
CSIRO Research Station, near Brisbane, Australia in
late 1950s and the other at the Waimanalo Research
Station, University of Hawaii in early 1960s (Brew-
baker 2016). In 1962, Brewbaker and his colleagues
collected 347 accessions of common leucaena from
different parts of the world. They also made six
expeditions in Latin America and collected *500
accessions of giant leucaena. The leucaena germplasm
collection by Brewbaker, known as ‘the Hawaii
Collection’ contains a total of 1100 accessions
including 967 from Central America. The leucaena
germplasm collection in Australia, known as the
‘CSIRO Collection’ contained 815 accessions
(Hughes et al. 1995). Hughes from Oxford Forestry
Institute in UK made explorations for leucaena seed
collection from Central America in mid 1980s. His
collection, known as ‘the Oxford collection’, included
seeds from a total of 1116 trees comprising 99
provenances that included all 22 species of Leucaena
(Hughes et al. 1995).
Evaluation of the leucaena germplasm from Central
America showed that L. leucocephala subsp glabrata
as the most significant leucaena for agriculture
(Brewbaker 2016). Seventy-two accessions of giant
leucaena were planted in a duplicate trial in Waima-
nalo, Hawaii and a number of outstanding giant
leucaena lines, including K8, K28, K29, K67, K72,
K584 and K636 were selected from these accessions.
Some of the giant leucaena accessions in the Hawaii
Collection grew to mature heights of about 45 feet in
4 years, and had high-quality wood and fodder
(Brewbaker 2010). The cultivar ‘‘Hawaiian Giant
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Agroforest Syst (2020) 94:251–268 253
K8’’ was selected from the progenies of line K8 with
emphasis on wood and forage yields (Brewbaker
2016). Leucaena cultivars K5 and K500, were intro-
duced to Hawaii from Australia (Brewbaker 2016). K5
is a highly branching, Peru type cultivar of L.
leucocephala subsp. glabrata, whereas K500 is a L.
leucocephala subsp. glabrata Salvador type cultivar
that originated from a cross made between the
Salvador type and the more branched Peru type of L.
leucocephala subsp. glabrata in Australia. Some of
the promising cultivars of giant leucaena are listed in
Table 2.
Molecular biology studies in leucaena
Among the Leucaena species, the molecular biology
of only L. leucocephala has been studied. Ishihara
et al. (2016) analyzed transcriptomes of L. leuco-
cephala subsp. glabrata cultivar K636 through Illu-
mina-based sequencing and de novo assembly, which
generated 62,299 and 61,591 unigenes from the root
and shoot, respectively. Through a microarray analysis
of more than 10,000 unigenes, they identified a
number of genes that were highly expressed in the
root compared to the shoot. A terpenoid biosynthesis
gene, and nicotianamine synthase were two genes
found to be upregulated more than 100-fold in the root,
indicating that these genes may have important roles in
the root. Similarly, through microarray analysis,
Honda et al. (2018) identified 73 and 39 drought-
responsive gene sequences in cultivar K636 that were
upregulated in the root and shoot, respectively. They
also validated the expression of some of the drought-
responsive genes by qRT-PCR analysis. Honda and
Borthakur (2019) identified a number of genes that
were highly expressed in the foliage of giant leucaena
compared with the roots and postulated that these
genes may contribute to the nutrient richness of
leucaena foliage. Only a few leucaena genes have been
cloned and characterized so far (Table 3). Kaomek
et al. (2003) cloned cDNAs encoding two antifungal
chitinases from L. leucocephala and expressed one of
them in E. coli. The recombinant leucaena chitinase
hydrolyzed colloidal chitin and inhibited growth of 13
of the 14 fungal strains tested. Shaik et al. (2013)
cloned and characterized a leucaena gene encoding a
glycosylhydrolase and analyzed its spatial and tem-
poral expression by qRT-PCR in shoot and root tissues
of young seedlings. Leucaena gene sequences for
phenylpropanoid pathway enzymes leading to mono-
lignol biosynthesis have been characterized to varying
extents. The complete protein coding sequences have
been identified for eight genes encoding important
steps in monolignol biosynthesis (Khan et al. 2012).
The individual downregulation of four of the mono-
lignol biosythesis genes (Cinnamate 4-Hydroxylase
C4H), cinnamoyl CoA reductase, coniferaldehyde
5-hydroxylase, cinnamyl alcohol dehydrogenase
(CAD) by antisense strategies resulted in reduced
lignin content and stunted seedling growth (Khan et al.
2012). Reduced expression of one of the monolignol
biosynthesis genes, 4-coumarate CoA ligase 1 (4CL),
did not affect growth of leucaena seedlings although
lignin content was reduced. Omer et al. (2013) cloned
and characterized a leucaena cDNA for a R2R3-type
MYB transcription factor gene, which is a regulator
of the phenylpropanoid pathway and a general
Table 1 Differentiating characteristics between giant leucaena (L. leucocephala subsp. glabrata) and common leucaena (L. leu-
cocephala subsp. leucocephala)
Characteristics Giant leucaena Common leucaena
General
features
Medium size tree that can grow up to 20 m in height; can be maintained as a
shrub by repeated pruning of its foliage 3–10 times a year
Bushy shrub, low growing, highly
branched, 3–5 m in height
Seed
production
a
Produces relatively less pods and seeds Produces a lot of pods and seeds
Young shoots
a
Glabrous Velutinous
Leaflets
a
16–21 mm long 9–13 mm long
Capitula
a
[18 mm in diameter 12–17 mm in diameter
Young pods
a
Glabrous Sparsely pubescent
a
Information obtained through personal communication from SA Harris, Oxford Forestry Institute
123
254 Agroforest Syst (2020) 94:251–268
Table 2 Promising cultivars of giant leucaena
Variety
a
Parent species Characteristics References
K5 L. leucocephala subsp glabrata cultivar of
Peru type
Highly-branched; high biomass yields; high
seedling vigor; susceptible to psyllids
Brewbaker
(2016)
K8 or
Hawaiian
Giant
One of the L. leucocephala subsp. glabrata
accessions collected from Zacatecas,
Mexico
Most widely grown leucaena cultivar in the
world. Vegetative vigor; aggressive arboreal
growth, high leaf and wood yield. Grown in the
Philippines for charcoal and fuel, and in
Hawaii as a windbreak. When harvested for
forage every 8–12 weeks it has produced much
higher forage yields than other common
cultivars; susceptible to psyllids
Brewbaker
(1975)
K28 One of the L. leucocephala subsp. glabrata
accessions collected from El-Salvador
Multipurpose cultivar; high foliage and wood
yield; high seedling vigor; tolerant to acidic
soils; widely distributed and considered
superior in wood yields to K8. Reported to
perform marginally better than K636 in acid
soils
Brewbaker and
Hylin (1965)
K29 One of the L. leucocephala subsp. glabrata
Salvador type accessions collected from
Honduras
Multipurpose cultivar; high foliage and wood
yield; high seedling vigor; low seediness but
full male fertility; difficult for seed
multiplication
Brewbaker and
Hylin (1965)
K67 One of the L. leucocephala subsp. glabrata
Salvador type accessions collected from
El-Salvador
High foliage and wood yield; high seed
production; high seedling vigor; similar to K8
in foliage yield
Brewbaker et al.
(1972)
K132 One of the L. leucocephala subsp. glabrata
Peru type accessions collected from
Zacatepec, Morelos, Mexico
Lower in branching; large pods favored as food
source; high foliage and wood yield
Brewbaker
(2016)
K500 or
Cunningham
Selected in Australia from the progeny of a
cross between Salvador and Peru types of
L. leucocephala subsp. glabrata
High foliage and wood yield; cold tolerant;
psyllid susceptible
Rengsirikul et al.
(2011)
K584 One of the L. leucocephala subsp. glabrata
accessions collected from Veracruz,
Mexico
Combined stature of both Salvador and Peru
type; has a form similar to K636 but has more
branching like the Peru type; highly resistant to
psyllids
Brewbaker
(2016)
K636 or
Tarramba
One of the L. leucocephala subsp. glabrata
accessions collected from Coahuila,
Mexico
High forage yield; high seedling vigor; cold
tolerant; low branching; moderate psyllid
resistance; less seedy, difficult for seed
multiplication; low tannin content
Brewbaker
(1987)
K748 Interspecies hybrid variety L. pallida 9L.
leucocephala
High forage and wood yields;highly resistant to
psyllids; high seedling vigor; high seed
production
Austin et al.
(1997)
K1000 Interspecies hybrid variety between L.
esculenta 9L. leucocephala subsp.
glabrata
High seedling vigor; sterile; cold tolerant; highly
resistant to psyllids
Hughes (1998b)
KU19 F3 line selected from the F2 hybrid of L.
leucocephala
High foliage and wood yields Rengsirikul et al.
(2011)
KU66 F3 line selected from the F2 hybrid of L.
leucocephala
High foliage and wood yields Rengsirikul et al.
(2011)
KX2 Interspecies hybrid variety between L.
leucocephala and L. pallida
Highest biomass yield High seedling vigor;
highly resistant to psyllids; low seed
production; self-incompatibility; high
digestible; low tannin content
Mullen et al.
(2003), Jones
and Palmer
(2002)
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Agroforest Syst (2020) 94:251–268 255
repressor of lignin biosynthesis. Overexpression of the
leucaena MYB using a strong constitutive promoter,
CaMV35S, in transgenic tobacco resulted in signifi-
cant downregulation of early phenylpropanoid path-
way genes phenylalanine ammonia lyase, C4H, 4CL,
and CAD. Downregulation of these lignin precursor
genes may help to reduce the lignin content of
leucaena.
Leucaena genes related to mimosine synthesis,
degradation, and transport are of particular interest
because of the toxic effects of mimosine and its
degradation products 3,4-dihydroxypyridine (3,4-
DHP) or its isomer 3-hydroxy-4-pyridone (3H4P).
Transgenic leucaena expressing Rhizobium sp. strain
TAL1145 gene pydA exhibited up to a 22.5% reduc-
tion in mimosine content (Jube and Borthakur 2010).
Negi et al. (2014) cloned the cDNA for mimosinase
from giant leucaena K636 and expressed it in E. coli.
The purified recombinant mimosinase degraded
mimosine into 3H4P, pyruvate and ammonia. The
mimosine-degrading enzyme activity of mimosinase
is very similar to that of rhizomimosinase (Negi et al.
2013).
Genes related to environmental stress response
(Negi et al. 2011) require further investigation as
leucaena is an extremely resilient to most abiotic
stresses. Out of 15 hypothetical proteins identified as a
response to prolonged drought, the complete coding
sequence is known for only metallothionein. Further
identification and characterization of stress-related
genes in leucaena may prove valuable in increasing
stress tolerance of other crops.
Total biomass and forage yields of giant leucaena
The biomass and forage yields of leucaena can vary
considerably depending on climatic conditions, cul-
tural practices, season, location, and occurrence of
psyllids. The forage yield of giant leucaena is 2.5 times
higher than that of common leucaena (Brewbaker
1975). Guevara et al. (1978) showed that total dry
matter and forage dry matter yields of giant leucaena
Table 2 continued
Variety
a
Parent species Characteristics References
KX3 Interspecies hybrid variety between L.
diversifolia 9L. leucocephala
High forage yields; high seedling vigor; highly
resistant to psyllids; cold and frost tolerant; self-
fertile
Mullen and
Gutteridge
(2002)
KX4 Triploid hybrid between L. esculenta and L.
leucocephala subsp. glabrata
High foliage and wood yields, fast growing; seedless,
lack pods; good wood quality; highly resistant to
psyllids; highly tolerant to drought
Brewbaker
(2013)
Lanang or
Male
Leucaena
Spontaneous hybrid between L.
leucocephala and L. pulverulenta, selected
in Indonesia
Fast growing; variable sterile; high nutritive value;
low mimosine content; high seedling vigor; high
wood yields; psyllid susceptible
Hughes
(1998b)
Peru Peru type variant of L. leucocephala subsp.
glabrata
High foliage and wood yields production Rengsirikul
et al.
(2011)
Redlands Developed in Australia from the progeny of
a cross between L. leucocephala and L.
pallida
Highest biomass yields, highly resistant to psyllids;
high tannin content; medium dry matter digestibility
Lambrides
(2017)
Rendang Developed in Malaysia from a cross
between L. leucocephala subsp.
glabrata 9L. diversifolia
Few seeds; highly resistant to psyllids; good dry
matter digestibility; moderately cool tolerant
Zarin et al.
(2016)
Wondergraze A selection from the progeny of a cross
between L. leucocephala subsp. glabrata
variety K636 with K584
High seedling vigor; shorter stature, basal branching,
and more bushy like the Peru type; similar to K636
for psyllid and cold tolerance; high forage yield;
good forage quality and palatable
Brewbaker
(2016)
a
Cultivars with the prefix ‘K’, ‘KX’, and ‘KU’ were developed in Hawaii
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256 Agroforest Syst (2020) 94:251–268
Table 3 L. leucocephala genes that have been cloned and characterized
Gene Accession no. Description References
Phenylalanine ammonia
lyase (PAL)
JN540043.1 A partial cDNA (1.1 kb) of an expected *2 kb coding sequence
was sequenced
Khan et al.
(2012)
Cinnamate
4-Hydroxylase (C4H)
JN874563.1
HQ191221.2
HQ191222.2
Three highly similar alleles of LlCH41 gene were isolated and
transcription levels measured by qPCR in various tissue types of
different ages. Antisense-LlCH41 expression resulted in stunted
growth
Kumar et al.
(2013)
4-coumarate CoA
Ligase 1 (4Cl)
FJ205490.1 Transgenic leucaena containg antisense-4Cl construct showed
2–7% reduction in lignin content but no detectable change in
morphology
Gupta (2008)
Caffeoyl-CoA-O-
methyltransferase
(CCoAOMT)
DQ431233.1
DQ431234.1
Isolation and cloning of two leucaena CCoAOMT isoforms
described. Three-dimensional models were proposed based on
either isoform to predict interaction with substrate
Pagadala et al.
(2009)
Cinnamoyl CoA
reductase (CCR)
EU195224.2
DQ986907.3
Spatial expression of Ll-CCR analyzed by qRT-PCR and ELISA
with respect to lignification over time
Srivastava
et al. (2011)
Coniferaldehyde
5-hydroxylase
(Cald5H)
EU041752.1 Transgenic leucaena and tobacco were made using sense and
antisense strategies respectively. Transgenic leucaena
expressingantisense-Cald5H construct did not show
morphological changes
Yadav (2009)
Cinnamyl alcohol
dehydrogenase (CAD)
EU870436.1 Cloned, expressed in E. coli, and purified the recombinant
leucaena CAD for kinetic studies
Pandey et al.
(2011)
Caffeic acid
O-methyltransferase
(COMT)
EF611249.1 Cloned, expressed in E. coli, and purified the recombinant
leucaena LlOMT in E. coli. The purified protein used for
enzyme kinetics and activity studies
Dwivedi et al.
(2014)
Peroxidase (POX) EU649680.1 Leucaena POX was purified in native form from stem tissue,
characterized and assayed
Pandey and
Dwivedi
(2011)
Cellulose synthase FJ871987.2
GQ267555.2
Tissue specific differential expression of two isoforms (Ll-7CesA
and Ll-8CesA) were studied in root, stem, and leaves by qRT-
PCR
Vishwakarma
et al. (2012)
MYB transcription
factor gene
GU901208.1 Isolated and characterized a R2R3-type MYB transcription factor
gene, which is a regulator of the phenylprepanoid pathway and a
general repressor of lignin biosynthesis
Omer et al.
(2013)
b-carbonic anhydrase KC924756.1
KC924757.1
Chloroplastic (cacp) and cytoplasmic (cacyt) isoforms of leucaena
b-carbonic anhydrase were isolated, structurally analyzed in
silico, and transcription levels were compared under various
abiotic conditions in different tissues
Pal and
Borthakur
(2014)
Metallothionine KC355441.1 One of the 15 hypothetical proteins identified by interspecies
suppression subtractive hybridization (iSSH); it was upregulated
48-fold under drought conditions
Negi et al.
(2011)
Mimosinase AB298597.1 Isolated, cloned, expressed in E. coli and purified the recombinant
mimosine-degrading enzyme from leucaena. Conducted
biochemical characterization of the enzyme and degradation
products of mimosine
Negi et al.
(2014)
Cy-O-acetylserine thiol
lyase
KF754356.1 Isolated, cloned, expressed in E. coli and purified the recombinant
leucaena cy-OAS-TL. The recombinant enzyme catalyzed
synthesis of cysteine but not of mimosine
Yafuso et al.
(2014)
Chitinase AF513017.2 Isolated and cloned cDNAs for two leucaena chitinases. One of
the chitinases was expressed in E. coli and the purified protein
was shown to have chitinase activities
Kaomek et al.
(2003)
Glycosylhydrolase I EU328158.1 Cloned and characterized the recombinant enzyme by glycone
specificity and kinetic properties. Spatial and temporal
expression analysis by qRT-PCR was performed on shoot and
root tissues of young seedlings
Shaik et al.
(2013)
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Agroforest Syst (2020) 94:251–268 257
depend on a number of factors including growing
season, cultivar, spacing, cutting height, and cutting
intervals. Based on their experimental results, they
recommended a cutting height of 25–35 cm above
ground and cutting interval of 3 months for obtaining
optimum forage yield. The forage dry matter yield of
giant leucaena cultivar Peru in one set of experiments
conducted in Mexico was 6.9 Mg ha
-1
year
-1
(Casa-
nova-Lugo et al. 2014), which was much lower than
the average forage dry matter yield of 26.6 Mg ha
-1
-
year
-1
from three Salvador type of giant leucaena
cultivars (K8, K28 and K67) grown in Hawaii
(Brewbaker et al. 1972). Austin et al. (1995) reported
a total dry mater biomass yield and a forage dry mater
yield of up to 63.7 and 34 Mg ha
-1
year
-1
, respec-
tively, for giant leucaena grown in Hawaii. Mullen and
Gutteridge (2002) observed that the total dry mater
biomass yield of the interspecies leucaena hybrids
KX2 and KX3 could be as high as 84 Mg ha
-1
-
year
-1
. They suggested that the high yields of KX2
and KX3 could be the result of heterosis and high
psyllid resistance of the hybrids.
Nutritional properties of leucaena
Leucaena is considered an important fodder legume
due to its palatability and high protein content in the
foliage. Because of its high nutritional value, it is often
referred to as the ‘alfalfa of the tropics’. Young shoots
have up to 31% protein on a dry weight basis, which
decreases to 14% after 10 weeks (Tangendjaja et al.
1986). Garcia et al. (1996) reviewed 65 publications
between 1946 and 1992 for nutritive value and forage
productivity of leucaena and found that the medial
concentration of crude fiber and crude protein was
19.2% and 29.2%, respectively. Soedarjo and Bortha-
kur (1996b) found that young leucaena leaves of
common leucaena contained only *18% protein.
They suggested that protein concentrations might have
been overestimated in some of the earlier reports,
because mimosine, a non-protein amino acid, present
in the samples interacts with the reagents for protein
estimation, giving an overestimate of the protein
content. They also described a more accurate method
of determining soluble protein content in leucaena
tissues containing mimosine. In spite of having high
protein contents and high palatability, leucaena
foliage has two negative attributes: (1) it has high
amounts of mimosine, which is toxic to animals, and
(2) it has high amounts of condensed tannin, which has
been identified as a major factor limiting the nutritive
value of leucaena foliage (Wheeler et al. 1995; Garcia
et al. 1996; Osborne and McNeill 2001; Chanchay and
Poosaran 2009). The mimosine contents of different
parts of the shoot vary from 1 to 12%; the growing tips
contain the highest amounts while the old stems
contain the lowest amounts (Jones 1979). Young
leaves contain *4.5% mimosine on a dry weight
basis, which decreased to *2% in 10-week-old
leaves (Tangendjaja et al. 1986). Chanchay and
Poosaran (2009) also found 4.4% mimosine in the
leaves of leucaena. Soedarjo and Borthakur (1996a)
determined that young leaves and pods of leucaena
contained as high as 6–10% mimosine on a dry weight
basis. Condensed tannins are polyphenolic compounds
that bind with soluble proteins and make them
insoluble and indigestible. Leucaena leaves contain
1–5% total tannin, comprising both hydrolysable and
condensed tannins (A. Bageel and D. Borthakur,
unpublished results).
Functions of mimosine in leucaena
The toxic non-protein amino acid mimosine is present
in all leucaena species and is generally considered as a
chemical defense mechanism against various biotic
stresses. Mimosine, its degradation product 3H4P, and
substituted derivative ‘mimosinol’ have been studied
for their nematocidal, insecticidal, herbicidal, and
antimicrobial properties (Anitha et al. 2005; Xuan
et al. 2006,2013; Tawata et al. 2008; Nguyen et al.
2015; Xuan et al. 2016). Mimosine was also found to
inhibit germination of rice and albizziine seeds
(Prasad and Subhashini 1994; Williams and Hoagland
2007). Leucaena extracts, which contain a high
amount of mimosine have been shown to have
anthelmintic and acaricidal properties (Kabore et al.
2012; Ademola and Idowu 2013; Auamcharoen and
Chandrapatya 2015). Soedarjo et al. (1994) showed
that inhibitory effects of mimosine on bacterial growth
are bacteriostatic and not bacteriocidal. Mimosine is
known to chelate multivalent metal ions such as Fe
3?
,
Zn
2?
,Cu
2?
,Ni
2?
,Co
2?
and Mn
2?
that serve as
cofactors for many enzymes. By chelating these ions,
mimoine inactivates these enzymes and thereby
inhibits bacterial growth. Mimosine also binds to
123
258 Agroforest Syst (2020) 94:251–268
pyridoxal 50-phosphate (PLP), and thereby inhibits all
PLP-requiring enzymes such as decarboxylases,
amino acid transferases, lyases, tryptophan synthase,
cysteine synthase etc. in microorganisms, and thus
prevents their growth. As previously mentioned, the
mimosine content of leucaena foliage can be as high as
10%. Negi et al. (2014) estimated that if the total
carbon and nitrogen used for production of mimosine
were diverted for growth, the leucaena tree would
have grown at least 21% larger. They also proposed
that mimosine may provide a mechanism of drought
resistance in leucaena. According to this idea, during
favorable weather conditions, when water and nutri-
ents are available, leucaena synthesizes mimosine and
accumulates in different parts of the plant, including
the foliage. Under drought conditions, mimosine is
degraded by the enzyme mimosinase present in
chloroplasts. They further suggested that during
drought conditions, some chloroplasts membrane
may be broken down, and mimosinase from the
chloroplast stroma come in contact with mimosine in
the cytoplasm (Fig. 2). Recent experimental results
showed that mimosine concentration in leucaena
foliage was increased when plants were grown with
added nitrogen but reduced under prolonged drought
treatment (Honda and Borthakur, unpublished results).
Tolerance to drought stress
Leucaena can grow successfully in soils with low
nutrient and moisture availability. It can survive
drought conditions for several months during a
prolonged dry season and recover quickly with
availability of water (Shelton and Brewbaker 1994).
Attributes of root competitiveness, such as taproot
length, lateral root length density, mycorrhizal colo-
nization, nodulation and nitrogen fixation, disease
resistance, and flexibility in response to water and
nutrient availability in the soil, are some of the
important determinants of leucaena’s success as a
stress-tolerant tree legume in tropical and subtropical
environments. Yige et al. (2012) showed that leucaena
seedlings had the ability to maintain high levels of leaf
water content (LWC), which did not decrease signif-
icantly until 9 days of drought. Ezenwa and Atta-Krah
(1992) noted that leucaena seedlings grown in soils
allocated more nutrient resources for growth of the
taproot than on lateral roots until about 12 weeks.
Leucaena is a deep-rooted species, which can extend
its roots up to 5 m to exploit underground water
(Brewbaker et al. 1972). This may be one of the
reasons why leucaena is naturally resistant to drought.
In dry areas, leucaena remains unaffected by drought
as long as its deep roots can reach groundwater.
Fig. 2 Mimosine may be recycled as a source of nutrients
during drought. aDuring rainy season, when the environmental
conditions for growth are favorable, leucaena leaves produce a
lot of mimosine, which is stored in the cell cytoplasm. A
mimosine-degrading enzyme, mimosinase, is located in the
chloroplast and thus mimosine and mimosinase are separated by
chloroplast membranes. bHowever, under drought conditions
some of these membranes may break, resulting in the release of
mimosinase from the chloroplast to the cytoplasm, where
mimosine is degraded by mimosinase. The degradation products
of mimosine are recycled for survival and growth by the
leucaena plant during drought (Negi et al. 2014)
123
Agroforest Syst (2020) 94:251–268 259
Leucaena also shows avoidance responses toward
drought condition through leaflet folding during dry
spells to prevent water loss and by shedding some
leaves under severe drought conditions (Brewbaker
1987). Rao et al. (2008) reported that the net
photosynthetic rate and transpiration rate decreased
and stomatal resistance increased in leucaena in
response to high water stress. They also observed that
under high water stress, leucaena maintained higher
water potential and proline content, indicating drought
resistance. Leucaena pastures also have been shown to
have high water use efficiency compared with other
pasture types (Dalzell et al. 2007). Once established,
leucaena shows excellent erosion control characteris-
tics. In many leucaena pastures, little runoff is
observed even after high intensity rainfall (Shelton
and Dalzell 2007).
Infestation by insects
The psyllid pest Heteropsylla cubana is known to
cause damage to leucaena plants by feeding on
juvenile leaflets and causing defoliation (Funasaki
et al. 1989). With a short life cycle of about 2 weeks
and the ability to lay up to 400 eggs in their lifetime,
this pest grows exponentially and quickly infests
plants, especially in warm, moist conditions. Psyllid
infestation on common leucaena was reported to be a
serious problem in the Caribbean, Hawaii, Mexico,
Philippines and Thailand (Othman and Prine 1984;
Sorensson and Brewbaker 1984; Ahmed et al. 2014;
Brewbaker 2016). Trials to test for psyllid tolerance in
various Leucaena species were performed in Thailand,
Mexico, Philippines, and USA (Brewbaker 2016).
Also, efforts have been made to develop psyllid-
resistant cultivars of giant leucaena by crossing them
with Leucaena species that have higher resistance
against the psyllid, such as L. esculenta and L. pallida
(Brewbaker 2008). Interspecies hybrids KX2, KX3
and KX4 have been found to be resistant to psyllids.
Currently, these psyllid-resistant hybrids are under
agronomic trials in Hawaii and Australia. Other
leucaena varieties that are selected for psyllid toler-
ance and extensively grown in Australia and Hawaii
are Tarramba and Wondergraze (Brewbaker 2016).
Bruchid beetle (Acanthoscelides macrophthalmus)
are host-specific seed destroying insects that can cause
considerable damage to leucaena; it damaged up to
44% of leucaena seeds in Ethiopia (Yirgu et al. 2015).
Interestingly, the bruchid beetle have also been used to
restrict the invasiveness of legume trees including
common leucaena in South Africa and Australia
(Neser and Kluge 1986; Jones and Jones 1996). In
Mexico, leucaena is naturally attacked by two genera
of seed beetle, Acanthoscelides and Stator. There are
five species of Acanthoscelides that feed on leucaena
but do not attack any other plant species. A. macroph-
thalmus is known to attack 18 different species of
Leucaena. With regard to genus Stator, it has two
species, which attack a broad range of Mimosoid
legume genera including Leucaena species (Hughes
and Johnson 1996).
Symbiotic nitrogen fixation
Leucaena forms nitrogen-fixing nodules in symbiosis
with specific Rhizobium species such as Rhizobium sp.
strain TAL1145 and Rhizobium tropici strain
CIAT899 (Martı
´nez-Romero et al. 1991; George
et al. 1994). Leucaena-Rhizobium symbiosis is very
specific. Rhizobium strains isolated from nitrogen-
fixing root nodules of leucaena generally cannot form
effective nodules on other legumes such as cowpeas,
beans, peas, etc. (Trinick 1968). Under laboratory
condition, strain TAL1145 can form only ineffective
nodules on common bean (Borthakur and Gao 1996).
In greenhouse experiments using the
15
N-labelling
method, leucaena was observed to have a consistently
increasing pattern of nodulation, dry biomass accu-
mulation, and nitrogen yield over a period of
16 months after planting (Kadiata et al. 1995). In
field experiments, using the
15
N isotope dilution and
the total N difference methods, leucaena K636 was
found to fix consistently high levels of atmospheric N
2
even after third cuttings following 36 months of
planting (Sanginga et al. 1989). Most of the Rhizobium
strains that nodulate leucaena in Hawaii can degrade
mimosine completely and use it as a source of carbon
and nitrogen (Soedarjo et al. 1994; Soedarjo and
Borthakur 1996a). TAL1145 was listed as a compet-
itive strain for nodulation of leucaena in several
reports (Moawad and Bohlool 1984; Somasegaran and
Martin 1986; George et al. 1994). In competition
experiments under field conditions using six indige-
nous Rhizobium strains on leucaena grown in oxisol
and mollisol soils in Hawaii, strain TAL1145 was
123
260 Agroforest Syst (2020) 94:251–268
found to be most competitive (Moawad and Bohlool
1984). Soedarjo and Borthakur (1998) constructed
several mimosine-non-degrading (Mid
2
) mutants of
TAL1145 and used them in competition experiments
with TAL1145 on leucaena. The results of their
experiments showed that the mimosine-degrading
ability of strain TAL1145 provides a competitive
advantage for nodulation of leucaena. By growing
leucaena under hydroponic conditions, Soedarjo and
Borthakur (1998) showed that some amount of
mimosine is secreted in the leucaena root exudates.
They proposed that mimosine in the rhizosphere binds
with Fe
3?
to produce mimosine-Fe
3?
complex, which
is then taken up by Rhizobium and used as a source of
nutrients. Rhzobium degrades mimosine into two
molecules each of pyruvate, formate and ammonia
(Borthakur et al. 2003, Awaya et al. 2005) (Fig. 3).
Soedarjo and Borthakur (1998) also showed that
mimosine is present in the leucaena root nodule, where
it is used as a source of carbon and nitrogen by resident
nodule rhizobia that have not differentiated into the
nitrogen-fixing bacteroid form. The genes for mimo-
sine degradation from TAL1145 have been isolated
and characterized (Fox and Borthakur 2001; Bortha-
kur et al. 2003; Awaya et al. 2005,2007). Negi et al.
(2013) characterized the protein encoded by the midD
gene of TAL1145 and showed that it had enzymatic
properties similar to mimosinase of leucaena. They
named this Rhizobium enzyme as rhizomimosinase,
which converted mimosine into 3H4P, pyruvate, and
ammonia. Rhizomimosinase and mimosinase do not
show much homology but both enzymes have similar
mimosine-binding and PLP-binding domains (Negi
et al. 2014).
Agricultural and ecological benefits of giant
leucaena
As previously mentioned, giant leucaena possesses a
number of traits that are beneficial in various agro-
forestry systems. These traits include (1) high adapt-
ability to a wide range of environmental conditions,
including drought and alkaline soils, (2) tolerance to
many biotic stresses, (3) accelerated growth, (4) high
biomass yields, and (5) symbiotic relationship with
nitrogen-fixing bacteria. The hardiness and rapid
growth of giant leucaena make it a suitable hedgerow
legume for alley cropping systems (Rosecrance et al.
1992). The height and diameter of teak tree (Tectona
grandis) were increased when it was intercropped with
leucaena (Kumar et al. 1998). Similarly, a number of
studies utilizing leucaena in alley cropping systems
with maize showed higher maize yields as well as
other beneficial effects such as improved soil nutrient
chemistry profile and even suppression of weed
growth (Jama et al. 1991; Dalland et al. 1993;Xu
et al. 1993a,b; Mureithi et al. 1994; Mugendi et al.
1999). Leucaena may also be used as a windbreak, live
fence, live scaffold for growing vines like yam, or
shade tree for production of coffee and cocoa (Hughes
2006; Youkhana and Idol 2011; Brewbaker 2013).
When leucaena was planted as a windbreak, it was
found to increase soil moisture availability as well as
the grain yield of agricultural crops (Swaminathan
1987). When used in crop rotation, as an alley crop,
cover crop, green manure, green mulch, or in cut-and-
burn cultivation, leucaena can help to manage N
cycling, increase organic carbon, and restore impor-
tant nutrients like N, P, and K in the soil (Atta-Krah
1990; Xu et al. 1993a,b; Grewal et al. 1994;
Heinemana et al. 1997; Kumar et al. 1998; Isaac
et al. 2003). As a fast-growing nitrogen-fixing legume,
leucaena is an ideal tree for reforestation of marginal
lands and watersheds; and because it thrives in steep
slopes, it can help to control soil erosion. Leucaena
grows well in steep slopes where it effectively controls
erosion by reducing surface run-off and soil loss
(Dijkman 1950; Parera 1982; Celestino 1985; Grewal
et al. 1994; Savale et al. 2007).
Leucaena in phytoremediation
Leucaena has been researched as a possible tool in
biological remediation of coal and metal mine tailings,
tannery and dye pollutants, waste oil pollutants,
lagoon ash, fly ash, textile waste, and heavy metal
contaminated soils (Cheung et al. 2000; Gupta et al.
2000; Song et al. 2005; Bisht et al. 2011; Jayanthy
et al. 2014; Edwin-Wosu and Nkang 2016; Ssenku
et al. 2017). Leucaena has been shown to uptake, store,
and to some degree, tolerate heavy metals such as
arsenic, lead, chromium, cadmium, and nickel (Rout
et al. 1999; Iqbal and Shazia 2004; Song et al. 2005;
Shafiq et al. 2008; Sakthivel and Vivekanandan 2009;
Dias et al. 2010; Ho et al. 2013; Adanikin and Kayode
2019). It was also found that leucaena biomass is a
123
Agroforest Syst (2020) 94:251–268 261
cheap and effective phytoadsorbent of various dyes
present in contaminated waters (Karthikeyan and
Rajendran 2010; Rajendran et al. 2015; Gayathri and
Jayanthi 2016). Radrizzani et al. (2011) found that
established leucaena-grass pastures accumulated
enough organic carbon to offset the carbon dioxide
produced from cattle, grazing on these same pastures.
Conclusions
Giant leucaena has a combination of key attributes
such as nitrogen-fixing ability, drought tolerance, easy
cultivation, and high protein content of foliage
because of which it is important for agroforestry.
The future of giant leucaena as an agroforestry species
depends largely on public understanding of the
Fig. 3 A possible role of
mimosine in the leucaena
rhizosphere. Mimosine
present in the leucaena leaf
liters is released to the soil,
where it binds with Fe
3?
to
form a mimosine-Fe
3?
complex, which is taken up
by free-living rhizobia or
other bacteria in the
leucaena rhizosphere;
rhizobia utilize mimosine by
degrading it into two
molecules each of pyruvate,
formate, and ammonia.
Rhizobia also converts Fe
3?
to Fe
2?
and release excess
Fe
2?
in the rhizosphere,
where it is taken up by the
leucaena roots
123
262 Agroforest Syst (2020) 94:251–268
difference between giant and common leucaena.
Unfortunately, most people know leucaena as an
invasive weed. They may not know that giant leucaena
is not invasive as common leucaena and it is a valuable
tree legume for high biomass productivity. The
biomass produced by giant leucaena can be harnessed
either as a nutritious fodder or as wood depending on
the method of growing and harvesting. It can be grown
either as a shrub by repeated harvest of the foliage
several times a year or as a woody tree by allowing it to
grow as a fast-growing medium-size tree. Giant
leucaena produces much more vegetative growth and
relatively few seeds while common leucaena produces
a lot of seeds relative to its vegetative growth. Efforts
must be made to bring farmers to experimental
research stations or demonstration plots where giant
leucaena is grown as a forage legume and also as a
woody tree. By seeing the benefits of giant leucaena
and its difference from common leucaena, farmers will
understand why giant leucaena was once called a
‘miracle tree’.
Leucaena produces mimosine, which has some
adverse effects on fodder quality. However, the
presence of mimosine in the leucaena foliage may
not be a big concern, because ruminants grazing on
leucaena can be inoculated with the rumen bacterium
Synergistes jonesii, which can detoxify mimosine
(Jones and Megarrity 1986; Allison et al. 1992).
Alternatively, mimosine present in the leucaena
foliage can be removed, easily and inexpensively
through simple processing and without significantly
reducing the soluble protein content of the foliage.
Soedarjo and Borthakur (1996b) observed that up to
97% mimosine in leucaena young leaves, pods, and
seeds can be removed by soaking it in water for 24 h.
The mimosine-free foliage can be then dried and fed to
animals immediately, or converted into silage for
future use. Additionally, the mimosine-free foliage
can be processed, mixed with grasses and additional
supplements, and developed into nutritious and palat-
able feed for all animals, including poultry, cows,
sheep, goats, pigs, and fishes (Varvikko et al. 1992;
Kaitho et al. 1996; Zakayo et al. 2000; Khan et al.
2009; Amisah et al. 2009).
There are variations among leucaena varieties for
resistance to psyllids, which can cause heavy infesta-
tion in susceptible varieties. A number of Leucaena
species such as L.collinsii, L. confertiflora,L.
esculenta,L. greggii, L. lempirana, L. matudae, and
L. pallida are highly resistant to psyllids. Therefore,
efforts have been made to develop psyllid resistant
varieties through interspecies crosses of L. leuco-
cephala subsp. glabrata cultivars with these species.
The wood of giant leucaena has been used for
timber and high quality paper production in India
(Prasad et al. 2011; Pandey and Kumar 2013). Giant
leucaena may provide opportunities for new indus-
tries in the future. After extraction of mimosine from
the leaves, the mimosine-free young leaves can be
dried to produce herbal tea (Tawata et al. 2008).
Mimosine extracted from leucaena and its degrada-
tion product 3H4P are used in biomedical research.
3H4P can be manufactured from mimosine, using a
recombinant enzyme mimosinase or rhizomimosi-
nase(Negietal.2013,2014; Negi and Borthakur
2016). Considering its potential for use in industry,
its use as a nutritious fodder, and its growing
acceptance among farmers, giant leucaena may
slowly replace common leucaena in many parts of
the world.
Acknowledgements This work was supported by the USDA
NIFA Hatch project HA05029-H, managed by CTAHR,
University of Hawaii at Manoa, Honolulu. Authors would like
to thank Dr. James Brewbaker for useful discussion.
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