importance of epicuticular wax cover for plant/insect interactions

POLISH JOURNAL OF ECOLOGY
(Pol. J. Ecol.)
61
1
183–186
2013
Research note
Agnieszka WÓJCICKA
University of Natural Sciences and Humanities in Siedlce, Department of Biochemistry and Molecular
Biology, Prusa 12B, 08-110, Siedlce, Poland,
e-mail: [email protected]
IMPORTANCE OF EPICUTICULAR WAX COVER
FOR PLANT/INSECT INTERACTIONS: EXPERIMENTS
WITH CEREAL APHIDS
ABSTRACT: The epicuticular wax is the
contact point between plants and the environment
and plays a crucial role in mediating biotic and
abiotic interactions. The associations between the
content of epicuticular waxes, on surface plants of
winter triticale with their acceptance by the grain
aphid Sitobion avenae and bird cherry -oat aphid
Rhopalosiphum padi were studied. In general,
waxy genotype DED 1137 of winter triticale was
less accepted by the cereal aphids than the wax
less one (RAH 366). The waxy genotype decreased
density of cereal aphids, prolonged maturity and
decreased fecundity. Moreover, the comparison
of abundance, development and fecundity of the
aphid species on the triticale genotypes proved
that tested genotypes differed in susceptibility
to Sitobion avenae and Rhopalosiphum padi. The
importance of the epicuticular wax compounds
in the acceptance of plants by the aphids is discussed. The results indicated that aphids fed on
waxy plants showed longer time of the prereproductive period and much lower total fecundity.
Furthermore, waxy genotype reduced value of the
cumulative aphid index and percentage of infested
plants.
KEY WORDS: epicuticular waxes, plant/insect interactions, triticale, Sitobion avenae, Rhopalosiphum padi
journal 33.indb 183
The plant surface is bordered by a cuticle,
which plays an important role in the physiology and autecology of the plant, but also
serves as the first contact zone in interactions
of plants with other organisms (R o st ás et al.
2008, Ko ch et al. 2009, Yi n et al. 2011). The
cuticle is composed of the cuticular layer and
the cuticle proper, which is covered by epicuticular waxes (Je tte r et al. 2007). The layer of
the epicuticular waxes may contain aliphatic
components, sugars and amino acids as well
as secondary metabolites (E ige nbro d e and
E sp el ie 1995, S cho on hove n et al. 2005,
Ko ch and B ar t h l ott 2006). Although the
primary role of epicuticular waxes is to prevent uncontrolled water loss, they might also
contribute to plant-insect interactions (Mü ll e r 2006, Pr ü m et al. 2012). They also show
a strong influence on aphid behaviour and
physiology which results in a reduction of the
aphid growth and development (Wój c i ck a
2007, 2009, 2011). Moreover, examples of epicuticular wax – herbivore interactions have
been identified and characterized in Eucalyptus globulus Labill (Bren nan and Wei nb au m 2001), Hordeum vulgare L. (Tsu mu k i
et al. 1989), Sorghum bicolour (L.) Moench
(Nwan z e et. al. 1992) and Triticum aestivum
L. (L owe et al. 1985).
2013-04-30 10:05:52
184
Agnieszka Wójcicka
The aim of our study was to compare the
effect of waxes on the acceptance of triticle
genotypes by the cereal aphids.
The experiments used two winter triticale
genotypes varied in wax layer (DED 1137 –
waxy covered and RAH 366 – wax less). Seed
samples of triticale were obtained from the
Plant Breeding and Acclimation Institute
(IHAR) in Radzików/Błonie near Warsaw
(Poland). A population study of two species
of aphids on the studied triticale plants were
estimated in natural field conditions at IHAR.
The grain aphids Sitobion avenae (Fabricius, 1775) (Hemiptera: Aphididae) and the
bird cherry-oat aphids Rhopalosiphum padi
(Linnaeus 1758) (Hemiptera: Aphididae)
were studied in the experiments.
The cereal aphids’ density on the studied
triticale was estimated according to the method described by Wratten et al. (1979) and
Ly kouressis (1984). Entomological observations were carried out from sixth leaf stage
to the stage of medium milk (G.S. 47-75).
The growth stages of winter triticale determined according to Tott man and Bro a d
scale (1987). The field observations were performed on 3.0 × 3.0 m experimental plots.
The population of the cereal aphids was studied on three replicated plots per genotype of
plant. Technique of counting the aphids on 50
randomly selected plants, diagonally across
the field was applied. Results of the observations were used to calculate the total number
of aphids living on an individual plant and
the percentage of infested plants.
Two selected genotypes of winter triticale: waxy (DED 1137) and wax-less (RAH
366) were examined for their antibiosis to
cereal aphids in the field at IHAR Radzików.
Adult apterous females were caged individually on flag leaves of the tested triticale genotypes and allowed to deposit nymphs. After
24 hours, one nymph remained on a single
flag leave and other offspring and the adult
were removed. When the nymph matured
and began producing offspring, the offspring
were counted and removed daily. The prereproductive period and daily fecundity were
estimated (L e s z cz y ńsk i 1996).
Differences in the aphid abundance and
growth and development in the conducted experiments were subjected to one-way
ANOVA, followed by Duncan’s test.
The obtained results showed that the
studied waxy genotype (DED 1137) of triticale was less accepted by the cereal aphids
than the wax less one (RAH 366). On the
basis of a field observations it was found that
the waxy genotype (DED 1137) was attacked
less by the cereal aphids, S. avenae and R. padi
than the wax-less one (RAH 366). Both aphid
species were characterized by higher population density and percentage of infested plants
on blades of RAH 366 genotype in comparison with DED 1137 genotype one. It was also
found that the higher number of aphids and
the percentage of plants inhabited for triticale
were obtained by the population of S. avenae,
the lower by R. padi (Fig. 1). Antibiosis experiment of the studied plants showed similar
Fig. 1. Occurrence of the cereal aphids on the studied plants in the field (A – population density, B –
percentage of plants infested). Values signed by various letters are significantly different at P £0.05
(Duncan’s test).
journal 33.indb 184
2013-04-30 10:05:52
12
10
8
6
A
a
a
b
waxy
wax less
b
4
2
0
S. avenae
R. padi
4
Daily fecundity per female
Prereproductive period (days)
Influence of plant surface waxes on interactions with aphids.
B
waxy
wax less
a
3
2
185
b
c
c
1
0
S. avenae
R. padi
Fig. 2. Prereproductive period (A) and daily fecundity (B) of the cereal aphids feeding on the studied
plants in the field. Values signed by various letters are significantly different at P £0.05 (Duncan’s test).
trends. The study showed that aphids, which
occurred on plants of waxy genotype, were
characterized by a longer prereproductive period and by lower values of daily fecundity,
than on wax less one (Fig. 2).
Degree of the preference of the studied
genotypes was strongly related to the epicuticular wax layer of the plants. She phe rd
et al. (1999) reported that the preference of
raspberry aphids (Amphorophora idaei Börner) for older leaves of raspberry genotype
Jawel may be related to lower wax coverage
on these leaves relative to the younger emerging leaves. This type of preference has previously been shown by spotted alfalfa aphids,
Therioaphis maculate (Buckton), in the foliar
canopy of alfalfa (Medicago sativa L.).
The performed experiments also demonstrated that the waxy genotype clearly affected biology of the cereal aphids. Detailed
antibiosis tests showed prolongation of prereproductive period and reduction of daily
fecundity of the aphids fed on the waxy genotype. The obtained results indicated that
wax less genotype was better host for cereal
aphids. The results were similar as the reported by others. For example, epicuticular waxes
have been well studied in Brassica crops, and
evidence shown that wax blooms on glaucous
surfaces reduce adult and larval feeding by
some herbivores (Eigenbro de and E sp eli e 1995, E igenbro de et al. 2000, Ag r aw a l
et al. 2009).
Moreover, volatiles emanating from plant
surface waxes can act as attractants or repellents (St äd ler and R eifenrat h 2009, Hi l k-
journal 33.indb 185
e r and Me i ne rs 2011). After an aphid lands
on a plant, various cues on the surface of
plants, such as epicuticular wax structure and
chemical composition, can influence aphid
behaviour, growth and development. For
example, removal of the surface waxes with
chloroform from seedlings of Sorghum bicolar (L.) caused their acceptance by nymphs
of Locusta migratoria L. (Wo o d he a d 1983).
Hexane extracts of surface lipids from resistant rice cultivars deterred feeding of the
brown planthopper, Nilaparvata lungens
(Stäl) (Wo o d he a d and Pa d g ham 1988).
Summing up the results presented here
suggest that epicuticular waxes of the triticale play an important role in its acceptance
by the grain aphid and bird cherry-oat aphid.
The results indicated that aphids fed on waxy
plants showed longer time of the prereproductive period and much lower total fecundity. Furthermore, waxy genotype reduced
value of the cumulative aphid index and percentage of infested plants.
REFERENCES
Ag rawa l A.A., Fishb ein M., Jetter R .,
Sa lminen J-P., G oldstein J.B. 2009 –
Phylogenetic ecology of leaf surface traits in
the milkweeds (Asclepias spp.): chemistry,
ecophysiology, and insect behaviour – New
Phytol. 183: 848–86
Brennan E.B., Weinb aum S.A. 2001 – Stylet
penetration and survival of three psyllid species on adult leaves and ‘waxy’ and ‘de-waxed’
juvenile leaves of Eucalyptus globules – Entomol. Exp. Appl. 100: 355–363.
2013-04-30 10:05:53
186
Agnieszka Wójcicka
Eigenbro de S.D., E sp elie K.E. 1995 – Effects of plant epicuticular lipids on insect herbivores – Ann. Rev. Entomol. 40: 171–194.
Eigenbro de S.D., Kab a lo N.N., Rut le dge
C.A. 2000 – Potential of reduced waxbloom
oilseed brassica for insect pest resistance – J.
Agric. Urban Entomol. 17: 53–63.
Hi l ker M., Meiners T. 2011 – Plants and
insect eggs: How do they affect each other? –
Phytochemistry, 72: 1612–1623.
Jetter R ., Kunst L., Samuels A.L. 2007 –
Composition of plant cuticular waxes (In: Biology of the plant cuticle, Eds: M. Riederer, C.
Müller) – Blackwell, Oxford, pp. 145–181.
Ko ch K., B ar t h lott W. 2006 – Plant epicuticular waxes: chemistry, form, function and selfassembly – Nat. Prod. Comm. 1: 1067–1072.
Ko ch K., Bhushan B., B ar t h lott W. 2009
– Multifunctional surface structures of plants:
An inspiration for biomimetics – Prog. Mater.
Sci. 54: 137–178.
L eszczy ńsk i B. 1996 – Kurs praktyczny w zakresie chemicznych interakcji owady-rośliny
na przykładzie mszyc (Aphidoidea) [Practical manual for chemical interactions betwen
insects and their host plants on the example
of Aphidoidea] – WSRP, Siedlce, pp. 205–215
(in Polish).
L owe H.J.B., Mur phy G.J.P., Parker M.L.
1985 – Non-glaucousness, a probable aphidresistance character of wheat – Ann. Appl.
Biol. 106: 555–560.
Ly kouresis D. 1984 – A comparative study of
different aphid population parameters in assessing resistance in cereals – Z. Ang. Entomol. 97: 77–84.
Mü l ler C. 2006 – Plant-insect interactions on
cuticular surface. (In: Biology of plant cuticle,
Eds: M. Riederer, C. Müller) – Blackwell Publishing, Oxford, pp. 398–422.
Nwanze K. F., Pr ing R .J., Sre e P.S., But ler D.R ., R e ddy Y.V.R ., S oman P. 1992
– Resistance in sorghum to the shoot fly,
Atherigona socata: Epicuticular wax and wetness of the central whorl leaf of young seedlings – Ann. Appl. Biol. 120: 373–382.
Pr üm B., S eidel R ., B ohn H. F., Sp e ck T.
2012 – Plant surface with cuticular folds are slippery for beetles – J. Royal Society, 9: 127–135.
R ost ás M., Ruf D., Z abka V. 2008 – Plant
surface wax affects parasitoid’s response to
host footprints – Naturwissenschaften, 95:
997–1002.
S cho on hoven L.M., Van L o on J.J. A.,
Dicke M. 2005 – Plant Chemistry: Endless
Variety. Insect-Plant Biology – Oxford Uni-
versity Press, Chapter 4, Chapman and Hall,
London UK, pp. 49–86.
Shepherd T., R ob er ts on G.W., Gr if f it hs
D.W., Birch A.N.E. 1999 – Epicuticular
wax ester and triacyloglycerol composition in
relation to aphid infestation and resistance in
red raspberry (Rubus idaeus L.) – Phytochemistry, 52: 1255–1267.
St äd ler E., R eifenrat h K. 2009 – Glucosinolates on the leaf surface perceived by insect herbivores: review of ambiguous results
and new investigations – Phytochem Rev. 8:
207–225.
Tott man D.R ., Bro ad H. 1987 – The decimal
code for the growth stages of cereals, with illustrations – Ann. Appl. Biol. 93: 221–234.
Tsumu k i H., Kanehis a K., Kawad a K.
1989 – Leaf surface wax as a possible resistance factor of barley to cereal aphids – Appl.
Entomol. Zoology 24: 295–301.
Wo o d he ad S. 1983 – Surface chemistry of Sorghum bicolor and its importance in feeding
by Locusta migratoria – Physiol. Entomol. 8:
345–352.
Wo o d he ad S., Padg ham D.E. 1988 – The
effect of plant surface characteristics on resistance of rice to the brown planthopper,
Nilaparvata lugens – Entomol. Exp. Appl. 47:
15–22.
Wój cicka A. 2007 – Effect of triticale surface
compounds on growth and development of cereal aphids – Aphids and Other Homopterous
Insects, 13: 191-197.
Wój cicka A. 2009 – Wpływ woskowości genotypów pszenżyta ozimego na parametry populacyjne mszyc zbożowych [Effect of waxes and
waxless triticale genotypes on survival and
fecundity of the cereal aphid species] – Prog.
Plant. Prot./Post. Ochr. Rośl. 49: 157–160 (in
Polish).
Wój cicka A. 2011 – Wpływ wosków powierzchniowych pszenżyta ozimego na elementy
biologii mszycy czeremchowo-zbożowej [Effect of surface waxes of winter triticale on
the biology of bird cherry-oat aphid Rhopalosiphum padi] – Prog. Plant. Prot./Post. Ochr.
Rośl. 51: 1590-1594.
Wratten S.D., L e e G., Ste vens D.J. 1979 –
Duration of cereal aphid populations and the
effects on wheat yield and quality – The BCPC
Pestsand Diseases, pp. 1–8.
Yin Y., Bi Y., C hen S., L i Y., Wang Y.,
G e Y., Ding B., L i Y., Zhang Z. 2011 –
Chemical composition and antifungal activity
of cuticular wax isolated from Asian pear fruit
(cv. Pingguoli) – Sci. Hort. 129: 577–582.
Received after revision October 2012
journal 33.indb 186
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