Next Article in Journal
Effect of Aqueous n-Butanol Treatments on Shelf-Life Extension of Longkong Fruit during Ambient Storage
Next Article in Special Issue
Role of Two Transcription Factors (TGA 1a and TGA 2.1) in the Mi-1-Mediated Resistance of Tomato to the Root-Knot Nematode Meloidogyne javanica
Previous Article in Journal
The Phosphoproteomic Response of Pepper (Capsicum annuum L.) Seedlings to Selenium Stress
Previous Article in Special Issue
Divergent Responses of Tomato Cultivars with Resistance to Tomato Yellow Leaf Curl Virus as Infected by Meloidogyne javanica
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 9
Issue 8
10.3390/horticulturae9080937
horticulturae-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Presenting the Secrets: Exploring Endogenous Defense Mechanisms in Chrysanthemums against Aphids

by
Changchen Xia
1,2,†,
Wanjie Xue
1,2,†,
Zhuozheng Li
1,2,
Jiaxu Shi
1,2,
Guofu Yu
2 and
Yang Zhang
1,2,*
1
Key Laboratory of Saline-Alkali Vegetation Ecology Restoration, Ministry of Education, College of Life Science, Northeast Forestry University, Harbin 150040, China
2
College of Life Science, Northeast Forestry University, Harbin 150040, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Horticulturae 2023, 9(8), 937; https://doi.org/10.3390/horticulturae9080937
Submission received: 18 July 2023 / Revised: 13 August 2023 / Accepted: 16 August 2023 / Published: 17 August 2023
(This article belongs to the Special Issue Plant-Parasitic Nematodes in Horticultural Crops)
Browse Figures
Review Reports Versions Notes

Abstract

:
As the second-largest cut flower plant globally and one of the top ten traditional flowers in China, chrysanthemums hold significant economic value, encompassing both ornamental and medicinal applications. However, aphids pose a considerable threat as one of the most critical pests affecting chrysanthemums. These pests not only diminish the ornamental value of chrysanthemums through feeding and reproduction but also transmit numerous plant viruses, causing irreversible damage. This review examines aphids’ feeding and damage patterns as a starting point, highlighting the unique endogenous defense mechanisms that have evolved in chrysanthemums during their continuous struggle against aphids. These mechanisms include constitutive defense and induced defense. In addition, we enumerate aphid-resistance genes that have been reported in chrysanthemums. Furthermore, this paper compares and predicts the aphid-resistance genes of other species based on the published Chrysanthemum nankingense genome, aiming to provide a valuable reference for future research on aphid-resistance genes in chrysanthemums.

1. Introduction

As the global economy expands, the ornamental plant industry has experienced rapid growth in recent years. Statistics indicate that the worldwide value of ornamental cut flower plants was estimated to reach USD17.6 million in 2021, accounting for one-third of the total global market share for ornamental plants [1]. Among these, chrysanthemums hold a significant position in the global ornamental plant market, being one of the ten most famous traditional flowers in China and the second-largest cut flower plant globally, following roses [2]. However, chrysanthemum cultivation faces challenges from various pests, with aphids posing a significant threat to their growth [3]. As hemipteran insects, aphids are widespread, encompassing around 4000 species [4]. Three primary species affect chrysanthemums: Macrosiphoniella sanborni, Aphis gossypii, and Myzus persicae [5,6]. These aphids uniquely select chrysanthemums as host plants and intensify the damage through their specific life history.
Research has shown that aphids are attracted to the odor of host plant extracts, while non-host plants repel them [7]. Under natural conditions, aphids employ a set of criteria to identify suitable host plants (Figure 1). It is the special color and volatile compounds in chrysanthemums that make aphids choose chrysanthemums as one of their host plants [8]. Additionally, aphids have developed a unique life history to adapt to the environment (Figure 2), which can allow better survival on the chrysanthemum. The mechanisms of parthenogenesis and sexual reproduction enable aphids to rapidly increase their population density and accelerate their encroachment on the host plant, the chrysanthemum. In contrast, sexual reproductive generations of aphids enhance their adaptability to host plant defenses through genetic recombination, which not only maintains the species’ characteristics but also produces mutations that ensure genetic diversity [9]. Furthermore, they can utilize a specific feeding strategy to minimize the plant defense response during infestations [10,11,12]. Therefore, aphids become a major pest of chrysanthemums during their growth and cultivation.
Under lengthy exposure to aphid attacks, chrysanthemums have developed a multi-tiered, three-dimensional defensive system consisting of two primary aspects: constitutive defense and induced defense [19]. Constitutive defense, the first line of defense, can interfere with aphids’ choice of chrysanthemums as host plants and then directly or indirectly slow down aphid infestation through physical barriers and chemicals produced by their metabolism. On the other hand, induced defense comes into play when chrysanthemums experience feeding damage caused by aphids. This type of defense diminishes the fitness of aphids to consume chrysanthemums by impacting food digestion and nutrient absorption, consequently inhibiting their further reproduction [20,21,22].
To preserve the ornamental and economic value of chrysanthemums, aphids are commonly managed through physical, chemical, and agricultural methods. However, physical control is labor-intensive, time-consuming, and can be costly [23]. Although chemical pesticides are progressively becoming more specific and less toxic, their misuse can heighten aphid resistance in plants, resulting in a vicious cycle of increased pesticide usage and resistance, as well as environmental pollution and ecological imbalance [24]. Agricultural control, such as regulating the growing environment and changing growing patterns, is more limited, subject to certain spatial and seasonal constraints, and is slower to show the effects of control. Therefore, this paper offers the possibility of controlling aphids by breeding transgenic crops by describing the endogenous defense mechanisms of chrysanthemums and tapping into the genes that can produce aphid-resistant characters in chrysanthemums.

2. Damage Caused by Aphids to Chrysanthemums

Aphids can cause damage to chrysanthemum growth, development, and ornamental value in the following three ways.

2.1. Aphid Feeding

The distribution of aphid damage on chrysanthemum plants is closely related to the plant’s physiological age. This may be due to varying nutrient levels and plant secondary metabolite requirements for aphid growth [7]. To obtain the necessary nutrients, aphids alter the chrysanthemum’s normal physiological resource allocation, such as transferring nitrogen from the apical growth zone to the feeding site and mobilizing amino acids from other plant organs to the sieve tube. This disruption can cause issues like leaf curling, slow growth, abnormal flower bud development, and even total death in chrysanthemums [11]. Aphids also release their saliva during the feeding process. Aphid saliva contains various enzymes, such as cellulases and pectinases, which facilitate the penetration of the aphids’ stylets into plant cell walls [25,26]. Additionally, polyphenol oxidase and peroxidases reduce the toxicity of phenolic compounds secreted by the plant, ensuring continuous feeding by aphids [27]. In legumes, the saliva contains calcium-binding proteins, preventing phloem blockage and allowing aphids to feed on the same part for several hours, which can cause more serious damage to plants [28,29]. However, the presence of this phenomenon in chrysanthemums needs to be further verified. Furthermore, aphid saliva interferes with metabolic activities such as photosynthesis and cell wall synthesis in plants [30].

2.2. Aphid Secretions

Honeydew secreted by aphids can block chrysanthemum leaf pores and negatively impact the plant’s photosynthesis [5]. As honeydew dries, its sugars produce a high osmotic pressure concentration, leading to the separation of plant leaf cell mass walls, making them thinner and more susceptible to pathogens. Additionally, honeydew can create a suitable environment for black molds, causing spots on chrysanthemum leaves. The aphid cuticle can also remain on the plant’s surface, affecting the plant’s ornamental value (Figure 3) [7].

2.3. Aphid-Borne Viruses

Aphids can transmit Chrysanthemum virus B (CVB), Tomato Aspermy virus V (TAV), and Tobacco Cucumber mosaic virus (CMV). CVB infection can cause brown scabs on chrysanthemum leaves and even necrotic streaks on petals [31]. TAV can lead to dwarfing and deformation of chrysanthemum plants, significantly reducing their ornamental value. The presence of aphid-borne plant viruses increases the attractiveness and suitability that aphids have for the host plant, promoting the production of winged aphids that can migrate with the virus [5,32]. Due to the mechanism of aphid selection of host plants [8], even non-host plants can become infected with plant viruses. In short, the virus carried by aphids is far more harmful to chrysanthemums than the aphids themselves are to chrysanthemums.

3. Constitutive Defense

Constitutive defenses refer to the physical and chemical factors that plants inherently possess to deter external attacks. These defenses can be categorized into physical and chemical defenses. Physical defenses involve creating mechanical barriers that impede aphids from feeding through the plant’s physical composition. In contrast, chemical defenses prevent aphids from feeding or poisons them using naturally occurring volatile or non-volatile substances.

3.1. Physical Defense

3.1.1. Leaf Structure

Chrysanthemum morifolium Ramat. (chrysanthemum) ‘Hangbaiju’ was grafted as scions and Artemisia annua (mugwort), which is highly resistant to aphids, was used as rootstocks. The aphid resistance of the grafted seedlings was significantly improved [33]. The leaves of grafted seedlings exhibit a tighter cell structure than the cuttings of ‘Hangbaiju’, such as thicker cell layers of fenestrated tissue and thinner cell layers of spongy tissue. Alterations in the leaf structure of grafted seedlings and cuttings can inform the characterization of highly resistant chrysanthemum varieties.

3.1.2. Leaf Color

As mentioned earlier, aphids initially select their hosts by detecting light waves reflected from the plant surface [34,35], meaning that the plant’s color is selected first. Aphids exhibit varying sensitivity to plant color, being more attracted to land when chrysanthemum leaves are yellow-green, brighter, and more colorful [16]. Consequently, aphid-resistant chrysanthemum leaves are dark green.

3.1.3. Leaf Surface Barriers

In several groups of experiments involving aphid-resistant and non-aphid-resistant chrysanthemums, it was discovered that aphid-resistant chrysanthemums tend to develop greater mechanical barriers to aphid feeding. These barriers manifest as increased height, length, and density of leaf epidermal hairs; thicker and more abundant leaf epicuticular waxes; and deeper location of vascular bundles within the plant [36,37]. When selecting a host plant (Figure 1), aphids must pierce the cells using their stylets to access the sap [13]. In summary, the chrysanthemum structure mentioned above prevents aphids’ mouthparts from penetrating the cells to reach the sieve tube, thereby exerting an anti-aphid effect.
Among the many structures of chrysanthemum leaf surface barriers, trichomes play a crucial role in physical defense and are classified into two types: glandular and non-glandular. The primary trichomes on the chrysanthemum surface are multicellular peltate glandular trichomes, T-trichomes, and others [38]. Glandular trichomes poison or trap aphids by secreting toxins and mucus on the plant surface [39], while non-glandular trichomes reduce chrysanthemum damage by mechanically preventing aphids from moving across the plant surface. Dendranthema morifolium (chrysanthemum) variety ‘Zhongshanjingui’ hybridizes with Artemisia vulgaris (mugwort) ‘Variegata’, which exhibits a higher abundance of glands and trichomes than their parent plants, making them more resistant to aphids [40].

3.2. Chemical Defense

3.2.1. Volatile Compounds

Volatile compounds, such as terpenoids and their oxygenated derivatives, play a crucial role in the interactions among chrysanthemums, aphids, and their natural enemies, forming a line of defense in the chemical defense of chrysanthemums. One significant factor contributing to the hybrid Chrysanthemum’s greater resistance to aphids compared to its parent is its increased capacity for terpenoid synthesis.
Among these compounds, germacrene D significantly inhibits arthropod feeding (Figure 4a) [41,42]. Furthermore, (E)-β-farnesene, an aphid alarm pheromone (Figure 4a), causes aphids to cease feeding and rapidly flee their hosts while strongly attracting the aphid’s natural enemy, the ladybird [43,44]. This compound can also be combined with pesticides for more effective aphid control [42,45]. Pyrethrins, unique aphid-resistant substances found in Tanacetum cinerariifolium (pyrethrum), consist of six compounds (Figure 4b): Pyrethrins I, Pyrethrins II, Cinerin I, Cinerin II, Jasmolin I, and Jasmolin II. These compounds exhibit repellent and touch-killing action against aphids and act as neurotoxins that inhibit excitation transmission [46].

3.2.2. Non-Volatile Compounds

Non-volatile secondary metabolites often protect chrysanthemums by allowing aphids to feed on them and subsequently producing toxic or repellent effects. The primary non-volatile secondary metabolites in chrysanthemums are flavonoid compounds, including flavonols and isoflavonoids. Due to their oxidation, these compounds are toxic to phytophagous insects, and their content is positively correlated with plant resistance to aphids [47]. Flavonoids can also cause aphids to reject food and limit their growth and development. The primary alkaloids in chrysanthemum are pyrrolizidine alkaloids, which are entomotoxic and exhibit toxic effects on aphids and other pests. These alkaloids interfere with insects’ nervous systems, causing nerve paralysis and ultimately death [48,49]. Chrysanthemum also contains various polyacetylenes (Figure 4c), such as Chrysindins A–D, which are cytotoxic [50]. However, their precise effect on aphids remains to be investigated.

4. Induced Defense

When chrysanthemums experience biotic stress from aphids, they initiate changes in their nutrient levels, phytohormones, and defense proteins to counter the aphid attack. These defense mechanisms involve repairing damaged cells, disrupting aphid nutrient uptake and digestion, and releasing toxins. This type of defense is referred to as induced defense. In contrast to constitutive defense, induced defense is only activated in response to biotic stresses.

4.1. Nutrients and Reactive Oxygen Species

Soluble sugars and soluble proteins are nutrients closely associated with induced defenses. When aphids attack chrysanthemums, soluble sugar metabolism will increase to synthesize other defensive substances. Thus, aphids have reduced sugar uptake due to the consumption of soluble sugars [51]. Aphid infestation also elevates soluble protein levels, likely because the plant requires numerous enzymes to initiate its defense system [52].
Upon mechanical damage to chrysanthemum cells, large clusters of reactive oxygen species (ROS) are produced, including hydroxyl free radical (OH-), alkyl free radical (RO-), nitrosyl free radical (NO-), hypochlorous acid (HOCl), peroxyl free radical (ROO-), hydrogen peroxide (H2O2), and superoxide anions (O2−) [53]. These ROS play a crucial role in defending chrysanthemums against aphids by directly preventing aphid feeding, such as causing oxidative damage to the aphid’s intestines and oxidizing plant nutrients required by the aphid, thereby preventing nutrient acquisition [54]. Moreover, ROS can act as secondary messengers, activating the plant’s internal defense system [55].

4.2. Defense Proteins

Chrysanthemum plants contain defense proteins, which are generally classified into two categories: antioxidant enzymes and defense enzymes. Antioxidant enzymes, including superoxide dismutase (SOD), ascorbate peroxidase (APX), and peroxidase (POD), primarily function to counterbalance the elevated oxidation levels caused by aphid-inflicted damage to chrysanthemum cells. In contrast, defense enzymes generate toxic secondary metabolites. Other substances that alleviate cell damage can be generated too. Upon exposure to aphid stress, defense protein content increases, with higher resistance in chrysanthemum plants correlating to a faster rate of defense protein augmentation [37].
When aphids penetrate the chrysanthemum’s epidermis, they disrupt the plant’s redox balance, leading to elevated ROS content and the accumulation of oxidants such as hydrogen peroxide. This accumulation can damage plant membrane structures [13,56]. However, the plant’s secondary metabolites and antioxidant enzymes can significantly reduce ROS levels, restoring the oxygen-reduction balance and preventing irreversible damage to chrysanthemums caused by excessive oxidant buildup [57].
Polyphenol oxidase (PPO) is a defense enzyme in chrysanthemums, serving four primary functions: (1) PPO catalyzes the synthesis of phenolic compounds into o-benzoquinone, which is toxic to aphids (Figure 5) [58]. (2) Due to quinones’ reactive nature, they can undergo complex chemical reactions with proteins containing nucleophilic groups, such as amino and sulfhydryl groups, resulting in phenolic complexes. The growth of aphids requires proteins containing lysine, histidine, cysteine, and methionine. However, treating these proteins with PPO leads to significant losses in these amino acids, which reduces the nutritional value of proteins for aphid feeding and provides further resistance (Figure 5) [59]. (3) When plant cells experience physical damage, PPO is released, initiating an enzymatic reaction in the presence of oxygen that produces a melanin-like brown pigment, which inhibits the spread of pathogenic bacteria [60]. (4) PPOs secondary metabolism promotes plant cell lignification, enhancing lignin synthesis, repairing damaged cell walls, and thickening undamaged cell walls. This process increases mechanical barriers to aphid feeding and deprives nutrients of pathogenic bacteria, ultimately leading to their death [61].
The phenylpropanoid pathway is a crucial defense signaling pathway in plants, with phenylalanine ammonia-lyase (PAL) serving as a key catalyst. In the presence of PAL, phenylalanine can be deaminated to form cinnamate, a precursor of numerous physiologically important compounds. This process enables the synthesis of essential plant compounds, such as lignans, lignin, flavonoids, and coumarins, catalyzed by p-coumaroyl CoA (Figure 6) [62]. Among these compounds, lignans and lignin strengthen the toughness of cell walls and promote lignification, creating mechanical barriers that hinder aphid feeding. Flavonoids can exhibit toxic effects on aphids [63]. Furthermore, peroxidase (POD) also functions as a defense enzyme, catalyzing the biosynthesis of lignin and suberin. This process reinforces the chemical connections between cell wall components, increasing stability and further impeding aphid feeding [64].

4.3. Cell Wall Modifications

The chrysanthemum, a type of vascular plant, illustrates an intriguing cellular composition. Its cell wall is composed of approximately 30% cellulose, 30% hemicellulose, and 35% pectin; the residual 1–5% consists of structural proteins [65]. Aphid resistance is primarily exhibited through two mechanisms involving plant cell wall modification. The first implicates key genes that govern the structural modification and composition of the cell wall, thereby enhancing resistance to aphids via mechanical fortification of the regulated cell wall structure. Secondly, the hydrolysis of cell wall polysaccharides by aphid saliva generates oligomers and small molecules. These compounds can be identified by resistance receptors, triggering a defensive response. And the two often work together because of their close association. Notably, the area of cell wall modification in chrysanthemums remains relatively underexplored; therefore, the references provided below should serve as potential subjects for future substantiation.
Pectin, a major component of plant cell walls, plays a significant role in both mechanisms of cell wall modifications, causing aphid resistance. Structurally, pectin can be classified into homogalacturonan (HG), rhamnogalacturonan I (RG-I), and rhamnogalacturonan II (RG-II) [66]. HG, which constitutes about 60% of cell wall pectin, is the most extensively investigated variety [67]. While feeding on plants, aphids secrete cell wall-modifying enzymes (CWMEs) within their saliva, such as pectin methylesterases (PMEs), polygalacturonases (PGs), and pectate lyase enzymes (PLs) [68]; these degrade cell wall polysaccharides, thereby extracting nutrients from the cells’ contents. One reaction involves HG undergoing unmethyl-esterification catalyzed by PMEs with increased activity. This reaction, along with depolymerization facilitated by PGs or PLs, results in the production of oligogalacturonides (OGs). Plants perceive OGs as damage-associated molecular patterns (DAMPs) [69,70], due to the binding of these OGs to the extracellular pectin-binding domain of wall-associated kinase receptors (WAK). And then, an innate defense response is triggered via the mitogen-activated protein kinase (MAPK) signaling pathway [71,72].
Beyond OGs, the process of unmethyl-esterification also produces methanol [73,74], a volatile compound—another DAMPs capable of initiating both personal and communal defenses across neighboring plants against aphids [73,75]. However, the timing and concentration of methanol emissions are inconsistent and can thus exhibit varying effects on aphid resistance, which may differ between species [76]. As such, further experiments are required in chrysanthemums.
Plants can produce modifying enzymes via their gene regulation. For example, pectin methylesterase inhibitors (PMEIs) inhibit the unmethyl-esterification of HGs to enhance the antimicrobial property of plants [77], while polygalacturonase inhibitors (PGIPs) specifically counteract pathogens’ efforts to hydrolyze HGs [78]. Extraordinarily, these alterations not only enhance the mechanical strength of the cell wall but also indirectly affect methanol release, amplifying the defensive capabilities of the cell wall against both pathogens and pests [75,79]. Concurrently, the plant reinforces its protective system by activating other defense pathways, such as those involving jasmonic acid and ethylene, releasing signaling molecules that further strengthen its defenses [11].

4.4. Plant Hormones

Constructing phytohormone overexpression vectors in chrysanthemum poses a challenge due to the complex metabolic pathways of phytohormones. Consequently, researchers have examined the impact of phytohormones on endogenous defense in chrysanthemums through spraying exogenous plant hormones.
It has been observed that abscisic acid (ABA) in chrysanthemums enhances the expression of CmTPS1 and CmTPS2 genes [80], increases resistance toward aphids, and elevates ROS content, thereby activating antioxidant enzyme activity. In conclusion, the regulation of aphid populations by ABA may be associated with the equilibrium between ROS concentrations and the activity of antioxidant enzymes in chrysanthemums [81].
In contrast, the salicylic acid (SA) pathway is more intricate [82]: (1) SA can induce a reduction in chlorophyll content, initiating the plant’s defenses for improved resistance against aphids. (2) SA can promote the conversion of soluble sugar metabolism toward the synthesis of other aphid-resistant materials. (3) SA can increase the total protein content, including soluble and insoluble in chrysanthemums, likely due to the replenishment of numerous enzymes required to initiate the plant’s defense system under stress. (4) After SA spraying, ROS and malondialdehyde (MDA) content in chrysanthemum increased in advance, but the increase was smaller than that in aphid stress alone, potentially protecting plant cells from high ROS concentration and acting as an advanced defense. (5) SA also promoted the early and efficient expression of flavonoid synthesis genes and significantly increased the flavonoid content in plants when exposed to aphid stress after spraying.
Methyl jasmonate (MeJA) is a well-studied phytohormone that plays a crucial role in aphid resistance in chrysanthemums. Although MeJA is not directly toxic to insects when ingested, it can be employed to control pests when spraying externally. This implies that MeJA achieves control not through inherent toxicity but by modulating the plant’s defense system [83]. The specific effects are as follows (Figure 7) [51,84,85]: (1) MeJA induces lignin accumulation, reinforcing the cell wall and acting as a defense against aphids by maintaining the activity of PAL and POD enzymes and enabling the responsive expression of lignin-synthesizing genes. (2) MeJA reduces the amount of MDA accumulation in cells, thereby decreasing cellular damage. (3) MeJA increases the activity of defense or antioxidant enzymes, such as SOD, POD, PAL, and PPO, which can prevent extensive cellular damage by ROS and synthesize other essential substances, including phenols and flavonoids that constitute the plant defense system. (4) MeJA rapidly enhances proline content to stabilize damaged plant structures, reduce cell acidity, and stabilize biomacromolecules. (5) MeJA increases the soluble protein content, thereby enhancing the enzyme content of the plant defense system and the content of defense proteins involved in aphid resistance. (6) MeJA decreases the soluble saccharides content of the plant body, which can be used by the metabolism to produce other defense tissues and reduce nutrient uptake by aphids. (7) MeJA increases the activity of trypsin proteinase inhibitor (TI) and chymotrypsin proteinase inhibitor (CI) to prevent important proteins in chrysanthemums from being hydrolyzed by their high protease content. Upon entering the aphid’s body, these substances can bind to proteases present within the insect, consequently inhibiting or impairing the aphid’s ability to absorb essential nutritional proteins. (8) MeJA increases the content of endogenous jasmonic acid by enhancing the activity of lipoxygenase (LOX), which activates the defense system in chrysanthemums.

5. Aphid-Resistance Genes

Through the observation of aphid resistance in various chrysanthemum varieties, it was discovered that certain strains stably inherit the aphid resistance trait, indicating the presence of specific aphid-resistance genes in the plant to maintain this characteristic. The identified aphid-resistance genes primarily contribute to the chrysanthemum plants’ constitutive defense mechanisms, such as synthesizing defensive substances and regulating phytohormone signaling pathways.
WRKY is a family of transcription factors that are unique to plants. It is associated with plant growth and development, responses to abiotic stresses such as salt damage, low temperature, high temperature, drought, and plant defense against pathogenic bacteria and aphid stresses [86]. As a defense response, SA can induce WRKY family gene expression [87]. Currently, CmWRKY33 (GenBank: AJF11718.1), CmWRKY48 (GenBank: AJF11724.1), and CmWRKY53 (GenBank: AJF11719.1) have been found to play crucial roles in aphid resistance in chrysanthemum, regulating secondary metabolites involved in plant defense and acting through the SA or MeJA pathway [88].
The MYB family of transcription factors has numerous roles in plants. MYB proteins serve as key elements in the regulatory network controlling plant hormone synthesis and regulation, primary and secondary metabolism, and responses to biotic or abiotic stresses [89]. Among them, CmMYB15 (GenBank: ALF46700.1) and CmMYB19 (GenBank: ALF46701.1) can promote lignin synthesis for defense against aphids [90,91]. Additionally, CgCOMT (GenBank: BAK42963.1) is identified to be expressed in roots, stems, and leaves for lignin synthesis, exhibiting the highest expression in the stem.
The initial step in pyrethrin synthesis depends on the chrysanthemol synthase (CHS), which is regulated by TcCHS (GenBank: AFZ61535.1) in Tanacetum cinerariifolium (pyrethrum). Moreover, TcCHS can generate pyrethrin derivatives as well as volatile chrysanthemol. The overexpression of the TcCHS gene in Chrysanthemum morifolium (chrysanthemum) results in the production of a chrysanthemol glycoside derivative, as well as volatile chrysanthemol. Volatile chrysanthemol functions to repel aphids, while non-volatile glycosides, stored in vacuoles, deter aphids by affecting them upon ingestion and discouraging further feeding [92].
Plants contain 200 times more carotenoids, the precursors of ABA, than ABA. They accumulate in large quantities, forming a “carotenoid pool” [93]. The 9-cis-epoxycarotenoid dioxygenase (NCED) has been demonstrated to be a crucial enzyme in the ABA synthesis pathway [94]. CmNCED3-1 (GenBank: BAF36655.1) is a key gene in Chrysanthemum that influences the ABA synthesis pathway, which can enhance the expression level of NCED, thereby utilizing ABA to regulate defense against aphids.
Aphid feeding-induced expression of CmHSFB1 (GenBank: AUG69001.1) enhances the expression of genes involved in the synthesis or positive regulation of ROS and stimulates the expression of downstream heat stress proteins. Both mechanisms contribute to aphid stress resistance [95].
In addition to the previously reported genes, we also selected genes from other species with aphid resistance functions for prediction in Chrysanthemum nankingense (Table 1). We compared the protein data obtained from NCBI: https://www.ncbi.nlm.nih.gov/ (accessed on 24 March 2023) with protein sequences from Chrysanthemum nankingense using local blast and selected those protein sequences with potential aphid resistance as our prediction in chrysanthemum. The protein sequence of Chrysanthemum nankingense was derived from www.amwayabrc.com, accessed on 24 March 2023.
Furthermore, apart from directly predicting based on the reported aphid-resistance genes, we also explored other potential aphid-resistance genes indirectly. For example, if epidermal wax thickness plays a crucial role in aphid defense, then genes in the synthetic epidermal wax pathway can also be predicted as aphid-resistance genes in chrysanthemums (Table 2) [103]. The predictions are made using the same method as the direct predictions.

6. Concluding Remarks

In recent years, the effectiveness of conventional physical methods and chemical pesticides for insect control has shown limited progress and significant drawbacks, including adverse side effects. As a result, biological control of aphids has become a prominent research topic. Studies on the mechanisms of aphid resistance in chrysanthemums and aphid-resistant transgenic research have attracted increasing attention. This paper presents an overview of the defense mechanisms and unique aphid-resistance genes that have evolved in the ongoing battle between chrysanthemums and aphids.
By analyzing the inherent defense mechanisms of chrysanthemums, several aspects of aphid resistance strategies beyond poisoning aphids have been identified, such as modifying the tissue structure of the chrysanthemum epidermis, increasing defense protein content, regulating phytohormone levels, and attracting aphids’ natural enemies. These factors are all closely related to the regulation of chrysanthemum genes. By using the reported and predicted aphid-resistance genes discussed in this paper, it is possible to further develop aphid-resistant plants at the genetic level. It is now crucial to examine the impact of chrysanthemum genes on their physical structure, secondary metabolites, and phytohormonal pathways. A comprehensive understanding of chrysanthemum genes may hold the key to addressing future pest challenges.

Author Contributions

Conceptualization, C.X. and Y.Z.; methodology, W.X.; software, Z.L., C.X. and G.Y.; validation, C.X., W.X. and Y.Z.; formal analysis, J.S.; investigation, C.X.; data curation, C.X.; writing—original draft preparation, C.X.; writing—review and editing, Y.Z. and W.X.; visualization, C.X.; supervision, W.X. and Y.Z.; project administration, Y.Z.; funding acquisition, Y.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by a grant from the Natural Science Foundation of Heilongjiang Province of China (grant number: LH2021C006).

Data Availability Statement

The sequence data of reference genes that were used and analyzed during this study are available in the NCBI (https://www.ncbi.nlm.nih.gov, accessed on 24 March 2023) and Chrysanthemum Genome Database (www.amwayabrc.com, accessed on 24 March 2023).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Mekapogu, M.; Kwon, O.-K.; Song, H.-Y.; Jung, J.-A. Towards the Improvement of Ornamental Attributes in Chrysanthemum: Recent Progress in Biotechnological Advances. Int. J. Mol. Sci. 2022, 23, 12284. [Google Scholar] [CrossRef] [PubMed]
  2. Teixeira da Silva, J.A.; Shinoyama, H.; Aida, R.; Matsushita, Y.; Raj, S.K.; Chen, F. Chrysanthemum Biotechnology: Quo Vadis? Crit. Rev. Plant Sci. 2013, 32, 21–52. [Google Scholar] [CrossRef]
  3. Nalam, V.; Louis, J.; Shah, J. Plant defense against aphids, the pest extraordinaire. Plant Sci. 2019, 279, 96–107. [Google Scholar] [CrossRef] [PubMed]
  4. Blackman, R.; Eastop, V. Taxonomic Issues; CABI International: Wallingford, UK, 2017; pp. 1–36. [Google Scholar]
  5. Vehrs, S.L.C.; Walker, G.P.; Parrella, M.P. Comparison of Population Growth Rate and Within-Plant Distribution between Aphis gossypii and Myzus persicae (Homoptera: Aphididae) Reared on Potted Chrysanthemums. J. Econ. Entomol. 1992, 85, 799–807. [Google Scholar] [CrossRef]
  6. Zhong, J.; Wang, Y.; Lu, Y.; Ma, X.; Zhang, Q.; Wang, X.; Zhang, Q.; Sun, M. Identification and Expression Analysis of Chemosensory Genes in the Antennal Transcriptome of Chrysanthemum Aphid Macrosiphoniella sanborni. Insects 2022, 13, 597. [Google Scholar] [CrossRef] [PubMed]
  7. Storer, J.R.; Emden, H.F. Antibiosis and antixenosis of chrysanthemum cultivars to the aphid Aphis gossypii. Entomol. Exp. Appl. 1995, 77, 307–314. [Google Scholar] [CrossRef]
  8. Guldemond, J.A.; Tigges, W.T.; De Vrijer, P.W.F. Host Races of Aphis gossypii (Homoptera: Aphididae) on Cucumber and Chrysanthemum. Environ. Entomol. 1994, 23, 1235–1240. [Google Scholar] [CrossRef]
  9. Simon, J.C.; Stoeckel, S.; Tagu, D. Evolutionary and functional insights into reproductive strategies of aphids. C. R. Biol. 2010, 333, 488–496. [Google Scholar] [CrossRef]
  10. Thompson, G.A.; Goggin, F.L. Transcriptomics and functional genomics of plant defence induction by phloem-feeding insects. J. Exp. Bot. 2006, 57, 755–766. [Google Scholar] [CrossRef]
  11. Goggin, F.L. Plant-aphid interactions: Molecular and ecological perspectives. Curr. Opin. Plant Biol. 2007, 10, 399–408. [Google Scholar] [CrossRef]
  12. Walling, L.L. Avoiding Effective Defenses: Strategies Employed by Phloem-Feeding Insects. Plant Physiol. 2008, 146, 859–866. [Google Scholar] [CrossRef] [PubMed]
  13. Powell, G.; Tosh, C.R.; Hardie, J. Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 2006, 51, 309–330. [Google Scholar] [CrossRef] [PubMed]
  14. Hewer, A.; Becker, A.; van Bel, A.J. An aphid’s Odyssey–The cortical quest for the vascular bundle. J. Exp. Biol. 2011, 214, 3868–3879. [Google Scholar] [CrossRef] [PubMed]
  15. Döring, T.F.; Kirchner, S. A model for colour preference behaviour of spring migrant aphids. Philos. Trans. R. Soc. B Biol. Sci. 2022, 377, 20210283. [Google Scholar] [CrossRef] [PubMed]
  16. Hardie, J. Spectral specificity for targeted flight in the black bean aphid, Aphis fabae. J. Insect Physiol. 1989, 35, 619–626. [Google Scholar] [CrossRef]
  17. Zhou, J.J.; He, X.L.; Liu, R.; Field, L.M.; Davies, T.G.E.; Williamson, M.S. Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol. 2010, 8, e1000313. [Google Scholar]
  18. Shu-xian, W. The Summary of Aphids’ Life Cycle. Heilongjiang Agric. Sci. 2009, 2, 74–75. [Google Scholar]
  19. Kempel, A.; Schädler, M.; Chrobock, T.; Fischer, M.; van Kleunen, M. Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc. Natl. Acad. Sci. USA 2011, 108, 5685–5689. [Google Scholar] [CrossRef]
  20. Agrawal, A.A. Induced Responses to Herbivory in Wild Radish: Effects on Several Herbivores and Plant Fitness. Ecology 1999, 80, 1713–1723. [Google Scholar] [CrossRef]
  21. War, A.R.; Paulraj, M.G.; Ahmad, T.; Buhroo, A.A.; Hussain, B.; Ignacimuthu, S.; Sharma, H.C. Mechanisms of plant defense against insect herbivores. Plant Signal. Behav. 2012, 7, 1306–1320. [Google Scholar] [CrossRef]
  22. Fürstenberg-Hägg, J.; Zagrobelny, M.; Bak, S. Plant defense against insect herbivores. Int. J. Mol. Sci. 2013, 14, 10242–10297. [Google Scholar] [CrossRef]
  23. Vincent, C.; Weintraub, P.; Hallman, G. Chapter 200—Physical Control of Insect Pests. In Encyclopedia of Insects (Second Edition); Resh, V.H., Cardé, R.T., Eds.; Academic Press: San Diego, CA, USA, 2009; pp. 794–798. [Google Scholar]
  24. Tang, F.H.M.; Lenzen, M.; McBratney, A.; Maggi, F. Risk of pesticide pollution at the global scale. Nat. Geosci. 2021, 14, 206–210. [Google Scholar] [CrossRef]
  25. Cherqui, A.; Tjallingii, W.F. Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J. Insect Physiol. 2000, 46, 1177–1186. [Google Scholar] [CrossRef] [PubMed]
  26. Harmel, N.; Létocart, E.; Cherqui, A.; Giordanengo, P.; Mazzucchelli, G.; Guillonneau, F.; De Pauw, E.; Haubruge, E.; Francis, F. Identification of aphid salivary proteins: A proteomic investigation of Myzus persicae. Insect Mol. Biol. 2008, 17, 165–174. [Google Scholar] [CrossRef] [PubMed]
  27. Urbanska, A.; Tjallingii, W.F.; Dixon, A.F.G.; Leszczynski, B. Phenol oxidising enzymes in the grain aphid’s saliva. Entomol. Exp. Appl. 1998, 86, 197–203. [Google Scholar] [CrossRef]
  28. Furch, A.C.; van Bel, A.J.; Will, T. Aphid salivary proteases are capable of degrading sieve-tube proteins. J. Exp. Bot. 2015, 66, 533–539. [Google Scholar] [CrossRef]
  29. Will, T.; Tjallingii, W.F.; Thönnessen, A.; van Bel, A.J. Molecular sabotage of plant defense by aphid saliva. Proc. Natl. Acad. Sci. USA 2007, 104, 10536–10541. [Google Scholar] [CrossRef] [PubMed]
  30. Giordanengo, P.; Brunissen, L.; Rusterucci, C.; Vincent, C.; van Bel, A.; Dinant, S.; Girousse, C.; Faucher, M.; Bonnemain, J.L. Compatible plant-aphid interactions: How aphids manipulate plant responses. C. R. Biol. 2010, 333, 516–523. [Google Scholar] [CrossRef]
  31. Chirkov, S.N.; Sheveleva, A.; Snezhkina, A.; Kudryavtseva, A.; Krasnov, G.; Zakubanskiy, A.; Mitrofanova, I. Highly divergent isolates of chrysanthemum virus B and chrysanthemum virus R infecting chrysanthemum in Russia. PeerJ 2022, 10, e12607. [Google Scholar] [CrossRef]
  32. Colvin, J.; Omongo, C.A.; Govindappa, M.R.; Stevenson, P.C.; Maruthi, M.N.; Gibson, G.; Seal, S.E.; Muniyappa, V. Host-Plant Viral Infection Effects on Arthropod-Vector Population Growth, Development and Behaviour: Management and Epidemiological Implications. In Advances in Virus Research; Academic Press: Cambridge, MA, USA, 2006; Volume 67, pp. 419–452. [Google Scholar]
  33. Zhang, X.Y.; Sun, X.Z.; Zhang, S.; Yang, J.H.; Liu, F.F.; Fan, J. Comprehensive transcriptome analysis of grafting onto Artemisia scoparia W. to affect the aphid resistance of chrysanthemum (Chrysanthemum morifolium T.). BMC Genomics 2019, 20, 776. [Google Scholar] [CrossRef]
  34. Gao, L.L.; Kamphuis, L.G.; Kakar, K.; Edwards, O.R.; Udvardi, M.K.; Singh, K.B. Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor expression profiling. New Phytol. 2010, 186, 980–994. [Google Scholar] [CrossRef] [PubMed]
  35. Ahmed, N.; Chamila Darshanee, H.L.; Fu, W.Y.; Hu, X.S.; Fan, Y.; Liu, T.X. Resistance of Seven Cabbage Cultivars to Green Peach Aphid (Hemiptera: Aphididae). J. Econ. Entomol. 2018, 111, 909–916. [Google Scholar] [CrossRef] [PubMed]
  36. Yang, B.Y.; Kong, X.Y.; Pan, H. A study on the structure of micromarphology and its resistant to aphis of chrysanthemum. J. South China Agric. Univ. 1992, S1, 66–68. [Google Scholar]
  37. He, J.; Chen, F.; Chen, S.; Lv, G.; Deng, Y.; Fang, W.; Liu, Z.; Guan, Z.; He, C. Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. J. Plant Physiol. 2011, 168, 687–693. [Google Scholar] [CrossRef]
  38. Sumitomo, K.; Nishijima, T.; Onozaki, T.; Shibata, M. Density, Length and Development of Non-Glandular Trichome on the Leaves of Wild Chrysanthemums and Chrysanthemum Cultivars. Hort. Res. 2006, 5, 351–356. [Google Scholar] [CrossRef]
  39. Ramirez, A.M.; Stoopen, G.; Menzel, T.R.; Gols, R.; Bouwmeester, H.J.; Dicke, M.; Jongsma, M.A. Bidirectional Secretions from Glandular Trichomes of Pyrethrum Enable Immunization of Seedlings. Plant Cell 2012, 24, 4252–4265. [Google Scholar] [CrossRef] [PubMed]
  40. Deng, Y.; Chen, S.; Lu, A.; Chen, F.; Tang, F.; Guan, Z.; Teng, N. Production and characterisation of the intergeneric hybrids between Dendranthema morifolium and Artemisia vulgaris exhibiting enhanced resistance to chrysanthemum aphid (Macrosiphoniellasanbourni). Planta 2010, 231, 693–703. [Google Scholar] [CrossRef]
  41. Bruce, T.J.; Birkett, M.A.; Blande, J.; Hooper, A.M.; Martin, J.L.; Khambay, B.; Prosser, I.; Smart, L.E.; Wadhams, L.J. Response of economically important aphids to components of Hemizygia petiolata essential oil. Pest Manag. Sci. 2005, 61, 1115–1121. [Google Scholar] [CrossRef]
  42. Li, J.; Hu, H.; Chen, Y.; Xie, J.; Li, J.; Zeng, T.; Wang, M.; Luo, J.; Zheng, R.; Jongsma, M.A.; et al. Tissue specificity of (E)-β-farnesene and germacrene D accumulation in pyrethrum flowers. Phytochemistry 2021, 187, 112768. [Google Scholar] [CrossRef]
  43. Aquilino, K.M.; Cardinale, B.J.; Ives, A.R. Reciprocal effects of host plant and natural enemy diversity on herbivore suppression: An empirical study of a model tritrophic system. Oikos 2005, 108, 275–282. [Google Scholar] [CrossRef]
  44. Zhang, Y.M.; Huang, Y.F.; Tao, L.; Huang, J.W. Chemical components of essential oils from Flos chrysanthemi Indici in different areas. Chin. J. Chin. Mater. Medica 2002, 27, 265–267. [Google Scholar]
  45. Li, J.; Hu, H.; Mao, J.; Yu, L.; Stoopen, G.; Wang, M.; Mumm, R.; de Ruijter, N.C.A.; Dicke, M.; Jongsma, M.A.; et al. Defense of pyrethrum flowers: Repelling herbivores and recruiting carnivores by producing aphid alarm pheromone. N. Phytol. 2019, 223, 1607–1620. [Google Scholar] [CrossRef] [PubMed]
  46. Matsuda, K. Pyrethrin biosynthesis and its regulation in Chrysanthemum cinerariaefolium. Top. Curr. Chem. 2012, 314, 73–81. [Google Scholar] [PubMed]
  47. Meng, F.; Wang, Z.; Zang, Z.; Song, X.P.; Sun, J.; Li, W.B. Relationship between Isoflavanones Content and Soybean Resistance to Soybean Aphid. Crops 2011, 3, 11–15. [Google Scholar]
  48. Fu, P.P.; Xia, Q.; Lin, G.; Chou, M.W. Pyrrolizidine Alkaloids—Genotoxicity, Metabolism Enzymes, Metabolic Activation, and Mechanisms. Drug Metab. Rev. 2004, 36, 1–55. [Google Scholar] [CrossRef] [PubMed]
  49. Lindigkeit, R.; Biller, A.; Buch, M.; Schiebel, H.M.; Boppré, M.; Hartmann, T. The two facies of pyrrolizidine alkaloids: The role of the tertiary amine and its N-oxide in chemical defense of insects with acquired plant alkaloids. Eur. J. Biochem. 1997, 245, 626–636. [Google Scholar] [CrossRef] [PubMed]
  50. Liu, L.L.; Wang, R.; Shi, Y.P. Chrysindins A–D, polyacetylenes from the flowers of Chrysanthemum indicum. Planta Med. 2011, 77, 1806–1810. [Google Scholar] [CrossRef]
  51. Fan, J.; Zhang, X.Y.; Sun, X.Z.; Xu, B.Y. Effect of methyl jasmonate on aphid resistance of chrysanthemum. Ying Yong Sheng Tai Xue Bao 2020, 31, 4197–4205. [Google Scholar]
  52. Castro, A.M.; Clúa, A.; Giménez, D.O.; Tocho, É.; Tacaliti, M.S.; Collado, M.B.; Worland, A.J.; Bottini, R.; Snape, J.W. Genetic Resistance to Greenbug is Expressed with Higher Contents of Proteins and Non-Structural Carbohydrates in Wheat Substitution Lines. In Proceedings of the Wheat Production in Stressed Environments: 7th International Wheat Conference, Mar del Plata, Argentina, 27 November–2 December 2005; Springer: Dordrecht, The Netherlands, 2007. [Google Scholar]
  53. Halliwell, B.; Gutteridge, J.M.C. Free Radicals in Biology and Medicine; Oxford University Press: Oxford, UK, 2015. [Google Scholar]
  54. Bi, J.L.; Felton, G.W. Foliar oxidative stress and insect herbivory: Primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 1995, 21, 1511–1530. [Google Scholar] [CrossRef]
  55. Orozco-Cardenas, M.; Ryan, C.A. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA 1999, 96, 6553–6557. [Google Scholar] [CrossRef]
  56. Moloi, M.J.; van der Westhuizen, A.J. The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J. Plant Physiol. 2006, 163, 1118–1125. [Google Scholar] [CrossRef] [PubMed]
  57. Foyer, C.H.; Noctor, G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 2005, 17, 1866–1875. [Google Scholar] [CrossRef] [PubMed]
  58. Vámos-Vigyázó, L. Polyphenol oxidase and peroxidase in fruits and vegetables. Crit. Rev. Food Sci. Nutr. 1981, 15, 49–127. [Google Scholar] [CrossRef] [PubMed]
  59. Felton, G.W.; Donato, K.K.; Broadway, R.M.; Duffey, S.S. Impact of oxidized plant phenolics on the nutritional quality of dietar protein to a noctuid herbivore, Spodoptera exigua. J. Insect Physiol. 1992, 38, 277–285. [Google Scholar] [CrossRef]
  60. Mishra, B.B.; Gautam, S.; Sharma, A. Purification and characterisation of polyphenol oxidase (PPO) from eggplant (Solanum melongena). Food Chem. 2012, 134, 1855–1861. [Google Scholar] [CrossRef]
  61. Kowalski, S.P.; Eannetta, N.T.; Hirzel, A.T.; Steffens, J.C. Purification and Characterization of Polyphenol Oxidase from Glandular Trichomes of Solanum berthaultii. Plant Physiol. 1992, 100, 677–684. [Google Scholar] [CrossRef] [PubMed]
  62. Vogt, T. Phenylpropanoid Biosynthesis. Mol. Plant 2010, 3, 2–20. [Google Scholar] [CrossRef]
  63. Dixon, R.A.; Achnine, L.; Kota, P.; Liu, C.J.; Reddy, M.S.; Wang, L. The phenylpropanoid pathway and plant defence–A genomics perspective. Mol. Plant Pathol. 2002, 3, 371–390. [Google Scholar] [CrossRef]
  64. Espelie, K.E.; Franceschi, V.R.; Kolattukudy, P.E. Immunocytochemical localization and time course of appearance of an anionic peroxidase associated with suberization in wound-healing potato tuber tissue. Plant Physiol. 1986, 81, 487–492. [Google Scholar] [CrossRef]
  65. Ochoa-Villarreal, M.; Aispuro, E.; Vargas-Arispuro, I.; Martínez-Téllez, M. Plant Cell Wall Polymers: Function, Structure and Biological Activity of Their Derivatives. Polymerization 2012, 4, 63–86. [Google Scholar]
  66. Caffall, K.H.; Mohnen, D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res. 2009, 344, 1879–1900. [Google Scholar] [CrossRef] [PubMed]
  67. Ridley, B.L.; O’Neill, M.A.; Mohnen, D. Pectins: Structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 2001, 57, 929–967. [Google Scholar] [CrossRef]
  68. Silva-Sanzana, C.; Estevez, J.M.; Blanco-Herrera, F. Influence of cell wall polymers and their modifying enzymes during plant-aphid interactions. J. Exp. Bot. 2020, 71, 3854–3864. [Google Scholar] [CrossRef] [PubMed]
  69. Kubicek, C.P.; Starr, T.L.; Glass, N.L. Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi. Annu. Rev. Phytopathol. 2014, 52, 427–451. [Google Scholar] [CrossRef] [PubMed]
  70. Lionetti, V.; Fabri, E.; De Caroli, M.; Hansen, A.R.; Willats, W.G.; Piro, G.; Bellincampi, D. Three Pectin Methylesterase Inhibitors Protect Cell Wall Integrity for Arabidopsis Immunity to Botrytis. Plant Physiol. 2017, 173, 1844–1863. [Google Scholar] [CrossRef] [PubMed]
  71. Bacete, L.; Mélida, H.; Miedes, E.; Molina, A. Plant cell wall-mediated immunity: Cell wall changes trigger disease resistance responses. Plant J. 2018, 93, 614–636. [Google Scholar] [CrossRef] [PubMed]
  72. Kohorn, B.D. Cell wall-associated kinases and pectin perception. J. Exp. Bot. 2016, 67, 489–494. [Google Scholar] [CrossRef]
  73. Dorokhov, Y.L.; Komarova, T.V.; Petrunia, I.V.; Frolova, O.Y.; Pozdyshev, D.V.; Gleba, Y.Y. Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLoS Pathog. 2012, 8, e1002640. [Google Scholar] [CrossRef]
  74. Von Dahl, C.C.; Hävecker, M.; Schlögl, R.; Baldwin, I.T. Caterpillar-elicited methanol emission: A new signal in plant-herbivore interactions? Plant J. 2006, 46, 948–960. [Google Scholar] [CrossRef]
  75. Hann, C.T.; Bequette, C.J.; Dombrowski, J.E.; Stratmann, J.W. Methanol and ethanol modulate responses to danger- and microbe-associated molecular patterns. Front. Plant Sci 2014, 5, 550. [Google Scholar] [CrossRef]
  76. Silva-Sanzana, C.; Celiz-Balboa, J.; Garzo, E.; Marcus, S.E.; Parra-Rojas, J.P.; Rojas, B.; Olmedo, P.; Rubilar, M.A.; Rios, I.; Chorbadjian, R.A.; et al. Pectin Methylesterases Modulate Plant Homogalacturonan Status in Defenses against the Aphid Myzus persicae. Plant Cell 2019, 31, 1913–1929. [Google Scholar] [CrossRef] [PubMed]
  77. An, S.H.; Sohn, K.H.; Choi, H.W.; Hwang, I.S.; Lee, S.C.; Hwang, B.K. Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 2008, 228, 61–78. [Google Scholar] [CrossRef] [PubMed]
  78. Agüero, C.B.; Uratsu, S.L.; Greve, C.; Powell, A.L.; Labavitch, J.M.; Meredith, C.P.; Dandekar, A.M. Evaluation of tolerance to Pierce’s disease and Botrytis in transgenic plants of Vitis vinifera L. expressing the pear PGIP gene. Mol. Plant Pathol. 2005, 6, 43–51. [Google Scholar] [CrossRef] [PubMed]
  79. Peñuelas, J.; Filella, I.; Stefanescu, C.; Llusià, J. Caterpillars of Euphydryas aurinia (Lepidoptera: Nymphalidae) feeding on Succisa pratensis leaves induce large foliar emissions of methanol. N. Phytol. 2005, 167, 851–857. [Google Scholar] [CrossRef] [PubMed]
  80. Wang, W.; Li, F.; Zhang, W.; Wang, Y.; Song, A.; Jiang, J.; Chen, F.; Chen, S. Cloning and expression characteristics of CmTPS1 like gene in Chrysanthemum morifolium. J. Nanjing Agric. Univ. 2020, 43, 58–64. [Google Scholar]
  81. Zhang, Z.; Wang, C.B.; Fang, W.M.; Chen, F.D.; Jiang, J.F.; Guan, Z.Y.; Chen, S.M. ABA spraying enhanced aphids resistance in chrysanthemum and corresponding physiological mechanisms. Zhiwu Shengli Xuebao/Plant Physiol. J. 2014, 50, 1857–1862. [Google Scholar]
  82. Mishra, A.K.; Baek, K.H. Salicylic Acid Biosynthesis and Metabolism: A Divergent Pathway for Plants and Bacteria. Biomolecules 2021, 11, 705. [Google Scholar] [CrossRef] [PubMed]
  83. Avdiushko, S.A.; Brown, G.C.; Dahlman, D.L.; Hildebrand, D.F. Methyl Jasmonate Exposure Induces Insect Resistance in Cabbage and Tobacco. Environ. Entomol. 1997, 26, 642–654. [Google Scholar] [CrossRef]
  84. Liu, Q.; Luo, L.; Zheng, L. Lignins: Biosynthesis and Biological Functions in Plants. Int. J. Mol. Sci. 2018, 19, 335. [Google Scholar] [CrossRef]
  85. Li, M.; Wang, G. Effect of Drought Stress on Activities of Cell Defense Enzymes and Lipid Peroxidation in Glycyrrhiza uralensis Seedlings. Acta Ecol. Sin. 2002, 22, 503–507. [Google Scholar]
  86. Jiang, J.; Ma, S.; Ye, N.; Jiang, M.; Cao, J.; Zhang, J. WRKY transcription factors in plant responses to stresses. J. Integr. Plant Biol. 2017, 59, 86–101. [Google Scholar] [CrossRef]
  87. Bi, M.; Li, X.; Yan, X.; Liu, D.; Gao, G.; Zhu, P.; Mao, H. Chrysanthemum WRKY15-1 promotes resistance to Puccinia horiana Henn. via the salicylic acid signaling pathway. Hortic. Res. 2021, 8, 6. [Google Scholar] [CrossRef] [PubMed]
  88. Zhang, W.; Gao, T.; Li, P.; Tian, C.; Song, A.; Jiang, J.; Guan, Z.; Fang, W.; Chen, F.; Chen, S. Chrysanthemum CmWRKY53 negatively regulates the resistance of chrysanthemum to the aphid Macrosiphoniella sanborni. Hortic. Res. 2020, 7, 109. [Google Scholar] [CrossRef] [PubMed]
  89. Carré, I.A.; Kim, J.Y. MYB transcription factors in the Arabidopsis circadian clock. J. Exp. Bot. 2002, 53, 1551–1557. [Google Scholar] [CrossRef] [PubMed]
  90. Wang, Y.; Sheng, L.; Zhang, H.; Du, X.; An, C.; Xia, X.; Chen, F.; Jiang, J.; Chen, S. CmMYB19 Over-Expression Improves Aphid Tolerance in Chrysanthemum by Promoting Lignin Synthesis. Int. J. Mol. Sci. 2017, 18, 619. [Google Scholar] [CrossRef]
  91. An, C.; Sheng, L.; Du, X.; Wang, Y.; Zhang, Y.; Song, A.; Jiang, J.; Guan, Z.; Fang, W.; Chen, F.; et al. Overexpression of CmMYB15 provides chrysanthemum resistance to aphids by regulating the biosynthesis of lignin. Hortic. Res. 2019, 6, 84. [Google Scholar] [CrossRef] [PubMed]
  92. Hu, H.; Li, J.; Delatte, T.; Vervoort, J.; Gao, L.; Verstappen, F.; Xiong, W.; Gan, J.; Jongsma, M.A.; Wang, C. Modification of chrysanthemum odour and taste with chrysanthemol synthase induces strong dual resistance against cotton aphids. Plant Biotechnol. J. 2018, 16, 1434–1445. [Google Scholar] [CrossRef]
  93. Parry, A.D.; Horgan, R. Carotenoids and abscisic acid (ABA) biosynthesis in higher plants. Physiol. Plant. 1991, 82, 320–326. [Google Scholar] [CrossRef]
  94. Ren, H.; Gao, Z.; Chen, L.; Wei, K.; Liu, J.; Fan, Y.; Davies, W.J.; Jia, W.; Zhang, J. Dynamic analysis of ABA accumulation in relation to the rate of ABA catabolism in maize tissues under water deficit. J. Exp. Bot. 2007, 58, 211–219. [Google Scholar] [CrossRef]
  95. Li, F.; Zhang, H.; Zhao, H.; Gao, T.; Song, A.; Jiang, J.; Chen, F.; Chen, S. Chrysanthemum CmHSFA4 gene positively regulates salt stress tolerance in transgenic chrysanthemum. Plant Biotechnol. J. 2018, 16, 1311–1321. [Google Scholar] [CrossRef]
  96. Niu, L.; Pan, L.; Zeng, W.; Lu, Z.; Cui, G.; Fan, M.; Xu, Q.; Wang, Z.; Li, G. Dynamic transcriptomes of resistant and susceptible peach lines after infestation by green peach aphids (Myzus persicae Sülzer) reveal defence responses controlled by the Rm3 locus. BMC Genom. 2018, 19, 846. [Google Scholar] [CrossRef] [PubMed]
  97. Feinbaum, R.L.; Ausubel, F.M. Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol. Cell. Biol. 1988, 8, 1985–1992. [Google Scholar] [PubMed]
  98. Theologis, A.; Ecker, J.R.; Palm, C.J.; Federspiel, N.A.; Kaul, S.; White, O.; Alonso, J.; Altafi, H.; Araujo, R.; Bowman, C.L.; et al. Sequence and analysis of chromosome 1 of the plant Arabidopsis thaliana. Nature 2000, 408, 816–820. [Google Scholar] [CrossRef] [PubMed]
  99. Tabata, S.; Kaneko, T.; Nakamura, Y.; Kotani, H.; Kato, T.; Asamizu, E.; Miyajima, N.; Sasamoto, S.; Kimura, T.; Hosouchi, T.; et al. Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. Nature 2000, 408, 823–826. [Google Scholar]
  100. Cho, A.; Jang, H.; Baek, S.; Kim, M.-J.; Yim, B.; Huh, S.M.; Kwon, S.-H.; Yu, H.-J.; Mun, J.H. An improved Raphanus sativus cv. WK10039 genome localizes centromeres, uncovers variation of DNA methylation and resolves arrangement of the ancestral Brassica genome blocks in radish chromosomes. Theor. Appl. Genet. 2022, 135, 1731–1750. [Google Scholar] [CrossRef] [PubMed]
  101. Yang, Z.; Liu, J.; Luo, L.; Ye, S.F.; Yang, Y.; Zhang, G.; Wang, X.; Zhang, J. The Cotton GhRac6 Gene Encoding a Plant ROP/RAC Protein Improves the Plant Defense Response to Aphid Feeding. Plant Mol. Biol. Rep. 2018, 36, 888–896. [Google Scholar] [CrossRef]
  102. Pitrat, M.; Lecoq, H. Inheritance of resistance to cucumber mosaic virus transmission by Aphis gossypii in Cucumis melo. Phytopathology 1980, 70, 958–961. [Google Scholar] [CrossRef]
  103. Laila, R.; Robin, A.H.; Yang, K.; Park, J.I.; Suh, M.C.; Kim, J.; Nou, I.S. Developmental and Genotypic Variation in Leaf Wax Content and Composition, and in Expression of Wax Biosynthetic Genes in Brassica oleracea var. capitata. Front. Plant Sci. 2016, 7, 1972. [Google Scholar] [CrossRef]
  104. Cheng, C.-Y.; Krishnakumar, V.; Chan, A.P.; Thibaud-Nissen, F.; Schobel, S.; Town, C.D. Araport11: A complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 2017, 89, 789–804. [Google Scholar] [CrossRef]
  105. Patwari, P.; Salewski, V.; Gutbrod, K.; Kreszies, T.; Dresen-Scholz, B.; Peisker, H.; Steiner, U.; Meyer, A.J.; Schreiber, L.; Dörmann, P. Surface wax esters contribute to drought tolerance in Arabidopsis. Plant J. 2019, 98, 727–744. [Google Scholar] [CrossRef]
  106. Takeuchi, M.; Kegasa, T.; Watanabe, A.; Tamura, M.; Tsutsumi, Y. Expression analysis of transporter genes for screening candidate monolignol transporters using Arabidopsis thaliana cell suspensions during tracheary element differentiation. J. Plant Res. 2018, 131, 297–305. [Google Scholar] [CrossRef]
Horticulturae 09 00937 g001
Figure 1. Aphid selection of host plants [13,14]: (a) The migrating aphid’s choice of landing on a particular plant depends on receiving the plant-reflected wavelengths (between about 500 nm and 600 nm) [15,16]; upon landing, antennal receptors detect the plant surface volatiles for initial assessment. (b) After making contact with the plant surface, the aphid briefly and tentatively pierces the epidermis using its stylet (<1 min) and ingests a small quantity of plant sap for further evaluation by a gustatory organ in the epipharyngeal area. (c) If the initial assessment is favorable, the aphid penetrates the epidermis to pierce the mesophyll and parenchyma tissues and briefly ingests more sap from vacuoles for additional evaluation and to determine the appropriateness of further ingestion (<1 min). (d) Upon identifying the host plant, the aphid pierces the epidermis of the leaf and passes through the intercellular air spaces of the mesophyll cells using its stylet to reach the sieve tube element in plant phloem, releasing salivary enzymes to protect the mouthparts and prevent plant tissue repair, enabling continuous sap consumption. If ingestion in the sieve tube exceeds 10 min, the host plant is deemed suitable for aphid reproduction and growth, allowing for extended feeding periods (>1 h).
Figure 1. Aphid selection of host plants [13,14]: (a) The migrating aphid’s choice of landing on a particular plant depends on receiving the plant-reflected wavelengths (between about 500 nm and 600 nm) [15,16]; upon landing, antennal receptors detect the plant surface volatiles for initial assessment. (b) After making contact with the plant surface, the aphid briefly and tentatively pierces the epidermis using its stylet (<1 min) and ingests a small quantity of plant sap for further evaluation by a gustatory organ in the epipharyngeal area. (c) If the initial assessment is favorable, the aphid penetrates the epidermis to pierce the mesophyll and parenchyma tissues and briefly ingests more sap from vacuoles for additional evaluation and to determine the appropriateness of further ingestion (<1 min). (d) Upon identifying the host plant, the aphid pierces the epidermis of the leaf and passes through the intercellular air spaces of the mesophyll cells using its stylet to reach the sieve tube element in plant phloem, releasing salivary enzymes to protect the mouthparts and prevent plant tissue repair, enabling continuous sap consumption. If ingestion in the sieve tube exceeds 10 min, the host plant is deemed suitable for aphid reproduction and growth, allowing for extended feeding periods (>1 h).
Horticulturae 09 00937 g001
Horticulturae 09 00937 g002
Figure 2. Common Aphid life history [9,17,18]. “♀” means females and “♂” means males. (a) Holocycle. (A) Generally, wingless female aphids reproduce through parthenogenesis, producing larvae in spring. (B) In the case of heteroecious aphids, winged female aphids are produced so that they can migrate to summer host plants at the end of spring. In summer, wingless females generate various larval types depending on environmental conditions: (C) when the host plant becomes unsuitable for aphid reproduction, winged females emerge to migrate to appropriate host plants for parthenogenesis; (D) when the host conditions and environment are favorable, wingless females continue parthenogenesis. Aphids alter their reproductive mode in response to impending seasonal changes which result in temperatures unfavorable for their survival. (E,F) As autumn approaches, wingless female aphids produce both male and female larvae. In general, antoecious aphids are wingless. In the case of heteroecious aphids, winged female and winged male aphids migrate to winter host plants. (G) Adult males and females engage in sexual reproduction through mating, generating eggs to withstand the harsh winter conditions. (H) In the subsequent spring, the eggs hatch into wingless female aphids, initiating a new reproductive cycle. (b) Anholocycle. Throughout its life history, no male aphids occur, and female aphids reproduce through parthenogenesis all over the year. When aphid population densities become too high, winged aphids are produced that migrate and spread between host plants.
Figure 2. Common Aphid life history [9,17,18]. “♀” means females and “♂” means males. (a) Holocycle. (A) Generally, wingless female aphids reproduce through parthenogenesis, producing larvae in spring. (B) In the case of heteroecious aphids, winged female aphids are produced so that they can migrate to summer host plants at the end of spring. In summer, wingless females generate various larval types depending on environmental conditions: (C) when the host plant becomes unsuitable for aphid reproduction, winged females emerge to migrate to appropriate host plants for parthenogenesis; (D) when the host conditions and environment are favorable, wingless females continue parthenogenesis. Aphids alter their reproductive mode in response to impending seasonal changes which result in temperatures unfavorable for their survival. (E,F) As autumn approaches, wingless female aphids produce both male and female larvae. In general, antoecious aphids are wingless. In the case of heteroecious aphids, winged female and winged male aphids migrate to winter host plants. (G) Adult males and females engage in sexual reproduction through mating, generating eggs to withstand the harsh winter conditions. (H) In the subsequent spring, the eggs hatch into wingless female aphids, initiating a new reproductive cycle. (b) Anholocycle. Throughout its life history, no male aphids occur, and female aphids reproduce through parthenogenesis all over the year. When aphid population densities become too high, winged aphids are produced that migrate and spread between host plants.
Horticulturae 09 00937 g002
Horticulturae 09 00937 g003
Figure 3. Aphid secretions and aphid-borne viruses’ damage to chrysanthemums.
Figure 3. Aphid secretions and aphid-borne viruses’ damage to chrysanthemums.
Horticulturae 09 00937 g003
Horticulturae 09 00937 g004
Figure 4. (a) Chemical structure formulae of germacrene D and (E)-β-farnesene, (b) Chemical structure formulae of pyrethrin I, pyrethrin II, cinerin I, cinerin II, jasmolin I, and jasmolin II; (c) Chemical structure formulae of chrysindins A-D.
Figure 4. (a) Chemical structure formulae of germacrene D and (E)-β-farnesene, (b) Chemical structure formulae of pyrethrin I, pyrethrin II, cinerin I, cinerin II, jasmolin I, and jasmolin II; (c) Chemical structure formulae of chrysindins A-D.
Horticulturae 09 00937 g004
Horticulturae 09 00937 g005
Figure 5. PPO catalyzes the synthesis of o-benzoquinone, toxic to aphids, and forms phenolic complexes which reduce the nutritional value of proteins ingested by aphids.
Figure 5. PPO catalyzes the synthesis of o-benzoquinone, toxic to aphids, and forms phenolic complexes which reduce the nutritional value of proteins ingested by aphids.
Horticulturae 09 00937 g005
Horticulturae 09 00937 g006
Figure 6. Phenylalanine ammonia lyase (PAL) synthesizes numerous compound precursors, cinnamic acid, and p-coumaroyl CoA catalyzes synthesis of physiologically important compounds.
Figure 6. Phenylalanine ammonia lyase (PAL) synthesizes numerous compound precursors, cinnamic acid, and p-coumaroyl CoA catalyzes synthesis of physiologically important compounds.
Horticulturae 09 00937 g006
Horticulturae 09 00937 g007
Figure 7. The pathways of methyl jasmonate for aphid resistance. MeJA, methyl jasmonate; MDA, malondialdehyde; LOX, lipoxygenase; TI, trypsin proteinase inhibitor; CI, chymotrypsin proteinase inhibitor; JA, jasmonic acid; PAL, phenylalanine ammonia lyase; POD, peroxidase; PPO, Polyphenol oxidase; SOD, superoxide dismutase; ROS, reactive oxygen species.
Figure 7. The pathways of methyl jasmonate for aphid resistance. MeJA, methyl jasmonate; MDA, malondialdehyde; LOX, lipoxygenase; TI, trypsin proteinase inhibitor; CI, chymotrypsin proteinase inhibitor; JA, jasmonic acid; PAL, phenylalanine ammonia lyase; POD, peroxidase; PPO, Polyphenol oxidase; SOD, superoxide dismutase; ROS, reactive oxygen species.
Horticulturae 09 00937 g007
Table 1. Predicted aphid-resistance genes in Chrysanthemum nankingense.
Table 1. Predicted aphid-resistance genes in Chrysanthemum nankingense.
Gene AbbreviationAccession NumberSourceFunctionReferencePredictive Protein% IdentityAlignment LengthE-Value
RmXP_007225245.1Prunus persicabeta-xylosidase/alpha-L-arabinofuranosidase 2[96]CHR00089971-RA77.2427470.0
CHSAAA32771.1Arabidopsis thalianaChalcone synthase[97]CHR00028844-RA85.7513860.0
CHR00062418-RA85.4593920.0
CHR00019175-RA84.9493920.0
Cu/ZnSODNP_001077494.1Arabidopsis thalianacopper/zinc superoxide dismutase[98]CHR00045542-RA82.5906590.0
CHR00083274-RA80.9806940.0
CHR00058326-RA78.2426940.0
CHR00001194-RA76.8711475.26 × 10−78
CHR00061843-RA76.7121465.72 × 10−78
PRX7NP_199033.1Arabidopsis thalianaPeroxidase superfamily protein[99]CHR00037301-RA73.8102943.63 × 10−166
TCH4KAJ4877013.1Raphanus sativusTyrosine decarboxylase 1[100]CHR00084602-RA73.2224780.0
GhRacNP_001314362.1Gossypium hirsutumROP/Rac protein[101]CHR00004359-RA93.3331808.85 × 10−127
VatXP_008465871Cucumis meloHeavy metal-associated isoprenylated plant protein 39[102]CHR00066820-RA93.056724.58 × 10−30
CHR00086923-RA93.056724.58 × 10−30
Table 2. Predicted epidermal wax synthesis genes in Chrysanthemum nankingense.
Table 2. Predicted epidermal wax synthesis genes in Chrysanthemum nankingense.
Gene AbbreviationAccession NumberSourceRecnameReferencePredictive Protein% IdentityAlignment LengthE-Value
LTP2Q9S7I3.1Arabidopsis thalianaNon-specific lipid-transfer protein 2[104]CHR00049734-RA
CHR00038208-RA		50.847
48.246		118
114		5.15 × 10−33
1.17 × 10−30
FAR3Q93ZB9.1Arabidopsis thalianaFatty acyl-CoA reductase 3[104]CHR00057591-RA
CHR00092239-RA		57.407
51.120		486
491		0.0
2.16 × 10−170
WSD1Q93ZR6.1Arabidopsis thalianaWax ester synthase/
diacylglycerol acyltransferase 1		[105]CHR00049351-RA
CHR00071533-RA		39.738
41.304		458
368		3.81 × 10−119
7.34 × 10−85
ABCG11Q8RXN0.1Arabidopsis thalianaABC transporter G family member 11[106]CHR00028885-RA
CHR00053055-RA		77.874
57.803		696
628		0.0
0.0
LACS1O22898.1Arabidopsis thalianaLong chain acyl-CoA synthetase 1[104]CHR00023806-RA
CHR00075383-RA		62.367
64.791		659
622		0.0
0.0
KCS1Q9MAM3.1Arabidopsis thaliana3-ketoacyl-CoA synthase 1[104]CHR00017132-RA71.7344670.0
CHR00049310-RA62.4754930.0
CHR00035436-RA62.3484940.0
KCR1Q8L9C4.1Arabidopsis thalianaVery-long-chain 3-oxoacyl-CoA reductase 1[104]CHR00038450-RA
CHR00022927-RA		64.762
61.538		315
312		9.70 × 10−159
1.42 × 10−140
ECRQ9M2U2.1Arabidopsis thalianaVery-long-chain enoyl-CoA reductase[104]CHR00089558-RA
CHR00031281-RA		78.333
66.304		300
276		0.0
2.50 × 10−130
CER3Q8H1Z0.1Arabidopsis thalianaVery-long-chain aldehyde decarbonylase CER3[104]CHR00091218-RA
CHR00066836-RA		66.341
61.280		615
625		0.0
0.0
MAH1Q9FVS9.1Arabidopsis thalianaAlkane hydroxylase MAH1[104]CHR00033702-RA
CHR00073663-RA		45.669
46.220		508
463		4.13 × 10−167
6.45 × 10−152
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Xia, C.; Xue, W.; Li, Z.; Shi, J.; Yu, G.; Zhang, Y. Presenting the Secrets: Exploring Endogenous Defense Mechanisms in Chrysanthemums against Aphids. Horticulturae 2023, 9, 937. https://doi.org/10.3390/horticulturae9080937

AMA Style

Xia C, Xue W, Li Z, Shi J, Yu G, Zhang Y. Presenting the Secrets: Exploring Endogenous Defense Mechanisms in Chrysanthemums against Aphids. Horticulturae. 2023; 9(8):937. https://doi.org/10.3390/horticulturae9080937

Chicago/Turabian Style

Xia, Changchen, Wanjie Xue, Zhuozheng Li, Jiaxu Shi, Guofu Yu, and Yang Zhang. 2023. "Presenting the Secrets: Exploring Endogenous Defense Mechanisms in Chrysanthemums against Aphids" Horticulturae 9, no. 8: 937. https://doi.org/10.3390/horticulturae9080937

APA Style

Xia, C., Xue, W., Li, Z., Shi, J., Yu, G., & Zhang, Y. (2023). Presenting the Secrets: Exploring Endogenous Defense Mechanisms in Chrysanthemums against Aphids. Horticulturae, 9(8), 937. https://doi.org/10.3390/horticulturae9080937

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop