Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars
Microsporida infection of Agrotis segetum Schiffermuller 
 larvae causes numerous changes of separate fractions activities belonging to carboxylesterase isoenzyme 
 complex. Such shifts are found to correlate with parasite development stages, activities of several fractions being inc...
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Інститут зоології ім. І.І. Шмальгаузена НАН України
2001
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| Zitieren: | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars / T.M. Yefimenko, O.V. Sundukov, I.V. Issi // Вестн. зоологии. — 2001. — Т. 35, № 4. — С. 45-50. — Бібліогр.: 30 назв. — англ. |
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| author | Yefimenko, T.M. Sundukov, O.V. Issi, I.V. |
| author_facet | Yefimenko, T.M. Sundukov, O.V. Issi, I.V. |
| citation_txt | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars / T.M. Yefimenko, O.V. Sundukov, I.V. Issi // Вестн. зоологии. — 2001. — Т. 35, № 4. — С. 45-50. — Бібліогр.: 30 назв. — англ. |
| collection | DSpace DC |
| description | Microsporida infection of Agrotis segetum Schiffermuller 
larvae causes numerous changes of separate fractions activities belonging to carboxylesterase isoenzyme 
complex. Such shifts are found to correlate with parasite development stages, activities of several fractions being increased early after Vairimorpha antheraeae incorporation up to the beginning of sporogony. During intensive sporogony and spore forming the enzyme activities are proved to decrease. Activities of multiple esterase molecular forms at different microsporidiosis stages may be correlated with 
cell pathology patterns and cell compartments damages taking part in the enzymes synthesis and transportation. These described changes may be also due to such Microsporidainduced pathological features 
as lipid metabolism and hormone balance impair followed by decreased reproductive function.
Сопоставлялись уровни суммарной эстеразной активности и активность отдельных эстеразных фракций в брюшных нервных цепочках здоровых и зараженных микроспоридией Vairimorpha antheraeae гусениц озимой совки Agrotis segetum Schiffermьller. Выявлено, что эстеразная активность увеличивается от момента внедрения паразита в ткани хозяина до начала спорогонии. Период наибольшей активности эстераз соответствует вегетативному размножению микроспоридий, а наименьшей - их массовому спорообразованию. Предполагается возможная взаимосвязь между изменением активности эстераз и такими проявлениями патогенеза микроспоридиоза насекомых, как нарушение липидного обмена, гормонального баланса и последующего снижения репродуктивных функций. Обсуждается сопряженность активности эстераз с особенностями патологии клетки и ее компартментов, учавствующих в синтезе и транспорте этих ферментов на разных этапах микроспоридиоза.
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Vestnik zoologii, 35(4): 45—50, 2001
© 2001 T. M. Yefimenko, O. V. Sundukov, I. V. Issi
Последним работал: AL Ostashko/DIMA; E:\My Documents\Verstka\Vestnik\2001\N4\05_Efimenko\Efimen_vz.doc; Дата сохранения 8/13/2001 5:25:00 PM; 1 станиц(ы); Число
16353
ÓÄÊ 632.937 : 595.786
EFFECT OF MICROSPORIDA INFECTION ON THE
ESTERASES ACTIVITIES IN AGROTIS SEGETUM CATERPILLARS
T. M. Yefimenko1, O. V. Sundukov2, I. V. Issi2
1Petro Prokopovych Apiculture Research Institute, Zabolotny str., 19, Kyiv, 03143 Ukraine
2All-Russian Plant Protection Institute, Tsarskoye Selo, S.-Petersburg, 189620 Russia
Accepted 5 December 2000
Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars. Ye-
fimenko T. M., Sundukov O. V., Issi I. V. – Microsporida infection of Agrotis segetum Schiffermüller
larvae causes numerous changes of separate fractions activities belonging to carboxylesterase isoenzyme
complex. Such shifts are found to correlate with parasite development stages, activities of several frac-
tions being increased early after Vairimorpha antheraeae incorporation up to the beginning of sporog-
ony. During intensive sporogony and spore forming the enzyme activities are proved to decrease. Ac-
tivities of multiple esterase molecular forms at different microsporidiosis stages may be correlated with
cell pathology patterns and cell compartments damages taking part in the enzymes synthesis and trans-
portation. These described changes may be also due to such Microsporida-induced pathological features
as lipid metabolism and hormone balance impair followed by decreased reproductive function.
Key wo r d s : microsporida infection, Vairimorpha antheraeae, Noctuidae, Agrotis segetum, carboxyles-
terase isoenzyme complex, lipid metabolism, hormone balance.
Âëèÿíèå ìèêðîñïîðèäèîçà íà àêòèâíîñòü ýñòåðàç ó ãóñåíèö îçèìîé ñîâêè Agrotis segetum. Åôèìåí-
êî Ò. Ì., Ñóíäóêîâ Î. Â., Èññè È. Â. – Ñîïîñòàâëÿëèñü óðîâíè ñóììàðíîé ýñòåðàçíîé àêòèâ-
íîñòè è àêòèâíîñòü îòäåëüíûõ ýñòåðàçíûõ ôðàêöèé â áðþøíûõ íåðâíûõ öåïî÷êàõ çäîðîâûõ è
çàðàæåííûõ ìèêðîñïîðèäèåé Vairimorpha antheraeae ãóñåíèö îçèìîé ñîâêè Agrotis segetum Schif-
fermüller. Âûÿâëåíî, ÷òî ýñòåðàçíàÿ àêòèâíîñòü óâåëè÷èâàåòñÿ îò ìîìåíòà âíåäðåíèÿ ïàðàçèòà â
òêàíè õîçÿèíà äî íà÷àëà ñïîðîãîíèè. Ïåðèîä íàèáîëüøåé àêòèâíîñòè ýñòåðàç ñîîòâåòñòâóåò âå-
ãåòàòèâíîìó ðàçìíîæåíèþ ìèêðîñïîðèäèé, à íàèìåíüøåé – èõ ìàññîâîìó ñïîðîîáðàçîâàíèþ.
Ïðåäïîëàãàåòñÿ âîçìîæíàÿ âçàèìîñâÿçü ìåæäó èçìåíåíèåì àêòèâíîñòè ýñòåðàç è òàêèìè ïðî-
ÿâëåíèÿìè ïàòîãåíåçà ìèêðîñïîðèäèîçà íàñåêîìûõ, êàê íàðóøåíèå ëèïèäíîãî îáìåíà, ãîðìî-
íàëüíîãî áàëàíñà è ïîñëåäóþùåãî ñíèæåíèÿ ðåïðîäóêòèâíûõ ôóíêöèé. Îáñóæäàåòñÿ ñîïðÿ-
æåííîñòü àêòèâíîñòè ýñòåðàç ñ îñîáåííîñòÿìè ïàòîëîãèè êëåòêè è åå êîìïàðòìåíòîâ, ó÷àâñò-
âóþùèõ â ñèíòåçå è òðàíñïîðòå ýòèõ ôåðìåíòîâ íà ðàçíûõ ýòàïàõ ìèêðîñïîðèäèîçà.
Êëþ÷åâûå ñëîâà : ïàòîãåíåç ìèêðîñïîðèäèîçà, Vairimorpha antheraeae, Noctuidae, Agrotis
segetum, àêòèâíîñòü ýñòåðàç, ëèïèäíûé îáìåí, ãîðìîíàëüíûé áàëàíñ.
Introduction
Pathological process during microsporidiosis infection (MI) in susceptible insects is thought to be due
to several factors including exhausting of bioenergetical systems of the host organism; damage of parasites-
invaded cells, tissues, and organs; hormonal balance impair; intoxication of the host organism by parasite's
metabolic products (Weiser, 1951; Issi, 1986). Some biochemical aspects of host-parasite interactions remain,
however, unclear.
Being sure that the changes in enzyme activities which are the main regulative factors of the cell me-
tabolism reflect the depth of the pathological process we have determined esterases activities in the nerve
chain of Agrotis segetum Schiffermüller (Noctuidae) abdomen on the different stages of MI. The changed
esterases activities level might have become a marker of MI caused physiological disturbances specific for
insect neural system.
Material and methods
In all the experiments we used A. segetum larvae originated from eggs of the same female, ranged and
selected according to their weight and age, the ecdysis for the next age having taken place at the same day.
They were incubated in entomological tubes and perorally infected by the same quantities of medium con-
taining a known dose of parasite spores. The insects which had not eaten all the food during 12 hs were se-
T. M. Yefimenko, O. V. Sundukov, I. V. Issi 46
lected out. The larvae were fed on the medium proposed by Lopatkin et al. (1986) at +24°C, the light day
lasted during 18 hs.
We worked with a Microsporida Vairimorpha antheraeae (Simtchuk, Lysenko, Tchetkartova, 1979)
(Burenellidae) passed a lot of times through Mamestra brassicae (Noctuidae) and A. segetum larvae. Antheraea
pernyi Guerin-Meneville is the original host of this parasite (Simtchuk et al., 1979) which is also highly
pathogenic for a lot of other Lepidoptera insects.
The time of insect infection was always chosen taking into consideration the necessity to have
microsporides of the different developmental stages at the day of analysis. To reach such a situation, 20
larvae in each experiment were infected belonging to the 2nd age and analysed at the 10—15th days post
infection (p. i.), next 20 larvae of the 3rd age were infected and analysed in 3—7 days p. i. etc. The infecting
doses were 10 times higher for the larvae of the next age comparing to those ones of the former one (100
spores/larva for 2nd-aged larvae, 1000 spores for 3rd-aged ones etc.).
So we had three variants in our experiment: control insects (healthy larvae), those ones with initial stages
of the parasite development (in 3—7 days p. i.), and the larvae with progressed disease (in 10—15 days p. i.).
To obtain electrophoretical esterases separation, we used a gel system with tris-veronal electrod buffer
(pH 7.0), acrylamide concentration in the separating gel being 7.5% (pH 7.5); this gel contained also Triton
X-100 (0.2%).
Each nervous chain was homogenised using 100 μl of 40% sucrose containing 1% Triton X-100. For
esterases composition assays, each tube was loaded by 50 μl of the sample; to estimate only choline esterase
reaction, we put into each tube 100 μl of the sample. Each experiment was carried out with four parallel
samples.
After electrophoresis the gels were incubated in the medium containing 0.56% I-naphtylacetate in
0.2 M phosphate buffer (pH 7.0), 2% acetone, and 0.2% fast blue PP (Šula, Weyda, 1983). Cholinesterase
activity was determined with acetylthiocholine iodide as a hydrolized substrate (Karnovsky, Roots, 1964)
without any preincubational gel fixation in formol. If the test-toxicant had been used the gels were preincu-
bated in the toxicant-containing medium during 5 min. The samples were then run at the apparatus PEFA-1
using 2 mA current during first 30 min and later 4 mA current.
Kinetic properties of esterases activities were obtained using p-nitropenylacetate (p-NPA) as a substrate
(Brick et al., 1977). For each sample, one nervous chain was homogenized in 1 ml of 0.2 M phosphate
buffer solution, pH 7.6. The p-NPA-containing incubation medium was prepared immediately before ex-
perimant and included homogenate (0.1 ml), 0.2 M phosphate buffer pH 7.6 (0.3 ml), water (0.2 ml), and
p-NPA (0.4 ml of the stock 1.5�10-3 M solution). The samples were incubated 2—4 min at +20—24°C, their
optical densities were measured at 390 nm. Each experimental variant had been tested in three tubes or more.
To determine the stage of Microsporida development and the density of parasite populations in the lar-
vae infected, we counted the average number of parasites under light microscope in stained smears, five fields
having been always used for count.
Results
Esterases electrophoresis using acetylthiocholine iodid permits to detect the local-
ization of E7 and E8 cholinesterase fractions (fig. 1, f). Using I-naphtylacetate we de-
tect according to their localization both non-specific esterases and also multiple mo-
lecular esterase forms hydrolyzing acetylthyocholine iodid (fig. 1, a–e). The activity of
all the non-specific esterase fractions E1—E6 being inhibited by diazoxone (10-7—
10-5 M), we thought these fractions to be carboxylase ones (EC 3.1.1.1.).
The larvae carrying parasites of different developmental stages (parasites prolifera-
tion was found at the 3—7th days p. i. and their sporogony and sporogenesis – at the
10—15th days p. i.) possessed different activities of separate carboxylesterase molecular
forms. At the 3rd day p. i. (fig. 1, b) we found the increase of E4-fraction activity, at the
7th day (fig. 1, c) it was also accompanied by higher activities of other molecular forms
of carboxylesterase – E1—E3, E5, E6.
The microscopic study of infected larvae fat body showed the 1—8-nuclei-
containing meronts of the first merogony to be the prevalent form at the 3rd day p. i. At
the 5—7th days p. i. we found mostly 1—8-nuclei-containing meronts of the second
merogony, sporonts being rather rare (tabl. 1). Fat bodies of such larvae rested white
and demi-transparent like these in healthy ones.
At the 13th day p. i. we detected step-wise drop of activities for all the multiple
molecular carboxylesterase forms (fig. 1, d). In the organisms of larvae survived up to
the 15th day p. i. only four molecular forms (E3—E6) were detected to express instead of
six ones (fig. 1, e).
Effect of microsporida infection on the esterases activities … 47
This period is marked with fat
body exhausting and cells separation.
All the space in the smears is filled
with parasite spores.
It should be noted esterases spec-
trum and esterases activities of control
healthy larvae remained without
changes during the period studied.
The study of kinetic parameters of
abdomen nerve chain esterases in
A. segetum larvae proved the highest
hydrolyzing activity was found in the
p-NPA concentration interval 0.2—
0.3 mM/l. So the levels of esterases
activities for healthy and infected in-
sects were compared in the limits of
this interval. Having added eserine to
the incubation media (10-5M) we noted
no drop of esterase activity; so we sug-
gest that in experiments with enzymatic
hydrolysis of p-NPA we detected the
activity of izoenzyme carboxylesterase
complex. The comparing of hydrolysis
curves (fig. 2) showed the activity level
of carboxylesterase to be significantly
decreased at the 10—13th days p. i.
Discussion
Esterases form a polyenzyme
complex hydrolyzing ester link of car-
bonic acids. Nowadays, the classifica-
tion of non-specific esterases is provisory because each of isolated esterase types pos-
sesses identical subunits composition; these subunits form a polymer molecule structure
with overlapping substrate and inhibitory specificity (Choudhoury, 1972). Such proper-
ties predetermine all the plurality of esterases functions in the animal organisms. In
insects these enzymes take part in the mobilization and energetic catabolism of fat sub-
stances (Lands, 1965; Ahmad, 1976); they control also juvenile hormone titers (Ham-
mock, 1985) and are important for reproduction and vitellogenesis processes (Hooper,
Wan, 1969; Kai, Hasegawa, 1973).
Fig. 1. Composition of esterase fractions in abdominal
nerve chain of A. segetum caterpillars, healthy and micro-
sporidiosis-diseased ones: a–e – the hydrolyzed substrate
is I-naphtylacetate; f – the hydrolyzed substrate is ace-
tylcholine iodide; a – control healthy caterpillars (with-
out infection); b – caterpillarsat the 3rd day p. i.; c –
caterpillars at the 7rd day p. i.; d – caterpillars at the 12th
day p. i.; e – caterpillars at the 15th day p. i.; E1—E8 –
multiple molecular esterase forms.
Ðèñ. 1. Ôðàêöèîííûé ñîñòàâ ýñòåðàç â áðþøíîé
íåðâíîé öåïî÷êå çäîðîâûõ è áîëüíûõ ìèêðîñïîðè-
äèîçîì ãóñåíèö îçèìîé ñîâêè: a–e – ãèäðîëèçóåìûé
ñóáñòðàò I-íàôãèëàöåòàò; f – ãèäðîëèçóåìûé ñóá-
ñòðàò àöåòèëòèîõîëèíèîäèä; à – êîíòðîëü (ãóñåíè-
öû áåç çàðàæåíèÿ); b – 3-é äåíü çàðàæåíèÿ; c – 7-é
äåíü çàðàæåíèÿ; d – 12-é äåíü çàðàæåíèÿ; e – 15-é
äåíü çàðàæåíèÿ; Å1—Å8 – ìíîæåñòâåííûå ìîëåêó-
ëÿðíûå ôîðìû ýñòåðàç.
Tab l e 1 . Predominant stages of microsporides development on the smears taken from A. segetum larvae tis-
sues at the time of biochemical analysis
Òàáëèöà 1 . Ïðåîáëàäàþùèå ôàçû ðàçâèòèÿ ìèêðîñïîðèäèé íà ìàçêàõ èç òêàíåé íàñåêîìûõ â ñðîêè
ïðîâåäåíèÿ áèîõèìè÷åñêèõ àíàëèçîâ
Stages of parasites development
meronts
Days post
infection
I II
sporonts sporoblasts spores
Control 0 0 0 0 0
3 3,4±0,68 0 0 0 0
5—7 0,8±0,37 5,4±0,89 0,4±0,22 0 0
10—13 0 0 4,1±1,07 0,4±0,24 62,0±10,7
15 0 0 0 0 90,0±7,07
T. M. Yefimenko, O. V. Sundukov, I. V. Issi 48
MI in insects causes the impair of some esterases-controlled physiological func-
tions. It is accompanied by such pathologies as ecdysis and metamorphosis disturbance,
decrease of fecondity; the complete castration and decreased resistance against unfa-
vourable environmental factors are more rare events (Issi, 1986).
We have found all the pathological patterns mentioned above in A. segetum and
M. brassicae larvae infected by V. antheraeae. If diseased larvae rested alive after meta-
morphosis, the butterflies from such larvae possessed a low reproductive possibili-
ties (Yefimenko et al., 1990; Yefimenko, 1992). The disturbances of ecdysis, metamor-
phosis, and diapause are usually due to juvenile hormone titers changed during MI-
infection (Issi, 1968; Metspalu, 1975, 1980; Metspalu, Hiyesaar, 1980) because of
parasite being able to synthesize this hormone (Fischer, Sanborn, 1962, 1964; Brand,
1972; Street, Brandfield, 1978). The esterases are known to take part in juvenile hor-
mone regulation (Hammock, 1985), so the interaction between hormonal disbalance
and esterases activity in insects after MI can be supposed.
It should be noted that host-parasite interactions during infection changed from
latent to clear antagonistic ones, these processes being detected both at cellular and
whole organism levels.
Non-specific esterases synthesized mostly in granular endoplasmatic reticulum are
then processed and go through Golgi apparatus; later they are transported from there to
lysosomes (Alberts et al., 1986). The inhibition of host lysosome system was described
as a pathological event especially specific for MI (Wiedner, Sibley, 1985; Sokolova,
1989). After Microsporida invasion into the host cell the endoplastic reticulum be-
comes shifted to the focus of pathogen development, the synthetic reactions being in-
creased (Vavra, 1965; Sprague, Vernik, 1969; Issi, 1983; Sokolova, 1989). In such a
way they assure the development of the parasite having no proper mitochondria. The
increase of carboxylesterase activity in our experiments may be due to the higher level
of synthesis processes during early MI period. At this stage there is also high oxygen
consumption by host's mitochondria because of parasite's increased ATP need (Soko-
lova, 1989). During vegetative development of V. antheraeae the body masses and the
3
3,5
4
4,5
5
5,5
6
6,5
7
7,5
0,1 0,2 0,3 0,4
Concentrate substrate nmol/min.mg
C
ar
bo
xy
le
st
er
as
e
ac
tiv
ity
, m
m
ol
/l
1. Control insects (larvae w ithout infection)
2. Larvae at the 10-th-15th day p.I.
Fig. 2. Carboxylesterase activity in the abdominal nerve chain of Agrotis segetum larvae, healthy and micro-
sporidiosis-diseased ones.
Ðèñ. 2. Àêòèâíîñòü êàðáîêñèëýñòåðàçû áðþøíîé íåðâíîé öåïî÷êè ó çäîðîâûõ è áîëüíûõ ìèêðîñïîðè-
äèîçîì ãóñåíèö îçèìîé ñîâêè.
Effect of microsporida infection on the esterases activities … 49
intensivity of respiration of Noctuidae larvae increased accompanied by higher resis-
tance to bacterial preparations (Yefimenko, 1989).
The V. antheraeae sporulation causes later the host cells damage and disintegra-
tion, the cell nuclei and mitochondria remain alive after destruction of other cell or-
ganellae (Issi, 1983, Sokolova, 1989); the dropped esterase activity in A. segetum larvae
at the 10—15th days p. i. may be due to such drastic intracellular changes. This stage of
host-parasite interactions is also marked with significant loss of larvae body mass, de-
creased respiration level of insects and of their isolated mitochondria, increased suscep-
tibility to bacterial infections (Yefimenko, 1989; Sokolova, 1989).
So, the increased esterase activities detected in these experiments in A. segetum lar-
vae during several early MI stages and the marked fall of such activities at the final
stage of the parasite development are patterns characteristic for MI pathogenesis; the
"increase of metabolism processes" necessary for complete developmental cycle of a
parasite generation is changed by the fall of all the host's physiological functions.
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Brand Th. Hormone und hormonartige Substanzen in Parasiten // Parasitenphysiologie. – 1972. – P. 201—
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Choudhury S. The nature of nonspecific esterases. A subunit concept // J. Histochem. Cytochem. – 1972. –
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Fisher F., Sanborn R. Production of insect juvenile hormone by the microsporidian parasite Nosema // Na-
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Fisher F., Sanborn R. Nosema as a source of juvenile hormone in parasitic insects // Biol. Bull. – 1964. –
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| id | nasplib_isofts_kiev_ua-123456789-9562 |
| institution | Digital Library of Periodicals of National Academy of Sciences of Ukraine |
| issn | 0084-5604 |
| language | English |
| last_indexed | 2025-12-07T16:30:23Z |
| publishDate | 2001 |
| publisher | Інститут зоології ім. І.І. Шмальгаузена НАН України |
| record_format | dspace |
| spelling | Yefimenko, T.M. Sundukov, O.V. Issi, I.V. 2010-07-02T14:15:22Z 2010-07-02T14:15:22Z 2001 Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars / T.M. Yefimenko, O.V. Sundukov, I.V. Issi // Вестн. зоологии. — 2001. — Т. 35, № 4. — С. 45-50. — Бібліогр.: 30 назв. — англ. 0084-5604 https://nasplib.isofts.kiev.ua/handle/123456789/9562 632.937 : 595.786 Microsporida infection of Agrotis segetum Schiffermuller 
 larvae causes numerous changes of separate fractions activities belonging to carboxylesterase isoenzyme 
 complex. Such shifts are found to correlate with parasite development stages, activities of several fractions being increased early after Vairimorpha antheraeae incorporation up to the beginning of sporogony. During intensive sporogony and spore forming the enzyme activities are proved to decrease. Activities of multiple esterase molecular forms at different microsporidiosis stages may be correlated with 
 cell pathology patterns and cell compartments damages taking part in the enzymes synthesis and transportation. These described changes may be also due to such Microsporidainduced pathological features 
 as lipid metabolism and hormone balance impair followed by decreased reproductive function. Сопоставлялись уровни суммарной эстеразной активности и активность отдельных эстеразных фракций в брюшных нервных цепочках здоровых и зараженных микроспоридией Vairimorpha antheraeae гусениц озимой совки Agrotis segetum Schiffermьller. Выявлено, что эстеразная активность увеличивается от момента внедрения паразита в ткани хозяина до начала спорогонии. Период наибольшей активности эстераз соответствует вегетативному размножению микроспоридий, а наименьшей - их массовому спорообразованию. Предполагается возможная взаимосвязь между изменением активности эстераз и такими проявлениями патогенеза микроспоридиоза насекомых, как нарушение липидного обмена, гормонального баланса и последующего снижения репродуктивных функций. Обсуждается сопряженность активности эстераз с особенностями патологии клетки и ее компартментов, учавствующих в синтезе и транспорте этих ферментов на разных этапах микроспоридиоза. en Інститут зоології ім. І.І. Шмальгаузена НАН України Экология Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars Влияние микроспоридиоза на активность эстераз у гусениц озимой совки Agrotis segetum Article published earlier |
| spellingShingle | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars Yefimenko, T.M. Sundukov, O.V. Issi, I.V. Экология |
| title | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars |
| title_alt | Влияние микроспоридиоза на активность эстераз у гусениц озимой совки Agrotis segetum |
| title_full | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars |
| title_fullStr | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars |
| title_full_unstemmed | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars |
| title_short | Effect of Microsporida Infection on the Esterases Activities in Agrotis segetum Caterpillars |
| title_sort | effect of microsporida infection on the esterases activities in agrotis segetum caterpillars |
| topic | Экология |
| topic_facet | Экология |
| url | https://nasplib.isofts.kiev.ua/handle/123456789/9562 |
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