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Article

Nutshell Physicochemical Characteristics of Different Hazel Cultivars and Their Defensive Activity toward Curculio nucum (Coleoptera: Curculionidae)

by
Xingpeng Li
1,
Dongying Xiu
2,
Jinbin Huang
1,
Bo Yu
2,
Shuxia Jia
1 and
Liwen Song
2,*
1
Jilin Provincial Key Laboratory of Insect Biodiversity and Ecosystem Function of Changbai Mountains, Beihua University, Jilin 132013, China
2
Jilin Provincial Academy of Forestry Science, Changchun 130033, China
*
Author to whom correspondence should be addressed.
Forests 2023, 14(2), 319; https://doi.org/10.3390/f14020319
Submission received: 4 January 2023 / Revised: 28 January 2023 / Accepted: 1 February 2023 / Published: 6 February 2023
(This article belongs to the Section Forest Ecophysiology and Biology)
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Abstract

:
Hazel (Corylus avellana) is easily attacked by Curculio nucum L. To better understand the physiological mechanisms underlying the different resistance of cultivars to C. nucum, we determined the insect-resistant compounds, plant hormones contents, and enzyme activities in the nutshells of three hazel cultivars (DW, B21, and MZ) before (preexisting defense) and after (induced defense) C. nucum chewing. The findings demonstrated that the resistance of three hazel cultivars to C. nucum differed significantly (p < 0.05): the damage rate of MZ with 17.57% was highest, followed by DW (11.23%), and then B21 (7.15%). The contents of insect-resistant compounds (total terpenoid, tannin, total phenol, flavonoids, cellulose, and lignin) varied with hazel cultivars, both before and after C. nucum chewing, except for cellulose and lignin before induction. The level of plant hormones and defense enzyme activities of hazelnut enhanced due to C. nucum induction. Pearson correlation results revealed that the hazelnut damage rate was significantly negatively correlated with jasmonic acid (JA) (R2 = 0.812), SOD (R2 = 0.671), salicylic acid (SA) (R2 = 0.878), and terpenoids (R2 = 0.774), and significantly positively correlated with flavonoids (R2 = 0.696), celluloses (R2 = 0.501), POD (R2 = 0.758), and abscisic acid (ABA) (R2 = 0.978). The hazelnut defense to C. nucum was negatively related to cellulose contents, and not to lignin contents, but was significantly positively related to the ratio of cellulose-to-lignin (R2 = 0.703). Our results suggested that the hazel against C. nucum attack responded by improving plant hormones contents and enzyme activities in the nutshells. A particular cellulose-to-lignin ratio provides the most effective physical structural defense properties in the nutshells.

1. Introduction

Plants as the primary producers with rich nutrients cannot move autonomously and are, thus, subject to be attacked by pathogens, arthropods, or adverse environmental conditions. Plants have evolved various physical and chemical defense systems against stress, which are critical to plant survival during their evolution. Plant defense against insect pests can be categorized into: (i) preexisting defense, which is determined by genetics, for instance, the cell wall, waxy layer in leaves [1], toxic protein, and high concentration of inorganic salts in tissues [2,3]; (ii) induced defense, which is defined by the ability of some proteases, secondary metabolites, and other compounds with insect-resistant activity in plant tissue to change rapidly after mechanical wound, insect feeding, and pathogen infection [4]. Inherent and induced defense both are regulated by plant morphology, as well as the type and content of insect-resistant compounds [5]. Induced defense is considered highly dynamic and is among the more important strategies of plants against insect herbivores [6]. Under the inherent defense system, plants are required to continuously allocate energy to prepare for the invasion of various potential biological and abiotic agents with the constant total available energy [7,8]. In contrast, induced defense systems are activated following plant invasion to conserve energy for growth and reproduction and increase the probability of survival and reproduction [9,10].
Plant physical traits, especially plant morphology differentiation, are driven by long-term natural selection and breeding, which determines different species’ in the same family or cultivar susceptibility to specific stress factors [11,12,13]. A previous study, for instance, revealed that the hardness of nut shells influenced the defense of hazel to Curculio nucum (Coleoptera: Curculionidae)—a higher shell hardness showed a lower proportion of nuts damaged by the nut weevil in different cultivars [14]. Another example of how the morphology of different cultivars influences plant defense is the trichome density in cotton (Gossypium hirsutum) leaf with different varieties, and the tolerant variety (Gcot-16) with longer trichome showed higher defense to Helicoverpa armigera and Spodoptera litura than the susceptible variety (Coker-312). The higher trichome density effectively prevents insects from feeding on their hosts from chewing [15].
In addition to the physical and morphology traits, the plant physiological traits of different species in the same family or different cultivars, such as pattern recognition receptors, defense enzyme activities, related transcription factors, and chromatin status of plant tissues after insect feeding induction, may induce different herbivory resistance [16,17]. Aldehydes and oxoacids are hypothesized to play a role in the defense response of potato (Solanum tuberosum) against Myzus persicae attacks. Hydroperoxide lyases (HPLs) have been thought to involve in the plant defense response against pest attack by the derived products [17]. A wild-type potato leaves with normal HPLs activity for cleaving 13-hydroperoxides to yield hexanal and 3-hexenal and showed a higher defense response against aphid than HPL-depleted potato with lower aldehyde levels, and the HPL depletion in transgenic potato reduced the production of hexanal and 3-hexenal during the 13-fatty acid hydroperoxide degradation [17]. Another study on the resistance of plants found that the ABA (abscisic acid)-deficient tomato (Lycopersicon esculentum) mutant showed a lower resistance to Bemisia tabaci than its wild type [18]. The effective defense of wild-type tomato against B. tabaci conferred through callose deposition is induced by the activation of ABA [16]. Similarly, the transcript levels of two genes, namely phenylalanine ammonia-lyase (PAL) and anthocyanin synthase (ANS) related to the phenylpropanoid pathway, were considerably higher in the tolerant cotton varieties (Bc-68-2 and Gcot-16) than in the susceptible variety (Coker-312) following 72 h induction by H. armigera [15]. The accumulation of secondary metabolites (insect-resistant compounds), such as phenols, condensed tannins, and flavonoids in plants, are commonly regulated by the genes in phenylpropanoid pathway [19]. In addition, other studies found that the differences in the activity and synthesis efficiency of antioxidant enzymes, such as the redox enzymes (superoxide dismutase, SOD; catalase, CAT), were involved in the homeostasis of reactive oxygen species in defense signaling and defense enzyme (peroxidase, POD) in different plant cultivars after feeding induction influenced plant resistance [20]. Although, the species and cultivars of plants showed different morphological and physiological responses to insect attacks. However, maximizing the yield through cultivating resulted in a change in the physical characteristics, genetic diversity, and insect defense of plants [21]. Understanding the physiological mechanisms of cultivars based on yield to pest attack will be helpful in enriching plant breeding strategies for the selection of elite genetic traits.
Corylus avellana is one of the most important nut species, widely distributed in Eurasia, North Africa, and America at different latitudes and altitudes [14]. The global hazelnut production area in 2020 was 101,500 ha, with a 67.13% increasing over 2010, while the yield only increased by 25.45% (FAO statistics, https://www.fao.org/faostat/zh/#data/QCL, accessed on 21 December 2021). The actual cause of the dramatic drop in hazelnut production is still unknown; nevertheless, in some locations, diseases and pests may play a dominant role in the decline of hazelnut yield [22,23]. The C. nucum is one of the most harmful pests to hazelnut. A previous study demonstrated that there are significant differences in the resistance to C. nucum of three hazelnut cultivars widely planted in China, although the mechanism of the difference in resistance remains elusive. We compared the resistance of three hazel cultivars to C. nucum, evaluated the changes in several resistance compounds in the nutshell before and after weevil feeding, and explored the potential physiological mechanism of these changes, which would provide a theoretical basis for cultivating insect-resistant hazel cultivars and reducing pesticide use.

2. Materials and Methods

2.1. Experimental Site and Stand

The experimental site is located at Xiushan village of Siping City, Jilin Province, China (43°55′66″ N, 125°07′45″ E, 408 m a.s.l.). The area of the experimental stand is 20 ha, and the tree composition is a zonal mix of 3 hazel cultivars: DW, B21, and MZ. DW and B21 are two main planted hazel cultivars in China, and MZ is a wild type. The tree space was 3 m, the row space was 5 m, and all trees for the experiment were 8 years old. No pesticide treatments were applied on the stand during the trials.

2.2. Experimental Design

Three rows of hazel trees were randomly selected from each hazel cultivar, and 10 trees were randomly selected from each row to determine the hazelnut damage rate by weevils at harvest. The yield of each tree was hand-collected on the ground from early August to mid-September, based on three-year (2019, 2020, and 2021) observation. Nuts were examined in the laboratory to determine if they were damaged by C. nucum. All the nuts of each sample were first counted and separated into two groups, damaged nuts with the emergence hole of mature weevil larvae and intact nuts without the hole. Then, the intact nuts were shelled and divided into damaged kernels and undamaged kernels by the nut weevil. Damaged nuts included the damaged nuts with holes and damaged kernels, and healthy nuts were these undamaged kernels with intact shells.
The experimental insects were the unmated adults of the C. nucum collected from the experimental site after overwintering in 2021. For each cultivar, six trees were randomly selected in three rows, with a total of 18 healthy trees at a similar stage of bear fruit in three cultivars, and the distance of those selected trees was more than 20 m to prevent allelopathy; all trees were coded and labeled.
A total of 18 healthy trees were covered with a 40-mesh nylon net to prevent the weevil escaping or entry of other insects on 20 April 2021 before the weevil excavation. Nine trees were randomly selected as the treatment trees by randomly selecting one tree from each line of each cultivar, and four 50 cm long branchs with hazelnuts of each tree were selected from the east, west, north, and south directions and then covered with 40 mesh nylon net, while the remaining nine trees served as control trees. The collected unmatched weevils were paired for free mating and oviposition and placed on each net for all nine treatment trees of three cultivars, the control was nine trees without weevils. We started the feeding observation of weevils daily from the next day of the experiment. Damaged nuts were picked after 24 h when the female weevil adults bored holes and laid eggs in hazelnuts, and the same number of nuts were picked from the branches at the same position of the control trees. The nutshells were peeled from the hazelnuts, placed into liquid nitrogen, transported to the laboratory, and then stored at −80 °C.

Determination of Insect-Resistant Compounds in the Hazelnut Shells

A portion of the frozen hazelnut shells was dried at 60 °C and then ground. Terpenoid contents were evaluated using the linalool chromogenic assay. The detailed procedures were described in ref. [24]. Other compounds were determined using assay kits, following the manufacturer’s instructions, i.e., Tannin Content Assay Kit, Plant Total Phenol Content Assay Kit, Plant Flavonoids Content Assay Kit, Cellulose (CLL) Content Assay Kit, and Lignin Content Assay Kit, respectively. These kits were all purchased from Beijing box Biotechnology Co., Ltd., Beijing, China.

2.3. Determination of Defense Enzymes in the Hazelnut Shells

Hazelnut shells for enzyme activity assessment were grounded with liquid nitrogen. Enzyme activity was determined according to the manufacturer’s instructions using the Peroxidase (POD) Activity Assay Kit, Catalase (CAT) Activity Assay Kit, Superoxide Dismutase (SOD) Activity Assay Kit, Phenylalanine Ammonia-Lyase (PAL) Activity Assay Kit, Plant Lipoxidase (LOX) Activity Assay Kit, and Polyphenol Oxidase (PPO) Activity Assay Kit, respectively. These kits were all purchased from Beijing box Biotechnology Co., Ltd., Beijing, China.

2.4. Determination of Phytohormones in the Hazelnut Shells

Hazelnut shells for phytohormone content analysis were first grounded in liquid nitrogen. Phytohormone contents were determined according to the manufacturer’s instructions, using the plant hormone abscisic acid (ABA) ELISA Kit, plants jasmonic acid (JA) ELISA kit, and plant salicylic acid (SA)ELISA Kit, respectively. These kits were all purchased Keming Biotechnology Co., Ltd., Suzhou, China.

2.5. Data Analysis and Statistics

Statistical analysis and data processing were performed in Excel and SPSS. The difference in damage rate and insect-resistant compounds contents in shells of different cultivars before and after chewing by C. nucum was analysed using a one-way analysis of variance (ANOVA). The independent-sample t-test was used to determine changes in defense enzyme activity and phytohormones content in shells of different cultivars before and after C. nucum chewing, and the results were graphed using Prism 9 software (GraphPad Software). The Pearson correlation was used to evaluate the association between insect-resistant compounds, phytohormones, defense enzymes, and hazelnut damage rate. Results were graphed using Cytoscape software (http://www.cytoscape.org/, accessed on 21 December 2021).

3. Results

3.1. Resistance of Different Hazel Cultivars to the C. nucum

The resistance to C. nucum differed significantly among the three hazel cultivars. MZ had the lowest resistance, with a damage rate of 17.57%, while B21 had the highest resistance, with a damage rate of 7.15% (Figure 1).

3.2. Insect-Resistant Compounds in Hazelnut Shells

Four detected insect-resistant compounds (total terpenoid, tannin, total phenol, and flavonoids) in the shells differed significantly among three cultivars before C. nucum feeding (Table 1 and Table 2). The total terpenoid content of MZ was significantly lower than DW and B21 by 22.5% and 24.6%, respectively. The tannin content in B21 shells was the highest, whereas the DW was the lowest. The total phenol content in the shells of B21 was higher than DW and MZ by 38.8% and 44.7%; The content of flavonoids in the shells of DW was significantly lower than B21 and MZ by 46.2% and 44.0%, respectively. There were no significant differences among the three cultivars for the cellulose and lignin contents with approximately 125.33 mg/g and 65.22 mg/g, respectively.

3.3. Effect of Chewing on Insect-Resistant Compounds in Hazelnut Shells

The insect-resistant compounds in the shells after induction by C. nucum varied with hazel cultivars and the type of compounds (Table 3 and Table 4). The cellulose content in shells of B21 was significantly lower than DW and MZ by 5.5% and 5.7%, respectively. DW had higher lignin content than B21 and MZ by 9.3% and 7.0%, respectively. MZ had the lowest total terpenoid and phenol content and the highest flavonoid content. There were significant differences of total terpenoid content and tannin content among the three cultivars.

3.4. Effect of Chewing on Defense Enzymes Activity and Phytohormones Contents in Hazelnut Shells

The CAT and PPO activities in the hazelnut shells of three hazel cultivars significantly increased after induction by weevil feeding. In contrast, the activity of the other four defense enzymes varied across the hazel cultivars (Table 5, Figure 2). The POD, SOD, and LOX activities were significantly increased in the shells of DW after chewing. The SOD activities in the shells of B21 and LOX activity in the shells of MZ were also significantly increased after weevil feeding. PAL activity increased dramatically in the shells of MZ after chewing by C. nucum (Table 5, Figure 2).
The ABA and JA contents in the shells of three cultivars were significantly increased after C. nucum chewing. Additionally, SA contents of MZ and B21 shells significantly increased after C. nucum chewing (Table 5, Figure 3).

4. Discussion

The differences in defense response signal pathways and interaction networks, which included phytohormone metabolism, signal transduction, transport, and defense enzyme activity induced by plant physiological characteristics and genetic backgrounds of different cultivars, following herbivore attack, eventually altered the plants’ self-healing ability and downstream anti-insect active products [12,15]. SA, JA, and ABA are the most important signaling molecules in the signal pathway network of the plant defense response [25,26,27,28]. Several plant defense genes regulate the synthesis of these signaling molecules, as well as the activation of the defense responsive gene [29]. The different activities of mitogen-activated protein kinase (MAPKs) in the tobacco (Nicotiana tabacum) leaves from different cultivars after insect feeding lead to the difference level of JA, SA, and their associated transcript accumulation (WRKYs) [30], which are an important transcription factors in plants that modulate defense responses [31]. Silencing COI1 gene, which mediated JA-elicited defense responses in N. attenuata, led to the decrease of defense secondary metabolites by restricting JA-dependent in tissues and thereby reduced tobacco resistance to Manduca sexta [32]. ABA was beneficial for the promotion of callose deposition through suppressing β-1, 3-glucanase and inducing synthase activity in plant tissues, which constituted a physical barrier and increased rice resistance to Nilaparvata lugens feeding [33]. In the present investigation, the defense enzyme activities and phytohormones contents in the shells of different hazel cultivars, except for SA of DW, increased after C. nucum chewing, which could explain the differences in the resistance of three hazel cultivars to C. nucum. It is interesting that MZ, with the highest accumulation rate (differenceof before and after chewing) of JA, SA, and ABA, had the lowest resistance to C. nucum. The present results do not reveal the reason for this phenomenon, and the higher ABA level may help maintain leaf water potential, which enhances the phloem-feeding time and increases Medicago truncatula abundance [34].
Aside from phytohormone signaling molecules, some crucial enzymes are involved in the inhibition of reactive oxygen radicals in plant tissues [20] and insect-resistant secondary metabolites regulated the defense responses of plants [35]. SOD, as the first line of defense against reactive oxygen species (ROS), could dismutate the excessive ROS to H2O2 produced by insects feeding on plant tissues [36], whilst H2O2 is consumed by CAT and POD to water and oxygen to maintaining cell membrane stability [20]. LOX catalyzes the conversion of polyunsaturated acids, such as linolenic acid and linoleic acid, into 13(S) hydroperoxy-linolenic acid, which eventually generates JA and links to the JA pathway through a series of oxidation reactions [37]. PAL is a critical and rate-limiting enzyme of secondary metabolism in plants that catalyzes the synthesis of phenols from phenylalanine. Plants use phenols in the SA metabolic pathway to transform into a variety of insect-resistant substances, including phytoprotegerin, lignin, flavonoids, isoflavones, alkaloids, etc [35].
The hazelnut damage rate was significant related to SOD and the POD activity of the hazel cultivars after C. nucum chewing. B21, with the highest the activity of PAL, LOX, PPO, and SOD and the lowest POD and CAT activity, showed significantly higher resistance to C. nucum than the other two cultivars (Figure 2). These findings imply that the activity of resistance-related enzymes influenced the hazel resistance to C. nucum by enhancing the SOD and reducing the CAT and POD activity in the nutshell. The interaction regulatory network between insect-resistant enzymes and plant hormone signaling molecules is extremely complex. H2O2, which is produced by plants’ response to insects attacks, as a second messenger, induced particular defense genes to synthesize defense enzymes and increase PAL and PPO activities [38]. PAL is a major regulator and rate-limiting enzyme for the SA metabolic pathway in the plant phenylalanine metabolism, which regulated SOD and POD in the ROS system [39]. Furthermore, when insects attacked the plants, JA was rapidly synthesized through the oxylipin biosynthesis pathway, and the JA-mediated defense responses were rapidly primed under LOX catalyzation; then, the activities of SOD, CAT, and POD in the ROS system increased, which induced plants to produce terpenoids and polyphenols in response to insect feeding stress [40,41,42]. In our study, Pearson correlation analysis revealed a complex interaction among the hazelnut damage rate, insect-resistant compounds in nut shells, plant hormone contents, and enzyme activities involved in resistance (Figure 4). The results of the interaction and regulation directly impacted the production of compounds that defended insects in plant tissues and determined the plant resistance to insects.
In the figure, the red line indicates a significant positive correlation (p < 0.05), and the blue line indicates a significant negative correlation (p < 0.05). The thickness of the line indicates the strength of the correlation (in this network, the minimum negative correlation coefficient between the two parameters is −0.671, the maximum is −0.990, the minimum positive correlation coefficient is 0.5007, and the maximum is 0.978).
Phenolic compounds, terpenoids, nitrogenous compounds, and defense proteins are well-reported to have a direct defense against insect herbivores [43]. However, these compounds may exhibit a specialist insect resistance at a certain stage of plant ontogeny or when they are damaged by a specialist insect herbivore [44]. In a previous investigation, the lack of DIM2BOA-Glc (2,4-dihydroxy-7,8-dimethoxy-1,4-benzoxazin-3-one-O-glucoside) and HDM2BOA-Glc (2-hydroxy-4,7,8-trimethoxy-1,4-benzoxazin-3-one glucoside) in maize (Zea mays) leaves drastically decreased the resistance to Rhopalosiphum maidis [45,46], but did not influence the resistance to chewing insects, such as Mythimna separata, S. exigua, and Diabrotica balteata [45], because chewing insects can reduce the toxicity of benzoxazinoids (such as DIM2BOA-Glc and HDM2BOA-Glc) in plants by re-glucosylating benzoxazinoid-ligand [47,48]. Sap-sucking insects (such as aphids and other insects) lack the aforesaid detoxification mechanism in comparison to chewing insects [45,49]. Our results suggested that cellulose, flavonoids, and terpenoids were potentially insect-resistant compounds with a direct protective effect against C. nucum. Flavonoids and terpenoids contribute a major role in the defense systems of plants to insect pests [50,51,52]. However, the information regarding the impact of cellulose on pest infestation is still not sufficient.
Few studies suggested that the hazelnut damage rate determined with boring holes (oviposition) on the surface by the weevil female was negatively correlated with the hazelnut shell hardness [14]. However, the mechanism of hazelnut defense to C. nucum was still unclear. It is commonly understood that cellulose and lignin are the primary chemical components of plant cell walls, and they play an important role in the hardness and toughness of plant tissue [53]. The contents of cellulose and lignin in the nutshells of hazelnuts may interfere with the construction of decayed holes and breeding corridors in the hazelnut shell. Surprisingly, our results showed a negative correlation between insect defense and cellulose contents in nutshells, but not with lignin (Figure 4). It is considered that the higher the cellulose contents, the greater the hardness and toughness of the plant cell wall [53]; however, a recent study found that the hardness and toughness of the plant cell wall were determined by the structure, arrangement, and contents of cellulose, not only the contents of cellulose [46]. Furthermore, some insects may bore through the strong xylem, and the higher hardness of plant tissue cannot effectively prevent their damage to the host [54]. The regression analysis revealed a significant correlation between hazelnut defense to C. nucum and the ratio of cellulose-to-lignin in the nutshell (Figure 5). Therefore, we think a specific ratio of cellulose-to-lignin in the nutshell may provide a more effective structural defense index. Nonetheless, further research is needed to prove our thought, combined with plant tissues (cell) structure and C. nucum feeding characteristics. Importantly, the hardness and other physical properties of these hazelnut shells should be determined and assessed before and after induction.

5. Conclusions

The hazelnut showed a positive response to C. nucum attack through enhancing the specific defense enzyme activities (SOD, CAT, LOX, PPO, and POD) and the level of plant hormones (JA, SA, and ABA) in the nutshells. However, insect-resistant compounds (terpenoids, flavonoids, celluloses) responded to C. nucum feeding differently with three hazel cultivars, the ratio of cellulose-to-lignin in nutshell is a better physical structural index for hazelnut defense to C. nucum, except for the physiological indexes. Although, parts of the secondary metabolites are the important determinants of hazelnut against insect pests. It is necessary to discover the resistance mechanisms of plant to feeding induction, especially the changes in plant internal tissue structure, cell conformation, and mechanical features after insect feeding induction would be an exciting prospect.

Author Contributions

Conceptualization, X.L. and L.S. Song; investigation, D.X., J.H. and B.Y.; writing—original draft preparation, X.L.; writing—review and editing, X.L. and S.J.; funding acquisition, X.L. and S.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Jilin Province Science and Technology Development Plan Project (20220202115NC) and the Science and Technology Research Project of Education Department of Jilin Province (JJKH20220061KJ).

Data Availability Statement

The data included in this study are available upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Forests 14 00319 g001 550
Figure 1. The damage rate by C. nucum at harvest in three cultivars investigated in Yitong country (NE China), based on three years (2019, 2020, and 2021). Bars with different letters are statistically different (Tukey test, p < 0.001, F = 397.894).
Figure 1. The damage rate by C. nucum at harvest in three cultivars investigated in Yitong country (NE China), based on three years (2019, 2020, and 2021). Bars with different letters are statistically different (Tukey test, p < 0.001, F = 397.894).
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Figure 2. The activities of defense enzymes (Mean ± SE) in the shells of different hazel cultivars before and after chewing by C. nucum. ns p ≥ 0.05, * p < 0.05, *** p < 0.001 and **** p < 0.0001.
Figure 2. The activities of defense enzymes (Mean ± SE) in the shells of different hazel cultivars before and after chewing by C. nucum. ns p ≥ 0.05, * p < 0.05, *** p < 0.001 and **** p < 0.0001.
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Figure 3. The hormone content (Mean ± SE) in the shells of different hazel cultivars before and after chewing by C. nucum. ns p ≥0.05, * p < 0.05, *** p < 0.001 and **** p < 0.0001.
Figure 3. The hormone content (Mean ± SE) in the shells of different hazel cultivars before and after chewing by C. nucum. ns p ≥0.05, * p < 0.05, *** p < 0.001 and **** p < 0.0001.
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Figure 4. Pearson correlation analysis among hazelnut damage rate (DR), resistant-insect compounds, enzyme activities, and plant hormones.
Figure 4. Pearson correlation analysis among hazelnut damage rate (DR), resistant-insect compounds, enzyme activities, and plant hormones.
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Figure 5. Regression analysis of hazelnut damage rate with cellulose contents, lignin content, and the ratio of cellulose−to−lignin in nutshell after damaged by C. nucum.
Figure 5. Regression analysis of hazelnut damage rate with cellulose contents, lignin content, and the ratio of cellulose−to−lignin in nutshell after damaged by C. nucum.
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Table
Table 1. One-way ANOVA of insect-resistant compounds in hazelnut shells of different hazel cultivars.
Table 1. One-way ANOVA of insect-resistant compounds in hazelnut shells of different hazel cultivars.
Test IndexesSum of SquaresDfMean SquareFSig.
Total terpenoids0.0014<0.00039.753<0.001
Tannins0.16140.081111.800<0.001
Total phenols0.00940.0047.4630.024
Flavonoids0.00340.0014.4330.066
Celluloses0.06040.0301.0000.422
Lignins0.13640.0681.6940.261
Table
Table 2. The content of insect-resistant compounds in hazelnut shells of different hazel cultivars.
Table 2. The content of insect-resistant compounds in hazelnut shells of different hazel cultivars.
CultivarTest Indexes (mg/g)
CellulosesLigninsTotal TerpenoidsTanninsTotal PhenolsFlavonoids
DW126.33 ± 1.20 a66.67 ± 0.88 a0.84 ± 0.02 a3.17 ± 0.19 c1.63 ± 0.09 b0.47 ± 0.09 b
B21125.33 ± 0.88 a63.67 ± 1.76 a0.87 ± 0.02 a6.40 ± 0.17 a2.27 ± 0.18 a0.87 ± 0.07 a
MZ124.33 ± 0.88 a65.33 ± 0.33 a0.65 ± 0.02 b5.27 ± 0.09 b1.57 ± 0.15 b0.83 ± 0.15 a
Note: Different lower letters represent the significant difference among hazelnut cultivars at the level of p < 0.05.
Table
Table 3. One-way ANOVA of insect-resistant compounds in hazelnut shells of different hazel cultivars after chewing by C. nucum.
Table 3. One-way ANOVA of insect-resistant compounds in hazelnut shells of different hazel cultivars after chewing by C. nucum.
Test IndexesSum of SquaresDfMean SquareFSig.
Total terpenoids0.01740.0081719.023<0.001
Tannins0.25740.129131.602<0.001
Total phenols0.00940.00411.4000.009
Flavonoids0.00340.0025.1480.050
Celluloses1.12740.5639.0540.015
Lignins0.52740.2636.2370.034
Table
Table 4. The content of insect-resistant compounds in hazelnut shells of different hazel cultivars after chewing by C. nucum.
Table 4. The content of insect-resistant compounds in hazelnut shells of different hazel cultivars after chewing by C. nucum.
CultivarTest Indexes (mg/g)
CellulosesLigninsTotal TerpenoidsTanninsTotal PhenolsFlavonoids
DW133.30 ± 1.63 a71.37 ± 0.41 a1.66 ± 0.01 a3.67 ± 0.12 c3.00 ± 0.15 a1.17 ± 0.12 ab
B21126.03 ± 1.64 b65.30 ± 0.66 b1.37 ± 0.01 b7.80 ± 0.21 a2.67 ± 0.09 a0.83 ± 0.09 b
MZ133.67 ± 1.76 a66.67 ± 1.09 b0.63 ± 0.01 c5.50 ± 0.20 b2.23 ± 0.09 b1.27 ± 0.09 a
Note: Different lower letters represent the significant difference among hazelnut cultivars at the level of p < 0.05.
Table
Table 5. Independent sample t-test of defense enzyme activity and hormone content of different hazel cultivars before and after chewing by C. nucum.
Table 5. Independent sample t-test of defense enzyme activity and hormone content of different hazel cultivars before and after chewing by C. nucum.
CultivarTest IndexesTest of Homogeneity of VariancesDfSig. (Bilateral)
FSig.
DWPOD1.9840.1978<0.001
CAT0.2470.6328<0.001
SOD0.0340.8588<0.001
PAL1.1420.31680.010
LOX0.8720.3788<0.001
PPO1.0430.3378<0.001
ABA0.7620.40880.045
JA0.1630.69780.001
SA0.0170.89980.803
B21POD2.8110.13280.083
CAT0.4520.5208<0.001
SOD0.0750.7918<0.001
PAL0.8890.37380.008
LOX0.0050.94780.052
PPO0.1300.7288<0.001
ABA0.0000.99980.012
JA0.0930.7688<0.001
SA0.2240.64980.036
MZPOD0.0130.91380.545
CAT0.0090.9258<0.001
SOD0.0620.81080.120
PAL0.0560.8198<0.001
LOX0.0740.79280.001
PPO0.0440.8398<0.001
ABA0.1890.6758<0.001
JA0.0380.8508<0.001
SA0.4880.5058<0.001
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Li, X.; Xiu, D.; Huang, J.; Yu, B.; Jia, S.; Song, L. Nutshell Physicochemical Characteristics of Different Hazel Cultivars and Their Defensive Activity toward Curculio nucum (Coleoptera: Curculionidae). Forests 2023, 14, 319. https://doi.org/10.3390/f14020319

AMA Style

Li X, Xiu D, Huang J, Yu B, Jia S, Song L. Nutshell Physicochemical Characteristics of Different Hazel Cultivars and Their Defensive Activity toward Curculio nucum (Coleoptera: Curculionidae). Forests. 2023; 14(2):319. https://doi.org/10.3390/f14020319

Chicago/Turabian Style

Li, Xingpeng, Dongying Xiu, Jinbin Huang, Bo Yu, Shuxia Jia, and Liwen Song. 2023. "Nutshell Physicochemical Characteristics of Different Hazel Cultivars and Their Defensive Activity toward Curculio nucum (Coleoptera: Curculionidae)" Forests 14, no. 2: 319. https://doi.org/10.3390/f14020319

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