© The Authors, 2025, Published by the Universidad del Zulia*Corresponding author: wceiroc@gmail.com
Keywords:
Distribution
Disease
Fungi
Intensity
Pathogenicity of Fusarium oxysporum f. sp. nicotinae and F. phyllophilum in tobacco in the
Granma region, Cuba
Patogenicidad de Fusarium oxysporum f. sp. nicotinae y F. phyllophilum en tabaco en la región de
Granma, Cuba
Patogenicidade de Fusarium oxysporum f. sp. nicotinae e F. phyllophilum no tabaco na região de
Granma, Cuba
Ramon Jaime Holguín-Peña
1
Daniel Ruiz-Juárez
2
Mónica Gutiérrez-Rojas
2
Wilson Geobel Ceiro-Catasú
3*
Rev. Fac. Agron. (LUZ). 2025, 42(2): e254226
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v42.n2.X.
Crop production
Associate editor: Dra. Lilia Urdaneta
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
1
Centro de Investigaciones Biológicas del Noroeste
(CIBNOR S.C), Programa de Agricultura en Zonas Áridas.
Km. 1, Carretera a San Juan de La Costa, El Comitán, 23205,
La Paz, B.C.S, México.
2
Departamento de Producción Agrícola y Animal-
Universidad Autónoma Metropolitana-Unidad Xochimilco.
Calzada del Hueso 1100, Coyoacán CP. 04960, Ciudad de
México, México.
3
Estancia Posdoctoral por México, SECIHTI. Centro de
Investigaciones Biológicas del Noroeste (CIBNOR S.C),
Programa de Agricultura en Zonas Áridas. Km. 1, Carretera
a San Juan de La Costa, El Comitán, 23205, La Paz, B.C.S,
México.
Received: 27-02-2025
Accepted: 20-04-2025
Published: 28-05-2025
Abstract
Diseases caused by Fusarium spp. are considered cosmopolitan
and aect a great diversity of crops worldwide. In the tobacco-
growing areas of Granma province, located in eastern Cuba, these
phytopathological problems cause signicant losses in tobacco leaf
yield and quality. To address this critical issue, a comprehensive
study was conducted, focusing on disease monitoring and the
identication of tobacco seeds and seedlings (cv. Corojo 2012)
aected by the diseases. The study also examined the variables
associated with the severity of the diseases. The results of the study
indicated that the vascular wilt was caused by two distinct fungal
pathogens: F. oxysporum f. sp. nicotinae and F. phyllophilum. The
study revealed that the disease exhibited levels of recurrence in both
space and time, reaching up to 62 % necrosis in seedlings with no
chance of survival. This disease severity, measured on a maximum
scale of ve, attained a maximum score of 4.20. The ndings
indicated a substantial inhibition in the germination and growth
variables of Nicotiana tabacum, which has a profound impact on
the yield and commercial quality of N. tabacum leaves, particularly
those intended for the Cuban cigar manufacturing industry. This
underscores the necessity for expeditious diagnosis of the disease
and the implementation of appropriate management strategies to
mitigate the risks of its propagation in producing regions of Cuba
and globally.
This scientic 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): e254226 April-June. ISSN 2477-9409.
2-6 |
Resumen
Las enfermedades causadas por Fusarium spp. son consideradas
cosmopolitas y afectan a una gran diversidad de cultivos en todo el
mundo. En las zonas tabacaleras de la provincia de Granma, ubicada
en el oriente de Cuba, estos problemas topatológicos provocan
pérdidas signicativas en el rendimiento y la calidad de la hoja de
tabaco. Por este motivo, se realizó un estudio basado en el monitoreo
de la enfermedad, en el cual se determinaron las afectaciones en las
semillas y plántulas de tabaco cv. Corojo 2012, así como las variables
asociadas a la severidad de la enfermedad. Los resultados mostraron
que el marchitamiento vascular fue causado por F. oxysporum f.
sp. nicotinae y F. phyllophilum. Se encontró una recurrencia de la
enfermedad en el espacio y el tiempo, con niveles máximos de un 62
% de necrosamiento en plántulas sin posibilidades de supervivencia,
además de una severidad de la enfermedad de 4,20 en una escala
máxima de cinco. Esto provocó una inhibición signicativa en las
variables de germinación y crecimiento de Nicotiana tabacum. Lo
anterior posee incidencia en el rendimiento y calidad comercial de
las hojas de N. tabacum, especialmente si se destinan a la industria de
fabricación de puros cubanos. Esto pone de maniesto la necesidad
de realizar diagnósticos tempranos de la enfermedad y aplicar las
alternativas de manejo correspondientes para minimizar los riesgos
de diseminación en regiones productoras de Cuba y el mundo.
Palabras clave: distribución, enfermedad, hongos, intensidad.
Resumo
As doenças causadas por Fusarium spp. são cosmopolitas e
afectam uma grande diversidade de culturas em todo o mundo.
Nas zonas de cultivo de tabaco da província de Granma, localizada
no leste de Cuba, estes problemas topatológicos causam perdas
signicativas no rendimento e na qualidade das folhas de tabaco. Por
este motivo, foi realizado um estudo baseado na monitorização da
doença, no qual se determinaram as afectações nas sementes e nas
plântulas da variedade de tabaco Corojo 2012, bem como as variáveis
associadas à severidade da doença. Os resultados mostraram que a
murcha vascular foi causada por F. oxysporum f. sp. nicotinae e F.
phyllophilum. Foi observada uma recorrência da doença no espaço e
no tempo, com níveis máximos de 62 % de necrose em plântulas sem
hipótese de sobrevivência, e uma severidade da doença de 4,20 numa
escala máxima de cinco. Este facto provocou uma inibição signicativa
da germinação e das variáveis de crescimento da Nicotiana tabacum.
Isto tem um impacto no rendimento e na qualidade comercial das
folhas de N. tabacum, especialmente se forem destinadas à indústria
cubana de fabrico de charutos. Este facto evidencia a necessidade de
um diagnóstico precoce da doença e a aplicação das alternativas de
gestão correspondentes para minimizar os riscos de disseminação nas
regiões produtoras de Cuba e do resto do mundo.
Palavras chave: distribuição, doença, fungos, intensidade.
Introduction
Tobacco (Nicotiana tabacum L.) is one of the most commercially
valuable solanaceae and the most widely cultivated non-edible
agricultural product in the world, with a major impact on the culture,
society and economy of tropical and subtropical countries. Its leaves,
rich in organic compounds, are the basis of the tobacco industry for
the production of cigarettes and cigars. Originally from the Andean
region, its cultivation has spread to more than 125 countries thanks
to its high adaptability to dierent agricultural ecosystems (Sosa-
Sánchez et al., 2022; Gui et al., 2024).
Cuba is renowned for the production and export of dark tobacco,
with growing demand in markets such as China, Spain and Germany.
In 2022, exports of tobacco products reached US$ 275 million,
representing more than 20 % of the national total. However, key
tobacco-growing regions have experienced a 62 % drop in yields,
attributed to lack of agricultural inputs, adverse weather conditions
and fungal diseases (National Oce of Statistics and Information
[ONEI], 2022; Observatory of Economic Complexity [OEC], 2024).
In this context, several dark tobacco varieties have been studied
with tolerance to infections of the fungi causing blue mould
(Peronospora hyocyami de Bary), tobacco blight (Phytophthora
parasitica Dast. var. Nicotianae Breda de Haan) and Fusarium
(Ha-Thanh et al., 2022). Specically, F. oxysporum, F. solani and
F. phyllophylum are the most recurrent soil species associated with
solanaceae and with the greatest impact on tobacco since, in addition
to causing the collapse of xylem vessels causing wilting, they also
aect the leaf of N. tabacum with the appearance of leaf spots and
eventual necrosis (Sosa-Sánchez et al., 2022; González et al., 2023).
Fusarium oxysporum is considered a complex of cryptic species,
whose phylogenetic complexity makes species identication dicult
(Ribeiro et al., 2022).
Specically, vascular wilt in Nicotiana tabacum is caused by
Fusarium f. sp. nicotianae, batatas and vasinfectum. Necrosis-
producing variants complicate agronomic management by aecting
leaves, which are key to premium cigar production. In addition,
some variants can remain dormant in the soil in the form of
chlamydospores, facilitating their spread on various hosts (Nikitin
et al., 2023). However, for Fusarium infection to occur, processes
such as degradation of host barriers, early signalling and interaction
of key metabolites and molecules, including enzymes, toxins and
membrane transporters, must be activated (Laraba et al., 2022). This
suggests that some dark tobacco varieties in Cuba may be susceptible
to Fusarium f. sp. associated with wilt.
Moreover, the symptoms are not only limited to the vascular
bundles, but also aect leaf quality, precisely one of the most
recognised characteristics of export tobacco (Sosa-Sánchez et al.,
2022). In view of the above, this research was conducted to determine
the phytopathogenicity of native isolates of Fusarium oxysporum and
F. phyllophylum on N. tabacum.
Materials and methods
Isolation of Fusarium spp.
Samples of roots, stems and leaves with Fusarium symptoms were
collected from commercial tobacco crops in Granma, Cuba, specically in
Bueycito (20°14’20. 5‘’N, 76°46’28.8‘’W), El Dorado (20°15’52.3‘’N,
76°44’43.8‘’W), Monjará (20°17’51.9‘’N, 76°36’08.7‘’W) and Los
Cayos (20°18’20.2‘’N, 76°50’00.6‘’W). Symptoms observed included
stunted growth, yellowing, leaf necrosis, vertical drying of leaves,
browning of vascular tissues and chlorosis at the top of the plant (Gilardi
et al., 2021). In addition, disease recurrence was recorded in two
consecutive periods in 2019 and 2020. The isolation and morphological
characterisation of the fungi was performed according to Sosa-Sánchez
et al. (2022) and they were deposited in collections of the Universidad
de Granma, Cuba, and the Centro de Investigaciones Biológicas del
Noroeste (CIBNOR S. C., Mexico).
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Holguín et al. Rev. Fac. Agron. (LUZ). 2025, 42(2): e254226
3-6 |
Primer-specic identication
DNA was amplied with the molecular marker for elongation factor
1α and primers EF1 [5‘-ATGGGTAAGGA(A/G)GACAAGAC-3’]
and EF2[5‘-GGA(G/A)GTACCAGT(G/C)ATCATGTT-3’] were
used to dierentiate Fusarium species (Nitschke et al., 2009; Retana
et al., 2018). The procedure was performed at the Laboratory of
Phytopathology, CIBNOR, La Paz, B.C.S., Mexico. DNA sequence
comparisons with the GenBank
®
database (https://www.ncbi.nlm.nih.
gov/genbank/) were used to determine species identity.
Seed and seedling conditioning
Seeds of the cultivar Corojo 2012 from the Unidad Empresarial
de Base (UEB) de Acopio y Benecio de Tabaco en Horno de Guisa,
Bayamo, Cuba, with a germination power ≥85 % were used. The
seeds, disinfected with 1 % sodium hypochlorite for 2 minutes, were
sown in 3 L pots with a substrate of soil and organic sheep manure
(3:1 v/v), sterilised at 150 ºC for 3 hours and rested for 12 hours
before use. Management conditions followed the recommendations
for cultivation (Espino et al., 2012).
Experimental inoculation of seeds and seedlings
At the Microbiology Laboratory of the Facultad de Ciencias
Agrícolas, Universidad de Granma, Cuba, 25 previously disinfected
seeds were placed in Petri dishes with sterilised lter paper. 600 µL
of a spore suspension (0.74.10
6
macroconidia.mL
-1
) of Fusarium spp.
(isolates FO-B, FO-D, FP-E and FP-F) were added and the plates
were incubated at 28 ± 2 °C, adjusting the humidity daily (≥85
%). After 7 days, Fusarium spp. colonies were counted and after
10 days the percentage of seed germination was assessed. After 28
days, whole seedling length (LP) and fresh mass per seedling (MFP)
were measured to calculate the percentage of inhibition in the early
developmental stages.
For inoculation, 10 homogeneous seedlings with the rst four
true leaves were used, a 1 cm cut was made at the apex of the main
root. They were then immersed in a suspension with macroconidia
(0.74.10
6
macroconidia.mL
-1
) of the isolates for three hours. Control
seedlings were immersed in sterile distilled water for the same time.
After this process, they were transplanted into 250 mL plastic jars
with sterilised substrate and watered every other day.
At 17 days post inoculation (dpi) disease intensity was measured
using the formula of Townsend and Heuberger (1943), I (%) = [(∑ a
x b) / N x K] x 100, where: a = number of plants or organs aected,
b = grade of the scale, K = last grade of the scale used, N = total
number of plants. Damage was recorded according to a scale of 0-5
degrees (table 1) and necrotic seedlings with no chance of survival
were counted.
Experimental design and statistical processing
A completely randomised design with four treatments, a control
without pathogen inoculation and 10 replicates was used for both
trials. Percentage data were transformed prior to ANOVA using RAIZ
2
(x+1). A one-way ANOVA was performed and, when signicant
dierences were found, Tukey’s multiple comparison of means test
(p≤0.05) was applied using InfoStat 2008 software (Balzarini et al.,
2008).
Results and discussion
Distribution of F. oxysporum f. sp. nicotianae and F.
phyllophylum in the tobacco-growing areas of Granma Province,
Cuba
In the monitored areas, the genus Fusarium was found to be
associated with vascular wilt. The species F. oxysporum f. sp.
nicotinae occurred in Bueycito and El Dorado, while F. phyllophylum
was found in Monjará and Los Cayos. Except for isolate FP-F (F.
phyllophilum), which was not observed in the second monitoring
cycle, the other isolates were recurrent in each locality. Molecular
tests with specic primers conrmed the identity of the species.
Fusarium recurrence is common and key to yield and quality losses
(Kema et al., 2021).
The morphological characteristics of the isolates coincided with
reference strains from the Microbiology Laboratory of the Universidad
de Granma (Sosa-Sánchez et al., 2022). Field symptoms included
wilting, stunting, yellowing, leaf and stem necrosis, interveinal
chlorosis and browning of vascular tissue caused by F. oxysporum
f. sp. nicotianae and F. phyllophylum (Pandey, 2023). Both species
were associated with vascular wilt of tobacco in Granma province
(table 2).
Native strains of F. oxysporum f. sp. nicotianae and F. phyllophilum
may be related to others that share alternate hosts (tomato, vanilla,
orchids). Recent studies suggest the possibility of forming lineages
within the same species (Luna-Rodriguez et al., 2023). Vascular wilt
disease is complex and multifactorial, with several species, variants
and virulence factors interacting. F. oxysporum is considered a key
pathogen because of its ecient seed and soil-borne transmission
(Hudson et al., 2021).
Table 1. Damage scale from 0-5 to determine the severity of the disease in the dierent organs of the seedlings of Nicotiana tabacum cv.
Corojo 2012.
Scale
1
Síntomas
2
Root Stem Leaves
0
Healthy plant Healthy plant Healthy plant
1
Slight root rot (< 10 %) 1-5 % vascular necrosis Yellowing of basal leaves
2
Dark lesions on 25 % of the roots 5-15 % necrosis in vascular tissue
Yellowing of basal leaves and wilting of one or
two leaves
3
50 % of the infected root. Severe necrosis on the
main root
15-35 % necrosis in the vascular tissue.
Severe yellowing of leaves. 50 % of leaves
wilted and growth inhibited.
4
75 % of the infected root. Crown lesions and
wilting of old leaves.
35-67.5 % necrosis in the vascular tissue.
Widespread yellowing, vascular and root
necrosis
5
100 % of the infected root. Wilt and death of
basal leaves
67.5-100 % necrosis in vascular tissue Necrotic plant
1
Scale.
2
Raíz (Cakir et al., 2014), stem (Akhter et al., 2015), leaves (Rongai et al., 2017).
This scientic 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): e254226 April-June. ISSN 2477-9409.
4-6 |
Table 2. Causal agent associated with vascular wilt and its spatio-temporal distribution in the tobacco growing region of Granma, Cuba.
Isolates Key Locality/Variety Targeted detection
1
Recurrence
2
(I cicle/II cicle)
F. oxysporum f. sp. nicotinae FO-B Bueycito/Habana 2000 + +/+
F. oxysporum f. sp. nicotinae FO-D El Dorado/Habana 92 + +/+
F. phyllophilum FP-E Monjará/Corojo 2012 + +/+
F. phyllophilum FP-F Los Cayos/Habana 2000 + +/-
1
Specic detection for F. oxysporum y F. phyllophilum (Retana et al., 2018).
2
Recurrence in the eld per cycle, (+) positive to the appearance of disease-associated symptoms under eld conditions.
(-) without apparent symptoms, monitoring performed in 2019 (I cycle) and 2020 (II cycle).
Eect of F. oxysporum f. sp. nicotianae and F. phyllophylum on
seed germination and early seedling development of N. tabacum
cv. Corojo 2012
Seed germination inhibition of tobacco cv. Corojo 2012 was
observed with both Fusarium species, being F. phyllophylum
FP-E the one that most aected this process (51.10 %). The other
isolates showed values between 29.31 % and 33.11 %. The highest
proliferation was recorded in isolates FP-E (5.25) and FP-F (3.25)
compared to FON-B (2.25) and FON-D (2.75). The most signicant
(Tukey, p≤0.05) reduction in seedling mass and length was caused by
isolates FP-E (56.31 %, 13.00 mm) and FON-B (51.58 %, 12.36 mm),
while FP-F and FON-D reached lower values (table 3).
Table 3. Eect of Fusarium isolates on inhibition of germination,
fresh mass and seedling length of Nicotiana tabacum cv.
Corojo 2012.
Isolates
1
Eect on seeds
2
Fresh mass
reduction
3
Length reduction
4
G (%) NC (%) (%)
FON-B 33.11
b
2.25
b
51.58
a
12.36
a
FON-D 31.02
b
2.75
b
33.34
b
10.56
b
FP-E 51.10
a
5.25
a
56.31
a
13.00
a
FP-F 29.31
b
3,25
ab
39.40
b
10.91
b
Control 0 0 0 0
CV
*
5.70 6.96 11.10 8.75
1
Fusarium isolates from the tobacco-growing region of Granma; F. oxysporum f. sp. nicotinae
(FO-B), F. oxysporum f. sp. nicotinae (FO-D), F. phyllophilum (FP-E), F. phyllophilum (FP-
F).
2
G = percentage of germination inhibition by the eect of the isolates of Fusarium spp.
NC = Number of colonies (n=10).
3
Reduction of fresh mass due to the eect of the isolates
of Fusarium spp.
4
Reduction of seedling length due to the eect of the isolates of Fusarium
spp. CV: coecient of variation. Dierent letters in the column show signicant dierences
(Tukey, p≤0,05). Percentage values were transformed prior to ANOVA by .
Several studies documented the inhibitory eect of Fusarium
on seed germination. Specically, F. oxysporum f. sp. vasinfectum
breed 4 (FOV4) reduces cotton germination by 5-20 % (Zhu et al.,
2023), while F. circinatum decreases the viability of Pinus greggii
seeds by 43 % (Garcia et al., 2017). In grasses, F. graminearum, F.
avenaceum, F. culmorum and F. poae can inhibit germination by 65.5
% to 92.5 % (Browne and Cooke, 2005). This eect is associated
with secondary metabolites, enzymes and toxins, as evidenced in
Orobanche ramosa, where at least 18 toxins inuenced germination
inhibition at concentrations ≥10 µM (Zonno and Vurro, 2002).
The colony-forming ability may indicate the proliferation
and possible pathogenicity of Fusarium on seed germination.
Autochthonous isolates of Fusarium spp. from tobacco-growing
areas in Granma, Cuba, showed high proliferation and infectivity
at concentrations ≥1.10⁶ macroconidia.mL
-1
(Sosa-Sánchez et al.,
2022). In addition, Fusarium spp. can colonise the seminal embryo
and prevent its germination (Pfenning et al., 2014).
This study conrmed that indigenous isolates of F. oxysporum f.
sp. nicotianae and F. phyllophilum signicantly reduce the fresh mass
of seedlings of N. tabacum cv. Corojo 2012. Previous studies reported
reductions of 86 % to 96 % in Glycine max and Cicer arietinum
due to Fusarium spp. This decrease in growth can be attributed to
damage to roots, stems and leaves, aecting water uptake, nutrients
and photosynthesis (Zhang et al., 2021). Hu et al. (2023) reported
that F. oxysporum f. sp. fabae caused vascular wilt in broad beans
(Vicia faba L.), reducing growth by 6-25 %. Pastuszak et al. (2021)
observed that F. culmorum infection of wheat (Triticum sp.) seedlings
caused a 37 % loss in fresh mass of leaves and roots, as well as a
reduction in chlorophyll a, b and carotenoid levels.
Severity of F. oxysporum f. sp. nicotianae and F. phyllophylum
on N. tabacum cv. Corojo 2012
Root and leaf organs were more severely aected than the stem.
Isolates FP-E and FON-B showed a higher disease severity on roots
and leaves compared to FON-D and FP-F. In the stem, there were no
signicant dierences between isolates. FP-E and FON-B also showed
higher disease intensity and necrosis in plants compared to FON-D and
FP-F, according to Tukey’s test (p≤0.05) (table 4, gure 1).
Isolates FP-E (F. phyllophilum) and FO-B (F. oxysporum f. sp.
nicotinae) showed higher virulence on the organs of N. tabacum cv.
Corojo 2012, with clear symptoms of vascular wilting, chlorosis and
necrosis in roots, stems and leaves 17 days after inoculation (dpi).
These damages aect yield and marketable leaf quality, underlining
the need for early diagnosis and management measures in the eld
(Qiu et al., 2023).
Results showed that inoculation of Fusarium by wounding the
root system of seedlings was ecient in expressing disease symptoms.
Retana et al. (2018) showed that F. oxysporum on Apium graveolens
reached maximum disease expression at 35 days post inoculation
(dpi). The pathogenicity of Fusarium spp. varies, with symptoms
appearing as early as 5 days and reaching maximum expression at 17
dpi, causing up to 17 % plant mortality (Shen et al., 2023).
Espinoza-Ahumada et al. (2019) observed a severity of Fusarium
spp. on melon cv. Top Mark with a damage gradology between 4 and
5 in seven days. Berruezo et al. (2021) noted severe F. oxysporum and
F. solani damage on Virginia type tobacco in northwestern Argentina,
attributable to pathogen virulence, inoculum concentration and variety
tolerance. Carmona et al. (2020) recorded a maximum infection
intensity of 94.5 % in tomato seedlings cv. Santa Cruz Kada at 30
days, slightly higher than the present investigation.
The highest averages of necrotic plants with no chance of survival
were observed for F. phyllophilum (FP-E) and F. oxysporum f. sp.
nicotinae (FO-B) at 12 days post inoculation (dpi). Khademi et al.
(2020) found that both transgenic and natural seedlings of
N. tabacum
showed wilt, chlorosis and necrosis symptoms within seven days after
inoculation with F. solani and F. oxysporum, with severe wilting and
death in less than three weeks.
(
+ 1)
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Holguín et al. Rev. Fac. Agron. (LUZ). 2025, 42(2): e254226
5-6 |
Table 4. Disease severity caused by Fusarium oxysporum f. sp. nicotinae and Fusarium phyllophilum on root, stem and leaf organs of N.
tabacum cv. Corojo 2012.
Isolates
Root Stem Leaves I
3
Necrotic plants
4
DS
1
± SD DS ± SD
2
DS ± SD (%) (%)
FON-B 4.17 ± 1.69 a 3.50 ± 1.72 b 4.31 ± 1.10 a 89.72 a 58.0 a
FON-D 3.40 ± 1.90 b 3.30 ± 1.83 b 3.70 ± 1.25 b 71.11 b 41.5 b
FP-E 4.26 ± 1.45 a 3.95 ± 1.45 b 4.40 ± 0.97 a 91.10 a 62.0 a
FP-F 3.80 ± 1.69 b 3.60 ± 1.90 b 3.80 ± 1.32 b 73.05 b 37.5 b
Control 0 0 0 0 0
1
DS: damage scale, maximum value of 5.
2
SD: Standard deviation.
3
I. Disease intensity was determined using the Townsend and Heuberger formula. (1943), I (%) = [(∑ a x b) / N x K] x 100, where:
a = number of plants or organs aected, b = scale grade, K = last scale grade used, N = total plants. Dierent letters in the columns indicate signicant dierences (Tukey, p≤0.05).
4
Percentage of
necrotic seedlings with no chance of survival.
Figure 1. Severity of Fusarium phyllophilum (FP-E) on Nicotiana
tabacum cv. Corojo 17 days after inoculation. A) control without
inoculation, B) wilted and necrotic seedling with no chance of
survival.
Conclusions
The vascular wilt disease caused by F. oxysporum f. sp. nicotinae
and/or F. phyllophilum represents a limiting factor for tobacco
production in Granma, Cuba. It was found a recurrence of 62 % with
seedling necrosis and a severity of 4.20 in a scale of 5 grades, which
aected the germination and seedling development variables. This has
an impact on the yield and commercial quality of leaves, especially
for the manufacture of Cuban cigars, underlining the importance of
early diagnosis to establish management measures to prevent the
spread of the pathogen in producing regions of Cuba and the world.
Literature cited
Akhter, A., Hage, K., Soja, G., & Steinkellner, S. (2015) Compost and biochar alter
mycorrhization, tomato root exudation, and development of Fusarium
oxysporum f. sp. lycopersici. Frontiers in Plant Science, 6(529), 1-13.
https://doi.org/10.3389/fpls.2015.00529
Ankati, S., Srinivas, V., Pratyusha, S., & Gopalakrishnan, S. (2021). Streptomyces
consortia-mediated plant defense against Fusarium wilt and plant growth-
promotion in chickpea. Microbial Pathogenesis, 157, 104961. https://doi.
org/10.1016/j.micpath.2021.104961
Balzarini, M. G., Gonzalez, L., Tablada, M., Casanoves, F., Di Rienzo, J. A., y
Robledo C. W. (2008). Manual del Usuario, Editorial Brujas, Córdoba,
Argentina. 316 p.
Berruezo, L. A., Harries, E. M., Galván, M. Z., Stenglein, S. A., y Mercado, G.
(2021). Evaluación de la tolerancia a Fusarium oxysporum and Fusarium
solani en variedades de tabaco (Nicotiana tabacum L.) tipo Virginia
bajo condiciones controladas en el noroeste de Argentina. Revista de
la Facultad de Ciencias Agrarias. Universidad Nacional de Cuyo,
53(2), 214-224. https://www.scielo.org.ar/pdf/refca/v53n2/1853-8665-
refca-53-02-214.pdf
Browne, R. & Cooke, B. (2005). A comparative assessment of potential
components of partial disease resistance to Fusarium head blight using a
detached leaf assay of wheat, barley and oats. European Journal of Plant
Pathology, 112, 247-258 https://doi.org/10.1007/s10658-005-2077-z
Cakır, B., Gül, A., Yolageldi, L., & Özaktan, H. (2014). Response to Fusarium
oxysporum f. sp. radicis-lycopersici in tomato roots involves regulation
of SA-and ET-responsive gene expressions. European Journal of Plant
Pathology, 139(2), 379-391. https://doi.org/10.1007/s10658-014-0394-9
Carmona, S. L., del Pilar Villarreal-Navarrete, A., Burbano-David, D., Gómez-
Marroquín, M., Torres-Rojas, E., & Soto-Suárez, M. (2020). Boosting
photosynthetic machinery and defense priming with chitosan application
on tomato plants infected with Fusarium oxysporum f. sp. lycopersici.
bioRxiv, 19, 1-35. https://doi.org/10.1101/2020.08.18.256628
Espino, E., Uriarte, B. E., Cordero, P. L., Rodríguez, N., Izquierdo, A., Blanco,
L. E., y Díaz, M. (2012). Instructivo técnico para el cultivo del tabaco
en Cuba. Ministerio de la Agricultura. Instituto de Investigaciones del
Tabaco, p. 148.
Espinoza-Ahumada, C. A., Gallegos-Morales, G., Hernández-Castillo, F. D.,
Ochoa-Fuentes, Y. M., Cepeda-Siller, M., y Castillo-Reyes, F. (2019).
Antagonistas microbianos a Fusarium spp., como agente causal
de pudrición de raíces y tallo en melón. Ecosistemas y Recursos
Agropecuarios, 6(16), 45-55. https://doi.org/10.19136/era.a6n16.1843
García, S. E., Aldrete, A., Alvarado, D., Cibrián, D., Méndez, J. T., Valdovinos, G.,
y Equíhua, A. (2017). Efecto de Fusarium circinatum en la germinación y
crecimiento de plántulas de Pinus greggii en tres sustratos. Agrociencia,
51(8), 895-908. https://www.scielo.org.mx/pdf/agro/v51n8/1405-3195-
agro-51-08-895.pdf
Gilardi, G., Matic, S., Guarnaccia, V., Garibaldi, A., & Gullino, M. L. (2021). First
report of Fusarium clavum causing leaf spot and fruit rot on tomato in
Italy. Plant Disease, 105(8), 2250. https://doi.org/10.1094/PDIS-05-20-
1096-PDN
González, L. C., Gonzalez, H. H. M., y Ochoa, X. G. R. (2023). Marchitez
por Fusarium oxysporum Schlthl en masaguaro (Pseudosamanea
guachapele) (Kunth). INGE CUC, 19(1), 11-21. https://doi.org/10.17981/
ingecuc.19.1.2023.02
Gui, Z.-Q., Yuan, X.-L., Yang, J., Du, Y.-M., & Zhang, P. (2024). An updated
review on chemical constituents from Nicotiana tabacum L.: Chemical
diversity and pharmacological properties. Industrial Crops and Products,
214, 118497. https://doi.org/10.1016/j.indcrop.2024.118497
Ha-Thanh, P., Ngoc Tuan, T., Van Van, N., Van Lu, N., Thai Binh, H., Van Chin,
N., & Do Dung, D. (2022). Results of trial oriental tobacco varieties
planting in Ninh Thuan and Dak Lak Province, Vietnam in 2021. Journal
of Experimental Agriculture International, 44(2), 78-87. https://doi.
org/10.9734/jeai%2F2022%2Fv44i230801
Hu, B., Zheng, Y., Lv, J., Zhang, J., & Dong, Y. (2023). Proteomic analysis of the
faba bean-wheat intercropping system in controlling the occurrence of
faba bean Fusarium wilt due to stress caused by Fusarium oxysporum f.
sp. fabae and benzoic acid. BMC Plant Biology, 23(1), 472. https://doi.
org/10.1186/s12870-023-04481-8
Hudson, O., Fulton, J. C., Dong, A. K., Dufault, N. S., & Ali, M. E. (2021).
Fusarium oxysporum f. sp. niveum molecular diagnostics past, present
and future. International Journal of Molecular Sciences, 22(18), 9735.
https://doi.org/10.3390/ijms22189735
Kema, G. H., Drenth, A., Dita, M., Jansen, K., Vellema, S., & Stoorvogel,
J. J. (2021). Fusarium wilt of banana, a recurring threat to global
banana production. Frontiers in Plant Science, 11, 628888. https://doi.
org/10.3389/fpls.2020.628888
Khademi, M., Varasteh-Shams, M., Nazarian-Firouzabadi, F., & Ismaili, A.
(2020). New recombinant antimicrobial peptides confer resistance to
fungal pathogens in tobacco plants. Frontiers in Plant Science, 11, 1236.
https://doi.org/10.3389/fpls.2020.01236
Laraba, I., Busman, M., Geiser, D. M., & O’Donnell, K. (2022). Phylogenetic
diversity and mycotoxin potential of emergent phytopathogens within
the Fusarium tricinctum species complex. Phytopathology, 112(6), 1284-
1298. https://doi.org/10.1094/PHYTO-09-21-0394-R
Luna-Rodríguez, M., González-Oviedo, N. A., Rivera-Fernández, A., y Flores-
de la Rosa, F. R. (2023). Detección del gen xyl3 en cepas de Fusarium
oxysporum f. sp. vanillae. Revista Mexicana de Ciencias Agrícolas, 14(6),
e2711. https://doi.org/10.29312/remexca.v14i6.2711
This scientic 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): e254226 April-June. ISSN 2477-9409.
6-6 |
Nikitin, D. A., Ivanova, E. A., Semenov, M. V., Zhelezova, A. D., Ksenofontova, N.
A., Tkhakakhova, A. K., & Kholodov, V. A. (2023). Diversity, ecological
characteristics and identication of some problematic phytopathogenic
Fusarium in soil: a review. Diversity, 15(1), 49. https://doi.org/10.3390/
d15010049
Nitschke, E., Nihlgard, M., & Varrelmann, M. (2009). Dierentiation of eleven
Fusarium spp. isolated from sugar beet, applying restriction fragment
analysis of polymerase chain reaction-amplied translation elongation
factor 1α gene fragment. Phytopathology, 99, 921-929. https://doi.
org/10.1094/PHYTO-99-8-0921
Observatory of Economic Complexity [OEC]. (2024, Noviembre 17). Cigarros,
cigarrillos del tabaco en Cuba. https://oec.world/es/prole/bilateral-
product/rolled-tobacco/reporter/cub
Ocina Nacional de Estadísticas e Información [ONEI]. (2022, Diciembre 10).
Sector agropecuario. Indicadores seleccionados 2019. Ocina Nacional
de Estadística e Información. http://www.onei.gob.cu/node/14215
Pandey, R. (2023). Controlling tobacco diseases: an overview of black shank
and Fusarium wilt. International Journal of Applied Sciences and
Biotechnology, 11(1):1-7. https://www.nepjol.info/index.php/IJASBT/
article/view/52440
Pastuszak, J., Szczerba, A., Dziurka, M., Hornyák, M., Kopeć, P., Szklarczyk, M.,
& Płażek, A. (2021). Physiological and biochemical response to Fusarium
culmorum infection in three durum wheat genotypes at seedling and full
anthesis stage. International Journal of Molecular Sciences, 22(14),
7433. https://doi.org/10.3390/ijms22147433
Pfenning, L. H., Da Silva, C. S., De Pereira, M. M., Costa, H., Aries, V. J., García,
A. C., & Dos Figueredo, S. A. (2014). First repor and characterization
of Fusarium circinatum, the causal agent of pitch canker in Brazil.
Tropical Plant Pathology, 39, 210-216. https://doi.org/10.1590/S1982-
56762014000300004
Qiu, R., Li, C., Li, X., Zhang, Y., Liu, C., Li, C., & Li, S. (2023). First report
of Fusarium sacchari causing root rot of tobacco (Nicotiana tabacum
L.) in China. Crop Protection, 174, 106437. https://doi.org/10.1016/j.
cropro.2023.106437
Retana, K., Ramírez-Coché, J. A., Castro, O., y Blanco-Meneses, M. (2018).
Caracterización morfológica y molecular de Fusarium oxysporum
f. sp. apii asociado a la marchitez del apio en Costa Rica. Agronomía
Costarricense, 42(1), 115-126. http://dx.doi.org/10.15517/rac.
v42i1.32199
Ribeiro, J. A., Albuquerque, A., Materatski, P., Patanita, M., Varanda, C. M.,
Félix, M. D. R., & Campos, M. D. (2022). Tomato response to Fusarium
spp. infection under eld conditions: study of potential genes involved.
Horticulturae, 8(5), 433. https://doi.org/10.3390/horticulturae8050433
Rongai, D., Pulcini, P., Pesce, B & Milano, F. (2017). Antifungal activity of
pomegranate peel extract against Fusarium wilt of tomato. European
Journal of Plant Pathology, 147(1), 229-238. https://doi.org/10.1007/
s10658-016-0994-7
Shen, H. F., Yang, Q. Y., Pu, X. M., Zhang, J. X., Sun, D. Y., Liu, P. P., Lin, B. R.,
& Deng, H. B. (2023). First report of Fusarium root rot of tobacco caused
by Fusarium fujikuroi in Guangdong Province, China. Plant Disease,
107(10), 3294.
https://doi.org/10.1094/PDIS-04-23-0658-PDN
Sosa-Sánchez, O., Romero-Bastias, M., Silva-Pupo, J. J., Gaibor-Fernández,
R. R., Rodríguez-Rodríguez, S. F., y Ceiro-Catasú, W. G. (2022).
Caracterización cultural-morfométrica como herramienta para la
identicación de Fusarium spp., asociado a Nicotiana tabacum L.
Agronomía Costarricense, 46(1), 111-118. https://doi.org/10.15517/RAC.
V46I1.49872
Townsend, G.R., & Heuberger, J. W. (1943). Methods for estimating losses caused
by diseases in fungicide experiments. Plant Disease Reporter, 27, 340-
343.
Zhang, Q., Zhong, T., E, L., Xu, M., Dai, W., Sun, S., & Ye, J. (2021). GT factor
ZmGT-3b is associated with regulation of photosynthesis and defense
response to Fusarium graminearum infection in maize seedling. Frontiers
in Plant Science, 12, 724133. https://doi.org/10.3389/fpls.2021.724133
Zhu, Y., Willey, K., Wheeler, T., Dever, J. K., Whitelock, D., Wedegaertner,
T., & Zhang, J. (2023). A rapid and reliable method for evaluating
cotton resistance to Fusarium wilt race 4 based on taproot rot at the
seed germination stage. Phytopathology, 113(5), 904-916. https://doi.
org/10.1094/PHYTO-08-22-0286-FI
Zonno, M. C & Vurro, M. (2002). Inhibition of germination of Orobanche ramosa
seeds by Fusarium toxins. Phytoparasitica, 30(5), 519-524. https://doi.
org/10.1007/bf02979757