African Journal of
Biotechnology

  • Abbreviation: Afr. J. Biotechnol.
  • Language: English
  • ISSN: 1684-5315
  • DOI: 10.5897/AJB
  • Start Year: 2002
  • Published Articles: 12267

Full Length Research Paper

Oxidative enzymes in coconut cultivars in response to Raoiella indica feeding

Carlos Vásquez
  • Carlos Vásquez
  • Facultad de Ciencias Agropecuarias, Universidad Técnica de Ambato, Cevallos, Province of Tungurahua, Ecuador.
  • Google Scholar
Marta Dávila
  • Marta Dávila
  • Facultad de Ciencias Agropecuarias, Universidad Técnica de Ambato, Cevallos, Province of Tungurahua, Ecuador.
  • Google Scholar
Naileth Méndez
  • Naileth Méndez
  • Universidad Centroccidental Lisandro Alvarado. Decanato de Agronomía. Departamento de Ciencias Biológicas. Barquisimeto, Lara state, Venezuela.
  • Google Scholar
María A. Jiménez
  • María A. Jiménez
  • Universidad Centroccidental Lisandro Alvarado. Decanato de Agronomía. Departamento de Ciencias Biológicas. Barquisimeto, Lara state, Venezuela.
  • Google Scholar
María F. Sandoval
  • María F. Sandoval
  • Instituto Nacional de Investigaciones Agrícolas. Unidad de Producción Vegetal. Laboratorio de Entomología. Maracay, Aragua state, Venezuela.
  • Google Scholar
Francisco J. Alcalá
  • Francisco J. Alcalá
  • Department of Civil Engineering, Catholic University of Murcia, 30107 Murcia, Spain.
  • Google Scholar


  •  Received: 14 April 2016
  •  Accepted: 11 July 2016
  •  Published: 17 August 2016

 ABSTRACT

The increase in oxidative enzyme activities is related to diminished mite infestation. Some biological aspects of Raoiella indica Hirst reared on the coconut cultivars (‘Jamaican Tall’ (JT), ‘Malayan Yellow Dwarf’ (MYD), Niu Leka (NL) and a hybrid JT x MYD) were studied under laboratory conditions. Aditionally, changes in oxidative enzyme activities (peroxidase and polyphenol oxidase) as response to R. indica feeding were studied in the cultivars where red palm mites showed highest and lowest biological parameters values. Longer time spans and lower oviposition rates observed on the JT suggest this cultivar to be more resistant to R. indica feeding. Cultivar JT showed the highest value in PPO/POX ratio, being about twice the value shown by MYD in the infested plants. The observed enzyme activity ratios in both genotypes showed a slight increase 24 h after mite infestation, suggesting these enzymes could be related to plant resistance to R. indica. However, this relationship is still unclear. The biological parameters of R. indica together with higher enzyme activity, particularly on JT suggest this cultivar could be considered as a more resistant cultivar as compared to MYD. More detailed studies are required to determine the effect of these enzymes on coconut resistance to red palm mites.

Key words: Coconut, peroxidase, polyphenol oxidase, red palm mite.


 INTRODUCTION

Plant defense mechanisms can be expressed permanently, without the presence of any stress factor (constitutive resistance), or can be induced in response to biotic or abiotic environmental stresses (induced resistance) (Agrawal and Karban, 2000; Kessler and Baldwin, 2002; Agrawal, 2005; Sunoj et al., 2014). Both permanent and induced responses are crucial for arthropod resistance management (Kant, 2006). Plant induced resistance involves defense mechanisms including structural barriers, increase of toxic substance level (Grubb and Abel, 2006), and protease inhibitors (Chen et al., 2005). However, some of these compounds obtained as a function of induced resistance can be auto-toxic (Gog et al., 2005) or activated relatively late in the interacting plant-herbivore (Morris et al., 2006), thus involving a high metabolic cost for the plant (Walters and Boyle, 2005). Oxidative stress is a complex chemical and physiological phenomenon that accompanies virtually all biotic and abiotic stresses in higher plants and develops as a result of overproduction and accumulation of reactive oxygen species (ROS) (Demidchik, 2015). Different ROS types are able to evoke oxidative damage to proteins, DNA and lipids (Apel and Hirt, 2004). The cellular damage by ROS appears to be due to their conversion into more reactive species such as the formation of •OH, which is dependent on both H2O2 and O2•− and, thus, its formation is subject to inhibition by both superoxide dismutase (SOD) and catalase (CAT) (Sharma et al., 2012). Besides SOD and CAT, there is a complex of enzymatic components of the antioxidative defense system that comprise several antioxidant enzymes such as guaiacol peroxidase (GPX), enzymes of ascorbateglutathione (AsA-GSH) cycle ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR) and glutathione reductase (GR) (Noctor and Foyer, 1998). Peroxidases (POX) are involved in many physiological processes in plants, involving responses to biotic and abiotic stresses, the biosynthesis of lignin in the polymerization of the precursors of lignin, and in the scavenging of reactive oxygen species (ROS). The ROS are partially reduced forms of atmospheric oxygen, highly reactive and capable of causing oxidative damage to the cell, and can either scavenge or be a source of hydrogen peroxide (H2O2) (Vicuña, 2005). Also, peroxidases may be involved in defense against pathogens (López-Curto et al., 2006) or insects (Dowd and Lagrimini, 1998). The expression of different peroxidase isoenzymes depends upon the plant developmental stage and on environmental stimuli (Valério et al., 2004). The increase in POX activity during pathogen/herbivore attack has been associated with phenolic compounds binding to the cell wall in soybeans and beans (Lamb and Dixon, 1997). POX activity has been shown to increase in tomato or hop after Tetranychus urticae Koch or Tetranychus cinnabarinus Boisduval feeding (Stout et al., 1994; Kielkiewicz, 2002; Trevisan et al., 2003). Similarly, higher oxidative enzyme activity has been associated with lower Steneotarsonemus spinki Smiley density on tolerant rice varieties (Fernández et al., 2005). Polyphenol oxidase (PPO) is considered an important oxidative enzyme involved in several physiological functions; however, greater activity has been reported in damaged tissue, therefore PPO’s are also considered plant defense proteins (Pinto et al., 2008). Sunoj et al. (2014) demonstrated that reduced activity of PPO and an increased membrane stability index in some coconut seedlings indicate that even under abiotic stress, oxidative stress was reduced by the enzymatic protection mechanisms in operation, suggesting that coconut seedlings were able to maintain membrane stability. Previous studies showed a negative relationship between PPO activity and developmental rate of Heliothis zea (Boddie) in tomato leaves, probably due to chelating of amino acids and leaf proteins, with subsequent nutritional quality reduced in the infested foliage (Felton et al., 1989). More recently, caterpillars of several noctuid species (Spodoptera exigua (Hübner), Spodoptera litura (F.) and Helicoverpa armigera Hübner) showed decreased weight gains and consumption rates when feeding on transgenic tomato lines showing PPO expression (Mahanil et al., 2008; Bhonwong et al., 2009).

The red palm mite, Raoiella indica Hirst, has been considered a serious pest for coconut (Cocos nucifera L.) and Areca palms (Areca catechu L.) in India (Daniel, 1981; NageshaChandra and Channabasavanna, 1984), and date palms (Phoenix dactylifera L.) in Egypt (Zaher et al., 1969). After being reported in the Caribbean in 2004, R. indica quickly spread through that region, reaching Florida (USA) and the northern area of South America (Gondim Jr. et al., 2012; Vásquez and Moraes, 2013). R. indica inflicted serious damage to Arecaceae, primarily to the coconut trees, but also to Musaceae and other botanical families (Carrillo et al., 2012; Rodrigues and Irish, 2012). It has been observed that coconut seedlings may die from pest attack, while older plants show discoloration and consequent yield reduction. This information has not been systematically quantified (Welbourn, 2005; Peña et al., 2006). Considering the economic impact of R. indica in the Caribbean area, resistance in coconut cultivars should be addressed in order to improve knowledge on how sustainable strategies could contribute in red palm mite population management. For this reason, peroxidase and polyphenol oxidase activities in response to R. indica feeding were evaluated in different coconut palm cultivars used commercially in Venezuela.


 MATERIALS AND METHODS

Plant material

A study was conducted at the Universidad Centroccidental Lisandro Alvarado, in the state of Lara, Venezuela (10°01’04” N; 69°17’03”W) during 2012. Forty 1-2 years-old plants from each of the coconut cultivars were planted in plastic containers (60×40 cm) containing a substrate of ground soil + rice hulls + sand (1:1:1). One month before the test was initiated, the plants were fertilized with NPK (15-20-20) and treated with Mancozeb (3 g) in 300 ml water per palm. Then, plants of each cultivar were divided into two groups; the first group being females infested with 25 R. indica on each one of the three leaflets of well-developed middle leaves, while the second group was kept mite free and used as a control. A leaf section (about 4 cm2) was taken from each of five infested plants per cultivar, and from the control group at 0, 24, 72, 120 and 264 h after mite infestation. Samples were wrapped in a piece of foil and brought in an icebox to the laboratory. Leaf samples were weighed and stored at -20°C until being processed.

 

Biological aspects of R. indica on several coconut genotypes

The biological cycle of R. indica was studied using rearing units on four distinct coconut cultivars. The cultivars studied were: the Jamaican Tall (JT), Malayan Yellow Dwarf (MYD), the Niu Leka (NL), and a hybrid cultivar (JT x MYD) provided by the Instituto Nacional de Investigaciones Agrícolas (INIA), Irapa, Sucre state, Venezuela. Each rearing unit consisted of a coconut leaf disc (3 cm diameter) placed with the lower surface on a polyurethane layer, continuously maintained wet by the daily addition of distilled water (Vásquez et al., 2015). One 3-5 day old female was put on each of the thirty rearing units of each cultivar to obtain one egg per rearing unit. After 24 h, the females were removed and just eggs were kept in rearing units. The units continued to be examined in 12-h intervals to determine the duration of each developmental stage. Leaf disks were replaced by new disks every 3-4 days to ensure a physiologically adequate rearing substrate throughout the work. Oviposition was studied in 30 mated-females for each cultivar. The study was carried out under room conditions (29 ± 1.0°C, 60 ± 10 % RH and 12 h photoperiod).

 

Biochemical changes in coconut cultivars induced by R. indica feeding

Total proteins (TP)

Content of total protein was determined using the Bradford (1976) method. Absorbance of each dilution was measured using a spectrophotometer (GENESYS 10S UV-Vis) at 595 nm. Induced biochemical response to R. indica feeding were determined on coconut cultivars in which R. indica showed the lowest and highest biotic potential in the experiment above, those being JT and MYD. Biochemical responses in leaf tissue included total protein (TP) content, polyphenol oxidase (PPO), peroxidase (POX) and lipid peroxidation.

 

Enzyme extract

Enzyme extract was done following Martínez et al. (2013), with some modifications. 300 mg of leaf sample from each cultivar (infested and uninfested plants) was ground in liquid nitrogen and homogenized with 50 mM Tris-HCl buffer (pH 5.7), containing 1% polyvinylpyrrolidone (PVP) and 1 mM EDTA. Plant extract was centrifuged at 12,000 rpm, 4°C for 20 min, and the supernatant was used to determine total proteins and enzyme activity.

 

Quantification of peroxidase (POX) activity

POX activity was measured by spectrophotometry. The guaiacol oxidation rate by POX mediated by H2O2 was measured on 470 nm absorbance of the light spectrum absorbed by oxidized guaiacol. Changes in optical density were determined every 15 s for 1 min. Enzymatic activity was expressed in mM of tetraguaiacol min-1 µg-1 of protein.

 

Quantification of polyphenol oxidase activity (PPO)

PPO activity was quantified by the oxidation rate of pyrogallol (Alexander et al., 1964). Pyrogallol was prepared in a buffer solution of sodium acetate (50 mM, pH 5.5). Enzyme activity was measured at 15 s intervals for 3 min in a spectrophotometer at 420 nm and expressed in mM of quinone min-1 µg-1 protein.

The PPO/POX ratio was used as an indirect measurement to visualize the behavior of the genotypes after herbivore feeding. This decision was made due to the lack of information on which specific PPOs or POXs are induced.

 

Statistical analysis

The results were subjected to variance analysis and mean values were compared by Tukey test at p< 0.05. POX and PPO activities were correlated with the number of mites per leaflet, using Statistix software version 8.0.


 RESULTS AND DISCUSSION

Biological aspects of R. indica reared on different coconut cultivars

Life cycle of R. indica was influenced by the coconut cultivar tested (Table 1). Higher developmental time was observed on JT cultivar (21.9 days), while it was about 23% lower on MYD cultivar. Developmental time was intermediate on JT×MYD hybrid and NL, being reduced by 9.6 and 13.4%, respectively in relation to JT. Furthermore, effect of coconut cultivar on R. indica oviposition was also observed (Table 1 and Figure 1). The highest oviposition rate was observed in R. indica females reared on MYD and on hybrid MYD×JT leaf disks (2.4 eggs female-1day-1), while the oviposition rate on the JT cultivar was about 30% lower than on MYD. Daily oviposition was intermediate on NL.

 

 

 

 

 

 

Host plant effect on phytophagous mite species reproduction was previously shown as growing, without effect, or decreasing (Ribeiro et al., 1988; Hilker and Meiners, 2002; Praslička and Huszár, 2004). Differences in R. indica developmental time was observed when reared on coconut cultivars, being 21.5 and 19.8 d on JT (in Trinidad) and on a hybrid MYDxJT (in Venezuela), respectively (Vásquez et al., 2015). Vásquez et al. (2008) hypothesized that reproductive parameters of Oligonychus punicae appeared to be negatively associated with flavonoid content in grape cultivars. These phenolic compounds can be synthesized in grapevine leaves and fruits in response to biotic or abiotic stress (Morrissey and Osbourn, 1999) and these compounds may act synergistically with tannins to provide plant resistance (Harborne, 1994; Bernards and Båstrup-Spohr, 2008).

 

Biochemical changes in coconut cultivars induced by R. indica feeding

Total proteins

TP content was significantly higher in JT cultivar as compared to MYD during the evaluation period (Figure 2). Although no significant variations were observed in TP content in JT after R. indica feeding, higher TP content was observed 72 h after infestation. In MYD, total protein content varied significantly (p<0.01, F= 0.000; df=14), being greater 120 h after infestation. Likewise, previous studies have shown TP increasing in response to different types of abiotic (García et al., 2003) or biotic stress (Kamal et al., 2010; Wang et al., 2011). This response has been considered as a protective strategy against stress factors, which may be associated with specific gene expression favoring induction of proteins only synthesized under non-optimal conditions (Pérez et al., 1997). Polyphenol oxidase (PPO) and peroxidase (POX) catalyze oxidation of phenols and consequently, quinones formed by oxidation of phenols, bind covalently to leaf proteins, and inhibit the protein digestion in herbivores (War et al., 2012). Consenquently, the conserved TP content in JT suggests this cultivar might be considered tolerant to the stress caused by mite feeding.

 

 

 

 

Enzyme activity

The PPO/POX ratio was similar in both non-infested genotypes in JT and MYD at 0 h. This ratio tended to decrease both in infested or non-infested JT plants, showing an increase after 72 h on infested plants. Ratio values were relatively similar along evaluation periods in MYD infested plants, ranging from 2.1 to 2.94 after 24 and 72 h, respectively (Figure 3). Mayer (2006) stated that resistant genotypes had localized elevated levels of PPO formation which was rapidly induced following infection. Susceptible cultivars failed to accumulate PPO even after considerable time. These results suggest that increases in PPO/POX ratio in response to R. indica feeding could be considered as the first evidence of resistance expressed by coconut cultivars to mite feeding. It is still unclear whether PPO may be involved in resistance to the red palm mite in coconut palms; however, the observed enzyme activity ratios in both genotypes show a slight increase 24 h after mite infestation. Simultaneously, the biological parameters of R. indica together with the above, particularly on JT (Table 1 and Figure 1), suggest this cultivar could be considered as a more resistant cultivar as compared to MYD.

 

 

 

 

Changes in total protein content and levels of oxidative enzymes are considered the first plant response to feeding herbivores (Felton et al., 1994; Ni et al., 2001). These biochemical responses are in function to plant growth stages and stress intensity (Constabel and Barbehenn, 2008). Furthermore, POX activity is influenced by plant species and sampling time and it reaches higher levels during the first 3 days and tends to diminish as stress decreases (Ni et al., 2001). Peroxidases and polyphenol oxidases are involved in plant defense against phytophagous mites and insects, by the production and polymerization of phenolics and lignification and hypersensitive responses in injured tissues (Kielkiewicz, 2002).

The production of PPO as a defense response to

herbivores involves a complex sequence of reactions starting with gene expression and then leading to the formation and activation of enzymes for substrate production (Mayer, 2006). However, the lower mRNA levels associated with this enzyme in some species suggests that its role in defense has evolved only in a few species (Constabel et al., 2000). Results associated with PPO activity and arthropod herbivore performance, using plant genotypes that vary in resistance to herbivory and ontogenetic variation in PPO activity within the plant and leaves treated with PPO, have been contradictory (Constabel and Barbehenn, 2008).

Previous studies dealing with the relationship between the plant resistance and the activity of POD and PPO are intriguing. Most of the results have shown that higher POX or PPO levels are associated with plant resistance to Steneotarsonemus spinki Smiley in rice cultivars (Fernández et al., 2005), T. urticae in strawberry (Steinite and Ievinsh, 2002) and hop (Trevisan et al. 2003), T. cinnabarinus (Kielkiewicz, 2002), common cutworm (Spodoptera litura) and the cotton bollworm (Heliothis armigera) in tomato (Thipyapong et al., 2006). More recently, Samsone et al. (2012) observed that high Vasates quadripes Shrimer infestation levels could evoke increases in POX activity in Acer saccharinum leaves. Conversely, higher levels of PPO in coffee leaves apparently was not associated with resistance to the coffee leaf miner (Leucoptera coffeella) (Melo et al., 2006; Ramiro et al., 2006). The induction of phenolic activity, and the enzymes peroxidase and polyphenol oxidase in response to insect attack might not be concrete evidence that these substances participate directly in plant defense mechanisms (Ramiro et al., 2006). In addition, Manduca quinquemaculata caterpillars surprisingly showed greater performance on younger tobacco leaves, which contain higher PPO levels (Kessler and Baldwin, 2002). Given the tremendous variation in PPO expression patterns, activity levels, and potential substrates in different species, similar variation in the adaptive roles played by PPO in defense and other processes may be anticipated. Thus, correlations of PPO activity with defense may be confounded by the complexity of PPO gene families (Constabel and Barbehenn, 2008).

Similar to PPO production in response to plant-arthropod interaction, peroxidases catalyze synthesis of products with antimicrobial activity in plants, suggesting a role in plant defense by participating in phytoalexin synthesis (Almagro et al., 2009). Peroxidases are also involved in the binding of cell wall components. Extensin, phenolic compounds and polysaccharides act as a mechanical barrier for pathogen penetration (Brisson et al., 1994). In addition, these mechanical barriers, formed as result of strengthening cell walls, have been reported as a resistance mechanism in pericarp (García-Lara et al., 2004) and embryo in maize grain (García-Lara et al., 2007) to Sitophilus zeamais. Moreover, quinone oxidation in the developing grain pericarp regulated by peroxidases may contribute to plant resistance reducing digestibility for insect pests (García-Lara et al., 2007).

The observed enzyme activity increase soon after mite infestation, suggesting that the role of this enzyme should be further investigated. In this regard, more detailed studies are required to better understand mechanisms of plant response to arthropod herbivores and thus use this information for crop protection and sustainable crop production.


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.


 ACKNOWLEDGEMENTS

The authors thank Dirección de Investigación y Desarrollo (DIDE, Universidad Técnica de Ambato) for partial funding of the project. Also we are grateful to Lcdo. M.A. Joel Dlouhy (Center of Languages, Univ Técnica de Ambato) for his valuable revision of English style. This study was partially financed by the Ecuadorian PROMETEO Research Project CEB-014-2015 and the Chilean FONDECYT Research Project 1161105.



 REFERENCES

Agrawal AA (2005). Future directions in the study of induced plant responses to herbivory. Entomol. Exp. Appl. 115(1):97-105.
Crossref

 

Agrawal AA, Karban R (2000). Specificity of constitutive and induced resistance: pigments glands influence mites and caterpillar on cotton plants. Entomol. Exp. Appl. 96:39-49.
Crossref

 
 

Alexander AG (1964). Sucrose enzyme relationship in immature sugar cane. J. Agr. Univ. Puerto Rico 4813:165-231.

 
 

Almagro L, Gómez LV, Belchi-Navarro S, Bru R, Ros-Barceló A, Pedre-o MA (2009). Class III peroxidases in plant defence reactions. J. Exp. Bot. 60(2):377-390.
Crossref

 
 

Apel K, Hirt H (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann. Rev. Plant Biol. 55:373-399.
Crossref

 
 

Bernards MA, Båstrup-Spohr L (2008). Phenylpropanoid metabolism induced by wounding and insect herbivory. In: Schaller A (ed) Induced plant resistance to insects. Springer, New York, pp. 189-213.
Crossref

 
 

Bhonwong A, Stout MJ. Attajarusit J, Tantasawat P (2009). Defensive role of tomato polyphenol oxidases against cotton bollworm (Helicoverpa armigera) and beet armyworm (Spodoptera exigua). J. Chem. Ecol. 35:28-38.
Crossref

 
 

Bradford MM (1976). A Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
Crossref

 
 

Brisson LF, Tenhaken R, Lamb C (1994) Function of oxidative cross-linking of cell wall structural proteins in plant disease resistance. Plant Cell 6:1703-1712.
Crossref

 
 

Carrillo D, Amalin D, Hosein F, Roda A, Duncan RE, Pe-a JE (2012). Host plant range of Raoiella indica (Acari: Tenuipalpidae) in areas of invasion of the New World. Exp. Appl. Acarol. 57(3-4):271-289.
Crossref

 
 

Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005). Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc. Natl. Acad. Sci. USA. 102(52):19237-19242.
Crossref

 
 

Constabel CP, Barbehenn R (2008). Defensive roles of polyphenol oxidase in plants. In: Schaller A. (ed.) Induced plant resistance to insects. Springer, New York, pp. 253-269.
Crossref

 
 

Constabel CP, Yip L, Patton JJ, Christopher ME (2000). Polyphenol oxidase from hybrid poplar: cloning and expression in response to wounding and herbivory. Plant Physiol. 124:285-296.
Crossref

 
 

Daniel M (1981). Bionomics of the predaceous mite Amblyseius channabasavanni (Acari: Phytoseiidae), predaceous on the palm mite Raoiella indica. First Indian Symposium in Acarology. Bangalore, India. Contributions to Acarology in India.

 
 

Demidchik V (2015). Mechanisms of oxidative stress in plants: From classical chemistry to cell biology. Environ. Exp. Bot. 109:212-228
Crossref

 
 

Dowd LM, Lagrimini LM (1998). Differential leaf resistance to insects of transgenic sweetgum (Liquidamber styraciflua) expressing tobacco anionic peroxidase. Cell. Mol. Life Sci. 54(7):712-720.
Crossref

 
 

Felton GW, Bi JL, Summers CB, Mueller AJ, Duffey SS (1994). Potential role of lipoxygenases in defense against insect herbivory. J. Chem. Ecol. 20:651-666.
Crossref

 
 

Felton GW, Donato K, Vecchio RJ, Duffey SS (1989). Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15(12):2667-2694.
Crossref

 
 

Fernández A, Solórzano E, Miranda I (2005). Actividad peroxidasa, glucanasa, polifenol oxidasa y fenilalanina amonio liasa en variedades de arroz con diferente grado de susceptibilidad al ácaro Steneotarsonemus spinki. Rev. Protección Veg. 20(2):132-136.

 
 

García A, Florido M, Lara RM (2003). Estudios bioquímicos para la selección in vitro de variedades de arroz con tolerancia a estrés hídrico. Biotecnol. Veg. 3(3):181-186.

 
 

García-Lara S, Arnason JT, Díaz-Pontones D, Gonzalez E, Bergvinson DJ (2007). Soluble peroxidase activity in maize endosperm associated with maize weevil resistance. Crop Sci 47:1125-1130.
Crossref

 
 

García-Lara S, Bergvinson DJ, Burt AJ, Ramputh AI, Diaz-Pontones DM, Arnason JT (2004). The role of pericarp cell wall components in maize weevil resistance. Crop Sci. 44:1546-1552.
Crossref

 
 

Gog L, Berenbaum MR, Delucia EH, Zangerl AR (2005). Autotoxic effects of essential oils on photosynthesis in parsley, parsnip, and rough lemon. Chemoecology 15(2):115-119.
Crossref

 
 

Gondim Jr. MGC, Castro TMMG, Marsaro Jr. AL, Návia D, Melo JWS, Demite PR, Moraes de GJ (2012). Can the red palm mite threaten the Amazon vegetation? Syst. Biodivers. 10(4):527-535.
Crossref

 
 

Grubb CD, Abel S (2006). Glucosinolate metabolism and its control. Trends Plant Sci 11(2):89-100.
Crossref

 
 

Guerreiro Filho O (2006). Coffee leaf miner resistance. Braz. J. Plant Physiol. 18(1):109-117.
Crossref

 
 

Harborne J (1994). Do natural plant phenols play a role in ecology? Acta Hortic 381:36-43.
Crossref

 
 

Hilker M, Meiners T (2002). Induction of plant responses to oviposition and feeding by herbivorous arthropods: a comparison. Entomol. Exp. Appl. 104:181-192.
Crossref

 
 

Kamal AHM, Kim K, Shin K, Kim D, Oh M, Choi J, Hirano H, Heo H, Woo S (2010). Proteomics-based dissection of biotic stress responsive proteins in bread wheat (Triticum aestivum L.). Afr. J. Biotechnol. 9(43):7239-7255.

 
 

Kant MR (2006). The consequences of herbivore variability for direct and indirect defenses of plants. Dissertation, University of Amsterdam.

 
 

Kessler A, Baldwin I (2002). Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299-328.
Crossref

 
 

Kielkiewicz M (2002). Influence of carmine spider mite Tetranychus cinnabarinus Boisd. (Acarida: Tetranychidae) feeding on ethylene production and the activity of oxidative enzymes in damaged tomato plants. In: Bernini F, Nannelli R, Nuzzaci G and de Lillo E (eds) Acarid phylogeny and evolution: adaptation in mites and ticks. Springer, Siena, pp. 389-392.
Crossref

 
 

Lamb C, Dixon RA (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:251-275.
Crossref

 
 

López-Curto L, Márquez-Guzmán J, Díaz-Pontones DM (2006). Invasion of Coffea arabica (Linn.) by Cuscuta jalapensis (Schlecht): in situ activity of peroxidase. Environ. Exp. Bot. 56:127-135.
Crossref

 
 

Mahanil S, Attajarusit J, Stout MJ, Thipyapong P (2008). Overexpression of tomato polyphenol oxidase increases resistance to common cutworm. Plant Sci. 174:456-466.
Crossref

 
 

Martínez MT, Cruz O, Colinas MT, Rodríguez JE, Ramírez SP (2013). Actividad enzimática y capacidad antioxidante en menta (Mentha piperita L.) almacenada bajo refrigeración. Agron. Mesoam 24(1):57-69.
Crossref

 
 

Mayer AM (2006). Polyphenol oxidases in plants and fungi: Going places? a review. Phytochemistry 67:2318-2331.
Crossref

 
 

Melo GA, Shimizu MM, Mazzafera P (2006). Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry 67(3):277-285.
Crossref

 
 

Morris WF, Traw MB, Bergelson J (2006). On testing for a tradeoff between constitutive and induced resistance. Oikos 112(1):102-110.
Crossref

 
 

Morrissey J, Osbourn AE (1999). Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol. Mol. Biol. Rev. 63:708-724.

 
 

NageschaChandra BK, Channabasavanna GP (1984). Development and ecology of Raoiella indica Hirst (Acari: Tenuipalpidae) on coconut. In: Griffiths DH, Bowman CE (eds) Acarology VI. Elis Horwood Publ., pp. 785-790.

 
 

Ni X, Quisenberry SS, Heng-Moss T, Markwell J, Sarath G, Klucas R, Baxendale F (2001). Oxidative responses of resistant and susceptible cereal leaves to symptomatic and non-symptomatic cereal aphid (Hemiptera: Aphididae) feeding. J. Econ. Entomol. 94:743-751.
Crossref

 
 

Noctor G, Foyer CH (1998). Ascorbate and glutathione: keeping active oxygen under control. Ann. Rev. Plant Biol. 49:249-279.
Crossref

 
 

Pe-a JE, Mannion CM, Howard FW, Hoy MA (2006). Raoiella indica (Prostigmata: Tenuipapidae): the red palm mite: a potential invasive pest of palms and bananas and other tropical crops of Florida. University of Florida IFAS Extension, ENY-837. 2006. Accessed 12 July 2012

 
 

Pérez I, Dell'Amico J, Rodríguez P, Reynaldo I (1997). Alteraciones fisiológicas y bioquímicas de los cultivares de tomate (Lycopersicon escuemtum Mill) ante condiciones de inundación. Cultivos Tropicales 18(3):30-35.

 
 

Pinto MST, Siqueira FP, Oliveira AEA, Fernandes KVS (2008). A wounding-induced PPO from cowpea (Vigna unguiculata) seedlings. Phytochemistry 69:2297-2302.
Crossref

 
 

Praslička J, Huszár J (2004). Influence of temperature and host plants on the development and fecundity of the spider mite Tetranychus urticae (Acarina: Tetranychidae). Plant Protect. Sci. 40(4):141-144.

 
 

Ramiro DA, Guerreiro-Filho O, Mazzafera P (2006). Phenol contents, oxidase activities, and the resistance of coffee to the leaf miner Leucoptera coffeella. J. Chem. Ecol. 32(9):1977-1988.
Crossref

 
 

Ribeiro LG, Villacorta A, Foerster LA (1988). Life cycle of Panonychus ulmi (Koch, 1836) (Acari: Tetranychidae) in apple trees, cultivar Gala and Golden Delicious. Acta Hort. 232:228.
Crossref

 
 

Rodrigues JCV, Irish BM (2012). Effect of coconut palm proximities and Musa spp. germplasm resistance to colonization by Raoiella indica (Acari: Tenuipalpidae). Exp. Appl. Acarol. 57:309-316.
Crossref

 
 

Samsone I, Andersone U, Ievinsh G (2012). Variable effect of arthropod-induced galls on photochemistry of photosynthesis, oxidative enzyme activity and ethylene production in tree leaf tissues. Environ. Exp. Biol. 10:15-26.

 
 

Sharma P, Bhushan Jha A, Shanker Dubey R, Pessarakli M (2012). Reactive Oxygen Species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany.
Crossref

 
 

Steinite I, Ievinsh G (2002). Wound-induced responses in leaves of strawberry cultivars differing in susceptibility to spider mite. J. Plant Physiol. 159:491-497.
Crossref

 
 

Stout MJ, Workman J, Duffey SS (1994). Differential induction of tomato foliar proteins by arthropod herbivores. J. Chem. Ecol. 20(10):2575-2794.
Crossref

 
 

Sunoj VSJ, Naresh Kumar S, Muralikrishna KS (2014). Effect of elevated CO2 and temperature on oxidative stress and antioxidant enzymes activity in coconut (Cocos nucifera L.) seedlings. Indian J. Plant Physiol. 19(4):382-387.
Crossref

 
 

Thipyapong P, Mahanil S, Bhonwong A, Attajarusit J, Stout MJ, Steffens JC (2006). Increasing resistance of tomato to lepidopteran insects by overexpression of polyphenol oxidase. Acta Hortic 724:29-38.
Crossref

 
 

Trevisan MTS, Schefferb JJC, Verpoorteb R (2003). Peroxidase activity in hop plants after infestation by red spider mites. Crop Protection 22:423-424.
Crossref

 
 

Valério L, De Meyer M, Penel C, Dunand C (2004). Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry 65: 1343-1350.
Crossref

 
 

Vásquez C, Aponte O, Morales J, Sanabria ME, García G (2008). Biological studies of Oligonychus punicae (Acari: Tetranychidae) on grapevine cultivars. Exp. Appl. Acarol. 45(1/2):59-69.
Crossref

 
 

Vásquez C, Colmenárez Y, de Moraes GJ (2015). Life cycle of Raoiella indica (Acari: Tenuipalpidae) on ornamental plants, mostly Arecaceae. Exp. Appl. Acarol. 65(2):227-235.
Crossref

 
 

Vásquez C, Moraes de GJ (2013). Geographic distribution and host plants of Raoiella indica and associated mite species in northern Venezuela. Exp. Appl. Acarol. 60(1):73-82.
Crossref

 
 

Vicu-a D (2005). The role of peroxidases in the development of plants and their responses to abiotic stresses. Doctoral Thesis. Dublin Institute of Technology.

 
 

Walters DR, Boyle C (2005). Induced resistance and allocation costs: what is the impact of pathogen challenge? Physiol. Mol. Plant Path. 66:40-44.
Crossref

 
 

Wang Y, Kim S, Kim S, Agrawal GK, Rakwal R, Kang KY (2011). Biotic stress-responsive rice proteome: an overview. J. Plant Biol. 54:219-226.
Crossref

 
 

War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma H (2012). Mechanisms of plant defense against insect herbivores. Plant Signal Behav. 7(10):1306-1320.
Crossref

 
 

Welbourn C (2005). Red palm mite Raoiella indica Hirst (Acari: Tenuipalpidae) pest alert. Accessed: 9 June 2012

 
 

Zaher MA, Wafa AK, Yousef AA (1969). Biological studies on Raoiella indica Hirst and Phyllotetranychus aegyptiacus Sayed infesting Date palm trees In: U. A. R. (Acarina: Tenuipalpidae). Z Angew Entomol. 63(1-4):406-411.
Crossref

 

 




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