Role of Chitinase in Plant Defense
Plants represent the major component of biota and have the capability to synthesize their food through the process of photosynthesis. Physiological and environmental changes affect their health and make them vulnerable to variety of diseases thus directly or indirectly affect other components of ecosystem. A large number of environmental issues are linked with the eradication of plant diseases with chemical compounds. Most of these diseases are caused by fungal and insect pathogens. Chitin is the main structural component of these organisms and thus the enzyme responsible to hydrolyze chitin content are receiving attention in regard to their development as biopesticides or chemical defense proteins in transgenic plants and in microbial biocontrol agents. Therefore, understanding the overview of chitinase will provide a basis for improving the pathogenic activity of potential biocontrol strains, for developing novel biological control strategies and for exploring their roles in the plant defense. The present review describes the properties of chitinase with respect to plant health improvement.
May 15, 2010; Accepted: May 29, 2010;
Published: September 24, 2010
A multitude of microorganisms are the pathogens of plant species worldwide
(Hopkins and Purcell, 2002). Crop losses due to pathogens
are often more severe in developing countries (e.g., in cereals, 22 percent
of total loss) and is it is roughly estimated an equal to loss of 200-300 US$
billion money on the basis of data provided by Oerke et
al. (1994). The most regular methods used to protect plants rely on
the chemical compounds those are available in various forms such as insecticide,
fungicide etc. The major problem associated with the use of such compounds is
the loss natural microflora of the soil which could be involved in the protection
of plants against infection caused by secondary pests. Besides this, the generation
of insecticidal resistance, safety risks for human and wildlife, contamination
of groundwater and riparian habitats and decrease in biodiversity are other
key issues which were commonly seen with the advent these compounds and need
to be thought prior to their use. The public concern over the harmful effects
of these chemical compounds on the environment and human health has enhanced
the search for safer, environment friendly control alternatives. Thus control
of plant pathogens like fungus and insect by the application of biological agents
holds great promise as an alternative to chemicals in this context.
Plants are equipped with a variety of defense mechanisms to protect themselves
against the attack of pathogens. Some of these are constitutive while others
are induced upon the attack by pathogens. The interaction between plants and
pathogens induces a variety of defense mechanisms which includes cell wall strengthening
(Bradley et al., 1992), de novo production of
antimicrobial compounds (pathogenesis response proteins and secondary metabolites
(Hammerschmidt, 1999; Misra and
Gupta, 2009; Gupta et al., 2010a) and rapid
localized cell death etc. (Alverez, 2000). In the category
of pathogenesis related proteins chitinase and glucanse (Sela-Buurlage
et al., 1993) have very important role since they attack directly
on the fungal and insect structural component. Besides these two, other enzymes
of plant secondary metabolite pathway including Chalcone synthase and isomerase
(Hahlbrock et al., 1981) Phenylalanine ammonia
lyase (Cramer et al., 1985) are also significant
due to antimicrobial nature of secondary metabolites.
Chitinase attack on chitin molecules which are the main structural component
in fungal cell wall and insects skeleton. In nature chitin is found to
be in the form of complex with other biomolecules such as carbohydrates and
proteins (Sietsma and Wessels, 1979). In Sponges it
forms a complex with silica (Ehrlich et al., 2007).
In arthropods, chitin is an integral part of skeleton (Merzendorfer
and Zimoch, 2003) and digestive tract lining (Lehane,
1997). It is known to be present in the eggshell (Mansfield
et al., 1992) and microfilarial sheath (Fuhrman
and Piessens, 1985) of nematodes also.
In these organisms chitin metabolism is directly controlled by the activity
of Chitin Synthases (CS) and Chitin Hydrolase (CH). Three types of chitin synthase
were observed in Saccharomyces cerevisiae: CS I which is involved in
repair functions at the end of cytokinesis; CS II, participating in the synthesis
of primary septum and CS III, responsible for the formation of the ring or bud
scar (Henar et al., 1999). Besides these enzymes,
the recycling of cell wall components also depends upon the activities of a
range of hydrolytic enzymes found intimately associated with the fungal cell
wall. Most of the fungal cell wall hydrolases characterized to date belong to
chitinase, glucanase and transglycosylase family (Adams,
2004). It is generally believed that chitinases are commonly found in organisms
which are possessing chitin as a structural component.
The enzyme chitinase (EC 184.108.40.206) hydrolyzes the chitin polymer into to N-acetyl
glucosamine by either endo or exo cleavages of the 1-3 and 1-4 bond (Van
Aalten et al., 2000). The enzyme is classified into several categories
on the basis of their isolation, structural and functional characteristics.
It belongs to families 18 and 19 of glycosyl hydrolases (Henrissat
and Davies, 1997) which are key enzymes for carbohydrate metabolism (Henrissat,
1991). Most of the prokaryotic and eukaryotic chitinases are grouped in
Family 18 whereas chitinase of higher plants and some of the Gram positive bacteria
like Streptomyces are included into Family 19 (Cohen-Kupeic
and Chet, 1998). These two families contain both endo and exo chitinases.
Endochitinases cleave randomly in the chitin chain while exochitinases cleave
off chitobiose (GlcNAc)2 or chitotriose (GlcNAc)3 from
the reducing or non reducing end of the chitin chain (Suzuki
et al., 1999). In addition to endo- and exochitinases, chitin degrading
organisms contain chitobioses (N-acetyl β-glucosaminidases), a third class
of chitinolytic enzymes that convert GlcNAc dimers into their monomers (Tews
et al., 1996a, b).
Chitinase was described for the first time in 1911 by Bernard in orchid bulbs
in which it behaves like a thermo sensitive and diffusible antifungal factor.
In animals the presence of chitinase was marked in snails by Flach
et al. (1992). Since then these molecules are unanimously considered
as a tool to strengthen plant immune response against a variety of pathogens
by various workers owing to its property to lyse fungal cell wall and components
of insect exoskeleton. Besides this, dramatic increase in chitinase levels by
numerous abiotic agents (ethylene, salicylic acid, salt solutions, ozone, UV
light) and by biotic factors (fungi, bacteria, viruses, viroids, fungal cell
wall components and oligosaccharides) also proved their role in plant defense
response (Punja and Zhang et al., 1993; Gupta
et al., 2010b).
In addition to it, insect pathogenic fungi have considerable potential for
the biological control of insect pests which apparently overcome physical barriers
of the host by producing multiple extracellular enzymes including chitinolytic
enzymes, which help to penetrate the cuticle and facilitate infection (Herrera-Estrella
and Chet, 1999).
Source of chitinase: Chitinolytic microbes occur widely in nature and
are preferred source of chitinase because their low production cost, easy availability
of raw materials for their cultivation. The ability of a microbial community
to degrade chitin is also important for the recycling of Nitrogen in the soil
(Chandran et al., 2007). Bacteria like Serratia
marcescens, Xanthomonas maltophilia, Stenotrophomonas maltophilia
and Paenibacillus illinoisensis (Kobayashi et
al., 1995; Zhang and Yuen, 2000; Jung
et al., 2003, respectively) etc. have been proved as potent chitinolytic
bacterial biocontrol agents while Myrothecium verrucavia, (Govindsamy
et al., 1998) and Trichoderma sp. (Howell,
2003) were found as main source of chitinase among fungi. In insects and
nematodes chitinases were found to be involved in molting process during their
development (Adam et al., 1996). Chitinases were
also reported in gastric juices of human being (Paoletti
et al., 2007) where they were being thought to be involved catabolic
activities. Further chitinase activity was also detected in human serum (Escott
and Adams David, 1995) and found very similar to plant chitinases those
are related in the process of inflammation and pathogen resistance (Chupp
et al., 2007).
Besides this, a number of proteins demonstrating chitinolytic activity were
also identified in plants. These proteins were isolated from all organs of plants
and tissues including apoplast and vacuoles. In plants these represent a large
and diverse group of enzymes which differ not only in spatial and temporal localization,
but also in molecular structure and substrate specificity (Brunner
et al., 1998). The apoplastic chitinases play a role in the early
stage of pathogenesis. They were thought to be helpful in the generation elicitor
molecules which are involved in the transfer of information from hyphae to the
intercellular space (Gerhardt et al., 1997).
While vacuolar chitinases degrade the newly synthesized chains of chitin and
thus repress fungal growth (Collinge et al., 1993).
Moreover the vacuolar chitinases were more active against crystalline chitin,
whereas apoplastic forms were found to be more active towards soluble chitin
(Collinge et al., 1993). In addition to it, the
chitinase gene was also expressed during seed developmental stages (Wu
et al., 2001) and fruit ripening process (Robinson
et al., 1997) which signifies its relation with plant defense.
Chitinase in plant defense: The exploitation of chitnase with respect
to plant defense can be done by a variety of ways. The enzyme can also be used
in free or immobilized form to kill fungi and insects in affected areas. The
micorganisms producing chitinase can also be used in soil as rhizobacterial
population or alternatively the gene encoding chitinase can be inserted in the
native microflora of soil. Sundheim et al. (1988)
inserted chitinase of Serratia marcescens into Pseudomonas fluorescens
which is normally present as normal flora of soil and obtained resistance
in radish plants against Fusarium oxysporum infection. Chernin
et al. (1997) were also able to decrease the onset of Rhizoctonia
solani infection in cotton plants by using recombinant E. coli in
rhizosphere expressing chitinase gene of Enterobacter agglomerans. Kirubakaran
and Sakthive (2007) also demonstrated a broad-spectrum antifungal activity
in Escherichia coli expressing chitinase gene of barley against Botrytis
cinerea (Blight of Tobacco), Pestalotia theae (Leaf Spot of Tea),
Bipolaris oryzae (Brown Spot of Rice), Alternaria sp. (Grain Discoloration
of Rice), Curvularia lunata (Leaf Spot of Clover) and Rhizoctonia
solani (Sheath Blight of Rice).
Besides these, the phenomena of synergism (the interaction of organisms or
proteins or elements that when combined, produce a total effect that is greater
than the sum of the individual element contributions) can be meaningful to fasten
the killing of pathogenic organism. Lorito et al.
(1993a) demonstrated that chitinolytic enzymes from Trichoderma harzianum
Rifai and the closely related fungus Gliocladium virens J.H. Miller,
J.E. Giddens and A.A. Foster act synergistically to inhibit the growth of a
variety of plant pathogenic fungi. Lorito et al.
(1993b) also demonstrated that bacterial biocontrol strains may also act
synergistically with chitinolytic enzymes to inhibit plant pathogenic fungi.
They determined strong synergism between Enterobacter cloacae and chitinolytic
enzymes of Trichoderma harzianum and found that chitinolytic enzymes
enhance the bacterial growth and their ability to bind to the fungal hyphae.
Mauch et al. (1988) observed rapid killing of
fungal cells by combining chitinases with β-glucanase. In addition to above
synergistic effects of a β-1, 6-glucanase and chitinase from Trichoderma
harzianum on the hydrolysis of fungal cell walls had been also reported
(De La Cruz et al., 1992; Misra
and Gupta, 2009).
Alternatively, the production of transgenic plants over expressing chitinase
gene had been also demonstrated to get resistance against pathogens. It was
achieved by manipulating the activity of extracellular enzymes through construction
of over producing mutants, enzyme negative mutants or even transgenic plants
expressing the enzyme. Brogue et al. (1991) showed
an increased ability to survive in tobacco plants in Rhizoctonia solani
infected soil and delayed development of disease symptoms in tobacco seedlings
by expressing chitinase. Dunsmuir et al. (1993)
also confirmed the reduction in occurrence of Rhizoctonia solani infection
in transgenic tobacco plants in which two bacterial chitinase gene were over
expressed at high levels. Besides the immunity against fungal pathogen, overexpression
of chitinase was also found be effective to raise resistance plants against
bacterial pathogens, salinity stress and heavy metals stress (Dana
et al., 2006).
It is not only the microbial chitinase but the plant chitinase had been also
used to improvement plant health by various workers. In oil seed rape (Brassica
napus var. oleifera) the importance of chitinase was also shown by various
researchers. Grison et al. (1996) were able to
increase tolerance in these plants against Cylindrosporium concentricum,
Phoma lingam, Sclerotinia sclerotiorum infection by expressing chitinase
gene. Transgenic wheat plants expressing chitinase of plants were also raised.
Oldach et al. (2001) observed enhanced resistance
to powdery mildew infection in wheat upon expression of chitinase of barley.
In another experiment the transgenic wheat lines carrying a combination of a
wheat β-1, 3- glucanase and chitinase exhibited delayed symptoms of Fusarium
Head Blight (Anand et al., 2003).
Chitinases were also used as a method to control insect and pest population
which indirectly suggests its role in plant defense. Lawrence
and Novak (2006) showed that the expression of poplar chitinase in tomato
leads to inhibition of development in colorado potato beetle. Lipmann
et al. (2009) investigated the secretome of a tobacco cell suspension
by a combined proteomic and metabolomic approach and identified chitinase alongwith
peroxidase and beta- 1,4,-xylosidase among the major defense protein. Wasano
et al. (2009) observed that the presence of 56-kDa defense protein
consisted of chitin like domain in mulberry latex was responsible to provide
strong insect resistance to lepidopteran caterpillars, including the cabbage
armyworm, Mamestra brassicae and the Eri silkworm, Samia ricini.
Similarly Kitajima et al. (2010) also reported
two chitinase like proteins LA-a and LA-b (latex abundant) from the latex of
Mulberry (Morus sp.) and found them associated with insecticidal activities
against larvae of Drosophila melanogaster.
Chitinases were also isolated from insects and they were also found to hold
equal promise in the improvement of plant defense. Chitinases have been isolated
from the tobacco hornworm and several other insect species. Ding
et al. (1998) developed transgenic tobacco plants expressing insects
chitinases and found them resistant to infection of tobacco budworm Heliothis
virescens. Transgenic plants constitutively expressing hornworm chitinase
had been generated and found to be resistant against infection (Kramer
and Muthukrishnan, 1997). Besides this a recombinant baculovirus expressing
chitinase of hard tick (Haemaphysalias longicornis) had been also used
as a bio acaricide for tick control by Assenga et al.
Although the relationship between chitinase production and generation of reactive
oxygen species is not clear, yet some experiments showed that these two both
act in a co-ordinated way to protect plant against a challenge. Ghaouth
et al. (2003) treated the peach fruit with UV-C light and noted a
rapid induction of chitinase, beta-1,3-glucanase and phenylalanine ammonia lyase
(PAL) activities and concluded that the response of peach fruit to elicitor
treatment is similar to that seen in other plant-elicitors interactions and
suggested the involvement of peach biochemical defense responses in UV-C-mediated
disease resistance. Xu et al. (2008) observed
significant stimulation in the activities of chitinase, beta-1,3-glucanase,
catalase (CAT), peroxidase (POD) genes in seeds upon infection with Pichia
membranaefaciens, Cryptococcus laurentii, Candida guilliermondii
and Rhodotorula glutinis and suggested that antioxidant defense response
may be involved in the mechanisms of microbial biocontrol agents against fungal
pathogen. Gorii et al. (2009) found appearance
of acidic chitinases and basic chitinase along with basic constitutive 1,3-beta-glucanases
in Annona fruits by high levels of CO2 and upon storage at chilling
temperature (6°C). They finally suggested that these modifications in the
proteome level were to enhance the synthesis of cryoprotectant proteins in
vivo. Kumar et al. (2009) also observed enhanced
level of chitinase activity along with increased level of Reactive Oxygen Species
(ROS), increase in the expression level of several defense-related genes, activation
of some pathogenesis response protein, increase in the level of enzymes of the
terpenoid pathway in various tissues as well as in the medium surrounding the
roots of transformants and hypothesized that elevated defensive state of the
transformants act synergistically with the potent transgene encoded chitinase
activity to confer a strong resistance to Rhizoctonia solani infection.
Chitinases are prime molecules of interest for plant pathologist and can be utilized by variety of ways to improve plant health. These enzymes are classified into various types on the basis of their structural and functional properties. One class of chitinase was not found equally active against chitin of another source. Thus there is a need to isolate and identify chitinase of broad spectrum activity. In addition to it, reactions conditions of the enzyme must be known prior to its use in open environment and in affected site. Besides these, there is an utmost requirement to enhance the basal level of chitinase production by using recent approaches of genetic engineering. Therefore a coordinated strategy by using above plans may be meaningful to assess the full potential of chitinolytic organisms in rendering plant defense.
Adam, R., B. Kaltmann, W. Rudin, T. Friedrich and T. Marti, 1996. Identification of chitinase as the immunodominant filarial antigen recognized by sera of vaccinated rodents. J. Biol. Chem., 271: 1441-1447.
Adams, D.J., 2004. Fungal cell wall chitinases and glucanases. Microbiology, 150: 2029-2035.
CrossRef | Direct Link |
Alverez, M.E., 2000. Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol. Biol., 44: 429-442.
PubMed | Direct Link |
Anand, A., T. Zhou, H.N. Trick, B.S. Gill and W.W. Bockus et al., 2003. Greenhouse and field testing of transgenic wheat plants stably expressing genes for thaumatin‐like protein, chitinase and glucanase against Fusarium graminearum. J. Exp. Bot., 54: 1101-1111.
CrossRef | Direct Link |
Assenga, S.P., M. You, C.H. Shy, J. Yamagishi and T. Sakaguchi et al., 2006. The use of a recombinant baculovirus expressing a chitinase from the hard tick Haemaphysalias longicornis and its potential application as a bioacaricide for tick control. Parasitol. Res., 98: 111-118.
Bradley, D.J., P. Kjellbomand and C.J. Lamb, 1992. Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell, 70: 21-30.
Brogue, K., I. Chet, M. Holliday, R. Cressman and P. Biddle et al., 1991. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science, 254: 1194-1197.
CrossRef | Direct Link |
Brunner, F., A. Stintzi, B. Fritig and M. Legrand, 1998. Substrate specificities of tobacco chitinases. Plant J., 14: 225-234.
Chandran, S., B. Parameswaran and A. Pandey, 2007. Microbial Chitinases: Effective Biocontrol Agents. In: Biological Control of Plant Diseases, Chincholkar, S.B. and K.G. Mukerji (Eds.) The Haworth Press, Inc., New York, pp: 381-382.
Chernin, L.S., L. De-la-Fuente, V. Sobolev, S. Haran, C.E. Vorgias, A.B. Oppenheim and I. Chet, 1997. Molecular cloning, structural analysis and expression in Escherichia coli of a chitinase gene from Enterobacter agglomerans. Applied Environ. Microbiol., 63: 834-839.
Direct Link |
Chupp, G.L., C.G. Lee, N. Jarjour, Y.M. Shim and C.T. Holm et al., 2007. A chitinase like protein in the lung and circulation of patients with severe asthma. New Engl. J. Med., 357: 2016-2027.
Cohen-Kupiec, R. and I. Chet, 1998. The molecular biology of chitin digestion. Curr. Opin. Biotechnol., 9: 270-277.
CrossRef | PubMed |
Collinge, D.B., K.M. Kragh, J.D. Mikkelsen, K.K. Nielsen, U. Rasmussen and K. Vad, 1993. Plant chitinases. Plant J., 3: 31-40.
Cramer, C.L., J.N. Bell, T.B. Ryder, J.A. Bailey and W. Schuch et al., 1985. Co-ordinated synthesis of phytoalexin biosyntheyic enzymes in biologically-stressed cells of bean (Phaseolus Vulgaris L.). The Embo J., 4: 285-289.
Dana, M.D.L.M., J.A. Pentor-Toro and B. Cubero, 2006. Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol., 142: 722-730.
De La Cruz, J., A. Hidalgo-Gallego, J.M. Lora, T. Benitez, J.A. Pintor-Taro and A. Llobell, 1992. Isolation and characterization of three chitinase in Trichoderma harzianum. Eur. J. Biochem., 206: 859-867.
Ding, X., B. Gopalakrishnan, L.B. Johnson, F.F. White and X. Wang et al., 1998. Insect resistance of transgenic tobacco expressing an insect chitinase gene. Transgenic Res., 7: 77-84.
Dunsmuir, P., W. Howie, E. Newbigin, L. Joe and E. Penzes et al., 1993. Resistance to Rhizoctonia solani in Transgenic Tobacco. In: Advance in Molecular Genetics of Plant-Microbe Interactions, Nester E.W. and D.P.S Verma (Eds.). Kluwer Academic Publishers, Netherlands, pp: 567-570.
Ehrlich, H., K. Manfred, H. Thomas, S. Paul and K. Christiane et al., 2007. First evidence of the presence of chitin in skeletons of marine sponges. Part II. Glass sponges (Hexactinellida: Porifera). J. Exp. Zool. B Mol. Dev. Evol., 308: 473-483.
Escott, G.M. and J. Adams David, 1995. Chitinase activity in human serum and leukocytes. Infect Immun., 63: 4770-4773.
Flach, J., P.E. Pilet and P. Jolles, 1992. What's new in chitinase research? Experientia, 48: 701-716.
CrossRef | Direct Link |
Fuhrman, J.A. and W.F. Piessens, 1985. Chitin synthesis and sheath morphogenesis in Brugia malayi microfilariae. Mol. Biochem. Parasitol., 17: 93-104.
Gerhardt, L.B., G. Sachetto-Martins, M.G. Contarini, M. Sandroni and R.D.P. Ferreira et al., 1997. Arabidopsis thaliana class IV Chitinase is early induced during the interaction with Xanthomonas campestris. FEBS Lett., 419: 69-75.
Ghaouth, E.I., C.L. Wilson and A.M. Callahan, 2003. Induction of chitinase, beta-1,3-glucanase and phenylalanine ammonia lyase in Peach fruit by UV-C treatment. Phytopathology, 93: 349-355.
Gorii, O., M.T. Sanchez-Ballesta, C. Merodio and M.I. Escribano, 2009. Regulation of defense and cryoprotective proteins by high levels of CO2 in Annona fruit stored at chilling temperature. J. Plant Physiol., 166: 246-258.
Govindsamy, V., K.R. Gunaratna and R. Balasubramanian, 1998. Properties of extracellular chitinase from Myrothecium verrucaria, an antagonist to the groundnut rust Puccinia arachidis. Can. J. Plant Pathol., 20: 62-68.
CrossRef | Direct Link |
Grison, R., B. Grezes-Besset, M. Schneider, N. Lucante, L. Olsen, J.J. Leguay and A. Toppan, 1996. Field tolerance to fungal pathogens of Brassica napus constitutively expressing a chimeric chitinase gene. Nat. Biotechnol., 4: 643-646.
Direct Link |
Gupta, V.K., A.K. Misra, A. Gupta, B.K. Pande and R.K. Gaur, 2010. Rapd-pcr of Trichoderma isolates and in vitro antagonism against Fusarium wilt pathogens of Psidium guajava L. J. Plant Protec. Res., 50: 256-262.
CrossRef | Direct Link |
Gupta, V.K., A.K. Misra, R.K. Gaur, P.K. Jain, D. Gaur and S. Sharma, 2010. Current Status of Fusarium Wilt Disease of Guava (Psidium guajava L.) in India. Biotechnology, 9: 176-195.
CrossRef | Direct Link |
Hahlbrock, K., C.J. Lamb, C. Purwin, J. Ebel, E. Fautz and E. Schafer, 1981. Rapid Response of suspension-cultured parsley cells to the elicitor from Phytophthora megasperma var. sojae: Induction of the enzymes of general phenylpropanoid metabolism. Plant Physiol., 67: 768-773.
Hammerschmidt, R., 1999. Phytoalexins: What have we learned after 60 years? Annu. Rev. Phytopathol., 37: 285-306.
CrossRef | Direct Link |
Henar, V.M., A. Duran and C. Roncero, 1999. Chitin synthases in yeast and fungi. EXS, 87: 55-69.
Henrissat, B. and G. Davies, 1997. Structural and sequence-based classification of glycosyl hydrolases. Curr. Opin. Structure Biol., 7: 637-644.
Direct Link |
Henrissat, B., 1991. A classification of glycosyl hydrolases based on amino acid Sequence similarities. Biochem. J., 280: 309-316.
PubMed | Direct Link |
Herrera-Estrella, A. and I. Chet, 1999. Chitinases in biological control. EXS, 87: 171-184.
Hopkins, D.L. and A.H. Purcell, 2002. Xylella fastidiosa: Cause of pierces disease of grapevine and other emergent diseases. Plant Dis., 86: 1056-1066.
Howell, C.R., 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases: The history and evolution of current concepts. Plant Dis., 87: 4-10.
CrossRef | Direct Link |
Jung, W.J., K.N. An, Y.L. Jin, R.D. Park and K.T. Lim et al., 2003. Biological control of damping-off caused by Rhizoctonia solani using chitinase-producing Paenibacillus illinoisensis KJA-424. Soil Biol. Biochem., 35: 1261-1264.
Kirubakaran, S.I. and N. Sakthivel, 2007. Cloning and overexpression of antifungal barley chitinase gene in Escherichia coli. Protein Exp. Purific., 52: 159-166.
Kitajima, S., K. Kamei, S. Taketani, M. Yamaguchi and F. Kawai et al., 2010. Two chitinase-like proteins abundantly accumulated in latex of mulberry show insecticidal activity. BMC Biochem., 11: 6-6.
Kobayashi, D.Y., M. Guglielmoni and B.B. Clarke, 1995. Isolation of the chitinolytic bacteria Xanthomonas maltophilia and Serratia marcescens as biocontrol agents for summer patch disease of turfgrass. Soil Biol. Biochem., 27: 1479-1487.
Kramer, K.J. and S. Muthukrishnan, 1997. Insect chitinases: Molecular biology and potential use as biopesticides. Insect Biochem. Mol. Bio., 27: 887-900.
Kumar, V., V. Parkhi, C.M. Kenerley and K.S. Rathore, 2009. Defense-related gene expression and enzyme activities in transgenic cotton plants expressing an endochitinase gene from Trichoderma virens in response to interaction with Rhizoctonia solani. Planta, 230: 277-291.
Lawrence, S.D. and N.G. Novak, 2006. Expression of poplar chitinase in tomato leads to inhibition of development in colorado potato beetle. Biotechnol. Lett., 28: 593-599.
Lehane, M.J., 1997. Peritrophic matrix structure and function. Annu. Rev. Entomol., 42: 525-550.
Lipmann, R., S. Kaspar, T. Rutten, M. Melzer and J. Kumlehn et al., 2009. Protein and metabolite analysis reveals permanent induction of stress defense and cell regeneration processes in a tobacco cell suspension culture. Int. J. Mol. Sci., 10: 3012-3032.
Lorito, M., A. Di Pietro, C.K. Hayes, S.L. Woo and G.E. Harman, 1993. Antifungal, synergistic interaction between chitinolytic enzymes from Trichoderma harzanium and Enterobacter cloacae. Mol. Plant Pathol., 83: 721-728.
Direct Link |
Lorito, M., G.E. Harman, C.K. Hayes, R.M. Broadway, A. Tronsmo, S.L. Woo and A. Di Pietro, 1993. Chitinolytic enzymes produced by Trichoderma harzianum: Antifungal activity of purified endochitinase and chitobiosidase. Phytopathology, 83: 302-307.
Direct Link |
Mansfield, L.S., H.R. Gamble and R.H. Fetterer, 1992. Characterization of the eggshell of Haemonchus contortus-I. Structural components. Comp. Biochem. Physiol. B, 103: 681-686.
Mauch, F., B. Mauch-Mani and T. Boller, 1988. Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiol., 88: 936-942.
CrossRef | PubMed | Direct Link |
Merzendorfer, H. and L. Zimoch, 2003. Chitin metabolism in insects: Structure, function and regulation of chitin synthases and chitinases. J. Exp. Biol., 206: 4393-4412.
Misra, A.K. and V.K. Gupta, 2009. Trichoderma: Biology, biodiversity and biotechnology. J. Eco-Friendly Agric., 4: 99-117.
Oerke, E.C., H.W. Dehnf, F. Schonbeck and A. Weber, 1994. Crop Production and Crop Protection: Estimated losses in Major Food and Cash Crops. 3rd Edn., Elsevier, Amsterdam, The Netherlands, ISBN-13: 9780444820952, Pages: 808.
Oldach, K.H., D. Becker and H. Lorz, 2001. Heterologous expression of the genes mediating enhanced fungal resistance in transgenic wheat. Mol. Plant Microbe Interact, 14: 832-838.
Paoletti, M.G., N. Lorenzo, D. Roberta and M. Salvatore, 2007. Human gastric juice contains chitinases that can degrade chitin. Ann. Nutr. Metab., 51: 244-251.
Punja, Z.K. and Y.Y. Zhang, 1993. Plant chitinases and their roles in resistance to fungal disease. J. Nematol., 25: 526-540.
Direct Link |
Robinson, S.P., A.K. Jacobs and I.B. Dry, 1997. A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol., 114: 771-778.
Direct Link |
Sela-Buurlage, M.B., A.S. Ponstein, S.A. Bres-Vloemans, L.S. Melchers, P.J.M. van den Elzen and B.J.C. Comelissen, 1993. Only specific tobacco (Nicotiana tabacum) chitinases and-1, 3-glucanase exhibit antifungal activity. Plant Physiol., 101: 857-863.
Direct Link |
Sietsma, J.H. and J.G.H. Wessels, 1979. Evidence for covalent linkages between chitin and β-glucan in a fungal wall. J. Gen. Microbiol., 114: 99-108.
Sundheim, L., A.R. Poplawsky and A.H. Hlingboe, 1988. Molecular cloning of two Chitinase gene from Serratia marcescens and their expression in Pseudomonas species. Physiol. Mol. Plant Pathol., 33: 483-491.
Suzuki, K., M. Taiyoji, N. Sugawara, N. Nikaidou and B. Henrissat et al., 1999. The third chitinase gene (chiC) of Serratia marcescens 2170 and the relationship of its product to other bacterial Chitinases. Biochem. J., 343: 587-596.
Tews, I., A. Perrakis, A. Oppenheim, Z. Dauter and K.S. Wilson et al., 1996. Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay-Sachs disease. Nat. Struct. Biol., 3: 638-648.
Tews, I., R. Vincentelli and C.E. Vorgias, 1996. N, Acetylglucosaminidase (chitobiase) from Serratia marcescens: Gene sequence and protein production and purification in Escherichia coli. Gene, 170: 63-67.
Van Aalten, D.M.F., B. Synstad, M.B. Brurberg., E. Hough and B.W. Riise et al., 2000. Structure of a two-domain chitotriose from Serratia marcescens at 1.9-Å resolution. Proc. Natl. Acad. Sci. USA., 97: 5842-5847.
Wasano, N., K. Konno, M. Nakamura, C. Hirayama and M. Hattori et al., 2009. A unique latex protein, MLX56, defends mulberry trees from insects. Phytochemistry, 70: 880-888.
Wu, C.T., G. Leubner-Metzger, F.J.R. Meins and K.J. Bradford, 2001. Class I β-1,3- glucanase and chitinase are expressed in the micropylar endosperm of tomato seeds prior to radicle emergence. Plant Physiol., 126: 1299-1313.
Xu, X., G. Qin and S. Tian, 2008. Effect of microbial biocontrol agents on alleviating oxidative damage of peach fruit subjected to fungal pathogen. Int. J. Food Microbiol., 126: 153-158.
Zhang, Z. and G.Y. Yuen, 2000. The role of chitinase production by Stenotrophomonas maltophilia strain C3 in biological control of Bipolaris sorokiana. Phytopathology, 90: 384-389.