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Article

Dwarf Interstocks Improve Aroma Quality of ‘Huahong’ Apple (Malus × domestica)

by
Xiang Lu
1,2,
Yuan Gao
1,
Kun Wang
1,
Simiao Sun
1,
Zhao Liu
1,2,
Peng Yan
3,
Jianrong Feng
2,
Qingshan Li
1,2,
Lianwen Li
1 and
Dajiang Wang
1,*
1
Research Institute of Pomology, Chinese Academy of Agricultural Sciences (CAAS), Key Laboratory of Horticulture Crops Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, No.98 Xinghai South Street, Xingcheng 125100, China
2
Agricultural College of Shihezi University, Xinjiang Production and Construction Corps Key Laboratory of Special Fruits and Vegetables Cultivation Physiology and Germplasm Resources Utilization, Shihezi 832003, China
3
Institute of Horticulture Crops, Xinjiang Academy of Agricultural Sciences, No.403 Nanchang Road, Urumqi 830091, China
*
Author to whom correspondence should be addressed.
Agriculture 2022, 12(10), 1710; https://doi.org/10.3390/agriculture12101710
Submission received: 23 September 2022 / Revised: 12 October 2022 / Accepted: 14 October 2022 / Published: 17 October 2022
(This article belongs to the Section Agricultural Product Quality and Safety)
Browse Figures
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Abstract

:
‘Huahong’ is a popular apple cultivar because of its anti-browning properties and appealing aroma and flavor. It is mainly planted by grafting on dwarf interstocks in Northeast China. We investigated the different aroma profiles of apple fruits grown from six dwarf interstocks (‘CG24’, ‘SH38’, ‘SH3’, ‘MD001’, ‘Mac9’, and ‘CX5’) and from no interstocks (CK). A total of 55 VOCs were detected, including esters (25), aldehydes (14), alcohols (8), ketones (3), alkane hydroxyls (3), and acids (2). Among the VOCs, 48 were detected in the skin and 21 in the pulp. The skin of ‘Huahong’ apples had a strong sweet aroma, and the pulp was green with a subtle aroma. The dominant compounds (>5% of total content) in the skin were 2-methyl butyl acetate, hexyl 2-methyl butyrate, caproic acid butyl ester, hexanal, (Z)-2-heptene aldehyde, and 6-methyl-5-heptene-2-ketone, while in the pulp, they were 2-methyl butyl acetate, methanol, 2-methyl-1-butanol, hexanol, and hexane. Compared with CK, ‘SH38’, ‘MD001’, and ‘SH3’ interstocks had increased total aroma content, and ‘CX5’ and ‘CG24’ had suppressed aroma. The effects of interstocks on aroma were mainly reflected in skin. The VOC content ranged from 3297.52 to 9895.75 µg·kg−1 in skin, and from 748.62 to 1369.21 µg·kg−1 in pulp. PCA revealed that use of interstock ‘SH38’ mainly affected esters. ‘MD001’ affected hexane and 4-pentene-1-acetate; ‘Mac9’ and ‘SH3’ affected octanoic acid-2-methyl butyl ester, hexyl butyrate, and 2-methyl-1-butanol; and ‘CX5’ and ‘CG24’ had a greater impact on isoamyl propionate and 1-pentene-3-ol. Finally, ‘SH38’ had the highest principal comprehensive score. ‘SH38’ and ‘SH3’ interstocks resulted in significantly increased apple VOC content.

1. Introduction

The apple (Malus × domestica Borkh.) is one of the most popular and widely cultivated fruits in the world, and it is an important part of people’s daily diet. The flavor of fruits is a vital factor affecting consumer choice. Consumers have higher requirements for the flavor of fruits when there is an improvement in living standards. Both aroma and taste form the basis of flavor. The intensity of aroma depends on the amount and content of volatile organic compounds (VOCs) [1]. Over 350 aromatic VOCs have been identified in apple varieties [2], including esters, alcohols, aldehydes, ketones, acids, alkenols, lactones, phenols, furans, and epoxy compounds. Esters, alcohols, and aldehydes are the main components of apple flavor, contributing to sweet, mellow, and grassy flavors, respectively [3]. Apple cultural practices (fruit bagging, rootstock/scion combinations, and other factors) directly affect the aroma quality; for example, fruit bagging was found to reduce the ester content of ‘Ruixue’ apples [4]. The rootstocks affect the whole life process of fruit production. Therefore, clarifying the impact of rootstocks on aroma is beneficial to selecting suitable rootstocks toward improving the aroma quality of apples.
China is the largest apple-producing country and exporter in the world, producing about half of the world’s apple supply [5]. At present, the apple planting model in China is in a critical period of transformation from the traditional vigorous rootstock model to dwarf planting as the dominant cultivation model [6]. Apple dwarf rootstocks are utilized in two ways: as self-rooted rootstock or interstock. Self-rooted rootstocks are propagated with weak taproots and shallow roots. They have poor soil fixation and adaptability and require a high level of soil management and a warm climate. Dwarf self-rooted rootstock methods are widely used in Europe, America, and other developed countries [7,8,9]. However, many apple dwarf self-rooted rootstocks are not suited to the planting environment in China because of their weak cold and drought resistance. Malus baccata (L.) Borkh (M. baccata), an apple rootstock with strong grafting affinity and a high survival rate, can tolerate low temperature and drought stresses [10]. High-quality cultivars/dwarf interstocks of M. baccata represent an effective planting model to adapt to the hilly and cold regions in China without sufficient water and fertilizer.
As an important part of apple trees, dwarf rootstocks affect the mineral nutrient absorption, tree development, and fruit yield and quality [11,12]. Fruit quality determines its commercial value. As an important part of fruit quality, aroma influences consumer acceptance [13], and the rootstock has a significant impact on aroma. Among citrus fruits, ‘Odem’ and ‘Redson’ fruit grown on ‘Volka’ rootstock had lower levels of linalool, β-pinene, and limonene [14]. ‘Clarabella’ rootstock could increase the content of (Z)-2-hexenal and (E)-2-hexenal in tomato from 35 to 65% [15]. The amounts of aromatic components in ‘Gold Finger’ grapes are widely altered by the type of rootstock [16]. Rootstock ‘110R’ increased the VOC content of Albariño and Merlot wine grapes [17,18]. Peach rootstocks strongly affect the types and contents of VOCs; the highest volatile content of peach cultivar ‘Cresthaven’ was found when ‘GF667’ was used as rootstock, and 91 VOCs in total have been identified [19]. Riccardo’s study found that ‘M9’ rootstock increased the volatile content of ‘Pink Lady’ fruits by partial rootzone drying irrigation [20]. ‘Fuji’ apples had higher ester content when grafted on ‘M9’ rootstocks and had higher ester contents compared with ‘MM111’ and ‘MM106’ [21].
‘Huahong’ (Malus × domestica) is a hybrid of ‘Golden Delicious’ and ‘Megumi’ apple cultivars. The hybrid seeds of ‘Golden Delicious’ and ‘Megumi’ were collected in 1976 and sown in 1977. The fruits were harvested in 1984. In 1986, the elite tree was selected from the hybrid group. The elite tree was planted in 14 provinces in North China in 1989. In 1991, it was named ‘Huahong’ [22]. The fruit is well known for its anti-browning properties, strong fragrance, and moderate sour and sweet taste. The average fruit weight, soluble solid, total acid content, vitamin C content, and juice yield are 245 g, 15.5%, 0.48%, 8.97 mg/100 g, and 82.2%, respectively. [23]. The effect of in interstocks on root growth, plant endogenous hormone content, and fruit mineral and polyphenol content of ‘Huahong’ has been studied [24,25,26]. However, there is little information on the aroma profile of ‘Huahong’ apple fruits and the effects of dwarf interstocks on aroma components. Therefore, the aims of the present study were (i) to identity the aroma profile in skin and pulp of ‘Huahong’ apples at maturity, (ii) to positively determine the effects on aroma components of dwarf interstocks, and (iii) to select interstocks that provide significant improvement in the aroma content of ‘Huahong’.

2. Materials and Methods

2.1. Plant Material

‘Huahong’ apple fruit samples were collected from a dwarf interstock demonstration garden in Huludao City, Liaoning Province, China (36°50′ N, 111°24′ E). Information of the trees with different dwarf interstock combinations is given in Table 1. The apple trees were 8 years old and had arrived full bearing period. Three trees were randomly selected from each dwarf interstock combination. When the color of the seeds turned black, mature fruits of uniform size and without visible damage were selected and transported to the laboratory for analysis. Three biological replicates for each combination were prepared, each consisting of 15 fruits. The skin or pulp of the fruit was carefully dissected. All samples were treated with liquid nitrogen and stored at −80 ℃ until extraction.

2.2. Enrichment of Apple VOCs by Solid-Phase Microextraction (SPME)

The fruit was cut into pieces and homogenized, and 10.0 g of each sample was weighed and placed in an injection bottle with 3.2 g of NaCl; then, 22 μL of the internal standard (2-octanol, 0.5 g·L−1) was added, mixed well, and then covered. After aging treatment at 270 °C for 1 h at the sample inlet, fiber was inserted into the headspace of the injection bottle. The fiber (Supelco, Bellefonte, PA, USA) was placed about 1 cm from the sample surface and incubated at 50 °C for 30 min. The fiber was inserted into the sample inlet, extracted at 250 °C for 4 min, and then desorbed for 3 min.

2.3. Test Instrument and Conditions of GC-MS

The GC–MS instrument (TSQ Quantum XLS, Thermo Fisher, Waltham, MA, USA) was used with a DB-1701 (60 m × 0.25 mm × 0.25 μm; Agilent Technologies, Santa Clara, CA, USA) chromatographic column, and the fibers (Supelco, Bellefonte, PA, USA) were filled with 65 μm polydimethylsiloxane and divinyl benzene.
Helium was used as the carrier gas in splitless mode at a flow rate of 1 mL·min−1. The oven temperature was initially held at 40 °C for 3 min, then increased to 130 °C at a rate of 3 °C·min−1 and held at 130 °C for 2 min, then to 250 °C at a rate of 8 °C min−1 and held at 250 °C for 10 min. The temperatures of the injection port, ion source, and MS transfer line were 250, 200, and 260 °C, respectively. The MS was operated under electron ionization of 70 eV with a scan range of 20–350 m/z.

2.4. Identification and Quantitation of VOCs

The solid-phase microextraction fibers enriched with apple fruit aroma components were quickly inserted into the gas chromatography injection port. Following gas chromatography separation, mass spectrometry was carried out, and the total ion flow chromatogram (TIC) was recorded in full scanning mode. The output was used in searching by computer for matches in two mass spectrometry libraries, NIST and Wiley. The chemical components of each chromatographic peak were identified in combination with the artificial atlas and data. The relative content was determined by the internal standard method, taking 2-octanol as the internal standard, quantifying it according to the peak area of various compounds and the concentration of 2-octanol.
The calculation formula for VOC content is as follows ( μ g · kg − 1 ):
VOC   content   μ g · kg − 1 = n 1 m   × C m   g · L − 1 × V m   μ L M   g × 1000
where m, Cm, and Vm are the peak area, concentration, and volume of internal standard, respectively, and n1 and M are the peak area of each component and sample quantity, respectively.

2.5. Data Analysis

Data are presented as the mean values of 3 biological replicates ± standard errors (SEs). The Origin 2019 software was used to conduct principal component analysis (PCA) and generate a PCA biplot and stacked histogram. The SPSS 22 software was used to conduct variance analysis (ANOVA). The hierarchical cluster analysis (HCA) heatmap was drawn by TBtools [27].

3. Results

3.1. VOCs in ‘Huahong’ Apples

3.1.1. Aroma Profile of ‘Huahong’ Apple Fruits

In order to avoid the influence of interstocks, we explored the VOCs found in apples grown from CK combinations. A total of 55 VOCs were identified in ‘Huahong’ apple fruit by SPME-GC–MS, including 48 in the skin and 21 in the pulp (Table 2 and Table 3). Esters comprised the most numerous components (25), followed by aldehydes (14), alcohols (8), ketones (3), alkane hydroxyls (3), and acids (2). As shown in Figure 1A, the content of esters was the highest, followed by aldehydes and alcohols, accounting for 45, 25, and 13% of the total aroma content, respectively. The compounds with contents >100 µg·kg−1 were 2-methyl butyl acetate, hexyl acetate, hexyl 2-methyl butyrate, caproic acid butyl ester, caproic acid ester, hexanal, (Z)-2-heptene aldehyde, (E)-2-octene aldehyde, nonanal, methanol, 2-methyl-1-butanol, hexane, 2-methylbutyric acid, and 6-methyl-5-heptene-2-ketone (Table 2 and Table 3).

3.1.2. Difference of VOCs between Skin and Pulp of ‘Huahong’ Apple

There were obvious differences in the VOC components and contents between the skin and pulp of ‘Huahong’ apples. The accumulated aroma content in skin was 4695.55 µg·kg−1, 5.56 times higher than in pulp (Figure 1B,C). The predominant VOC types were esters and aldehydes in skin and esters and alcohols in pulp. Esters detected in pulp were all present in skin; β-cyclocitral, 3,4-dimethylphenylacetaldehyde, pentanal, 2-methyl-1-hexanol, cis-α,α-5-trimethyl-5-vinyltetrahydrofuran-2-methanol, and 2-octanone were only present in pulp. The dominant compounds (>5% of total content) in the skin were 2-methyl butyl acetate, hexyl 2-methyl butyrate, caproic acid butyl ester, hexanal, (Z)-2-heptene aldehyde, and 6-methyl-5-heptene-2-ketone, while those in the pulp were 2-methyl butyl acetate, methanol, 2-methyl-1-butanol, hexanol, and hexane (Table 2 and Table 3).

3.2. Effects of Dwarf Interstock on VOCs in ‘Huahong’ Apple

3.2.1. Content Differences in Interstock/Scion Combinations

The impact of interstock on apple fruit aroma was mainly reflected in content rather than amount. The total aroma content in different combinations, from high to low, was SH38 (10,763.87 µg·kg−1, 50 VOCs) > SH3 (9576.94 µg·kg−1, 48 VOCs) > MD001 (7442.48 µg·kg−1, 49 VOCs) > Mac9 (7067.91 µg·kg−1, 49 VOCs) > CK (5540.10 µg·kg−1, 53 VOCs) > CX5 (5052.37 µg·kg−1, 50 VOCs) > CG24 (4253.25 µg·kg−1, 49 VOCs) (Figure 1A, Table 2 and Table 3).

3.2.2. Differences in VOCs in Apple Skin and Pulp of Different Interstock/Scion

Combinations

The content of VOCs in the skin and pulp of apples grown from different dwarf interstocks was analyzed by HCA. As shown in Figure 2A, SH38, MD001, SH3, and Mac9, as one category, increased the aroma content in skin compared with CK, while CG24 and CX5, as the other category, had little influence on aroma. As shown in Figure 2B, SH3 and MD001, as one category, increased the aroma content in pulp compared with CK, while CX5, CG24, SH38, and Mac9, as the other category, had little influence on aroma.
The VOC content of the skin ranged from 3297.52 to 9895.75 µg·kg−1 (Figure 1B). SH38 had the highest aroma content of 9895.75 µg·kg−1, followed by SH3 (8514.33 µg·kg−1), which were 2.11 and 1.81 times higher, respectively, than CK (4695.55 µg·kg−1). The VOCs with greater changes in skin were hexyl 2-methyl butyrate and 6-methyl-5-heptene-2-ketone. Their content ranged from 421.80 to 2161.38 µg·kg−1 and 291.15 to 1006.83 µg·kg−1, respectively (Table 2). The VOC content of skin was not significantly different in different combinations, ranging from 748.62 to 1369.21 µg·kg−1 (Figure 1C). The VOCs with greater change in pulp were 2-methyl butyl acetate and hexanol, and their content ranged from 93.6 to 355.4 µg·kg−1 and 84.2 to 298.9 µg·kg−1, respectively (Table 3). Dwarf interstocks had a greater impact on these VOCs.

3.3. Principal Component Analysis

PCA revealed the impact of dwarf interstock on VOCs of ‘Huahong’ apples. The first and second principal components (PC1 and PC2) can, together, explain 74.1% of the impact in skin and 69.1% in the pulp, respectively (Figure 3). According to the loading plot, PC1 is mainly correlated with VOC content and PC2 mainly with VOC amount. In skin, the VOCs of CK, CX5, and CG24 are closer together on the score plot, indicating their similarity, with isoamyl propionate and 1-pentene-3-ol being the main contributors. SH38 on the plot is surrounded by many esters and a few aldehydes, including valerate-3-methyl-2-butenyl ester, butyl propionate, hexanoic acid-3-methyl-2-butenyl ester, hexyl acetate, butyl acetate, ethyl 3-methylvalerate, caproic acid propyl ester, hexanal, nonanal, and butyl aldehyde. MD001 is associated with hexane, with some contribution from 4-pentene-1-acetate; Mac9 is associated with octanoic acid-2-methyl butyl ester; and SH3 is associated with hexyl butyrate and 2-methyl-1-butanol (Figure 3A). In pulp, CK, CX5, and CG24 are associated with 2-methyl-1-hexanol. MD001 had the highest aroma content, and 2-methyl-1-butanol, hexanal, 2-methyl butyl acetate, and hexane are the main contributing factors. The main factors in Mac9 are hexyl acetate and hexyl 2-methyl butyrate. SH3 is associated with alcohols, such as cis-α,α-5-trimethyl-5-vinyltetrahydrofuran-2-methanol and hexanol. SH38 is associated with aldehydes, such as 3,4-dimethylphenylacetaldehyde, 2-hexene aldehyde, and β-cyclocitral (Figure 3B).
Finally, a principal component comprehensive score was formed to evaluate the effect of interstocks on the aroma of ‘Huahong’ apple. As shown in Figure 4, the variation range of comprehensive score for skin (−3.788–5.213) is larger than that for pulp (−0.653–0.945), indicating that dwarf interstocks had a stronger impact on volatile components in skin. SH38 had the highest comprehensive score for skin, at 5.213, and CG24 had the lowest, at −3.788. In conclusion, SH38 had the most significant positive promoting effect on the skin aroma of ‘Huahong’ apple, while CG24 and CX5 weakened the skin aroma.

4. Discussion

4.1. Aroma Profile of ‘Huahong’ Apple

Aroma is an important characteristic of apple that attracts consumers and stimulates their desire to purchase [28]. Aroma is an important cultivar-associated trait; apples of the ‘Golden Delicious’-strain (cultivars derived from the cross of ‘Golden Delicious’ and other cultivars) are mainly green and have a subtle flavor [29]. As a member of this strain, ‘Huahong’ apple was found to have more esters (45% of total content), aldehydes (25% of total content), and alcohols (13% of total content). Esters mainly contribute to the fresh fruity and sweet flavor, while aldehydes and alcohols contribute to the characteristic green apple and grass flavors [30,31,32,33,34]. The aroma profile of ‘Huahong’ is different from that of other ‘Golden Delicious’-strain cultivars, which suggests that hybridization could increase the amount and content of VOCs in apple, similarly as hybridization enriches the flavor of ‘Fuji’-strains [29,35]. This reflects the importance of selecting apple cultivars with higher VOC and fruit aroma content as parents when breeding for this characteristic.
The total aroma varies greatly between the skin and pulp of ‘Huahong’ apples. In this study, all aroma contents (esters, aldehydes, alcohols, ketones, acids, and alkane hydroxyls) were significantly higher in skin than in pulp. The total aroma content in the skin was 4.42–12.32 times higher than that in the pulp of ‘Huahong’ apples when considering all dwarf interstock combinations. Yang et al. [36,37] characterized the aroma of apple skin corresponding to 40 cultivars and of apple pulp corresponding to 85 cultivars, showing that apple VOCs are mainly present in the skin. The higher aroma content in skin is probably due to both its higher abundance of fatty acid and amino acid substrates and its higher metabolic activity [3,38,39]. For example, the enzyme activity of lipoxygenase (LOX) and alcohol acyl transferase (AAT) was higher in the skin than pulp of ‘Fuji’ apples [40].

4.2. Effects on Aroma of ‘Huahong’ Apples of Different Interstocks

The aroma content of ‘Huahong’ apples showed great differences among dwarf interstock combinations. In this study, the total aroma content in the different combinations, from high to low, was SH38 > SH3 > MD001 > Mac9 > CK > CX5 > CG24, and the order is similar to that of the scion/interstock value, which is an important parameter of grafting affinity [41]. Grafting affinity has a broad influence on scion cultivars by altering the nutrient, mineral, and water uptake, phytohormones, and transcript levels of related structural and regulatory genes, even miRNA [42,43,44,45,46]. This suggests that ‘SH38’ and ‘SH3’ were more capable of accumulating substrates for aroma synthesis because of their high grafting affinity.
Research has demonstrated that dwarf rootstocks are generally more capable at sending nutrients to fruits because there is less competition with vegetative organs, such as shoots and leaves [47]. Kviklys [48] suggested that the phenolic acid mass fractions of fruit were generally higher when grown from scions grafted on super-dwarf rootstocks than those grafted on dwarf and semi-dwarf rootstocks. Research has shown that dwarf rootstocks generally increase the aroma content of fruits such as grapes, citrus fruits, peaches, and apples [19,21,49,50].
In order to discuss the effect of dwarf interstocks on fruit aroma, we divided the dwarf interstock combinations into two groups according to the scion/interstock value: (i) SH3 and SH3 and (ii) MD001, Mac9, and CX5. There were slight differences in aroma content and tree height in members of the first group, while in the second group, MD001 had higher aroma content, but its height was between Mac9 and CX5. In addition, the aroma content was lower in CX5 and CG24 than CK. CX5 and had weak dwarf ability and CG24 had poor grafting affinity. A good grafting affinity will facilitate easier transport of nutrients from aerial parts, and dwarf ability can give fruits an advantage in terms of competition with shoots and leaves for nutrients. Thus, these characteristics can lead to the higher accumulation of substrates for aroma synthesis.
Our subsequent work showed that the impact of interstock on ‘Huahong’ aroma is mainly reflected in the skin. The variation range of total content for skin (3297.52 to 9895.75 µg·kg−1) is larger than that for pulp (748.62 to 1369.21 µg·kg−1) The range difference of skin (6598.25 μg·kg−1) was 10.63 times that of pulp (620.59 μg·kg−1). The compounds responsible for the aroma of apples mainly accumulate in the skin [36]. These results mean that dwarf interstocks had a significant influence on the aroma of apples by changing the total aroma content in the skin. In addition, we found a more significant effect of dwarf interstocks on total polyphenol content in skin than pulp of ‘Huahong’ apples in our previous study [26].
The different dwarf interstocks showed various effects on for the different VOCs of ‘Huahong’ apples. Stronger effects were associated with the content of esters; for example, SH38 was seen to be associated with numerous esters and SH3 with a few alcohols in the PCA biplot. In the LOX pathway, AAT is the key enzyme in the synthesis of esters from alcohols [51]. Rootstocks reduced the AAT activity of oriental sweet melon, causing decreased aroma content [39]. However, the molecular mechanisms by which rootstock regulate aroma synthesis are still unclear. Studies have shown that higher plants transport RNA between the aerial parts and the roots via the phloem in the regulation of whole-plant growth [52,53]. Thus, studying the function of RNA delivered from interstocks may be important in clarifying the mechanisms by which dwarf interstocks exert effects on aroma synthesis.
Environmental factors, such as sunlight, water availability, fertilization, and chemical applications, affect fruit flavor. For example, heavy rains dilute flavor compounds in tomatoes before harvest, and mild water deficit and moderate nitrogen supply can increase grape aroma content [54]. The synthesis and release of VOCs in apples are mainly during maturation and post-harvest ripening [55,56]. The harvest time of ‘Huahong’ is usually in early October at Xincheng. During the month before harvest, the temperature, humidity, precipitation, and sunshine time are 20–30 °C, 50–80%, 64–141 mm, and 12 h, respectively [57]. ‘Huahong’ has been planted in Xingcheng for more than 30 years, and its fruit quality was stable in the past years. In this study, we randomly selected the trees to collect enough fruits, aiming to eliminate the error caused by local weather and climate factors. Therefore, our research could represent the aroma profile of ‘Huahong’ planted in Xingchneeg. Undeniably, the change in global climate has had a certain impact on fruit quality, and the water absorption capacity of rootstock could affect the accumulation of VOCs [20]. We plan to explore the influence of weather and climate on fruit quality and how interstocks play a role in adversity environments.

5. Conclusions

In total, 55 VOCs were identified from ‘Huahong’ apples, 48 in skin and 21 in pulp, with esters, aldehydes, and alcohols being the main types of VOCs found. We found that the skin had a strong sweet flavor and the pulp had a subtle green flavor, in accordance with the content and olfactory characteristics of the constituent VOCs. ‘SH38’ and ‘SH3’ interstocks resulted in significantly increased content of VOCs that improve the flavor of ‘Huahong’ apple fruit. These results confirm that a stronger relationship exists between the interstock/scion combination and the concentration of volatile compounds in apple. The content of aroma volatile compounds should be considered as a key parameter for the determination of rootstock-induced effects. More interestingly, we found that interstocks strongly affected esters, which was conducive to the establishment of sweet and fruity flavors.

Author Contributions

X.L., P.Y. and D.W. planned and designed the experiments; X.L., S.S. and Q.L. were involved in the methodology; X.L., Y.G. and Z.L. performed experiments and investigated and recorded data during the experiments; Z.L. and Q.L. were responsible for software; L.L. and K.W. were responsible for field management; X.L. analyzed the data and wrote the manuscript; J.F. and D.W. reviewed and edited the final manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Laboratory of Horticulture Crops Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, grant number NYZS202201, and by the Agricultural Science and Technology Innovation Program, grant number CAAS-ASTIP-2016-RIP-02.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Content of aroma components of ‘Huahong’ apples in different dwarf interstock combinations. (A) Total aroma component content in skin and pulp. (B) Aroma component content in skin. (C) Aroma component content in pulp. Percentage represents relative content of each category in each combination. Values followed by the same letter within the same substances were not significantly different (p < 0.05) according to Duncan’s assay significant difference test. * significant difference in total content between interstock combinations (p < 0.05), Duncan’s assay.
Figure 1. Content of aroma components of ‘Huahong’ apples in different dwarf interstock combinations. (A) Total aroma component content in skin and pulp. (B) Aroma component content in skin. (C) Aroma component content in pulp. Percentage represents relative content of each category in each combination. Values followed by the same letter within the same substances were not significantly different (p < 0.05) according to Duncan’s assay significant difference test. * significant difference in total content between interstock combinations (p < 0.05), Duncan’s assay.
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Figure 2. HCA heatmap of aroma compounds in (A) fruit skin and (B) pulp of ‘Huahong’ apples. Columns were standardized (scale method was zero to one). Color range from blue to red represents low to high aroma content, gray indicates substance was not detected.
Figure 2. HCA heatmap of aroma compounds in (A) fruit skin and (B) pulp of ‘Huahong’ apples. Columns were standardized (scale method was zero to one). Color range from blue to red represents low to high aroma content, gray indicates substance was not detected.
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Figure 3. PCA of aroma components of ‘Huahong’ apples: score plot and loading plot of aroma components in (A) skin and (B) pulp.
Figure 3. PCA of aroma components of ‘Huahong’ apples: score plot and loading plot of aroma components in (A) skin and (B) pulp.
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Figure 4. Principal component comprehensive score for the skin (black) and pulp (red) of ‘Huahong’ apples grown from different dwarf interstock combinations.
Figure 4. Principal component comprehensive score for the skin (black) and pulp (red) of ‘Huahong’ apples grown from different dwarf interstock combinations.
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Table
Table 1. Information of dwarf interstock combinations. Scion/interstock value and tree height expressed as average and standard error (mean ± SE; n = 3).
Table 1. Information of dwarf interstock combinations. Scion/interstock value and tree height expressed as average and standard error (mean ± SE; n = 3).
CodeInterstock/Scion CombinationsScion/Interstock ValueTree Height (m)Breeding Unit
CG24Huahong/CG24/M. baccata0.52 ± 0.052.89 ± 0.04Cornell University and New York State Agricultural Experiment Station, Geneva
SH38Huahong/SH38/M. baccata0.99 ± 0.022.97 ± 0.09Pomology Institute, Shanxi Academy of Agricultural Sciences
SH3Huahong/SH3/M. baccata1.02 ± 0.022.95 ± 0.07Pomology Institute, Shanxi Academy of Agricultural Science
MD001Huahong/MD001/M. baccata0.76 ± 0.023.20 ± 0.10Mudanjiang Branch of Heilongjiang Academy of Agricultural Sciences
Mac9Huahong/Mac9/M. baccata0.79 ± 0.052.63 ± 0.04Michigan State University (USA)
CX5Huahong/CX5/M. baccata0.81 ± 0.023.30 ± 0.12Research Institute of Pomology, Chinese Academy of Agricultural Sciences
CKHuahong/M. baccata-4.20 ± 0.00
Scion/interstock value = scion diameter/interstock diameter. Diameters were measured at a point 5 cm from grafting.
Table
Table 2. Average content and standard error (mean ± SE; n = 3) of VOCs in skin of ‘Huahong’ apples (µg/kg) grown from different dwarf interstocks (CG24, SH38, SH3, MD001, Mac9, CX5) as determined by GC–MS.
Table 2. Average content and standard error (mean ± SE; n = 3) of VOCs in skin of ‘Huahong’ apples (µg/kg) grown from different dwarf interstocks (CG24, SH38, SH3, MD001, Mac9, CX5) as determined by GC–MS.
CodeCompoundCG24SH38SH3MD001Mac9CX5CK
E1Butyl acetatend45.74 ± 26.4627.05 ± 2.5528.56 ± 3.1nd13.11 ± 0.4821.37 ± 2.31
E22-Methyl butyl acetate284.49 ± 51.15709.52 ± 355.62340.53 ± 129.65612.7 ± 208.25nd488.3 ± 14.31524.06 ± 35.19
E3Isoamyl propionate39.86 ± 5.08nd53.77 ± 9.1888.02 ± 43.150.41 ± 7.1845.83 ± 4.1238.29 ± 1.27
E4Ethyl acetate160.29 ± 4.91b487.33 ± 161.46a199.33 ± 21.66b293.05 ± 81.2ab239.04 ± 11.6ab164.72 ± 7.67b210.23 ± 27.56b
E52-Methyl butyl 2-methyl butyrate34.05 ± 1.16105.7 ± 56.3199.73 ± 16.9975.17 ± 40.2683.72 ± 21.6572.14 ± 19.2164.97 ± 13.58
E6Hexyl 2-methyl butyrate352.9 ± 90.13c1695.17 ± 704.76ab2161.38 ± 393.29a687.29 ± 383.93bc930.68 ± 108.17bc421.8 ± 97.97c473.34 ± 156.53bc
E7Butyl propionate14.72 ± 2.3145.99 ± 24.9430.75 ± 1.1538.27 ± 2.0923.38 ± 1.2212.01 ± 1.1511.47 ± 1.22
E84-Pentene-1-acetate10.28 ± 1.22b23.36 ± 2.31and16.73 ± 4.5abnd15.94 ± 0.66ab13.96 ± 1.22b
E9Propyl 2-methyl butyratend43.16 ± 11.0724.75 ± 2.6nd20.39 ± 1.37ndnd
E10Butyl butyrate15.14 ± 2.2585.19 ± 48.4157.13 ± 11.7746.16 ± 9.2651.93 ± 3.1424.14 ± 5.7232.53 ± 4.13
E11Ethyl 3-methylvaleratend49.84 ± 17.8341.33 ± 7.6642.74 ± 14.7124.98 ± 1.6129.24 ± 12.7226.88 ± 5.78
E12Butyl 2-methyl butyrate41.69 ± 11.8b259.21 ± 137.31a257.04 ± 50.83a146.64 ± 41.85ab140.01 ± 6.62ab56.26 ± 0.65ab63.61 ± 19.75ab
E13Caproic acid propyl ester19.79 ± 1.96101 ± 60.3655.62 ± 12.0754.39 ± 19.1160 ± 9.6843.14 ± 7.2738.68 ± 11.14
E14Propionic acid ester31.86 ± 5.8168.92 ± 92.74114.58 ± 17.7268.58 ± 47.3670.48 ± 15.8232.89 ± 6.4636.57 ± 12.27
E15Octylic acid methyl ester9.72 ± 0.2559.38 ± 24.8747.15 ± 8.637.5 ± 22.6135.32 ± 3.3923.52 ± 6.9924.3 ± 6.49
E16Amyl 2-methyl butyrate7.81 ± 0.83b36.3 ± 17.19a33.27 ± 5.81ab23.28 ± 1.21ab16.71 ± 3.48ab12.24 ± 1.07ab19.35 ± 1.81ab
E17Hexyl butyratendnd47.33 ± 1.15and20.09 ± 3.61b11.87 ± 1.15b15.37 ± 2.95b
E18Valerate-3-methyl-2-butenyl ester14.48 ± 0.22b42.49 ± 10.85a24.93 ± 1.17ab28.39 ± 11.89ab17.67 ± 2.3b21.29 ± 3.32ab16.51 ± 1.75b
E19Caproic acid butyl ester66.87 ± 17.38b802.98 ± 456.36a558.67 ± 95.39ab226.43 ± 108.49ab535.44 ± 57.81ab224.8 ± 60.09ab254.99 ± 98.49ab
E20Octanoic acid ethyl ester12.48 ± 1.3353.76 ± 21.31nd38.64 ± 15.4119.14 ± 1.9428.95 ± 5.4720.54 ± 5.58
E21Hexanoic acid-2-methyl butyl ester13.96 ± 2.7774.68 ± 43.5361.94 ± 8.3324.08 ± 5.8785.27 ± 12.6459.14 ± 15.0550.33 ± 16.17
E22Caproic acid butyl ester8.61 ± 0.975.63 ± 43.9nd25.19 ± 11.1353.24 ± 1.1327.11 ± 6.6325.99 ± 10.07
E23Hexanoic acid-3-methyl-2-butenyl ester5.95 ± 0.75b29.69 ± 12.56a22.33 ± 1.24ab26.91 ± 1.21ab22.23 ± 1.42ab24.31 ± 4.86ab17.95 ± 5.65ab
E24Caproic acid ester72.32 ± 20.16c569.99 ± 268.32a432.97 ± 58.69abc159.76 ± 68.7bc497.13 ± 15.39ab210.14 ± 43.57abc225.13 ± 65.03abc
E25Octanoic acid-2-methyl butyl esterndnd16.34 ± 1.1ab8.57 ± 0.52b18.98 ± 1.82a12.08 ± 0.74ab13.61 ± 4.55b
A1Hexanal398.65 ± 38.45b788.46 ± 197.49a609.3 ± 105.75ab682.01 ± 66.07ab511.76 ± 34.78ab458.62 ± 19.39ab432.32 ± 37.99b
A22-Hexene aldehyde44.2 ± 6.7486.87 ± 24.0363.18 ± 9.7254.04 ± 6.5759.9 ± 6.1446.81 ± 4.3446.99 ± 7
A3Z-2-Heptene aldehyde155.44 ± 8.97bc216.64 ± 34.31abc236.08 ± 49.47ab157.85 ± 31.67bc120.68 ± 3.59c147.53 ± 15.01bc297.56 ± 23.11a
A4E-2-Octene aldehyde114.75 ± 5.17b295.36 ± 80.51a229.35 ± 34.95ab184.93 ± 47.06ab150 ± 8.32b138.65 ± 17.12b154.55 ± 13.66ab
A52-Methylbutyraldehyde17.26 ± 2.5435.17 ± 11.5935.82 ± 3.3234.26 ± 13.6719.84 ± 1.7920.56 ± 1.8315.18 ± 2.04
A6Butyl aldehyde22.88 ± 1.85b54.49 ± 16.01a40.22 ± 6.25ab41.58 ± 9.13ab31.13 ± 1.56ab27.32 ± 0.75ab21.28 ± 3.65b
A7Caprylic aldehyde97.88 ± 39.52b109.7 ± 23.7ab97.62 ± 34.25ab154.84 ± 12.99a85.44 ± 16.28ab82.63 ± 11.96ab79.25 ± 30.83ab
A8Nonanal160.77 ± 31.76381.73 ± 124.42344.72 ± 88.87427.74 ± 55.91276.3 ± 31.47177.76 ± 15.9175.48 ± 70.02
A92-Nonene aldehyde15.16 ± 3.3644.74 ± 15.88nd28.41 ± 7.51nd14.88 ± 1.9516.81 ± 2.7
A10E-2-Decyl olefine aldehyde19.8 ± 3.6630.11 ± 7.4727.67 ± 8.1228.74 ± 2.8728.79 ± 4.820.35 ± 2.6528.45 ± 7.91
AL1Methanol113.36 ± 6.98167.67 ± 30.22132.53 ± 25.32120 ± 8.93128.35 ± 8.21113.92 ± 9.5112.96 ± 10.24
AL2Butanol35.01 ± 4.04b72.33 ± 1.35and33.92 ± 0.33b43.5 ± 7.78b17.45 ± 2.17c18.74 ± 1.28c
AL32-Methyl-1-butanol89.7 ± 18.4121.88 ± 30.93148.91 ± 11.6123.58 ± 31.1164.84 ± 10.11137.37 ± 2.91113.45 ± 12.97
AL4Hexanol89.12 ± 20.45bc191.09 ± 67.43ab227.16 ± 35.1a81.82 ± 25.58bc151.04 ± 7.53abc77 ± 10.36c87.27 ± 2.29bc
AL51-Pentene-3-ol14.57 ± 2.32nd0 ± 1.2121.43 ± 4.1114.96 ± 0.8415.03 ± 1.0324.02 ± 4.43
AL62-Octene-1-ol41.32 ± 13.39131.59 ± 56.6291.67 ± 47.83149.46 ± 34.8198.27 ± 1.64nd82.08 ± 3.53
AH1Hexane127.2 ± 8.52137.1 ± 16.34117.95 ± 10.11168.26 ± 26.28138.81 ± 12.97127.62 ± 12.65131.94 ± 20.89
AH2Tetradecane12.09 ± 0.51ndnd28.02 ± 5.84ndndnd
AH37-Methyl-pentadecanend5.79 ± 0.98cnd18.6 ± 0.55a16.19 ± 2.02abnd14.16 ± 1.04b
AC12-Methylbutyric acid154.72 ± 16.63305.56 ± 107.74290.39 ± 28203.72 ± 45.57243.32 ± 19.22187.62 ± 17.45192.61 ± 17.48
AC2Caproic acid42.25 ± 10.5692.44 ± 31.1287.04 ± 13.7173.84 ± 7.8666.69 ± 14.0444.9 ± 2.151.42 ± 11.06
K16-Methyl-5-heptene-2-ketone291.15 ± 46.92c1006.83 ± 393.99a971.28 ± 40.35ab449.29 ± 232.85abc649.51 ± 84.46abc372.75 ± 51.19abc341.22 ± 81.47bc
K23,4,5-Trimethyl-2-cyclopenten-1-one22.96 ± 4.16ab55.14 ± 18.7a55.53 ± 7.77a28.46 ± 8.84ab27.9 ± 2.51abnd17.79 ± 1.81b
Values followed by the same letter within the same row were not significantly different (p < 0.05) according to Duncan’s assay significant difference test. nd: not detected.
Table
Table 3. Average content and standard error (mean ± SE; n = 3) of VOCs in pulp of ‘Huahong’ apples (µg/kg) grown from different dwarf interstocks (CG24, SH38, SH3, MD001, Mac9, CX5) as determined by GC–MS.
Table 3. Average content and standard error (mean ± SE; n = 3) of VOCs in pulp of ‘Huahong’ apples (µg/kg) grown from different dwarf interstocks (CG24, SH38, SH3, MD001, Mac9, CX5) as determined by GC–MS.
CodeCompoundCG24SH38SH3MD001Mac9CX5CK
E1Butyl acetate10.2 ± 1.15b15.36 ± 2.46ab13.03 ± 3.52ab23.01 ± 6.2a16.3 ± 2.95ab8.04 ± 1.58b14.95 ± 2.16ab
E22-Methyl butyl acetate143.29 ± 52.0793.6 ± 36.13110.09 ± 17.38355.4 ± 203.25206.31 ± 19.71172.94 ± 11.96195.13 ± 57.51
E4Ethyl acetate38 ± 5.3545.39 ± 12.3647.82 ± 9.9943.81 ± 15.360.14 ± 7.6927.96 ± 2.3839.76 ± 5.03
E6Hexyl 2-methyl butyrate11.99 ± 2.75ab21.63 ± 8.38ab22.48 ± 4.18a22.33 ± 4.09a20.03 ± 1.01ab7.14 ± 0.95b10.73 ± 1.52ab
A1Hexanal45.56 ± 17.2721.7 ± 1.5531.91 ± 3.3453.19 ± 16.1938.9 ± 14.128.18 ± 7.3331.77 ± 8.84
A22-Hexene aldehyde15.37 ± 3.4910.07 ± 1.3414.94 ± 3.09nd11.56 ± 1.8511.04 ± 0.4211.18 ± 0.76
A3Z-2-Heptene aldehyde17.72 ± 0.95ab11.51 ± 1.98a21.19 ± 7.98abnd8.66 ± 0.76a15.56 ± 2.58ab27.6 ± 4.28a
A4Benzaldehyde16.59 ± 6.8nd9.67 ± 1.96nd10.48 ± 1.19nd12.04 ± 0.34
A11E-2-Octene aldehyde9.88 ± 0.989.09 ± 1.4511.65 ± 1.96ndnd9.55 ± 0.5210.89 ± 0.57
A12β-Cyclocitral 4.77 ± 0.59ab4.01 ± 1.35ab5.42 ± 0.31andnd3.62 ± 0.37ab2.24 ± 1.01b
A133,4-Dimethylphenylacetaldehyde7.18 ± 0.257.77 ± 0.578.2 ± 0.81nd6.69 ± 1.097.61 ± 0.587.04 ± 1.22
A14Pentanal10.64 ± 0.54abnd12.16 ± 0.75ab13.44 ± 2.93a9.05 ± 0.42abnd8.16 ± 0.29b
AL1Methanol68.51 ± 6.162.84 ± 5.2767.89 ± 6.5887.86 ± 28.0562.27 ± 1.8355.21 ± 5.0852.05 ± 1.73
AL2Butanol27.87 ± 0.57ab25.37 ± 7.82ab43.42 ± 15.76b48.73 ± 17.91a29.91 ± 3.2ab11.87 ± 1.39ab14.76 ± 3.75ab
AL32-Methyl-1-butanol128.79 ± 34.0284.19 ± 10.09136.47 ± 7.94256.79 ± 124.98146.85 ± 9.48128.03 ± 4.71112.95 ± 21.46
AL4Hexanol147.6 ± 42.7bc273.3 ± 9.48ab298.86 ± 62.54a169.74 ± 67.15abc198.58 ± 28.91abc84.21 ± 12.13c103.62 ± 24.27c
AL72-Methyl-1-hexanol13.66 ± 3.9913.56 ± 3.2ndndnd5.51 ± 0.695.92 ± 0.52
AL8cis-α,α-5-Trimethyl-5-vinyltetrahydrofuran-2-methanolnd9.67 ± 0.61bc14.03 ± 0.61a7.56 ± 0.03d10.06 ± 0.6b8.02 ± 0.27cd8.7 ± 0.94bcd
AH1Hexane200 ± 53.23116.79 ± 14.21126.2 ± 2.6233.44 ± 88.55136.46 ± 7.6125.65 ± 9.99129.14 ± 11.43
AC12-Methylbutyric acid12.95 ± 4.11b24.67 ± 7.34ab40.04 ± 10.83a25.83 ± 6.58ab29 ± 0.92ab15.26 ± 1.75b22.37 ± 7.62ab
K32-Octanone25.16 ± 1.0723.38 ± 0.6327.13 ± 2.4528.1 ± 3.1723.19 ± 1.7723.23 ± 0.2523.57 ± 0.68
Values followed by the same letter within the same row were not significantly different (p < 0.05) according to Duncan’s assay significant difference test., nd, not detected.
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MDPI and ACS Style

Lu, X.; Gao, Y.; Wang, K.; Sun, S.; Liu, Z.; Yan, P.; Feng, J.; Li, Q.; Li, L.; Wang, D. Dwarf Interstocks Improve Aroma Quality of ‘Huahong’ Apple (Malus × domestica). Agriculture 2022, 12, 1710. https://doi.org/10.3390/agriculture12101710

AMA Style

Lu X, Gao Y, Wang K, Sun S, Liu Z, Yan P, Feng J, Li Q, Li L, Wang D. Dwarf Interstocks Improve Aroma Quality of ‘Huahong’ Apple (Malus × domestica). Agriculture. 2022; 12(10):1710. https://doi.org/10.3390/agriculture12101710

Chicago/Turabian Style

Lu, Xiang, Yuan Gao, Kun Wang, Simiao Sun, Zhao Liu, Peng Yan, Jianrong Feng, Qingshan Li, Lianwen Li, and Dajiang Wang. 2022. "Dwarf Interstocks Improve Aroma Quality of ‘Huahong’ Apple (Malus × domestica)" Agriculture 12, no. 10: 1710. https://doi.org/10.3390/agriculture12101710

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