© The Authors, 2025, Published by the Universidad del Zulia*Corresponding author: jquiroz@ipn.mx
Keywords:
Indole acetic acid
Tryptophan
Tryptamine
Pyruvic Indole
Pathway IAA
Identication of indole acetic acid biosynthesis pathways in Trichoderma asperellum and
Trichoderma koningiopsis
Identicación de las vías de biosíntesis de ácido indolacético en Trichoderma asperellum y
Trichoderma koningiopsis
Identicação das vias de biossíntese de ácido indolacético em Trichoderma asperellum e Trichoderma
koningiopsis
Eliezer Romero Juarez
José Luis Hernández Mendoza
Juan Manuel Gonzalez Prieto (†)
Sanjuana Hernández Delgado
Amanda Alejandra Oliva Hernández
Jesús Di Carlo Quiroz Velásquez*
Rev. Fac. Agron. (LUZ). 2025, 42(2): e244229
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v42.n2.XIII
Crop production
Associate editor: Dr. Jorge Vilchez-Perozo
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
1
Centro de Biotecnología Genómica - Instituto Politécnico
Nacional, Blvd. del Maestro esq. Elías Piña, Col. Narciso
Mendoza, Reynosa, Tamaulipas, México C.P. 88710.
Received: 26-02-2025
Accepted: 31-05-2025
Published: 02-06-2025
Abstract
Trichoderm spp. produces secondary metabolites associated
with plant growth promotion, especially the production of indole
acetic acid (IAA), the main plant hormone. The tryptophan-
dependent (TRP-D) and tryptophan-independent (TRP-I) production
pathways, depending on the precursor involved in IAA synthesis,
are well known. The objective of this study was to investigate the
tryptophan-dependent (TRP-D) production pathway under in vitro
liquid culture conditions (Potato Dextrose), supplemented with
tryptophan (TRP). The presence of auxinic compounds in TRP-D
was quantied using high-performance liquid chromatography
(HPLC). Additionally, the morphology of corn seeds was analyzed
using scanning electron microscopy (SEM). The interaction of
Trichoderma spp. with corn seed germination was evaluated under
controlled laboratory conditions, conducting the assay in triplicate
and performing an analysis of variance (ANOVA). The results
showed that the species T. asperellum and T. koningiopsis can
degrade TRP and synthesize IAA through the tryptamine (TRM)
and indole acetamide (IAM) pathways. However, IAA synthesis
was not detected through the indole pyruvic acid (IPyA) and
3-indole acetonitrile (IAN) pathways. In particular, T. asperellum
produced signicantly higher concentrations of IAA compared
to T. koningiopsis. Additionally, it was observed that tryptophan
supplementation increased IAA production in both species. Finally,
T. koningiopsis showed a strong relationship with the maize root
system, invading the root and establishing a benecial interaction
that could contribute to plant growth and development. These
ndings suggest that T. koningiopsis has signicant potential as a
biofertilizer in agricultural systems.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2025, 42(2): e254229 April-June. ISSN 2477-9409.
2-6 |
Resumen
El hongo Trichoderma spp. produce metabolitos secundarios
asociados a la promoción del crecimiento vegetal, especialmente
la producción de ácido indol acético (AIA), la principal hormona
vegetal. Las vías de producción de triptófano dependiente (TRP-D)
y de triptófano independiente (TRP-I), dependiendo del precursor
implicado en la síntesis de AIA, son bien conocidas. El objetivo
del presente trabajo fue estudiar la vía de producción de triptófano
dependiente (TRP-D) en condiciones de medio de cultivo líquido
in vitro (Papa Dextrosa), suplementado con triptófano (TRP).
La presencia de compuestos auxínicos en TRP-D se cuanticó
mediante cromatografía líquida de alta resolución (HPLC).
Además, la morfología de las semillas de maíz fue analizada
utilizando microscopía electrónica de barrido (SEM). La interacción
de Trichoderma spp. con la germinación de las semillas de maíz
se evaluó en condiciones controladas de laboratorio, realizando
el ensayo por triplicado y llevando a cabo un análisis de varianza
(ANOVA). Los resultados mostraron que las especies T. asperellum
y T. koningiopsis pueden degradar TRP y sintetizar AIA a través de
las vías de triptamina (TRM) e indol acetamida (IAM). Sin embargo,
no se detectó la síntesis de AIA a través de las vías de ácido indol
pirúvico (IPyA) y 3-indol acetonitrilo (IAN). En particular, T.
asperellum produjo concentraciones signicativamente más altas
de AIA en comparación con T. koningiopsis. Además, se observó
que la suplementación con triptófano aumentó la producción de
AIA en ambas especies. Finalmente, T. koningiopsis mostró una
fuerte relación con el sistema radical del maíz, invadiendo la raíz y
estableciendo una interacción beneciosa que podría contribuir al
crecimiento y desarrollo de la planta. Estos hallazgos sugieren que T.
koningiopsis tiene un potencial signicativo como biofertilizante en
sistemas agrícolas.
Palabras clave: ácido indol acético, triptófano, triptamina, indol
pirúvico, vía IAA.
Resumo
O microorganismo Trichoderma spp. produz metabólitos
secundários associados à promoção do crescimento vegetal,
especialmente a produção de ácido indolacético (AIA), o principal
hormônio vegetal. As vias de produção dependentes de triptofano
(TRP-D) e independentes de triptofano (TRP-I), dependendo do
precursor envolvido na síntese de AIA, são bem conhecidas. O objetivo
deste estudo foi investigar a via de produção dependente de triptofano
(TRP-D) em condições de cultura líquida in vitro (Batata Dextrose),
suplementada com triptofano (TRP). A presença de compostos
auxínicos em TRP-D foi quanticada usando cromatograa líquida
de alta eciência (HPLC). Além disso, a morfologia das sementes de
milho foi analisada usando microscopia eletrônica de varredura (SEM).
A interação de Trichoderma spp. com a germinação das sementes
de milho foi avaliada em condições controladas de laboratório,
conduzindo o ensaio em triplicado e realizando uma análise de
variância (ANOVA). Os resultados mostraram que as espécies T.
asperellum e T. koningiopsis podem degradar TRP e sintetizar AIA
através das vias de triptamina (TRM) e indol acetamida (IAM). No
entanto, a síntese de AIA não foi detectada através das vias de ácido
indol pirúvico (IPyA) e 3-indol acetonitrilo (IAN). Em particular, T.
asperellum produziu concentrações signicativamente mais altas de
AIA em comparação com T. koningiopsis. Além disso, observou-se
que a suplementação com triptofano aumentou a produção de AIA
em ambas as espécies. Finalmente, T. koningiopsis
mostrou uma
forte relação com o sistema radicular do milho, invadindo a raiz e
estabelecendo uma interação benéca que poderia contribuir para o
crescimento e desenvolvimento da planta. Esses achados sugerem que
T. koningiopsis tem um potencial signicativo como biofertilizante
em sistemas agrícolas.
Palavras-chave: ácido indol acético, triptofano, triptamina, indol
pirúvico, via IAA.
Introduction
The microorganism Trichoderma spp. is widely distributed
throughout the world; it can be isolated from soil, decomposing
organic matter or agricultural waste, and is associated with the
control of agents causing root diseases in wild and cultivated plants
(Braithwaite et al., 2017; Lopez et al., 2016). Trichoderma parasitizes
phytopathogenic fungi (Yao et al., 2023), and it has also the ability
to set up symbiotic relationships with plants, promoting their
development and growth. It secrets secondary metabolites such as
auxins, antibiotics, and phytoalexins, as well as compounds involved
in the defense system of plants such as salicylic and jasmonic acids
(Guzmán-Guzmán et al., 2017; Lubna et al., 2018). Furthermore,
it releases enzymes that degrade cell walls and contribute to the
bioavailability of nutrients (Ghasemi et al., 2020).
Indirectly, Trichoderma spp. can alter the microora present in the
soil. In greenhouse and eld, it has been proved that Trichoderma spp.
stimulates growth and production of biomass in Arabidopsis, tomato,
lettuce, pepper, papaya, passion fruit and beans, among others (SAS,
2004). Trichoderma spp. stimulates plant growth through changes in
the concentration of plant hormones such as IAA, gibberellic acid,
cytokinin, and ethylene (Cai et al., 2015; Lubna et al., 2018). It has
also been reported that when the culture medium contains indole 3
ethanol (IE) the microorganism can use it to synthesize IAA from
tryptophan (TRP) via tryptamine (TAM) and tryptophol (TIF)
(Leontovyčová et al., 2020). When Trichoderma spp. is grown in a
medium supplemented with IE uses it to synthesize IAA from TRP
through the synthesis pathway of TAM and TIF.
In plants, IAA induces the formation of lateral roots and increases
the number of root hairs, which helps with nutrient absorption,
embryogenesis, growth, and the development of many organs,
including roots, hypocotyls, leaves, stems, and owers; it also
contributes to tropism and apical dominance, including the regulatory
responses of the plant against environmental changes (Fu et al., 2015;
Yao et al., 2023). The mechanisms of IAA synthesis are described
as TRP-Dependent (TRP-D) or TRP-Independent (TRP-I) pathways.
The TRP-I pathway starts with chorismic acid, which is transformed
into anthranilic acid (AA) and then to indole 3-glycerol phosphate or
indole (Fu et al., 2015; Uribe-Bueno et al., 2020).
The TRP-D pathway is made up of 4 large pathways: 1) the indole
pyruvic acid (IPyA) pathway; 2) the tryptamine (TRM) pathway; 3)
the 3-indole acetonitrile (IAN) pathway; 4) the indole-3-acetamide
(IAM) pathway (Tariq & Ahmed 2022). It has been found that IAA
can be stored in plants such as corn, Arabidopsis and Lotus japonicus,
by conjugating with amino acids such as N-β-D-glucopyranosyl
indole-3-acetic acid, and then recovered through a metabolic pathway
(Yin et al., 2021; Yao et al., 2023). Of the pathways, the IAN
pathway has great importance, since when this molecule converts to
IAA, a nitrogenous group is lost, remaining in the soil in the form
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Romero et al. Rev. Fac. Agron. (LUZ). 2025, 42(2): e254229
3-6 |
of nitrogen assimilable by plants. In other cases, IAN is an alternate
pathway to camalexin, a substance associated with the resistance of
plants to phytopathogens (Abu-Zaitoon et al., 2016). The presence
of TAM, IAN, IPyA and IAM as pathways for the synthesis of IAA
does not automatically translate into an increase for IAA generated,
since this compound has a complex regulatory system and can be
transformed into similar metabolites such as Indole-3-butyric Acid,
4-chloroindole-3-acetic acid, or associate with amino acids (Zuo et
al., 2019).
The present study analyzed by HPLC the synthesis pathways of
IAA in the fungal species Trichoderma asperellum and T. koningiopsis,
under liquid culture media conditions supplemented with tryptophan
as well as interacting with corn seeds.
Materials and methods
Biological material
Pure cultures of native strains of Trichoderma asperellum
(NRRL50191) were used, originating from the rhizosphere of
sunower (Helianthus annuus), and Trichoderma koningiopsis
(NRRL50190), collected from soils cultivated with sorghum
(Sorghum bicolor) in northern Mexico. Both T. asperellum and T.
koningiopsis were independently grown in Potato Dextrose Broth
(PDB) medium, supplemented with 100 ppm of TRP, and inoculated
at a concentration of 1x10
6
spores.mL
-1
for each fungus. PDB medium
without TRP was used as a control for each treatment. The cultures
were incubated for 72 h at 25 °C with continuous stirring at 200 rpm.
Samples of 3 mL were taken every 24 h for a total of 120 h. These
samples were centrifuged at 10,000 rpm for 10 minutes, and the
supernatants were stored at -20 °C until analysis.
Interaction of Trichoderma spp. with corn seed germination
Ten seeds of corn (Zea mays, Pioneer 30P49) were placed in a
60 mm Petri dish containing 10 mL of a spore suspension (1×10
6
spores.mL
-1
) for each strain: MTES (Corn control), MTaTES (Corn
+ T. asperellum), MTaTRP (Corn + T. asperellum + Tryptophan),
MTkTES (Corn + Control), MTkTRP (Corn + T. koningiopsis +
Tryptophan), and MTkIAA (Corn + T. koningiopsis + Indole-3-acetic
acid). The assays were conducted in triplicate. Samples of 1 mL
were taken every 12 h up to 96 h post-inoculation. These samples
were centrifuged, ltered, and analyzed by High-Performance
Liquid Chromatography (Hewlett Packard-Agilent™, model 1100;
Waldbronn, Germany). The concentration of IAA and other auxinic
compounds was determined for each treatment. Analysis of variance
(ANOVA) was performed using Tukey‘s test to compare signicant
means of treatments, utilizing SAS38 software, version 8 for
Windows.
Analysis by HPLC
The supernatants collected from the culture media and corn
seeds inoculated with Trichoderma spp. were ltered through nylon
membranes (0.45 μm, Millipore™; Cork, Ireland) and injected into
a High-Performance Liquid Chromatography (HPLC) system using
a C18 ultrasphere column (150 x 4.6 mm) (Beckman Ultrasphere™;
Fullerton, USA). The mobile phase consisted of 80/20 (deionized
water-acetonitrile) with a pH of 3, at a ow rate of 1 mL.min
-1
.
Detection was performed using a UV detector (G1314A, Hewlett-
Packard Agilent™; Waldbronn, Germany) at a wavelength of 220 nm
(Hernandez-Mendoza et al., 2010). The obtained data were compared
with runs performed using commercial standards (gure 1).
175
150
mAU
125
100
75
50
25
0
0
2 4 6 8 10
Time
1.881
1.999
2.681
4.237
5.496
7.408
9.117
Figure 1. Chromatogram where the standads of the auxinic
compounds that were evaluated in this study are
integrated. Retention time for Kyn = 1.881 min;
L-tryptophan TRP = 1.999 min; tryptamine TRM =
2.681 min; indole acetamide IAM = 4.237 min; indole 3
acetonitrile IAN = 5.496 min; indole-3-pyruvic acid IPyA
= 7.408 min; indoleacetic acid IAA = 9.117 min.
Scanning electron microscopy (SEM)
The morphology of corn seeds was analyzed using scanning
electron microscopy (SEM) with a Jeol JSM-820 microscope (Jeol
Mexico SA de CV, Mexico). The corn samples were recovered from
trays and dried before being sent for scanning.
Results and discussion
Synthesis pathways of IAA in Trichoderma spp.
The results obtained show that both T. asperellum and T.
koningiopsis (gures 2A and 2B), when grown in PDB medium
alone or supplemented with TRP, were able to metabolize TRP and
synthesize IAA, IAM, and TRM. Neither IPyA nor IAN were detected
in the HPLC analysis, suggesting that the microorganisms under study
lack the capability to synthesize these compounds. This indicates that,
among the reported pathways of IAA synthesis in dierent organisms,
T. asperellum and T. koningiopsis utilize only two active pathways:
IAM and TRM. The IAM pathway has been described in both bacteria
and plant species (Tang et al., 2023).
When T. asperellum was grown in media without TRP, it produced
up to 61 ppm of IAA at 96 h. In contrast, T. koningiopsis synthesized
only 16 ppm of IAA in the same period. This increase in IAA synthesis
can be attributed to the strain. When TRP was added to the medium,
both microorganisms showed an increase in IAA production. These
results are consistent with previous ndings in P. veronii, P. uorescens,
P. putida, and Rhizobium spp. (Bajguz et al., 2023; Peñael-Jaramillo
et al., 2016; Nieto-Jacobo et al., 2017).
Based on the dierent amounts of TRP detected over time in
media with or without the addition of TRP, we estimated that its
availability is determined by the conditions of the medium and the
metabolism of the organism itself (Hirayama & Mochida, K., 2022;
Peñael-Jaramillo et al., 2016; Saleem et al., 2024). The Tukey test
detected signicant dierences (p<0.05) in the production of IAA,
which was higher when the microorganism was grown in media
supplemented with TRP (gure 2B).
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2025, 42(2): e254229 April-June. ISSN 2477-9409.
4-6 |
Interaction of corn seeds with Trichoderma spp.
The analysis of auxin compounds in corn germination, both alone
and in interaction with T. asperellum and T. koningiopsis (gures
3A, 3B, and 3C), did not reveal the presence of IAA. These results
are consistent with previous studies on Trichoderma spp. strains,
where IAA synthesis depended on the culture conditions and the
physiological state of the seeds (Nieto et al., 2017). It is possible that
IAA was not detected because it is intracellularly linked with sugars,
amino acids, and/or peptides in the seeds, as previously reported.
Figure 2. Kinetics of production of auxinic compounds in T. asperellum and in culture medium alone (A) and medium enriched with
TRP (B).
A high production of IPyA (between 1199 and 1313 ppm) was
observed in the three control treatments at the end of the kinetics. In
the Corn-Control treatment (Figure 3A, MTES), there was an increase
in TRM from 1 to 4 ppm after 12 h, with a tryptophan production of
2 ppm between 12 and 36 h. In contrast, in the T. asperellum-control
treatment (gure 3B, MT a TES), there was a lower production of
TRM (2 ppm) at the end of the kinetics, and the concentration of
TRP was 7 ppm. In the T. koningiopsis-control treatment (Figure 3C,
MTkTES), TRM production was 1 ppm at 72 h, with a concentration
of 5 ppm at the end of the kinetics.
Regarding auxin compounds, the tryptamine pathway (TRM)
is not the major precursor of IAA, as high accumulated levels of
tryptamine do not cause any change in IAA levels (Sztein et al.,
2002). As for IPyA, it is an important pathway for IAA biosynthesis
in many microorganisms and plants (Feng et al., 2024; Pirog et al.,
2022; Mory & Strader, 2020), but it was not detected in the assays
conducted here.
The presence of IAA was detected in the treatments where TRP
was added to the corn seeds (Figures 4A and 4B). Furthermore, the
IAA synthesis pathway through tryptamine remained active, with an
increased production of this auxin in treatment B (MTkTRP). The
IAA accumulated due to the availability of TRP. Similar responses
have been seen in T. atroviride IMI206040, T. virens Gv29.8, T.
atroviride B LU132, and T. reesei QM6a, when TRP was added to the
culture medium (Etesami & Glick, 2024; Nieto-Jacobo et al., 2017).
Our data indicated that the indole-3-pyruvic acid (IPyA) pathway was
stimulated in treatments with inoculated corn (Figure. 4). In other
cases, the production of IAA was inuenced by the abiotic factors
aecting the plants and microorganisms, including the content of
nutrients, humidity and pH (Etesami & Glick, 2024). This work
demonstrates the chemical interaction of Trichoderma spp. with corn
seeds as been reported in earlier works (Naveed et al., 2015; Dam &
Bouwmeester, 2016), by detecting synthesis of IAA in T. asperellum
(NRRL50191) at 36 h; the concentration of IAA increased until it
reached a maximum of 6 ppm at 60 h and decreased later to 3 ppm.
Figure 3. Detection of metabolites in corn germination (Pionner
30P49). A) Corn seeds; B) Corn seed interacting with T.
asperellum (Ta); C) Corn seed interacting with T. koningiopsis
(Tk). (IAA= Indole acetic acid; TRM= Tryptamine; TRP=
Tryptophan; IPyA= Indole Pyruvic acid).
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Romero et al. Rev. Fac. Agron. (LUZ). 2025, 42(2): e254229
5-6 |
Figure 4. Detection of auxin metabolites in corn seeds germinating
(Pionner 30P49) in a medium supplemented with TRP
(Tryptophan). A) Interacting with T. asperellum (Ta); B)
Interacting with T. koningiopsis (Tk). (IAA= Indole acetic
acid; TRM= Triptamine; IAM= Indole acetamide; TRP=
tryptophan; IPyA= Indole Pyruvic acid).
In the case of T. koningiopsis (NRRL50190) the production
of IAA started at 24 h and reached its maximum (5 ppm) at 36 h.
This is a signicant dierence (p<0.05) with the inoculation of corn
seeds with Trichoderma. Both isolates stimulate germination by
activating biochemical and transcriptional processes more quickly
through chemiosmotic reactions, favored by the pH gradient in the
plant cells and the excretion of exudates, which are captured by the
microorganisms, increasing the synthesis of IAA (Li et al., 2015;
Peñael-Jaramillo et al., 2016). There were no signicant dierences
(Tukey 0.05) in the production of IAA between corn seeds interacting
with T. asperellum in media supplemented with TRP and between the
treatments MTaTRP (T. asperellum average 2.288889a) and MTkTRP
(T. koningiopsis average 1.833333ab), but there were signicant
dierences between these treatments and the control (MTaTES,
average 1.011111ab and MTkTES, average 0.844444b) (Table 2).
In the assays where the interaction of Trichoderma with corn seeds
was evaluated in a medium rich in IAA (gures 5A and 5B), no
signicant dierences (p<0.05) in the synthesis of IAA and IPyA
were observed between the two microorganisms, nor when compared
with the control. Furthermore, regarding the synthesis of TRP, the
highest concentration (5 ppm) was detected in the treatment Corn-T.
asperellum-IAA. With respect to the degradation of IAA, there were
no signicant dierences (p<0.05) between treatments.
The interaction between the corn radicle and Trichoderma spp.
was conrmed by the colonization of the root. Scanning electron
microscopy showed hyphal penetration and the formation of haustoria
next to the site where the mycelium enters the radicular cortex (gure.
6). In this case, the most important thing is that the hyphal cell that
penetrates the cortex has a cell wall with distinct characteristics than
the rest of the mycelium, which remains outside. This hyphal cell
has a thinner and more exible cell wall, while the hyphal cells that
remain outside have a thicker and more solid cell wall.
Figure 5. Detection of auxins in corn seeds germinating (Pionner
30P49) in a medium supplemented with IAA (indole
acetic acid) and interacting with: A) T. asperellum (Ta);
B) T. koningiopsis (Tk). (ACM=Indole acetonitrile; TRM=
Triptamine; IAM=Indole acetamide; TRP=tryptophan;
IAA= Indole acetic acid; IPyA= Indole Pyruvic acid).
Figure 6. Hyphae of T. koningiopsis penetrating the root cortex
of a corn seedling (30P49 Pioneer) six days after
germination.
Conclusions
The fungi T. asperellum NRRL50191 and T. koningiopsis
NRRL50190 produce IAA through the TRM and IAM pathways, but
they are unable to convert IAN and IPyA into IAA. The production
of IAA changed when corn seeds were inoculated with spores of
Trichoderma, forming a close association due to the fungal hyphae
penetrating the rootlets of the seedlings.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2025, 42(2): e254229 April-June. ISSN 2477-9409.
6-6 |
Acknowledgments
Romero-Domínguez had a CONACYT scholarship during his
Master of Science studies (B091484). Hernández-Mendoza, Quiroz-
Velásquez, and Hernández-Delgado are EDI-IPN. Hernandez-
Delgado is COFAA-IPN. Hernández-Mendoza and Quiroz-Velásquez
are SNI.
Literature cited
Abu-Zaitoon, Y., Aladaileh, S., and Tawaha, A. R. A.. (2016). Contribution of the
IAM Pathway to IAA Pool in Developing Rice Grains. Brazilian Archives
of Biology and Technology, 59, e16150677. https://doi.org/10.1590/1678-
4324-2016150677
Bajguz A. & Piotrowska-Niczyporuk A. (2023). Biosynthetic Pathways of
Hormones in Plants. Metabolites, 13(8), 884. https://doi.org/10.3390/
metabo13080884.
Braithwaite, M., Johnston, P. R., Ball, S. L., Nourozil, F., Hay, A. J., Shoukouhi,
P., Chomic, A., Lange, C., Ohkura, M., Nieto-Jacobo, M. F., Cummings,
N. J., Bienkowski, D., Mendoza-Mendoza, A., Hill, R. A., McLean, K.
L., Stewart, A., Steyaert, J. M. and Bissett, J. (2017). Trichoderma down
under: species diversity and occurrence of Trichoderma in New Zealand.
Australasian Plant Pathology. 46, 11–30. https://doi.org/10.1007/s13313-
016-0457-9
Cai, F., Chen, W., Wei, Z., Pang, G., Li, R., Ran, W.and Shen, Q. (2015).
Colonization of Trichoderma harzianum strain SQR-T037 on tomato
roots and its relationship to plant growth, nutrient availability and soil
microora. Plant Soil, 388, 337–350. https://doi.org/10.1007/s11104-
014-2326-.
Dam, N. M.& Bouwmeester, H. J. (2016). Metabolomics in the Rhizosphere:
Tapping into Belowground Chemical Communication. Trends in Plant
Science, 21, 256-265. https://doi.org/10.1016/j.tplants.2016.01.008
Feng, Y., Tian, B., Xiong, Lin,G., Cheng L., Zhang T., Lin B.,, Ke Z., and Xin
L. (2024). Exploring IAA biosynthesis and plant growth promotion
mechanism for tomato root endophytes with incomplete IAA synthesis
pathways. Chemical and Biological Technologies in Agriculture, 11, 187.
https://doi.org/10.1186/s40538-024-00712-8
Fu, S.F., Wei, J.Y., Chen, H.W., Liu, Y.Y., Lu, H.Y., and Chou, J.Y. (2015). Indole-
3-acetic acid: A widespread physiological code in interactions of fungi
with other organisms. Plant Signaling & Behavio,10(8), e1048052. doi:
10.1080/15592324.2015.1048052.
Ghasemi, S., Safaie, N., Shahbazi, S., Shams-Bakhsh, M., and Askari, H. (2020).
The Role of Cell Wall Degrading Enzymes in Antagonistic Traits of
Trichoderma virens Against Rhizoctonia solani. Iraniab Journal of
Biotechnology, 18(4), e2333. doi: 10.30498/IJB.2020.2333.
Guzmán-Guzmán, P., Aleman-Duarte, M. I., Delaye, L., Herrera-Estrella, A.,
and Olmedo-Monl, V. (2017). Identication of eector-like proteins
in Trichoderma spp. and role of a hydrophobin in the plant-fungus
interaction and mycoparasitism. BMC Genetics, 18, 16. https://doi.
org/10.1186/s12863-017-0481-y.
Etesami, H., & Glick B. (2024). Bacterial indole-3-acetic acid: A key regulator
for plant growth, plant-microbe interactions, and agricultural adaptive
resilience, Microbiological Research, 281, 127602. https://doi.
org/10.1016/j.micres.2024.127602.
Hernández-Mendoza, J. L., Moreno-Medina, V. R., Quiroz-Velásquez, J. D.,
García-Olivares, J. G., & Mayek-Pérez, N. (2010). Efecto de diferentes
concentraciones de ácido antranílico en el crecimiento del maíz. Revista
Colombiana de Biotecnología, XII(1),57-63. doi: https://www.redalyc.
org/articulo.oa?id=77617786007
Hirayama, T., & Mochida, K. (2022). Plant Hormonomics: A Key Tool for Deep
Physiological Phenotyping to Improve Crop Productivity. Plant and Cell
Physiology, 63(12), 1826-1839. https://doi.org/10.1093/pcp/pcac067.
Leontovyčová, H., Trdá, L., Dobrev, P.I., Šašek, V., Gay, E., Balesdent, M.H.,
and Burketová, L. (2020). Auxin biosynthesis in the phytopathogenic
fungus Leptosphaeria maculans is associated with enhanced transcription
of indole-3-pyruvate decarboxylase LmIPDC2 and tryptophan
aminotransferase LmTAM1. Research in Microbiology, 171(5-6), 174-
184. https://doi.org/10.1016/j.resmic.2020.05.001.
Lopez-Coria, M., Hernández-Mendoza, J. L., and Sánchez-Nieto, S. (2016). T.
asperellum induces maize seedling growth by activating the PM H+ 1
-2 ATPase. Molecular Plant-Microbe Interactions
, 29, 797-806. doi.
org/10.1069/MPMI-07-16-0138-R.
Lubna, Asaf, S., Hamayun, M., Gul, H., Lee, I. J., and Hussain, A. (2018).
Aspergillus niger CSR3 regulates plant endogenous hormones and
secondary metabolites by producing gibberellins and indoleacetic acid.
Journal of Plant Interactions, 13(1), 100–111. https://doi.org/10.1080/1
7429145.2018.1436199.
Naveed, M., Amjad, Q. M., Zahir, Z. A., Hussain, M. B., Sessitsch, A., and Mitter,
B. L. (2015). Annals of Microbiology, 65:1381-1389. doi: 10.1007/
s13213-014-0976-y
Mory, N. & Strader, L. (2020) Old Town Roads: routes of auxin biosynthesis
across kingdoms, Current Opinion in Plant Biology, 55, 21-27, https://
doi.org/10.1016/j.pbi.2020.02.002.
Nieto-Jacobo, M. F., Steyaert, J. M., Salazar-Badillo, F. B., Nguyen, D.V.,
Rostás, M., Braithwaite, M., and Mendoza-Mendoza, A. (2017).
Environmental Growth Conditions of Trichoderma spp. Aects Indole
Acetic Acid Derivatives, Volatile Organic Compounds, and Plant Growth
Promotion Frontiers in Plant Science. 8, 102. https://doi.org/10.3389/
fpls.2017.00102.
Peñael-Jaramillo, M. F., Torres-Navarrete, E. D., Barrera-Álvarez, A. E., Prieto-
Encalada, H. G., Morante, C. J., and Canchignia-Matínez, H. F. (2016).
Ciencias agrarias producing indole-3acetic acid using Pesudomonas
veronii R4 and in vitro formation of roots in Thompson seedless grapevine
leaves. Ciencia y Tecnología, 9, 31-36. https://revistas.uteq.edu.ec/index.
php/cyt/article/view/158/172
Pirog, T.P. & Piatetska, D.V. & Klymenko, N.O. and Iutynska, G.O.. (2022). Ways
of Auxin Biosynthesis in Microorganisms. Microbiological Journal, 84,
57-72. doi: https://doi.org/10.15407/microbiolj84.02.057.
SAS Institute Inc. (2004). SAS/STAT ® 9.1 User’s Guide. Cary, NC: SAS Institute
Inc.
Saleem, A., Qasim, M. W., Ahmad, A., Bibi, A., Haq, I. U., Khan, A. A., and
Sajjad, M. (2024). Recent Advances in Photosynthesis, Plant Hormones
and Applications in Plant Growth. Haya: The Saudi Journal of Life
Sciences, 9(1), 17-22. http://dx.doi.org/10.36348/sjls.2024.v09i01.003
Sztein, A.E., Ilić, N., Cohen, J.D. et al. (2002). Indole-3-acetic acid biosynthesis
in isolated axes from germinating bean seeds: The eect of wounding on
the biosynthetic pathway. Plant Growth Regulation 36, 201–207. https://
doi.org/10.1023/A:1016586401506
Tang, J. Li, Y., Zhang, L., Mu, J., Jiang, Y., Fu, H., Zhang, Y., Cui, H., Yu, X.,
and Ye, Z. (2023) Biosynthetic Pathways and Functions of Indole-3-
Acetic Acid in Microorganisms. Microorganisms, 11(8), 2077. https://doi.
org/10.3390/microorganisms11082077
Tariq, A., & Ahmed, A. (2022). Auxins-Interkingdom Signaling Molecules.
IntechOpen. doi: 10.5772/intechopen.102599
Uribe-Bueno, M., Hernández-Mendoza, J.L., García, C., Ancona V., Larios-Serrato,
V. (2020). Independent Tryptophan pathway in Trichoderma asperellum
and T koningiopsis: New insights with bioinformatic and molecular
analysis. bioRxiv preprint doi: https://doi.org/10.1101/2020.07.31.230920.
Yao, X., Guo, H., Zhang, K., Zhao, M., Ruan, J., and Chen, J. (2023).Trichoderma
and its role in biological control of plant fungal and nematode
disease. Frontiers in Microbiology, 3(14), 1160551. doi: 10.3389/
fmicb.2023.1160551.
Yin, Q., Zhang, J., Wang, S.
Jintang Cheng, Han Gao, Cong Guo, Lianbao
Ma, Limin Sun, Xiaoyan Han, Shilin Chen, An Liu. (2021).
N-glucosyltransferase GbNGT1 from ginkgo complements the auxin
metabolic pathway. Hortic Res 8, 229 https://doi.org/10.1038/s41438-
021-00658-0
Zuo W.L., Okmen B., Depotter J.R.L., Ebert M.K., Redkar A., Villamil J.M., and
Doehlemann G. (2019). Molecular Interactions between smut fungi and
their host plants. Annual Review of Phytopathology, 57, 411–430. doi:
10.1146/annurev-phyto-082718-100139.
