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The Use of Fungal Endophyte Penicillium citrinum on Tree Seedling: Applicability and Limitation

January 2020
BIO Web of Conferences 20(5):03005

DOI:10.1051/bioconf/20202003005

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CC BY 4.0

Authors:

Safinah Surya Hakim

National Research and Innovation Agency

Tri Wira Yuwati

National Research and Innovation Agency (BRIN)

Penicillium citrinum is an endophyte fungus isolated from plant tissues that live in tropical peatland. Various study reveals that endophytic fungi give advantages to plant health. Since 2015, series of experiments were conducted to investigate the capability of P. citrinum P3.10 as biofertilizer of plant tree in nursery stage which are: pathogenicity test, in vitro assay, direct application to seeds, dosage test, and fertilizer formulation. This paper presents a review from our research of P. citrinum isolate P3.10 from the isolation stage to the biofertilizer product formulation. Resear ch results showed that the application of endophytic fungi to seedlings gave positive responses. However, during the research process there were also obstacles in the application of endophytic fungi to plants, which are: (a) difficulties in application due to the varied response, (b) formulation, (c) storage, (d) isolate viability, and (d) fungal isolate maintenance. Risk management was needed during biofertilizer production. Hence, the utilization of biofertilizer made from endophyte fungi is applicable and can be used not only on an experimental scale but also on a larger scale.

The research process of bioprospection of microbial peat swamp forest.

…

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*Correspoding author: safinah.hakim@gmail.com

The Use of Fungal Endophyte Penicillium citrinum on Tree

Seedling: Applicabilit y and Limitation

Safinah Surya Hakim1* and Tri W . Yu wa t i1

1Banjarbaru Environment and F orest ry Research Development Institute, Banjarbaru, 70721. Indonesia

Abstract. Penici llium citr inum is an endophyte fungus isolated from plant tissues that live in t ropical

peatland. Various st udy reveals that endop hytic fungi give advantages to p lant health. Since 2015,

series of experiments were conducted to investigate the capability of P. citrinum P3.10 as biofertilizer

of plant tree in nursery stage which are: pathogenicity test, in vitro assay, direct application to seeds,

dosage test, and fertilizer formulation. This pap er presents a review from our research of P. citrinum

isolate P3.10 from the isolation stage to the biofertilizer product formulation. Research results showed

that the application of endophytic fungi to seedlings gave p ositive responses. However, during the

research process there were also obstacles in the application of endophytic fungi to plants, which are:

(a) difficult ies in application due t o the varied response, (b) formulation, (c) storage, (d) isol ate

viabil ity, and (d) fungal isolate maintenance. Risk management was needed during biofertilizer

production. Hence, the utilization of biofertilizer made from endophyt e fungi is applicable and can be

used not only on an experimental scale but also on a larger scale.

1 Introduction

Naturally, plants have certain relationships with

endophytes. It is reported that 90% of the plant do

symbiosis with microbes, including endophyte fungi.

Unlike mycorrhiza; which has specialized structures

within its pla nt-fungus interaction such as arbuscules,

Hartig net, vesicles; plant-endophyte interaction is

deficient in specialized structures [1]. Nevertheless ,

plant-endophyte relationship according to many studies

have significant benefits for the plant as follow: (a)

Enhance plant growth [2-6], (b) Source of secondary

metabolites that can be a benefit for plant and

pharmaceutical needs [7-10], and (c) Induce plant

resistance to pest and diseas e [10-12].

Many fungi identified as endophytic fungi,

including Penicillium citrinum. During this research, P.

citrinum s how the ability to improve the growth of the

plant [13]. P. citrinum produced hormone Indole Acetic

Acid (IAA), extracellular enzymes , and au xin which can

increase the growth of the inoculated plants [14].

Besides, endophytic fungi Penicillium sp. was indicated

able to increase plant growth by increasing plant

nutrient absorption [15].

To gain information on the biology and function

of endophytic fungi in peat swamp forest, Banjarbaru

Forestry Research and Development Institute has

conducted a multi-year-research focusing on endophyte

bioprospection. The research main purpose was

bioprospecting microbe in peatland, p artic ula rly

mycorrhizal and endophytic fungi. At the early stage of

the research in 2015, exploration, isolation, and

screening were carried out to identify endophytic fungi

that could potentially increase plant growth. In the

second year (2016), research activities were done to

obtain information on the effectiveness of endophytic

fungi on the plant through inoculation. At the next stage

(2017), the research activ ities aimed to find out the best

inoculation techniques and dosages for microbial

applications in plants. In the last year (201 8), the

formulation was done to investigate the effective carrier

for endophytic fungi-ba s ed b io logical fert i lizer. Th is

paper presents a review and s ummary of the research

re s ult s that illustrate the applicability and limitation

occurs in the development of biofertilizers .

2 Research Process

Several processes were done in this research (Fig. 1).

Exp loration was the first stage of research activity to

isolate endophyte fungi of trees in the peat swamp

forest. Endophytic fungi isolated fro m leaves of the peat

swamp forest tree (Fig. 2). Collected leaves were stored

in the cooler bag and processed in the laboratory.

Leaves cut into small pieces, surface sterilized, and

moved into Malt Extract Agar medium. Diffe rent

morphologies of fungi were tested on a specific

Pikovskhaya (PVK) Agar medium, to test its ability in

phosphate solubilization (Fig. 3). Twelve endophytic

fungi found able to produce clear zones on PVK Agar,

which means it has the potential to help phosphate

absorption in plants. We identified four species of

endophytic fungi which showed the best performance in

PVK A gar, i.e. G1.12 (Pestalopsis sp.), M2.6

(Phyllosticta sp.), K1.4 (Endophytic fungi sp.), An d

P3.10 (P. citrinum).

Fig ure 1. The research p rocess of bioprospection of

microbial peat swamp forest.

BIO Web of Conferences 20, 03005 (2020) https://doi.org/10.1051/bioconf/20202003005

ICWEB 2019

License 4.0 (http://creativecommons.org/licenses/by/4.0/).

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Fig ure 1. Phy logenetic tree of isolated endophy tic fungi of

peat-swamp forest in Central Kalimantan.

Fig ure 2. Clear zone in PVK media indicated fungal ability

to solubilize phosphate.

Investigating the ability of isolated endophytic fungi

acted as a plant growth enhancer in vivo became the

ma in aim of the second year research. Liquid fungi

inoculants were inoculated to plant in the greenhouse.

After a 12 week observation, endophytic fungi

inoculation on Gerunggang (Cratoxylon glaucum)

seedlings significantly affected the height but not the

plant diameter gro wth and leaf numbers. To achieve a

better understanding of plant responses to endophyte

fungi, inoculation tests were done to several plant

species at different dosages and application methods.

The result of this study showed that variation in dosage

and application method, different inoculation frequency,

and diffe rent plant species did not bring about the

different responses to the plant growth. Five months of

observation showed there were no differences in plant

growth parameters, including height, diameter, leaf

numbers, dry weight of plants, soil P content, an d

chlorophyll content, between inoculated plants to

uninoculated plants (control). Double inoculation which

combining endophyte and mycorrhiza was done to

obtain a better result. However, the double inoculation

method did not significantly affect the growth of nyatoh

and sengon in the nursery. The summary of the

inoculation test presented in Table 1.

Tabl e 1. Plant response to endophyte inoculation.

Plant species

Research

Treatment

Growth performance

H eigh t

Diamet er

Leaf number

Biomass

Gerunggang

(Cratoxylon glaucum)

Root

inoculation

Pos itive neutral neutral neutral Negative

Leaf drop

inoculation

Pos itive

neutral

Negative

Belangeran

(Shorea belangeran)

5 ml, once

neutral

5 ml, twice

neutral

3 ml, once

neutral

3 ml, twice

neutral

1 ml, once

neutral

1 ml, twice

neutral

Gerunggang

(Cratoxylon glaucum)

5 ml, once

neutral

5 ml, twice

neutral

3 ml, once

neutral

3 ml, twice

neutral

1 ml, once

neutral

1 ml, twice

neutral

Ramin

(Gonystylus

bancanus)

5 ml, once

neutral

5 ml, twice

neutral

3 ml, once

neutral

3 ml, twice

neutral

1 ml, once

neutral

1 ml, twice

neutral

*neutral: non-significant result compare to control ; *na: data not available

The "formulation" refers to the laboratory or

industrial process of unifying the carrier with the

microbial s train . "Inoculant" refers to the ﬁnal product

of formu lation containing a carrie r and microbial agent

or consortium of microorganis ms. Formulation became

the last stage of this multi-year research. In this stage,

BIO Web of Conferences 20, 03005 (2020) https://doi.org/10.1051/bioconf/20202003005

ICWEB 2019



Fig ure 1. Phy logenetic tree of isolated endophy tic fungi of

peat-swamp forest in Central Kalimantan.

Fig ure 2. Clear zone in PVK media indicated fungal ability

to solubilize phosphate.

Investigating the ability of isolated endophytic fungi

acted as a plant growth enhancer in vivo became the

ma in aim of the second year research. Liquid fungi

inoculants were inoculated to plant in the greenhouse.

After a 12 week observation, endophytic fungi

inoculation on Gerunggang (Cratoxylon glaucum)

seedlings significantly affected the height but not the

plant diameter gro wth and leaf numbers. To achieve a

better understanding of plant responses to endophyte

fungi, inoculation tests were done to several plant

species at different dosages and application methods.

The result of this study showed that variation in dosage

and application method, different inoculation frequency,

and diffe rent plant species did not bring about the

different responses to the plant growth. Five months of

observation showed there were no differences in plant

growth parameters, including height, diameter, leaf

numbers, dry weight of plants, soil P content, an d

chlorophyll content, between inoculated plants to

uninoculated plants (control). Double inoculation which

combining endophyte and mycorrhiza was done to

obtain a better result. However, the double inoculation

method did not significantly affect the growth of nyatoh

and sengon in the nursery. The summary of the

inoculation test presented in Table 1.

Tabl e 1. Plant response to endophyte inoculation.

Plant species

Research

Treatment

Growth performance

H eigh t

Diamet er

Leaf number

Biomass

Gerunggang

(Cratoxylon glaucum)

Root

inoculation

Pos itive

neutral

Negative

Leaf drop

inoculation

Pos itive

neutral

Negative

Belangeran

(Shorea belangeran)

5 ml, once

neutral

5 ml, twice

neutral

3 ml, once

neutral

3 ml, twice

neutral

1 ml, once

neutral

1 ml, twice

neutral

Gerunggang

(Cratoxylon glaucum)

5 ml, once

neutral

5 ml, twice

neutral

3 ml, once

neutral

3 ml, twice

neutral

1 ml, once

neutral

1 ml, twice

neutral

Ramin

(Gonystylus

bancanus)

5 ml, once

neutral

5 ml, twice

neutral

3 ml, once

neutral

3 ml, twice

neutral

1 ml, once

neutral

1 ml, twice

neutral

*neutral: non-significant result compare to control ; *na: data not available

The "formulation" refers to the laboratory or

industrial process of unifying the carrier with the

microbial s train . "Inoculant" refers to the ﬁnal product

of formu lation containing a carrie r and microbial agent

or consortium of microorganis ms. Formulation became

the last stage of this multi-year research. In this stage,



three different carriers. such as sawdust, rice bran, and

peat soil, were tested to find out what is the best carrier

for P .citrinum. Observation of fungal viability indicated

that P. citrinum did not growth optimally on these

carriers (Hakim et al. unpublished)

3 Limitation in Endophyte Study and

Application

In general, the three years (2015-2017) of the

inoculation study of endophytic fungi on tree seedling

showed that the results were ranging from negative to

neutral (Table 1). This study contributed to the

amb iguity and uncertainty effect of the application of

endophyte fungi to plant growth. Moreover, p lan t

responses to endophytic fungi are generally negative

[16]. It was also noted th at the variability in describing

plant response to endophyte inoculation [16] . The s tudy

of the endophytic fungi defines that in the plant-fungus

interaction, comple x environ mental parameters affect

the interaction [17 ]. The study revealed that the highes t

colonization was found in secondary forests compared

to the open area. This difference colonization

percentage caused by several environmental parameters

including microclimate (humidity, water level, soil

nutrition, etc.) and habitat condition. Humidity and

rainfa ll have an important role in determining the

percentage of endophytic foliar colonization [18].

Several assumptions may clarify the reasons of

endophytic fungi to be less optimal on plants. First,

inoculated endophytic fungi have difficulty competing

with native endophytic fungi in a plant. According to

[19] Suryanarayanan (2012 ), endophytes have

properties that are not easy to infect other types of

leaves due to the presence of several microbial

communities such as native endophytes in these plants,

bacteria, etc. Also, the presence of the uncultured fungi

th a t exis t in s ide p lant t is sue could be a competitor to

endophytic fungi. Second, the presence of secondary

metabolites also affects the endophytic inoculation

process [19].

To increase the effectiveness and feasibility of

endophytic fungi as a plant growth enhancer,

endophytic fungi were formu lated with a carrier so that

it can be used as biological fe rtilizer. The formulation

result during this study showed that the abilit y of the

fungi decreased after 4-week storage. Storage affected

the viability of the fungi. Fo r e xa mp le , Bauveria

bassiana fungus was influenced by several factors such

as fungal species, carrier properties, storage temperature,

and incubation time [ 20]. A better formulation is

needed to make a good biofertilizer. Inputs of

technology such as drying method, fluid bed drying

method, and nano biofertilizer, can be required to

increase the quality of fungal based biofertilizer.

The endophyte study remains many questions as

follows: dosage, whether endophyte general or specific

fungal type, application method, etc. Despite many

references that presented data on the advantage of

endophyte fungi, most of the research still co nferred

data on a laboratory scale. Th ere fo re, research on the

endophytic fungi in plants on the application scale still

needs to be done and developed.

4 Conclusion

1. Penicillium citrinum showed the capability to

produce clear zones in Pikovskhaya agar which

indicated its ability to solubilize phosphate.

2. After 12 weeks of observation, the result showed

that inoculation of endophyte Penicillumcitrinum

isolate P3.10 on gerunggang (Cratoxylon

glaucum) seedlings performed a significant effect

on seedling height .

3. Different plant species, dosage, inoculation

methods, formu lation caused different effects on

tree seedling. As an exa mple: inoculation of

endophyte P. citrinum isolate P3.10 showed a

positive effect on Ge ronggang height. However, in

merapat seedling, there was no significant

difference between inoculated and uninoculated

s ee d ling

4. Biofertilizer made fro m Penicillium citrinum in

three different carriers (rice barn, sawdust, and

peat soil) can be stored only for a maximu m of 28

days th at in d icat ed th e difficu lties o f b io fert i li ze r

formulation, handling, and storage.

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The genus Pestalotiopsis has received consider-able attention in recent years, not only because of its role as a plant pathogen but also as a commonly isolated endophyte which has been shown to produce a wide range of chemically novel diverse metabolites. Classification in the genus has been previously based on morphology, with conidial characters being considered as important in distinguishing species and closely related genera. In this review, Pestalotia, Pestalotiopsis and some related genera are evaluated; it is concluded that the large number of described species has resulted from introductions based on host association. We suspect that many of these are probably not good biological species. Recent molecular data have shown that conidial characters can be used to distinguish taxa; however, host association and geograph-ical location is less informative. The taxonomy of the genera complex remains confused. There are only a few type cultures and, therefore, it is impossible to use gene sequences in GenBank to clarify species names reliably. It has not even been established whether Pestalotia and Pestalotiopsis are distinct genera, as no isolates of the type species of Pestalotia have been sequenced, and they are morphologically somewhat similar. When selected GenBank ITS accessions of Pestalotiopsis clavispora, P. disseminata, P. microspora, P. neglecta, P. photiniae, P. theae, P. virgatula and P. vismiae are aligned, most species cluster throughout any phylogram generated. Since there appears to be no living type strain for any of these species, it is unwise to use GenBank sequences to represent any of these names. Type cultures and sequences are available for the recently described species P. hainanensis, P. jesteri, P. kunmingensis and P. pallidotheae. It is clear that the important species in Pestalotia and Pestalotiopsis need to be epitypified so that we can begin to understand the genus/genera. There are numerous reports in the literature that various species produce taxol, while others produce newly discovered compounds with medicinal potential and still others cause disease. The names assigned to these novel compound-producing taxa lack an accurate taxo-nomic basis, since the taxonomy of the genus is markedly confused. Until the important species have been epitypi-fied with living strains that have been sequenced and deposited in public databases, researchers should refrain from providing the exact name of species.

Fungal endophytes: An untapped source of biocatalysts

Article

Full-text available

May 2012

Horizontally transmitted endophytes are an ecological group of fungi that infect living plant tissues and survive in them without causing any disease symptoms. Even as facets of the endophyte-plant symbiotic relationship are being uncovered, there is an increasing appreciation of the different growth substrates exploited by endophytes and the vast repertoire of secreted enzymes of these fungi. These attributes exemplify the striking biodiversity of fungal endophytes and should motivate bioprospecting these organisms to identify novel biocatalysts that might help address challenges in medicine, food security, energy production and environmental quality.

Plant growth promotion by phosphate solubilizing fungi - Current perspective

Article

Full-text available

Feb 2010
Arch Agron Soil Sci

Phosphorus is abundant in soils in both organic and inorganic forms; nevertheless, it is unavailable to plants. Accordingly, soil becomes phosphorus (P)-deficient, making P one of the most important nutrient elements limiting crop productivity. To circumvent the P deficiency, phosphate-solubilizing microorganisms could play an important role in making P available for plants by dissolving insoluble P. The dissolution of inorganic P by microbial communities including fungi is though common under in vitro conditions; the performance of phosphate-solubilizing microbes in situ has been contradictory. Fungi exhibit traits such as mineral solubilization, biological control, and production of secondary metabolites. As such, their potential to enhance plant growth when present in association with the roots is clear. The challenge is how to make use of such biological resources to maintain soil health while increasing the crop productivity by providing P to plants through the application of phosphate-solubilizing fungi. The present review focuses on the mechanisms of phosphate solubilization, development and mode of fungal inoculants application and mechanisms of growth promotion by phosphate-solubilizing fungi for crop productivity under a wide range of agro-ecosystems, and the understanding and management of P nutrition of plants through the application of phosphate-solubilizing fungi will be addressed and discussed.

Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content

Article

Full-text available

Aug 2011
FUNCT ECOL

1. Cool-season grasses can be simultaneously infected by foliar fungal endophytes and colonised by mycorrhizal fungi, the integrated functions of which are strong predictors of plant fitness within grassland ecosystems. Evidence has been presented previously that infection of grass species with foliar endophytes can negatively affect mycorrhizal colonisation. Here, we tested the hypothesis that mycorrhizal colonisation in turn adversely affects Neotyphodium endophyte concentrations and that the competitive interaction between the two endosymbionts is affected by resource supply.

Nutrient Concentration in Growth Medium Affects Relationship between Root Endophytic Fungi and Host Plant

Article

Jan 2017

Ethnomedicinal uses, pharmacological activities, and cultivation of Lignosus spp. (tiger׳s milk mushrooms) in Malaysia – A review

Article

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The effects of fungal root endophytes on plant growth: A meta-analysis

Article

Jul 2012
MYCORRHIZA

Fungal root endophytes are plant associates that colonize root tissue internally without causing any obvious harm to their host. Although ubiquitous, this relationship is not well understood. Our objectives were to determine the effects of fungal root endophyte inoculation on plant biomass and nitrogen concentration by conducting an extensive meta-analysis. We also explored the effects of experimental conditions on the host-endophyte relationship. We performed analyses weighted with non-parametric variance on plant response to root endophytes from the Ascomycetes (excluding the Clavacipitaceae), including categorical analyses of 21 experimental factors, ranging from the identity of the host and the endophyte, to the composition of the growing medium. The response of total biomass to endophyte inoculation was 18 % lower than non-inoculated controls, while individually, root biomass, shoot biomass, and nitrogen concentration responses to endophyte inoculation were neutral. The identities of both the host and the endophyte had an influence, as did the original source of the endophyte (whether or not the isolate used originated from the same host species). Experimental conditions also influenced the plant-endophyte relationship, with the most important being the availability and sources of carbon and organic nitrogen, particularly peat moss. Although our analysis demonstrates that overall plant biomass and nitrogen concentration responses to ascomycetous root endophyte inoculation is neutral to negative, these results are somewhat confounded by among-study differences in experimental conditions, which undoubtedly contribute to the high levels of variability in plant response seen in the literature.

Positive association between mycorrhiza and foliar endophytes in Poa bonariensis, a native grass

Article

Mar 2008

The interaction between mycorrhiza and leaf endophytes (Neotyphodium sp.) was studied in three Poa bonariensis populations, a native grass, differing significantly in endophyte infection. The association between endophytes and mycorrhizal fungi colonisation was assessed by analysing plant roots collected from the field. We found that roots from endophyte-infected populations showed a significantly higher frequency of colonisation by mycorrhizal fungi and that soil parameters were not related to endophyte infection or mycorrhiza colonization. In addition, we did not observe significant differences in the number of AM propagules in soils of the three populations sites. We also report the simultaneous development of Paris-type and Arum-type mycorrhiza morphology within the same root systems of P. bonariensis. The co-occurrence of both colonisation types in one and the same root system found in the three populations, which differed in Neotyphodium infection, suggests that foliar endophytes do not determine AM morphology. The percentage of root length colonised by different types of fungal structures (coils, arbuscules, longitudinal hyphae and vesicles) showed significant and positive differences in arbuscular frequency associated with endophyte infection, whereas the much smaller amounts of vesicles and hyphal coils did not differ significantly.

The Use of Fungal Endophyte Penicillium citrinum on Tree Seedling: Applicability and Limitation

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