© The Authors, 2022, Published by the Universidad del Zulia*Corresponding author: marina.garcía@utm.edu.ec
Yonis Hernández
1
Marina García
2*
Rafael Mejías
1
Rev. Fac. Agron. (LUZ). 2022, 39(4): e223947
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v39.n4.02
Crop Production
Associate editor: Dr. Jorge Vilchez-Perozo
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
Keywords:
Cauline histology
Bacterial infection
Potato
Anatomical changes caused by Ralstonia solanacearum Smith and Pectobacterium carotovorum
(Jones) in Solanum tuberosum L. stems
Cambios anatómicos provocados por Ralstonia solanacearum Smith y Pectobacterium carotovorum
(Jones) en tallos de Solanum tuberosum L.
Alterações anatômicas causadas por Ralstonia solanacearum Smith e Pectobacterium carotovorum
(Jones) em caules de Solanum tuberosum L.
1
Universidad Central de Venezuela, Facultad de Agronomía,
Instituto de Botánica Agrícola, Laboratorio de Bacterias
Fitopatógenas. Maracay, estado Aragua, Venezuela.
2
Universidad Técnica de Manabí, Facultad de Ingeniería
Agronómica, Departamento de Ciencias Agronómicas,
Portoviejo, 130105, Manabí, Ecuador.
Received: 24-08-2022
Accepted: 17-09-2022
Published: 05-10-2022
Abstract
Potato (Solanum tuberosum L.) is a crop notably affected by various
pathogens, including bacterial, and it is important to study the histological
changes that they produce to understand the symptoms associated with each
disease. The objective of this research was to determine the anatomical
changes that occur in potato stems due to the infection caused by Ralstonia
solanacearum and Pectobacterium carotovorum. An assay was carried out
with 45-day-old plants of the Kennebec variety, which were inltrated in
the basal part of the main stem with a suspension of 10
8
CFU.mL
-1
of R.
solanacearum and P. carotovorum, including a control treatment in which the
plants were treated with sterile distilled water. Twelve days after inoculation,
segments were taken from the second internode of the main stem and they
were xed in FAA (formaldehyde-acetic acid-ethanol 70 %) until processing
to obtain cross sections of the stem. In the plants inoculated with R.
solancaearum, invasion of the xylem vessels by the bacterium and formation
of tyloses in some of them was observed. In the case of P. carotovorum,
necrosis in the form of discontinuous bands in the epidermal cells, cortex,
vascular cylinder, and pith was observed, as well as obstruction in xylem
vessels by the bacteria and tylosis in some of them. The anatomical changes
in the stem, induced by the two bacteria studied, are directly linked to the
symptomatology of the disease that each of them causes in the potato crop.
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). 2022, 39(4): e223947. October-December. ISSN 2477-9407.
2-6 |
Resumen
La papa (Solanum tuberosum L.) es un cultivo notablemente
afectado por diversos patógenos, incluyendo los bacterianos, y es
importante el estudio de las alteraciones histológicas que éstos producen
para comprender los síntomas asociados a cada enfermedad. En esta
investigación se determinaron los cambios anatómicos provocados
por Ralstonia solanacearum y Pectobacterium carotovorum en
tallos de Solanum tuberosum. Se realizó un ensayo con plantas de la
variedad Kennebec de 45 días de edad, las cuales fueron inltradas
en la base del tallo principal con una suspensión de 10
8
UFC.mL
-1
de
R. solanacearum y P. carotovorum, incluyendo un tratamiento testigo
en el que las plantas fueron tratadas con agua destilada estéril. Doce
días después de la inoculación, se tomaron segmentos del segundo
entrenudo del tallo principal y se jaron en FAA (formaldehido-ácido
acético-etanol 70 %) hasta su procesamiento para la obtención de
secciones transversales del tallo. En las plantas inoculadas con R.
solancaearum, se observó invasión en los vasos xilemáticos por la
bacteria y formación de tílides en algunos de ellos. En cuanto a P.
carotovorum, se evidenció necrosis en forma de bandas discontinuas
en las células de la epidermis, corteza, cilindro vascular y médula, así
como obstrucción en vasos del xilema y tilosis en algunos de ellos.
Los cambios anatómicos en el tallo, inducidos por las dos bacterias
estudiadas, están directamente vinculados con la sintomatología de
la enfermedad que cada una de ellas provoca en el cultivo de papa.
Palabras clave: histología caulinar, infección bacteriana, papa
Resumo
A batata (Solanum tuberosum L.) é uma cultura notavelmente
afetada por vários patógenos, incluindo bacterias, sendo importante
estudar as alterações histológicas que eles produzem para entender
os sintomas associados a cada doença. O objetivo desta pesquisa
foi determinar as alterações anatômicas que ocorrem em caules de
batata devido à infecção causada por Ralstonia solanacearum e
Pectobacterium carotovorum. Foi realizado um ensaio com plantas
da variedade Kennebec com 45 dias de idade, que foram inltradas
na base do caule principal com uma suspensão de 10
8
UFC.mL
-1
de
R. solanacearum ou P. carotovorum, e um tratamento foi incluído.
controle em que as plantas foram tratadas com água destilada estéril.
Doze dias após a inoculação, foram retirados segmentos do segundo
entrenó do caule principal e xados em FAA (formaldeído-ácido
acético-etanol 70 %) até o processamento, para obtenção de cortes
transversais do caule. Nas plantas inoculadas com R. solancaearum,
observou-se a invasão dos vasos do xilema pela bactéria e a formação
de tilos em algumas delas. Em relação ao P. carotovorum, foi
encontrada necrose na forma de bandas descontínuas nas células da
epiderme, córtex, cilindro vascular e medula, além de obstrução nos
vasos do xilema pela bactéria e tilose em algumas delas. Los cambios
anatómicos en el tallo, inducidos por las dos bacterias estudiadas,
están directamente vinculados con la sintomatología de la enfermedad
que cada una de ellas provoca en el cultivo de papa.
Palavras chave: histologia de caulina, infecção bacteriana, papa.
Introduction
Potato (Solanum tuberosum L) is the fourth most important crop
in the world after corn (Zea mays L.), rice (Oryza sativa L.), and
wheat (Triticum aestivum L.), with an estimated world production of
359.07 million metric tons by 2020 (FAOSTAT, 2022).
In Venezuela, this crop is located in the Andean region, as well
as in the Central and Eastern zone of the country. In the Central area,
‘‘High Valleys of Carabobo’’ stand out where the sowing is carried
out between November to January, when night temperatures are
below 20°C, favoring the good development of the crop (Olivares
and Hernández, 2019).
In eld visits and through sampling analysis of sick plants,
the presence of bacterial infections in potato has been detected,
the most recurrent being soft rot by P. carotovorum and wilt by R.
solanacearum. These two bacterial pathogens constitute a threat to
the crop because as they spread, they affect plantations, drastically
reducing yields (Fiers et al., 2012; Yuliar et al., 2015; Charkowski et
al., 2020).
The host range of R. solanacearum is quite wide and includes
53 different botanical families, being distributed at various altitudinal
levels (Karim et al., 2018; Lowe-Power et al., 2018a). The bacterium
penetrates through the roots, either through wounds or natural
openings, causing plant wilting due to its rapid colonization and
multiplication in vascular tissues (Yuliar et al., 2015; Lowe-Power
et al., 2018b). According to Buddenhagen and Kelman (1964) and
Hayward (1991), bacterial colonization of the stem results in xylem
browning, leaf epinasty, and generalized lethal wilting
In sections of tomato stems (Solanum lycopersicum L.) observed
under the light microscope, the presence of bacterial masses of R.
solanacearum densely stained in the xylem and in microscopic
preparations studied under the transmission microscope was
observed; in addition, the bacterium was detected in the primary
xylem of a resistant material, but not in the secondary xylem; while
in sensitive material, it was visualized in both primary and secondary
xylem (Grimault et al., 1994; Nakaho et al., 2000).
In an anatomical study on tomato stems infected with R.
solanacearum, Hernández et al. (2005) detected bacterial invasion
in the xylem and part of the phloem, mainly in the conducting cells
with the largest diameter, while observations made under the electron
microscope showed that the invasion also occurred in the parenchyma
cells associated with the conducting tissue.
In this same crop, it has been shown that the invasion of this
bacterium in a single lateral vascular bundle of the petiole causes leaf
decay (epinasty), while the invasion of all vascular bundles causes
wilting (Alvarez et al., 2010; Karim et al., 2018), likewise, it has been
indicated that in tomato stems whose vascular bundles are invaded by
R. solanacearum, there is a tendency to form adventitious roots that
develop externally to the invaded vascular bundle.
The wilting caused by this bacterium may be due to the gradual
mechanical obstruction of the xylem vessels, or to metabolites
produced by the pathogen; among them, putrescine has been
mentioned, which acts as well as physical factors in the production
of symptoms (Khokhani et al., 2017; Lowe-Power et al., 2018b; Xue
et al., 2020).
In the case of P. carotovorum, a polyphagous pathogen with
a wide host range (Czajkowski et al., 2009; Pérombelon, 2002;
Charkowski, 2018), its mode of action is associated with a set of
depolymerizing activities such as the production of pectinases,
cellulases, proteases, phospholipases and xylanases that can cause
degradation of cell wall components in cells of different plant tissues
(Pérombelon, 2002; Charkowski, 2015; Agyemang et al., 2020). Rot
symptoms vary according to the initial bacterial concentration in seed
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Hernández et al. Rev. Fac. Agron. (LUZ). 2022, 39(4): e2239473-6 |
potato tubers, cultivar susceptibility, and environmental conditions,
particularly temperature and soil moisture content (Pérombelon,
2002; Charkowski, 2015; Charkowski et al., 2020).
Based on the above remarks and considering the scarce
documented information on histological alterations in S. tuberosum
stems affected by R. solanacearum and P. carotovorum in varieties
commonly used by farmers in the country, the present research was
proposed with the objective of determining the anatomical changes
in the stem of potato plants infected with R. solanacearum and P.
carotovorum bacteria.
Materials and methods
Plant material. To carry out the trial, 45-day-old potato plants of
the Kennebec variety, were grown in pots of 1.5 kg capacity, containing
a substrate composed of a mixture of sand and sterile soil (3:1), which
were kept until inoculation in a shade house with protection against
insects, located at the Institute of Agricultural Botany of the Faculty
of Agronomy, in Maracay, Aragua state, Venezuela.
Inoculation. Bacterial cultures of R. solanacearum and P.
carotovorum of 48 h of growth on YCA medium (yeast extract
calcium carbonate agar) were used. From each bacterial strain, a
suspension adjusted to a concentration of 10
8
CFU.mL
-1
was made,
using tube number 3 of the McFarland scale (Gayathiri et al., 2018).
The inoculation of plants was made by inltrating them
with the bacterial suspension in the basal part of the stem using a
hypodermic needle. Three treatments were used: (i) inoculation
with R. solanacearum; (ii) inoculation with P. carotovorum and
(iii) control (inoculation with distilled water) and a total of 6 plants/
treatments were arranged. After inoculation, the plants were placed
in a humid chamber for 48 hours and then transferred back to the
shade house where they were distributed according to a completely
randomized design and watered daily with tap water. During the
trial, the average climatic conditions inside the shade house were:
minimum temperature 20 ºC, maximum temperature 32 ºC, and
relative humidity 66 %.
Anatomical study. At 12 days after inoculation, approximately
1.5 cm long segments were taken from the second internode (base-
to-apex direction) of the main stem of four plants per treatment. Stem
segments were gently washed with distilled water and xed in FAA
(formaldehyde-acetic acid-ethanol 70 %) until processing. With the
xed material, freehand cross sections approximately 20 µm thick
were made using a razor blade; the sections obtained were stained
with 0.1 % aqueous toluidine blue, mounted in a water-glycerin
solution (v:v), and sealed with transparent enamel, to obtain semi-
permanent slides that were examined under a NIKON E-200 optical
microscope to make the corresponding descriptions, and additionally,
digital images were taken of the different sections using an Evolution
LC Color camera incorporated to the microscope.
Results and discussion
Anatomical description of the stem of S. tuberosum var.
Kennebec
The control plants did not show any symptomatology and when
analyzing the cross sections under the microscope, a uniseriate
epidermis, cortex made up of 6-7 layers of angular collenchyma and
4-5 layers of parenchyma with cells of variable size were observed; the
pith was totally parenchymatous and the vascular system consisted of
open bicollateral bundles, as is characteristic in Solanaceae (Metcalfe
and Chalk, 1950), further distinguishing a poorly developed secondary
structure with a greater proportion of secondary vascular tissue in the
fascicular zone, and in the case of the xylem, the conduction elements
presented empty lumen, without any obstruction (Figures 1A, 1B),
as was expected in healthy plants. These histological characteristics
coincided with those reported by Shtein et al. (2020), who studied the
anatomical structure in mature internodes of Solanum tuberosum cv.
Nicola.
Figure 1. Details of the cross-section of the stem in control plants
of S. tuberosum and inoculated with R. solanacearum.
A-B: control; C-D: inoculated plant; E-F: xylem tissue
of the inoculated plant, with arrows indicating tyloses in
formation. ep: epidermis; co: collenchyma; pc: cortical
parenchyma; fe: external phloem; : internal phloem; xi:
xylem; pm: medullary parenchyma; vo: obstructed xylem
vessel. Scale bars: 300 µm (A, B, C); 100 µm (D); 30 µm
(E, F).
Symptomatology and stem anatomical changes in plants of
Solanum tuberosum inoculated with R. solanacearum
The plants inoculated with R. solanacearum, started to show
symptoms 6 days after inoculation, with decay and subsequent
wilting of lower leaves, which then spread to the other leaves and
newer branches, while 12 days after inoculation, total wilting was
already observed in some plants. These symptoms coincide with those
reported by several authors in plants infected by R. solanacearum
(Karim et al., 2018; Charkowsky et al., 2020).
Likewise, Hernández et al. (2005) observed in tomato plants a total
collapse of them at 12 days after inoculation with R. solanacearum.
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). 2022, 39(4): e223947. October-December. ISSN 2477-9407.
4-6 |
Figure 2. Details of the cross-section of the stem in control plants
of S. tuberosum and inoculated with P. carotovorum.
A:
control plant; B-D: inoculated plant; note tissue lysis
in the epidermis, cortex, vascular cylinder, and pith; E-F:
conducting tissue in the inoculated plant, note maceration
and necrosis in the xylem tissue (E) and obstruction of
vessels and tyloses in formation indicated by arrow
(F). tm: meristematic tissue. Scale bars: 300 µm (A, B,
C); 100 µm (D); 30 µm (E, F).
These degenerative changes in the anatomical structure of the
stem correspond to the symptoms of soft rot that characterize the
damage by P. carotovorum (Pérombelon, 2002; Charskowsky,
2015; Charskowsky, 2018), a bacterium that produces a series of
enzymes such as cellulases, pectinases, proteases, phospholipases,
among others, which cause degradation of the cell wall components
that form different tissues (Barras et al., 1994).
The appearance of layers of meristematic tissue was also
observed in some regions of the bark, possibly originating from the
dedifferentiation of cortical parenchyma cells, which seems to be a
defense mechanism of the plant to ensure the development of new
tissues.
It should be noted that in potato plants affected by “blackleg”
produced by P. atrosepticum, Artschwager (1920) found an extensive
lignication of vascular tissues and the development of sclereids
in the stem bark and pith, which according to Pérombelon (2002)
tends to increase the plant resistance to infection since lignication
offers greater resistance to cell wall degradation by peptic enzymes;
however, this response was not observed in the present study.
Similarly, to what was observed in plants inoculated with
R. solanacearum, in those inoculated with P. carotovorum the
In relation to the stem anatomy, in plants inoculated with R.
solanacearum only changes were observed in the xylem conduction
elements, specically in the xylem vessels, where obstruction of
their lumen was detected (Figures 1C - 1F). This alteration in
the xylem structure coincides with what was observed by other
researchers, who point out that R. solanacearum affects water
conduction and consequently causes wilting, due to the blockage
in the xylem conducting cells (Álvarez et al., 2010; Yadeta and
Thomma, 2013; Planas-Marqués et al., 2020). It has been indicated
that the multiplication of the bacterium and the production of large
amounts of extracellular polysaccharides, would be the cause of the
blockage of xylem conducting cells and the typical wilting caused
by this bacterium in infected plants of different species, including
S. tuberosum (Van der Wolf and De Boer, 2007; Genin and Denny,
2012, Khokhani et al., 2017).
In plants inoculated with R. solanacearum, the presence of
balloon-shaped tyloses was also evident in some of the vessels,
mainly in the secondary xylem (Figures 1E, 1F), structures to
avoid the advance of the bacterium towards the upper portions of
the stem, however, the evident wilting observed in potato plants of
the Kennebec variety inoculated with this bacterium showed that
the formation of tyloses in the xylem vessels was not effective in
stopping the invasion of the bacterium and therefore the progress
of the disease.
The formation of this type of structure is reported as a response
of the plant to the attack by vascular pathogens, to avoid their
invasion through the conducting tissue (Kashyap et al., 2021).
Similarly, to what was observed in this research, Ferreira et al.
(2017) detected the presence of vessels plugged by balloon-shaped
tyloses in potato clone 09509.6 inoculated with R. solanacearum
bacteria, suggesting that infected xylem vessels may induce the
formation of these.
Symptomatology and stem anatomical changes in plants of
S. tuberosum inoculated with P. carotovorum
Three days after the inoculation of the plants with P.
carotovorum, softening and maceration of the tissue around the
point of inoculation was observed, which spread to cover the entire
circumference of the stem; being also notorious the presence of
certain areas with necrosis, and additionally wilting occurred in
some plants. This symptomatology has been reported in potatoes
as well as in other species such as paprika (Capsicum annuum),
eggplant (Solanum melongena), tobacco (Nicotiana tabacum)
(Pérombelon, 2002; Charkowski, 2015; Charkowski, et al., 2020),
and it has been indicated that, under favorable conditions for the
development of this bacterium, the affected organs rot in two to
three days, and the plants can wither (Charkowsky, 2018).
The stem anatomy was severely affected in plants inoculated
with P. carotovorum (Figures 2B - 2F), in relation to control plants
(Figures 1A, 1B, 2A). One of the most evident changes was the
lysis and disintegration of the cells of the epidermis, as well as
those of the cortex, vascular cylinder, and pith tissues, observing
severe necrosis in the form of discontinuous bands in those areas
of the stem cross-section, being also notorious the obstruction in
the xylem vessels by the attack of this bacterium (Figures 2B -
2D). According to Charskowsky (2018), high concentrations of P.
carotovorum in the xylem can cause necrosis in the vascular tissue.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Hernández et al. Rev. Fac. Agron. (LUZ). 2022, 39(4): e2239475-6 |
formation of globose tyloses in the conducting cells of the xylem was
also noticeable (Figures 2E, 2F). The systemic invasion of bacteria of
the Pectobacterium and Dickeya genus through the xylem has been
documented by several authors (Kastelein et al., 2020; Czajkowski et
al., 2010; Pérombelon, 2002).
Regarding the presence of tyloses in the xylem of plants affected
by P. carotovorum, there are no previous reports in the available
literature; however, it is assumed that it is possibly a defense reaction
of the plants of the potato variety studied to the attack of the bacterium,
as occurs with R. solanacearum and other vascular pathogens (Yadeta
and Tomma, 2013). It should be noted that the fact that tylosis is due
to a reaction to mechanical damage is ruled out since these were not
observed in the plants of the control treatment.
Conclusions
R. solanacearum and P. carotovorum caused histological changes
in the stem of S. tuberosum of the Kennebec variety. In the case of
R. solanacearum, obstruction was predominantly observed in the
secondary xylem due to the formation of tyloses, which explains the
wilting of the plants, while in the case of P. carotovorum, the most
noticeable anatomical change was maceration of the stem tissues, in
addition to the obstruction in the conducting cells of the xylem due
to tylosis.
Acknowledgment
The authors express their gratitude to the Council for Scientic
and Humanistic Development of the Central University of Venezuela
(CDCH-UCV), for funding this research through Project No. PG- 01-
8720-2013/1.
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