2023.08.03.48
Files > Volume 8 > Vol 8 No 3 2023

Characterization of Fusarium
species causing dry rot of potato mini tubers produced by biotechnological
approaches

Michel Leiva-Mora 1*
, Mayrebi
Herrera-Capote2, Mayra Acosta-Suárez3
, Catherine Lizzeth
Silva Agurto4
, Natalys Solis5
, Walter Oswaldo Veloz
Naranjo6
, Rodrigo Núñez7
; Miguel Angel Osejos Merino8







1
Laboratorio
de Biotecnología. Departamento de Agronomía, Facultad de Ciencias
Agropecuarias, Universidad Técnica de Ambato.
2
Facutad de
Ciencias Agrpecuarias, Universidad Central Marta Abreu de Las Villas. Santa
Clara, Cuba.
3
Instituto
de Biotecnología de las Plantas, Universidad Central Marta Abreu de Las Villas.
Santa Clara, Cuba.
4
Laboratorio
de Biotecnología. Departamento de Agronomía, Facultad de Ciencias
Agropecuarias, Universidad Técnica de Ambato.
5
Laboratorio
de Bioinsumos. Departamento de Agronomía, Facultad de Ciencias Agropecuarias,
Universidad Técnica de Ambato.
6
Departamento
de Agronomía, Facultad de Ciencias Agropecuarias, Universidad Técnica de
Ambato.
7
Facultad de
Ingeniería en Alimento y Biotecnología. Departamento de Agronomía, Facultad de
Ciencias Agropecuarias, Universidad Técnica de Ambato.
8
Carrera de
Ingeniería Ambiental de la Facultad de Ciencias Naturales y de la Agricultura. Universidad
Estatal del Sur de Manabí.
* Correspondence: [email protected]
Available
from: http://dx.doi.org/10.21931/RB/2023.08.03.48
ABSTRACT
Soil-borne diseases affect potatoes and
cause severe damage to tubers. Several Fusarium species have been associated as
causal agents of potato dry rot. This research focused on characterizing fungal
species causing dry rot in potato mini tubers produced using biotechnological
approaches. Minitubers with typical symptoms of tuber dry rot were selected
from freeze store chambers at Instituto de Biotecnología de las Plantas and
processed in the applied microbiology laboratory. Potato Dextrose Agar (PDA,
Fluka) with components reduced by 50% was used for fungal isolation, and
Spezieller Nährstoffarmer Agar (SNA) was used for morphological
characterization. Ten isolates were obtained from potato mini tubers. Mycelia
growth was speedy in the culture media used, and CCIBP-Fp-1 had the greatest
growth velocity. Cottony colonies were observed in isolates CCIBP-Fp-1, CCIBP-Fp-6,
CCIBP-Fp-7 and CCIBP-Fp-9; felty texture was common in isolates CCIBP-Fp-2,
CCIBP-Fp-3, CCIBP-Fp-4 and CCIBP-Fp-8, while subfelty texture was seen in
isolates CCIBP-Fp-5 and CCIBP-Fp-10. CCIBP-Fp-2 and CCIBP-Fp-4 isolates showed
characteristics similar to Fusarium solani, while CCIBP-Fp-3, CCIBP-Fp-5,
CCIBP-Fp-6, CCIBP-Fp-7, CCIBP-Fp-8, CCIBP-Fp-9 and CCIBP-Fp-10 corresponded
with Fusarium oxysporum. With the results of this work, potato tuber
seeds may be protected with better conservation procedures and improve the
health of Cuban Potato seeds produced by biotechnological approaches.
Keywords:
biotechnology;
fungi; post-harvest; Solanum tuberosum
INTRODUCTION
Potato
(Solanum tuberosum L.) is the fourth main food crop in the world after
maize, rice and wheat1. Evidence suggests that this crop was
domesticated 10,000 years ago close to Titicaca Lake (between Bolivia and
Peru), where the most incredible diversity of wild species is found. Spain 1573
introduced potato in Europe, but only in the early seventeenth century, it
became a critical food2.
Approximately
40 soil-borne diseases affect potatoes Worldwide and cause severe damage to
tubers, the economically most important part of the plant. The occurrence and
development of soil-borne diseases depend on factors affecting the pathogen or
the plant. Favorable conditions for potato disease development are frequently
the same needed for potato growth3. Potato dry rot caused by the
fungal pathogen is an essential disease causing postharvest rotting and loss of
tuber seed quality. Potato seed infected with Fusarium species may
reduce crop sprouting and vigor, affecting crop yield in field plantation4.
Numerous
Fusarium species have been identified
as causal agents of potato dry rot worldwide. Potato dry rot may cause
postharvest severe losses6. In Cuba some Fusarium spp. Pathogens have been identified as causing dry rot of
tubers on imported seed from Canada and Holland (Baraka 57 %, Desirée 50 %,
Atlantic 32.5 %, Chieftain 25 % and Red Pontiac 12.5 %)7.
Dry
rot is regulated by seed certification standards in several potato seed-producing
countries8. Micropropagation using plant biotechnological approaches
may help produce better quality potato seeds and facilitate large-scale
production of disease-free planting material9.
Minitubers
are commonly used like seeds in potato production programs to increase seed
tubers and as planting material in fields 10. Cuban potato seed
production program has incorporated micropropagation methods to improve the health
of tuber seeds and efficiency in propagative systems11. However,
none of the studies has focused on characterizing fungal species causing potato
mini tubers dry rot. This work aimed to identify and characterize Fusarium
species causing dry rot to Cuban Potato mini
tubers produced using biotechnological approaches.
MATERIALS
AND METHODS
Sampling sites.
Based
on the occurrence of dry rot associated with seed potato (mini tubers),
affected mini tubers (Romano variety) from store chambers at Instituto de Biotecnología
de las plantas (Cuba) were selected. Minitubers were produced using
biotechnological approaches and preserved at long-term (6-8 months)
conservation conditions (5-8 ºC). Selected mini tubers with typical symptoms of
dry rot were further processed in the applied microbiology laboratory.
Cultivation and isolation of fungi
Potato
Dextrose Agar (PDA, Fluka) with components reduced by 50% was used for fungal
isolation to prevent saprophytic fungi and bacteria growth and facilitate
recovery of the Fusarium species. Spezieller Nährstoffarmer Agar (SNA)
medium composed of glucose, 0.2 g; MgSO4.7H2O, 0.5 g;
KCl, 0.5 g; KNO3, 1 g; KH2PO4, 1 g; Agar, 20
g; water, 1 L and pH was adjusted to pH 5.612. Media were sterilized
using an autoclave (model Sakura) at 121°C for 15. SNA culture media was used
to stimulate macroconidia and microconidia formation.
Streptomycin
stock solution was prepared by adding 5 g in 100 mL distilled and sterilized
using sterile disposable filters (0.22 µm pore size), then 10 µL of suspension
was used. The antibiotic solution was added before the medium was poured into
Petri dishes (70 mm diameter).
Potato
mini tubers from the Romano variety with dry rot symptomatology were washed
under running tap water for 20 min and air dried in a laminar flow cabin (Model
FASTER Bio 60). They were disinfected in 2 % (v/v) hypochlorite solution for 15
s and rinsed thrice in sterile distilled water. Minituber was placed in a wet
chamber at 25°C for 7 days in the dark.
Mycelial
growth from mini tuber was transferred using a metallic scalpel to Petri dishes
containing 25 mL of PDA media. After 5 days of incubation at 25ºC temperature,
fungal colonies using stereoscopic microscopy (Carl Zeiss, Stemi
100 model) were identified by microscopic observations and purified at least
twice by serial transfers to PDA Petri dishes.
From
purified colonies, 5 mycelia discs were introduced in Eppendorf tubes of 1.5 mL
containing sterile glycerol solution at 25%(v/v). Ten tubes per fungal isolate
were preserved at – 80 °C.
Cultural characterization
One
disc from Eppendorf tubes, preserved at 4ºC, was used to inoculate Petri dishes
(70 mm in diameter) containing 10 mL of PDA. Inoculated plates were incubated
at 28 ºC in the dark for 10 days.
Growth
velocity, the color of colonies, the color of the reverse of colonies, texture,
presence of transpired liquid, and pigmentation of culture medium were
evaluated as cultural characteristics.
Morphological characterization
The
Spezieller Nährstoffarmer Agar (SNA) medium was poured into Petri dishes of 50
mm (diameter). Pieces of sterile filter paper (Whatman No. 1) of approximately
1 cm² were placed on the agar surface of each Petri dish to stimulate
sporulation. Mycelia discs of 4 mm were placed in contact with sterile filter
papers for each isolate and incubated for 10 days at 28ºC in dark conditions.
Microcultures
for each isolate were mounted to facilitate sporulation and improve
visualization of conidial morphology according to the method proposed by Riddel
(1950)12. Characteristics of hyphae, microconidia, macroconidia, and
chlamydospores were observed under a clinical microscope (model Olympus) with
400× magnification, and pictures were captured by a digital camera (Model CANON
A-630).
Statistical analysis
Statistical
analyses were performed using SPSS (Statistical Package for the Social Sciences
Version 18.0) software (SPSS Inc., Chicago, IL, USA). The normal distribution
was determined using the Shapiro-Wilk test, and variance homogeneity was
determined using the Levene test. A nonparametric test of Kruskall-Wallis was
used for variables without normal distribution or variance homogeneity.
RESULTS
Isolation and cultural
Characterization
Ten
isolates were obtained from potato mini tubers (Romano variety) with dry rot
symptomatology. The cultural characteristics of isolates were similar to those
of Fusarium genera. According to the characterization of all isolates,
mycelia growth was speedy in the culture media used, and CCIBP-Fp-1 had the
most incredible growth velocity (16 mm day-1, significant at p <
0.05). Potato dextrose agar (PDA) effectively isolated fungi without
saprophytic fungi and bacterial growth.
Textures
were different among isolates. Cottony colonies were observed in CCIBP-Fp-1,
CCIBP-Fp-6, CCIBP-Fp-7, and CCIBP-Fp-9 isolates. The mat's texture was erect,
with mycelium spreading in all directions. Felty texture with a mat composed of
cottony or woolly mycelium forming a surface like felt was common in isolates
CCIBP-Fp-2, CCIBP-Fp-3, CCIBP-Fp-4, and CCIBP-Fp-8, while poor aerial mycelium
attached to agar surface contributing to subtlety texture was seen in isolates
CCIBP-Fp-5 and CCIBP-Fp-10. The color of colonies' surfaces (white, pink,
purple, orange, and violet) and reverses (white, yellow, purple, red, and
violet) differed among isolates. Transpired liquid was observed only in
CCIBP-Fp-1, CCIBP-Fp-6, and CCIBP-Fp-8 colonies. All isolates showed hyphal
tissue with intricate texture types.
Morphological characterization
Morphological
characteristics of asexual reproductive structure (macroconidia and microconidia),
conidiophores, and chlamydospores,
matched with Fusarium, excepting the isolate CCIBP-Fp-1. CCIBP-Fp-2 and CCIBP-Fp-4 showed
characteristics similar to Fusarium
solani, while CCIBP-Fp-3, CCIBP-Fp-5, CCIBP-Fp-6, CCIBP-Fp-7, CCIBP-Fp-8,
CCIBP-Fp-9 and CCIBP-Fp-10 corresponded with Fusarium oxysporum.
SNA
culture media was suitable to promote macroconidia and microconidia development
in analyzed isolates. F. solani
isolates showed macroconidia rounded in the basal cell, blunt and rounded in
the apical cell, 0 to 3 septa, and 23.4-66.3 µm long. Abundant microconidia
were observed in aerial mycelial, single-celled, 1–2 septa, and oval to
kidney-shaped, associated in chain with 7.8-19.5 µm long. Conidiophores were
short and long monophialides with apical spore mass. Chlamydospores were globose,
lonely or forming pairs (Figure 1).

Figure 1. Morphological
characteristics of Fusarium solani
isolates. Presence of macroconidia and microconidia (A), Short and long
conidiophore (B), Long mono phialides with apical spores mass (C), Short mono
phialides with apical spores mass (D), Chain of microconidia (E),
Chlamydospores lonely or forming pairs (F).

Figure
2. Morphological
characteristic of Fusarium oxysporum. A- Macroconidia
slightly curved. B- Microconidia in false heads at aerial mycelial. C- microsclerotia.
D- Chlamydospores globose and lonely.
F.
oxysporum
showed macroconidia slightly curved, thin-walled, foot-shaped basal cell,
curved apical cell, 0 to 5 septate, and 23.4-62.4 µm long. Abundant
microconidia were observed in aerial mycelial with false heads, oval to
kidney-shaped or elliptic, 0-4 septa, and 3.9-19.5 µm long. Few microsclerotia
were observed. Conidiophores were short monophialides, hyaline, and simple with
apical spores mass. Chlamydospores were globose and lonely.
DISCUSSION
Until
now, no authors have reported fungal pathogens associated with potato seed mini
tubers produced by biotechnological approaches, but fungi causing tuber dry rot
have been very well documented in common potato tubers. A similar method for
isolating Fusarium species associated
with tuber dry rot was used to determine the diversity of Fusarium spp.,
affecting potato tubers in Upper Egypt13.
García-Bayona
(2011) described the macroscopic and microscopic morphology of two strains of F. oxysporum causing potato dry rot in Solanum
tuberosum in Colombia14 and observed similar characteristics
with some of the obtained isolates from mini tubers. 2006 Leslie and Summerell
suggested that PDA is unsuitable for Fusarium isolation. However,
Peptone-PCNB Agar, Carnation Leaf-piece Agar, and SNA were the most effective
mediums for the recovery of Fusarium
species; nevertheless, in our study, PDA components were reduced at 50%.
Cultural
characteristics observed in fungal isolates associated with potato mini tubers
Dry Rot were similar to those described by Tiwari et al. (2021)15. The
results presented in this paper were identical to some cultural features defined
by this group.
Anand
et al. (2018) described variability in cultural characteristics of F.
oxysporum sp. chrysanthemi causing wilt to chrysanthemum plants in Kovilur
village of Madurai, Tamil Nadu in India16. They detected significant
differences among isolates concerning mycelia growth velocity in semisolid
media and differences in mycelial dry weight using liquid culture media. Our
results showed that cultural characteristics were variable among isolates of F.
oxysporum. Similarly, Tiwari et al. (2020) have also found significant
variability in cultural factors (color of surface colonies, texture and
pigmentation) of colonies of F. solani,
causing potato dry rot disease17.
On
the contrary, our results showed that cultural characteristics were similar
among isolates of F. solani. In Fusarium genera, it is common to observe
significant differences in cultural traits among isolates of different species
and from the same species as well18. Several cultural
characteristics of Fusarium isolates
(growth velocity, abundance of aerial mycelia, pigment diffusion in agar,
dimensions of conidia19.
The
preserved isolates of F. solani and F. oxysporum could be used as
referenced strains in culture collection with fungal pathogens associated with
Potato Dry Rot of mini tubers. According to morphological characteristics
observed among fungal isolates, F.
oxysporum and F. solani were the morphospecies associated with
Potato Dry Rot of mini tubers. Other authors recorded similar morphology
(dimension of macroconidia, microconidia, chlamydospores and conidiophores) in
Fusarium strains from various substrates and geographic areas 20.
Similarly,
Yli-Mattila et al. (2004) determined differences in morphological
characteristics among Fusarium species (F. avenaceum, F. arthrosporioides,
F. sporotrichioides, F. culmorum, F. arthrosporioides, F. culmorum, F.
sporotrichioides and F. graminearum) and they observed correspondence
with molecular identification21. Many Fusarium species have
been associated with potato tubers dry rot (F. sulphureum22; F.
solani var. coeruleum23; F. oxysporum24
and F. avenaceum25 Fr Sacc. Cullen et al. (2005) considered
that the number of Fusarium species associated with this fungal disease
may exceed 13, and they are worldwide distributed26. Contrary to
these results, only two species of Fusarium
were identified in the present study.
F.
oxysporum
has a cosmopolitan distribution, inhabiting soil fungus, causing vascular wilt,
damping off, and rot on crops with economic importance27. Approximately
41 years ago, Correll (1991) reported that F.
oxysporum has a high level of host specificity with over 120 described
formae species and races that may cause vascular wilt diseases28.
Some
morphological characteristics of F.
oxysporum, including the production of microconidia in false heads and short
phialides, the presence of chlamydospores, and the shape of macroconidia and
microconidia were defined by Leslie and Summerel (2008)29. These
authors argued that F. oxysporum is similar to F. solani and F.
subglutinans, but F. solani is distinguishable from F. oxysporum
because the first form of microconidia in false heads and very long phialides
inserted into hyphae. F. subglutinans is only distinct from F.
oxysporum because of its microconidia form in poliphialides and the absence
of chlamydospores.
On
the other hand, F. solani is one of the most common species causing
potato dry rot worldwide. It is associated with soil, causing wilt, root rot,
basal rot, and canker in the stem. It is frequently associated with damages, as
opportunistic or attacking weaken hosts30. Furthermore, F. solani is a soil inhabitant in
tropical forests with high humidity. A wide range of plants of economic
interest is attacked by this fungal species (potato, avocado, beans, citric,
cocoyam, cowpea, orchid, passion fruit, pea, and pepper)31.
Pathogenicity
and virulence of F. solani-causing
plant diseases may be explained by cutinase activity, modes of spore attachment,
and penetration of the host's surface. Taxonomy and classification of F. solani is complex because this
species has approximately 15 formae speciales, closely associated with
different crops32. In Cuba, F. solani has been reported in
Cuba33 but not in potato mini tubers.
Therefore,
this work made a valuable characterization of Fusarium species causing
dry rot of Cuban microtubes and may facilitate better conservation procedures
and health of Cuban Potato seeds produced by biotechnological approaches.
CONCLUSIONS
The
present study concluded that 10 isolates from Fusarium were recovered from potato mini tubers. F. solani
and F. oxysporum were the species causing dry rot of potato mini tubers.
Better conservation procedures may be developed to improve the health of Cuban
Potato seeds produced by biotechnological approaches.
Contribuciones de los autores: Conceptualización, Michel Leiva Mora, Metodología,
Michel Leiva Mora y Mayra Acosta Suárez,
Software, Michel Leiva Mora y Mayrebi Herrera-Capote, Validación, Michel Leiva Mora y Mayra Acosta Suárez,
Análisis formal, Michel Leiva Mora, Mayra Acosta Suárez ; Investigación,
Catherine Silva Agurto y Natalys Solis; Recursos, Michel Leiva Mora, Catherine Silva Agurto, Walter Oswaldo Veloz Naranjo, Curado de datos, Michel Leiva Mora y Rodrigo Núñez; Redacción Mayrebi Herrera-Capote redacción borrador original y la corrección realizada
por Michel Leiva Mora, Revisión y edición, Michel Leiva Mora, Miguel y Angel Osejos Merino;
supervisión, Catherine Silva Agurto; administración del proyecto, Michel Leiva
Mora, adquisición del financiamiento, Michel Leiva Mora y Catherine Silva
Agurto; Todos los autores han leído y están de acuerdo con la versión publicada
del manuscrito.
Agradecimientos: Agradecemos al apoyo ofrecido por la
coordinadora de investigación Deysi Alexandra Guevara Freire y a las
autoridades de la Facultad de Ciencias Agropecuarias de la Universidad Técnica
de Ambato, así como a la Dirección de Investigación y Desarrollo (DIDE-FCAGP-UTA)
por reconocer y brindar el apoyo a los esfuerzos realizados. Parte de este
proyecto fue realizado en el Instituto de Biotecnología de las plantas,
Universidad Central Marta Abreu de las Villas, Villa Clara, Cuba
y la otra parte fue desarrollada en la Facultad de Ciencias Agropecuarias de la
Universidad Técnica de Ambato.
Conflictos de interés:
“Los autores declaran no tener conflicto de interés”..
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Received: 25 June 2023/ Accepted: 26 August 2023 /
Published:15 September 2023
Citation: Leiva-Mora M,
Herrera-Capote M, Acosta-Suárez M, Silva Agurto C L, Solis N, Veloz Naranjo W
O, Núñez R; Osejos Merino A. Characterization of Fusarium species causing dry rot of
potato mini tubers produced by biotechnological approaches. Revis
Bionatura 2023;8 (3) 48. http://dx.doi.org/10.21931/RB/2023.08.03.48