Total Polyphenol Content,Antioxidant Activity,and Individual Phenolic Composition of Different Edible Parts of 4 Sweet Potato Cultivars

Abstract

The quest to determine and use polyphenolic compounds present in fruits and vegetables as natural antioxidants has recently attracted much attention due to their beneficial health effects. In this study, the total polyphenol content (TPC), total flavonoid content (TFC), total anthocyanin content (TAC), antioxidant activity (AA), and individual polyphenol components of Simon No. 1, Yuzi No. 7, Shangshu 19, and Pushu 32 sweet potato cultivars (edible parts: leaf, stalk, stem, skin, and flesh) were investigated. TPC, TFC, and TAC values ranged from 440 ± 0.17-12080 ± 0.58 CAE mg/100 g DW, 94 ± 0.08-4210 ± 0.74 QE mg/100 g DW, and 7 ± 0.01-1010 ± 0.54 CGE mg/100 g DW, respectively. Yuzi No. 7 sweet potato cultivar contained significantly higher amounts of TPC, TFC, TAC, and AA in all its edible parts, followed by Pushu 32, Simon No. 1, and Shangshu 19 in that order. Regardless of the sweet potato cultivar used, TPC, TFC, and TAC of sweet potato leaves were significantly higher than those of other edible parts. High-performance liquid chromatography revealed 19 individual phenolic compounds. In general, 3,5-di-O-caffeoylquinic acid, astragalin, and cyanidin were the predominant phenolic acid, flavonoid, and anthocyanin compounds, respectively. The correlation analysis suggested that higher AA could be attributed to higher polyphenol content. Based on our results, edible parts of Yuzi No. 7 sweet potato cultivar presented the highest amounts of polyphenol content and AA suggesting the possibility of utilizing this cultivar by farmers and the food industry as a functional food product.

Keywords

sweet potato edible parts polyphenol content individual phenolic composition antioxidant activity flavonoids anthocyanin phenolic acids

Polyphenols, secondary plant metabolites widely distributed in fruits and vegetables,¹ have several reported health-enhancing properties, for example, antibiotic, antioxidant, antidiabetic, antiobesity, anticarcinogenic, and antimutagenic effects.² In recent decades, there has been a rise in lifestyle-related diseases due to changes in eating habits, behavior, and exercise regimes among humans.³ This has led to an increased demand for healthy and minimally processed foods, with some health-conscious consumers opting to eat raw natural plant foods. Accordingly, natural alternatives to synthetic antioxidants have gained immense attention and research focus in recent years.⁴

Sweet potato (Ipomoea batata L.) is a dicotyledonous plant belonging to the family Convolvulaceae. Sweet potato is considered one of the major food crops of the world.⁵ Global sweet potato production is approximately 112.8 million tons.⁶ China accounts for 90.5% and 63.8% of sweet potato production in Asia and the world, respectively.

It has been reported that edible parts of sweet potato, such as leaves, stems, and roots, are good sources of essential amino acids, vitamins, and minerals important for animal and human nutrition.⁷ A study by Sun et al⁸ on the proximate composition of sweet potato leaves (SPL) obtained 16.69 ± 0.09-31.08 ± 0.09, 9.15 ± 0.49-14.26 ± 0.38, 2.08 ± 0.06-5.28 ± 0.15, 42.03 ± 0.03-61.36 ± 0.90, and 7.39 ± 0.86-14.66 g/100 g dry weight (DW) crude protein, crude fiber, crude fat, carbohydrates, and ash contents, respectively. Moreover, as attested by the nutritional quality indices, SPL was found to be an excellent source of proteins, fibers, and minerals.⁸ Similarly, recent studies have underscored sweet potato as an important source of natural antioxidants,⁹ and its high levels of anthocyanins make it a valuable crop in the functional food market.¹⁰ Furthermore, the content of polyphenols in SPL was found to be higher than that of spinach and kales.¹¹ Increasingly, health-conscious consumers are preferring sweet potato cultivars with high levels of polyphenol compounds.

Reports suggest that considerable variation exists in the total polyphenol content (TPC), individual phenolic composition, and antioxidant activity (AA) among various cultivars of sweet potato.⁷ These variations are ascribed to differences in color, variety, and environmental and processing conditions.¹² Bioactive components described in sweet potato comprise phenolic acids, such as caffeic acid and caffeoylquinic acid derivatives, including mono-, di- and tri-caffeoylquinic acids¹³; flavonoids, such as astragalin, quercetin, kaempferol, and myricitrin¹⁴; and cyanidin or peonidin-type anthocyanins.^9,15

Zengin et al¹⁶ investigated TPC in SPL and found a range of 73.10 ± 3.75 to 89.26 ± 1.34 gallic acid equivalents (GAE) mg/g extract. Liu et al¹⁴ recorded a 5.63 ± 0.21 quercetin equivalent (QE) g/100 g DW total flavonoid content (TFC) in SPL. Kourouma et al¹⁷ reported 3.13 ± 0.38-9.38 ± 0.10 GAE mg/g DW TPC, 0.16-2.54 rutin mg/g DW TFC, and 0.02-1.02 ± 0.02 mg/g DW total anthocyanin content (TAC) in different sweet potato cultivars.

While several reports are available on contents of polyphenols and AA in various sweet potato cultivars, however, to date, there has not been a comprehensive study to determine the extent of variation in TPC, individual phenolic composition, and AA in all the edible parts of sweet potato. Additionally, most published reports have focused on the phenolic composition and AA in specific edible parts, that is, leaves and roots, rather than in all edible parts. A literature survey of all published work to date revealed that information on TPC, individual phenolic composition, and AA in all the edible parts of sweet potato was scarce. Therefore, due to the importance of polyphenols to human health and the ever-increasing demand for natural sources of antioxidants, we evaluated TPC, TFC, TAC, individual phenolic composition, individual flavonoid composition, individual anthocyanin composition, and AA in the edible parts (leaves, stalk, stem, skin, and flesh) of 4 selected cultivars of sweet potato. The information obtained could be useful in using sweet potato as a functional constituent in the food and pharmaceutical industries.

Results and Discussion

Evaluation of TPC, TFC, and TAC Values

As depicted in Table 1, significant differences (P < 0.05) in TPC, TFC, and TAC values were reported among the edible parts of the 4 sweet potato cultivars. However, no significant differences were observed for TAC values between Simon No.1 and Shangshu 19 leaves.

Table 1

Total Phenolic Content, Anthocyanin Content, Flavonoid Content, and Antioxidant Activities of 5 Edible Parts in 4 Sweet Potato Cultivars.

Cultivar	Edible part	TPC(CAE mg/100 gDW)	TFC(QE mg/100 gDW)	TAC(CGE mg/100 gDW).	FRAP(TE mg/100 gDW)	DPPH(AAE mg/100 gDW)	ABTS(AAE mg/100 gDW)
Yuzi No. 7	Leaf	12080 ± 0.58^a	4210 ± 0.74^a	1010 ± 0.54^a	550 ± 0.21^a	2920 ± 0.34^a	5300 ± 0.19^a
Pushu 32		9950 ± 0.91^b	2730 ± 0.63^b	830 ± 0.15^b	470 ± 0.22^b	2720 ± 0.37^b	4840 ± 0.14^b
Simon No. 1		7130 ± 0.23^c	1810 ± 0.43^c	790 ± 0.15^c	460 ± 0.12^c	2600 ± 0.22^c	4270 ± 0.54^c
Shangshu 19		6050 ± 0.16^d	1560 ± 0.41^d	790 ± 0.25^c	440 ± 0.52^d	2580 ± 0.33^d	3950 ± 0.11^d
Yuzi No. 7	Stalk	930 ± 0.16^a	157 ± 0.32^a	ND	79 ± 0.12^a	730 ± 0.13^a	820 ± 0.32^a
Pushu 32		750 ± 0.31^b	136 ± 0.12^b	ND	51 ± 0.05^b	560 ± 0.24^b	730 ± 0.33^b
Simon No. 1		710 ± 0.12^c	115 ± 0.21^c	ND	45 ± 0.03^c	460 ± 0.23^c	720 ± 0.22^c
Shangshu 19		620 ± 0.22^d	94 ± 0.08^d	ND	41 ± 0.02^d	360 ± 0.51^d	630 ± 0.31^d
Yuzi No. 7	Stem	870 ± 0.23^a	350 ± 0.12^a	41 ± 0.07^a	50 ± 0.06^a	440 ± 0.21^a	840 ± 0.31^a
Pushu 32		750 ± 0.12^b	200 ± 0.15^b	ND	37 ± 0.04^b	440 ± 0.14^a	780 ± 0.22^b
Simon No. 1		700 ± 0.22^c	150 ± 0.21^c	ND	35 ± 0.11^c	320 ± 0.11^b	700 ± 0.22^c
Shangshu 19		610 ± 0.14^d	120 ± 0.27^d	ND	30 ± 0.07^d	250 ± 0.12^c	510 ± 0.21^d
Yuzi No. 7	Skin	1090 ± 0.48^a	487 ± 0.11^a	230 ± 0.22^a	47 ± 0.03^a	410 ± 0.21^a	880 ± 0.16^a
Pushu 32		680 ± 0.14^b	171 ± 0.23^b	60 ± 0.02^b	34 ± 0.01^b	350 ± 0.16^b	730 ± 0.14^b
Simon No. 1		610 ± 0.26^c	162 ± 0.12^c	50 ± 0.07^c	31 ± 0.11^c	300 ± 0.13^c	680 ± 0.15^c
Shangshu 19		560 ± 0.31^d	116 ± 0.21^d	11 ± 0.01^d	28 ± 0.04^d	230 ± 0.13^d	610 ± 0.14^d
Yuzi No. 7	Flesh	980 ± 0.40^a	460 ± 0.33^a	170 ± 0.13^a	46 ± 0.03^a	330 ± 0.13^a	710 ± 0.23^a
Pushu 32		570 ± 0.28^b	160 ± 0.21^b	50 ± 0.03^b	31 ± 0.12^b	270 ± 0.12^b	680 ± 0.14^b
Simon No. 1		500 ± 0.12^c	110 ± 0.51^c	10 ± 0.01^c	28 ± 0.52^c	260 ± 0.22^c	570 ± 0.11^c
Shangshu 19		440 ± 0.17^d	100 ± 0.31^d	7 ± 0.01^d	26 ± 0.11^d	190 ± 0.25^d	570 ± 0.03^c

TPC, total polyphenol content; TFC, total flavonoid content; TAC, total anthocyanin content; FRAP, ferric reducing antioxidant potential; DPPH, 2, 2-diphenyl-1-picrylhydrazyl; ABTS, 2,2′-azino-bis (3-ethylbenzthiazoline-6-sulfonic acid); CAE, chlorogenic acid equivalent; QE, quercetin equivalent; CGE, cyanidin 3-glucoside equivalent; TE, trolox equivalent; AAE, ascorbic acid equivalent; DW, dry weight; ND, not detected; and ANOVA, analysis of variance.

Different uppercase letters showed significant differences in each group of data (P < 0.05) for 4 sweet potato cultivars (ANOVA).

TPC values ranged from 440 ± 0.17 (obtained for flesh of Shangshu 19) to 12080 ± 0.58 (obtained for leaves of Yuzi No. 7) CAE mg/100 g DW. The TPC value for leaves of Yuzi No. 7 was 12080 ± 0.58 CAE mg/100 g DW, which was significantly higher than all the other samples (Table 1, P < 0.05), and was approximately 1.21, 1.69, and 2.00 times higher than the values obtained for leaves of Pushu 32, Simon No. 1, and Shangshu 19, respectively. As observed in this study, color was an important factor influencing polyphenol levels in sweet potato cultivars. For example purple (Yuzi No. 7) and orange (Pushu 32) sweet potato cultivars ranked higher in terms of TPC levels than their white counterparts, that is, Simon No. 1 and Shangshu 19 cultivars, confirming the influence of color on polyphenol content. Moreover, TPC levels in SPL were significantly higher than in other edible parts. For example, in Yuzi No. 7 cultivar, TPC values in SPL (12080 ± 0.58 CAE mg/100 g DW) were 12.99, 13.89, 11.08, and 12.33 times greater than that of stalk, stem, skin, and flesh, respectively. The average TPC value in SPL was 8803 ± 0.47 CAE mg/100 g DW, which was in agreement with the corresponding values reported by Sun et al⁸ (2730 ± 0.02-12460 ± 0.62 CAE mg/100 g DW). The values obtained in our study for TPC in the flesh obtained from sweet potatoes (440 ± 0.17-980 ± 0.40 CAE mg/100 g DW) were similar to those reported by Musilová et al¹⁸ (1.161 ± 0.08-13.998 ± 0.387 CAE mg/g dry matter). Overall, Yuzi No. 7 sweet potato cultivar contained significantly higher amounts of TPC in all its edible parts followed by Pushu 32, Simon No. 1, and Shangshu 19, in that order.

TFC values ranged from 94 ± 0.08 QE mg/100 g DW in the stalk of Shangshu 19 to 4210 ± 0.74 QE mg/100 g DW in the leaves of Yuzi No. 7 (Table 1). TFC values obtained for Yuzi No. 7 leaves were 4210 ± 0.74 QE mg/100 g DW, which was 1.54, 2.33, and 2.70 times higher than Pushu 32, Simon No.1, and Shangshu 19 SPL, respectively (P < 0.05). Variations in TFC levels among these 4 sweet potato cultivars could be assigned to the differences in colors of sweet potatoes as discussed earlier, and also to the differences in edible parts. Our results showed that polyphenol compounds accumulated in higher quantities in the leaves than in the other edible parts. For example, TFC of Yuzi No. 7 leaves (4210 ± 0.74 QE mg/100 g DW) was 26.82, 12.03, 8.65, and 9.15 times higher than those obtained for stalk, stem, skin, and flesh, respectively. Our results for TFC in SPL were slightly lower when compared with those reported by Liu et al¹⁴ (5.63 ± 0.21 QE g/100 g DW). Liu et al¹⁴ optimized an ultrasonic-synergistic extraction method for flavonoids from SPL, and their method might have led to higher flavonoid recovery.

For TAC determination, the values obtained varied between 7 ± 0.01 CGE mg/100 g DW in flesh of Shangshu 19 to 1010 ± 0.54 CGE mg/100 g DW in leaves of Yuzi No. 7 (Table 1). TAC values obtained in our study for SPL (790 ± 0.25-1010 ± 0.54 CGE mg/100 g DW) were significantly higher than the value of 3.27 ± 0.29 mg/100 g DW reported by Su et al¹⁹ and 9.40-227.53 mg/100 g FW reported by Jyothi et al²⁰ on different SPL varieties. In our study, the variation in the TAC levels between the edible parts of different sweet potato cultivars could be due to the differences in color as higher levels of TAC were achieved in the purple sweet potato cultivar (Yuzi No. 7) than in the orange and the white-colored sweet potato cultivars.

Antioxidant Activities

Table 1 presents the results obtained for ferric reducing antioxidant potential (FRAP), 2, 2-diphenyl-1-picrylhydrazyl (DPPH), and 2,2′-azino-bis (3-ethylbenzthiazoline-6-sulfonic acid) (ABTS) assays of edible parts of the 4 sweet potato cultivars. The FRAP AA varied from 26 ± 0.11 TE mg/100 g DW in the flesh of Shangshu 19 to 550 ± 0.21 TE mg/100 g DW in the leaves of Yuzi No. 7. Regardless of the sweet potato cultivar analyzed, the order of AA in different edible parts was as follows: leaves > stalk > stem > skin > flesh. In general, samples with high TPC levels exhibited higher AA and vice versa. The DPPH and ABTS assay results were also in good agreement with the FRAP results and were not examined in detail for brevity. The reported data for AA as assessed by FRAP, DPPH, and ABTS activities were significantly different. The differences in AA values could be ascribed to the individual AA measurement methods, that is, FRAP, DPPH, and ABTS assays, which measure different antioxidant effects.²¹Overall, based on our reported values for TPC, TFC, TAC, and AA, edible parts of Yuzi No. 7 sweet potato cultivar was considered as the best cultivar, suggesting a possibility of utilizing this cultivar by farmers and the food industry as a functional food.

Correlation analysis for the obtained values of TPC, TFC, TAC, and AA was done (Figure 1A–I). In this study, the correlation values for all the edible parts were measured except for SPL. This is because TPC, TFC, TAC, and AA values of SPL were significantly higher compared with other edible parts, that is, stalk, stem, skin, and flesh. Therefore, taking these correlations for SPL would result in high values that are statistically insignificant. As illustrated in Figure 1, low positive correlations were reported between TPC and DPPH (r = 0.3969, P = 0.009, Figure 1A), and between TFC and ABTS assays (r = 0.3992, P = 0.009, Figure 1E). In contrast, moderate correlations were reported between TPC and ABTS (r = 0.6871, P = 0.000, Figure 1B), and also between TPC and FRAP assays (r = 0.535, P = 0.001, Figure 1C). Our findings were partly similar to those reported by Fu et al,²² who showed that phenolics (phenolic acids) were the main factors influencing AA of SPL. Moreover, in their study, flavonoids and anthocyanins weakly affected the AA of SPL. In a similar manner, Albuquerque et al⁷ observed phenolic compounds as the main contributing factor to AA. A study conducted by Sun et al¹² reported strong AA in SPL polyphenols. Sun et al²³ also reported di and tricaffeoylquinic acids as the main contributors to the AA of SPL polyphenols.

Figure 1

(A) Schematic drawing showing all the five edible parts (leaves, stalk, stem, skin and flesh) of sweet potato plant. (B) Photograph of the four sweet potato cultivars (freeze dried flesh powders). Pushu 32 (skin and flesh are orange in colour), Yuzi No. 7 (skin and flesh are purple in colour), Simon No. 1 (skin and flesh are white in colour), and Shangshu 19 (skin is orange in colour while flesh is white in colour). All other edible parts, i.e., leaves, stalks, and stems, were green in colour. (C) Photograph of the four sweet potato cultivars (freeze dried leaf powders). (D) Representative photos of sweet potato anthocyanin extract.

Individual Phenolic Composition

As depicted in Table 2 and 19 individual phenolic compounds were detected in the edible parts of sweet potatoes (leaf, stalk, stem, skin, and flesh). The obtained retention times of authentic standards were used to identify the individual phenolic compounds. In addition, previously published data on retention times for phenolic acids,²³ flavonoids,¹⁴ and anthocyanins²⁴ guided our study.

Table 2

Contents of Individual Phenolic Compounds in Edible Parts of 4 Sweet Potato Cultivars (mg/100 g DW).

Cultivar	Edible part	Phenolic acids
		Peak 1	Peak 2	Peak 3	Peak 4	Peak 5	Peak 6	Peak 7	Peak 8
		5-CQA	3-CQA	4-CQA	CA	4,5-diCQA	3,5-diCQA	3,4-diCQA	3,4,5-triCQA
Yuzi No. 7	Leaf	93 ± 0.15^d	110 ± 0.02^d	290 ± 0.03^d	20 ± 0.02^c	2231 ± 0.61^a	3338 ± 0.28^a	1316 ± 0.37^a	310 ± 0.11^a
Pushu 32		296 ± 0.22^b	349 ± 0.12^a	607 ± 0.13^a	22 ± 0.13^b	813 ± 0.14^d	3152 ± 0.25^b	533 ± 0.12^b	77 ± 0.03^d
Simon No. 1		502 ± 0.13^a	189 ± 0.33^c	322 ± 0.22^c	28 ± 0.23^a	1518 ± 0.26^b	2109 ± 0.15^c	302 ± 0.12^c	114 ± 0.13^b
Shangshu 19		196 ± 0.02^c	273 ± 0.11^b	501 ± 0.41^b	11 ± 0.00^d	1005 ± 0.23^c	1855 ± 0.17^d	202 ± 0.19^d	82 ± 0.01^c
Yuzi No. 7	Stalk	33 ± 0.02^b	41 ± 0.02^b	112 ± 0.04^a	13 ± 0.00^c	164 ± 0.04^a	186 ± 0.05^a	61 ± 0.02^a	28 ± 0.01^a
Pushu 32		42 ± 0.01^a	52 ± 0.03^a	90 ± 0.03^b	17 ± 0.01^a	76 ± 0.02^c	123 ± 0.13^b	31 ± 0.01^d	21 ± 0.01^b
Simon No. 1		24 ± 0.03^c	40 ± 0.02^c	82 ± 0.02^c	10 ± 0.01^d	96 ± 0.03^b	116 ± 0.05^d	55 ± 0.02^b	20 ± 0.01^c
Shangshu 19		33 ± 0.01^b	24 ± 0.01^d	74 ± 0.01^d	14 ± 0.01^b	69 ± 0.01^d	117 ± 0.21^c	46 ± 0.02^c	17 ± 0.00^d
Yuzi No. 7	Stem	39 ± 0.02^a	41 ± 0.11^b	111 ± 0.31^a	13 ± 0.03^a	84 ± 0.02^a	126 ± 0.13^b	55 ± 0.02^a	27 ± 0.21^b
Pushu 32		27 ± 0.04^c	55 ± 0.02^a	72 ± 0.32^c	13 ± 0.17^a	65 ± 0.32^d	145 ± 0.22^a	24 ± 0.11^d	20 ± 0.13^c
Simon No. 1		20 ± 0.01^d	38 ± 0.11^c	63 ± 0.13^d	12 ± 0.00^b	71 ± 0.01^b	113 ± 0.24^c	51 ± 0.02^b	43 ± 0.01^a
Shangshu 19		37 ± 0.02^b	32 ± 0.01^d	78 ± 0.16^b	5 ± 0.00^c	69 ± 0.03^c	107 ± 0.25^d	49 ± 0.13^c	17 ± 0.14^d
Yuzi No. 7	Skin	101 ± 0.23^a	49 ± 0.14^c	126 ± 0.23^a	34 ± 0.33^a	29 ± 0.21^d	148 ± 0.06^a	22 ± 0.01^c	14 ± 0.01^b
Pushu 32		63 ± 0.03^b	55 ± 0.05^a	89 ± 0.06^b	24 ± 0.00^b	32 ± 0.03^b	105 ± 0.12^b	26 ± 0.11^b	11 ± 0.00^d
Simon No. 1		37 ± 0.01^d	48 ± 0.02^d	56 ± 0.02^d	11 ± 0.00^d	76 ± 0.12^a	95 ± 0.08^c	27 ± 0.05^a	24 ± 0.16^a
Shangshu 19		46 ± 0.02^c	50 ± 0.02^b	65 ± 0.21^c	23 ± 0.01^c	31 ± 0.04^c	81 ± 0.13^d	20 ± 0.04^d	13 ± 0.07^c
Yuzi No. 7	Flesh	47 ± 0.02^b	73 ± 0.02^a	93 ± 0.13^a	10 ± 0.00^d	68 ± 0.32^a	129 ± 0.04^a	29 ± 0.06^a	17 ± 0.01^a
Pushu 32		48 ± 0.21^a	30 ± 0.51^d	82 ± 0.02^b	25 ± 0.01^a	21 ± 0.05^c	119 ± 0.07^b	25 ± 0.04^b	4 ± 0.00^d
Simon No. 1		26 ± 0.11^d	31 ± 0.01^c	60 ± 0.22^d	12 ± 0.05^c	36 ± 0.01^b	109 ± 0.04^c	24 ± 0.11^c	13 ± 0.08^b
Shangshu 19		42 ± 0.02^c	36 ± 0.32^b	64 ± 0.26^c	20 ± 0.01^b	17 ± 0.03^d	75 ± 0.09^d	13 ± 0.01^d	9 ± 0.00^c

5-CQA, 5-O-caffeoylquinic acid; 3-CQA, 3-O-caffeoylquinic acid; 4-CQA, 4-O-caffeoylquinic acid; CA, caffeic acid; 4,5-diCQA, 4,5-di-O-caffeoylquinic acid; 3,5-diCQA, 3,5-di-O-caffeoylquinic acid; 3,4-di CQA, 3,4-di-O-caffeoylquinic acid; 3,4,5-triCQA, 3,4,5-tri-O-caffeoylquinic acid; and ANOVA, analysis of variance; DW, dry weight.

Different uppercase letters showed significant differences in each group of data (P < 0.05) for 4 sweet potato cultivars (ANOVA).

Table 2 shows the detected individual phenolic acids. The most predominantly detected phenolic acids were di-, followed by mono-, and tri-O-caffeoylquinic acids or caffeic acid, depending on the cultivar used and the specific edible part. The content of 3,5-di-O-caffeoylquinic acid was highest (P < 0.05) in all the edible parts of sweet potatoes. Yuzi No. 7 leaves had the highest content of 3,5-di-O-caffeoylquinic acid (3338 ± 0.28 mg/100 g DW), followed by Pushu 32 leaves (3152 ± 0.25 mg/100 g DW), Simon No. 1 leaves (2109 ± 0.15 mg/100 g DW), and Shangshu 19 leaves (1855 ± 0.17 mg/100 g DW), with significant differences among them (Table 2, P < 0.05). Our findings were in agreement with those reported by Lu et al²⁵ and Sun et al¹² in SPL. Our results also showed differences in phenolic acid composition which might be attributed to the differences between cultivars, the state of maturity, genotype, and environmental conditions, resulting in different phenolic acid constituents (ie, mono-, di-, and tri-caffeoylquinic acids). The percentages of TPC constituting the sum of peaks 1-8 for the edible parts of different sweet potato cultivars, that is, leaf, stalk, stem, skin, and flesh, respectively, were as follows: Yuzi No. 7 cultivar, 63.8%, 68.6%, 57.0%, 48.0%, 47.5%; Pushu 32 cultivar, 58.8%, 60.3%, 56.1%, 59.56%, 62.1%; Simon No. 1 cultivar, 71.3%, 62.4%, 58.7%, 61.3%, 62.2%; and Shangshu 19 cultivar, 68.2 %, 63.5%, 64.6%, 58.7%, and 62.7%. Notably, the values for TPC as determined in our study by the Folin-Ciocalteu method were higher than those determined by high-performance liquid chromatography (HPLC) analysis. This observation indicated that additional phenolic compounds other than the measured individual phenolic compounds might be present in higher amounts. We were not able to identify and quantify all the individual phenolic acids due to limited standards used. Another possibility was the overestimation of TPC by the Folin-Ciocalteu method, that is, all the hydroxyl groups in the amino acids and sugars might have reacted in addition to the phenolic groups.^18,22

Table 3 shows the values obtained for individual flavonoids in edible parts of different sweet potato cultivars. Astragalin was the most predominant flavonoid, followed by either isoquercitrin or quercitrin, depending on the edible parts of cultivars. Yuzi No. 7, Pushu 32, Simon No. 1 and Shangshu 19 leaves showed high contents of astragalin (1729.9 ± 0.55, 1056.6 ± 0.42, 738.3 ± 0.25, and 491.3 ± 0.26 mg/100 g DW, respectively), with significant differences among them (Table 3, P < 0.05). These findings were consistent with those described by Liu et al.¹⁴The percentages of TFC constituting the sum of peaks 1-8 for the edible parts of different sweet potato cultivars, that is, leaf, stalk, stem, skin, and flesh, respectively, were as follows: Yuzi No. 7 cultivar, 60.1%, 60.4%, 54.2%, 42.9%, and 53.6%; Pushu 32 cultivar, 60.9%, 55.1%, 49.9%, 40.6%, and 38.7%; Simon No. 1 cultivar, 58.9%, 53.8%, 59.5%, 49.9%, and 48.6%; and Shangshu 19 cultivar, 56.5%, 48.4%, 45.9%, 33.4%, and 36.9%.

Table 3

Contents of Individual Flavonoid Compounds in Edible Parts of 4 Sweet Potato Cultivars (mg/100 g DW).

Cultivar	Edible part	Flavonoid compounds
		Peak 1	Peak 2	Peak 3	Peak 4	Peak 5	Peak 6	Peak 7	Peak 8
		Myricetrin	Isoquercitrin	Astragalin	Quercitrin	Tiliroside	Quercetin	Apigenin	Kaempferol
Yuzi No. 7	Leaf	36.7 ± 0.71^c	268.3 ± 0.26^a	1729.9 ± 0.55^a	172.6 ± 0.95^a	154.5 ± 0.20^a	87.7 ± 0.71^a	20.1 ± 0.02^b	60.9 ± 0.02^a
Pushu 32		22.9 ± 0.16^d	175.2 ± 0.14^b	1056.6 ± 0.42^b	152.0 ± 0.68^b	103.0 ± 0.22^b	77.0 ± 0.35^b	18.2 ± 0.02^c	57.2 ± 0.17^b
Simon No. 1		111.8 ± 0.16^a	126.8 ± 0.36^d	738.3 ± 0.25^c	32.5 ± 0.47^c	ND	29.6 ± 0.05^d	10.6 ± 0.03^d	16.6 ± 0.11^d
Shangshu 19		77.7 ± 0.68^b	157.3 ± 0.30^c	491.3 ± 0.26^d	22.6 ± 0.65^d	ND	34.8 ± 0.59^c	57.7 ± 0.10^a	39.6 ± 0.12^c
Yuzi No. 7	Stalk	3.1 ± 0.00^a	21.1 ± 0.05^a	38.9 ± 0.01^a	17.9 ± 0.38^a	ND	7.3 ± 0.04^a	1.9 ± 0.01^a	4.7 ± 0.01^a
Pushu 32		2.7 ± 0.02^b	17.8 ± 0.06^b	29.0 ± 0.55^b	9.7 ± 0.40^c	3.3 ± 0.02^a	6.9 ± 0.06^b	1.7 ± 0.02^b	3.9 ± 0.01^b
Simon No. 1		2.4 ± 0.03^c	14.9 ± 0.04^c	22.2 ± 0.73^c	14.5 ± 0.03^b	ND	6.5 ± 0.01^c	1.4 ± 0.04^c	ND
Shangshu 19		2.1 ± 0.00^d	7.5 ± 0.06^d	23.0 ± 0.51^d	7.6 ± 0.03^d	ND	3.4 ± 0.01^d	1.9 ± 0.01^a	ND
Yuzi No. 7	Stem	5.5 ± 0.13^a	39.0 ± 0.09^a	70.8 ± 0.14^a	29.1 ± 0.55^a	ND	34.7 ± 0.07^a	2.1 ± 0.01^c	8.4 ± 0.03^a
Pushu 32		2.8 ± 0.00^c	23.1 ± 0.09^b	39.0 ± 0.61^c	11.5 ± 0.40^b	10.6 ± 0.02^a	6.6 ± 0.01^c	1.7 ± 0.00^d	4.5 ± 0.00^c
Simon No. 1		1.9 ± 0.00^d	18.8 ± 0.02^c	43.9 ± 0.42^b	10.0 ± 0.25^c	ND	9.1 ± 0.01^b	5.6 ± 0.01^a	ND
Shangshu 19		4.4 ± 0.05^b	12.6 ± 0.08^d	19.1 ± 0.05^d	9.8 ± 0.56^d	ND	6.6 ± 0.02^c	2.6 ± 0.01^b	ND
Yuzi No. 7	Skin	20.6 ± 0.16^a	33.9 ± 0.38^a	88.4 ± 0.42^a	32.5 ± 0.06^c	ND	31.5 ± 0.01^a	1.9 ± 0.01^b	ND
Pushu 32		ND	ND	12.1 ± 0.01^d	40.4 ± 0.02^a	ND	16.9 ± 0.01^b	ND	ND
Simon No. 1		ND	16.8 ± 0.82^b	20.0 ± 0.27^c	34.8 ± 0.20^b	ND	9.3 ± 0.01^c	ND	ND
Shangshu 19		2.4 ± 0.02^b	ND	23.2 ± 0.04^b	7.8 ± 0.41^d	ND	3.2 ± 0.01^d	2.1 ± 0.04^a	ND
Yuzi No. 7	Flesh	42.1 ± 0.01^a	59.9 ± 0.32^a	97.5 ± 0.11^a	27.3 ± 0.24^b	ND	19.9 ± 0.10^a	ND	ND
Pushu 32		ND	ND	12.1 ± 0.01^d	34.2 ± 0.36^a	ND	15.6 ± 0.01^b	ND	ND
Simon No. 1		5.5 ± 0.02^b	14.4 ± 0.05^b	20.9 ± 0.05^c	ND	4.6 ± 0.63^a	8.1 ± 0.00^c	ND	ND
Shangshu 19		ND	3.7 ± 0.03^c	27.1 ± 0.03^b	ND	ND	6.1 ± 0.00^d	ND	ND

ND, not detected; ANOVA, analysis of variance; DW, dry weight.

Different uppercase letters showed significant differences in each group of data (P < 0.05) for 4 sweet potato cultivars (ANOVA).

For individual anthocyanin analysis, acid hydrolysis of the samples was performed to release the major anthocyanidins (aglycons).²⁶ Table 4 shows 3 anthocyanidins identified as cyanidin, pelargonidin, and peonidin. Yuzi No. 7 leaves had the highest amount of cyanidin (763.1 ± 0.76 mg/100 g DW), while Shangshu 19 flesh contained the lowest amount of cyanidin (1.0 ± 0.00 mg/100 g DW) (Table 4, P < 0.05). Peonidin content was highest in Pushu 32 leaves (619.4 ± 0.16 mg/100 g DW) and lowest in Shangshu 19 skin (2.1 ± 0.02 mg/100 g DW) (Table 4, P < 0.05). An earlier study used different techniques to measure the range of cyanidin and peonidin contents of purple-colored sweet potato flours; values of 6.67 ± 0.1–157.56 ± 1.4 µg/g DW and 105.39 ± 0.9–610.40 ± 4.8 µg/g DW, respectively, were obtained.²⁷ These results were partly in accordance with the results presented in this study for sweet potato flesh (Table 4). More importantly, contrary to many previous findings, pelargonidin was detected in SPL. Lee et al²⁸ described pelargonidin in purple-colored sweet potato roots. We believe that further studies are required to explore the existence of pelargonidin in SPL. The percentages of TAC constituting the sum of peaks 1-3 for the edible parts of different sweet potato cultivars were 94.1%, 76.0%, 84.8%, and 92.0% (leaf, stem, skin, and flesh) for Yuzi No. 7 cultivar; 92.7%, 76.5%, and 81.0% (leaf, skin, and flesh) for Pushu 32 cultivar; 80.2%, 86.6 %, and 72.3% (leaf, skin, and flesh) for Simon No. 1 cultivar and 80.7%, 80.9%, and 85.4% (leaf, skin, and flesh) for Shangshu 19 cultivar, respectively.

Table 4

Contents of Individual Anthocyanidin Compounds in Edible Parts of 4 Sweet Potato Cultivars (mg/100 g DW).

Cultivar	Edible part	Anthocyanidin compounds
		Peak 1	Peak 2	Peak 3
		Cyanidin	Pelargonidin	Peonidin
Yuzi No. 7	Leaf	763.10 ± 0.76^a	0.90 ± 0.03^a	186.87 ± 0.26^b
Pushu 32		149.22 ± 0.51^d	0.76 ± 0.05^b	619.40 ± 0.16^a
Simon No. 1		506.47 ± 0.19^c	0.64 ± 0.00^c	126.54 ± 0.47^c
Shangshu 19		511.47 ± 0.16^b	ND	126.16 ± 0.20^d
Yuzi No. 7	Stem	25.54 ± 0.11	ND	5.64 ± 0.01
Yuzi No. 7	Skin	153.38 ± 0.22^a	0.81 ± 0.01^a	40.83 ± 0.87^a
Pushu 32		34.60 ± 0.14^b	ND	11.30 ± 0.02^c
Simon No. 1		27.24 ± 0.10^c	ND	16.05 ± 0.15^b
Shangshu 19		6.79 ± 0.07^d	ND	2.11 ± 0.02^d
Yuzi No. 7	Flesh	125.19 ± 0.13^a	0.62 ± 0.01^a	30.53 ± 0.89^a
Pushu 32		11.30 ± 0.05^b	ND	29.19 ± 0.03^b
Simon No. 1		1.42 ± 0.00^c	ND	5.81 ± 0.04^c
Shangshu 19		1.01 ± 0.00^d	ND	4.97 ± 0.02^d

ND, not detected; ANOVA, analysis of variance; DW, dry weight.

Different uppercase letters showed significant differences in each group of data (P < 0.05) for 4 sweet potato cultivars (ANOVA).

As observed in our study, differences in AA were noted among the different cultivars and edible parts. Sun et al²³ reported higher AA for individual phenolic compounds containing more hydroxyl groups, such as di and tricaffeoylquinic acids, than monocaffeoylquinic acids. Additionally, phenolic composition, molecular structure (number of mono-substituted or disubstituted caffeoylquinic acids), and the electron-donating abilities of molecules in sweet potato polyphenols greatly influenced their AA.¹² The aforementioned reasons, therefore, confirmed the differences in AA and phenolic composition among the different cultivars and the different edible parts as reported in this study.

In summary, this study has comprehensively explored the polyphenol abundance and AA in all the edible parts of sweet potato cultivars which are commercially available in China. To the best of our knowledge, this is the first elaborate investigation on the polyphenol content, polyphenol composition, and AA in the edible parts of sweet potatoes. TPC, TFC, TAC, AA, and individual phenolic contents displayed notable differences in all the 4 sweet potato cultivars (edible parts; leaf, stalk, stem, skin, and flesh). Overall, Yuzi No. 7 sweet potato cultivar contained significantly higher amounts of TPC, TFC, TAC, and AA in all the edible parts followed by Pushu 32, Simon No. 1, and Shangshu 19. Regardless of the sweet potato cultivar, TPC, TFC, TAC, and AAs of SPL were significantly higher than in other edible parts. Altogether, 19 individual phenolic compounds were analyzed by HPLC. In all the samples analyzed, the predominant phenolic acid, flavonoid, and anthocyanin compounds were 3,5-di-O-caffeoylquinic acid, astragalin, and cyanidin, respectively. Additionally, high positive correlations were reported between TAC and DPPH, TAC and FRAP, and TPC and ABTS assays. Our findings, therefore, provide new insights into the differences that exist in phenolic composition and AA among the edible parts of sweet potato cultivars. Furthermore, this study provides consumers with the option of utilizing sweet potato cultivars with high polyphenol contents. In conclusion, based on the aforementioned results, the edible parts of Yuzi No. 7 sweet potato cultivar presented the highest amount of polyphenol content (ie, TPC, TFC, and TAC) and AA suggesting the possibility of utilizing this cultivar by farmers and the food industry as a functional food product.

Materials and Methods

General

Edible parts of 4 sweet potato cultivars (Simon No. 1, Yuzi No. 7, Shangshu 19, and Pushu 32) were obtained from Haileda Food Co., Ltd., Beijing, China (Figure 2A). The characteristics of the 4 cultivars were as follows: Simon No. 1 (skin and flesh white), Yuzi No. 7 (skin and flesh purple), Shangshu 19 (skin orange, while flesh is white), and Pushu 32 (skin and flesh orange). All other edible parts, that is, leaves, stalks, and stems, were green. The criteria used for choosing these specific cultivars was based on their specific applications in the food industry, that is, Simon No. 1, Yuzi No. 7, Shangshu 19, and Pushu 32 are used as a medicine, as a source of anthocyanin, in starch processing, and for fresh consumption, respectively. These 4 sweet potato cultivars were cultivated in June 2018, under identical standard conditions in an experimental farm of Haileda Food Co., Ltd in Beijing, China. The average growth temperatures were 24°C, 27°C, and 25°C for June, July, and August, respectively. The 4 sweet potato cultivars were harvested in the middle of August and separated into 5 edible portions, that is, leaves, stalk, stem, skin, and flesh. These 4 cultivars were harvested based on previous research by our research group (data not published) and other published data on polyphenol content present in fruits and vegetables at different maturity stages.^19,29
-31 The extracts from leaves, stalk, or stem were pooled from as many plants as possible (usually 10-15 plants) and combined before extraction. Also, tissues were pooled from 3-5 tubers for each skin and flesh sample. For flesh or skin extracts, whole roots of sweet potato plants were taken, their skin and flesh separated, and then combined before extraction. All independent experiments for each edible part were replicated 3 times. Finally, the samples were cleaned, freeze-dried, ground into powder, and kept at 4°C until further use.

Figure 2

(A) Schematic drawing showing all the 5 edible parts (leaves, stalk, stem, skin, and flesh) of sweet potato plant. (B) Photograph of the 4 sweet potato cultivars (freeze-dried flesh powders). Pushu 32 (skin and flesh are orange in color), Yuzi No. 7 (skin and flesh are purple in color), Simon No. 1 (skin and flesh are white in color), and Shangshu 19 (skin is orange in color while flesh is white in color). All other edible parts, that is, leaves, stalks, and stems, were green in color. (C) Photograph of the 4 sweet potato cultivars (freeze-dried leaf powders). (D) Representative photos of sweet potato anthocyanin extract.

Reagents

Folin-Ciocalteu reagent, 2,4,6‐tri-(2‐pyridyl)‐1,3,5‐triazine, ABTS, DPPH, 6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid (Trolox), l-ascorbic acid, and chromatography-grade standards of anthocyanidins (cyanidin, pelargonidin, and peonidin) were purchased from Sigma Aldrich, Inc. (St. Louis, MO, USA). Chromatography-grade phenolic acid standards of 3-O-caffeoylquinic acid (3-CQA), 4-O-caffeoylquinic acid (4-CQA), 5-O-caffeoylquinic acid (5-CQA), 3,4-di-O-caffeoylquinic acid (3,4-diCQA), caffeic acid (CA), 3,5-di-O-caffeoylquinic acid (3,5-diCQA), 4,5-di-O-caffeoylquinic acid (4,5-diCQA), and 3,4,5-tri-O-caffeoylquinic acid (3,4,5-triCQA) were purchased from AMRESCO Biotechnology Co. Ltd. (Solon, OH, USA). Chromatography-grade flavonoid standards (quercetin, kaempferol, myricitrin, astragalin, tiliroside, quercitrin, isoquercitrin, and apigenin) were obtained from Apoptosis and Epigenetics Company (Houston, USA). All other analytical and HPLC grade solvents were obtained from Fisher Chemicals (Beijing, China).

Polyphenol Extraction

The crude polyphenol extract was obtained according to the published procedure of Sun et al.²³ Briefly, 200 mL of ethanol (70% v/v) was used to dissolve 10 g of the sweet potato edible part powder. The contents were subjected to ultrasonic wave treatment (59 kHz) for 30 minutes at 50°C prior to centrifugation at 5000 ×g for 10 minutes at 4°C. The residue obtained was extracted twice using ethanol as reported previously, and the crude polyphenol extract was obtained by concentrating the supernatant in a rotary evaporator at 45°C. Next, the obtained crude polyphenol extracts were freeze-dried and the final weights recorded (Figure 2B, C D). All obtained samples were kept at 4°C in sealed aluminum bags until further use.

Total Polyphenol Content

TPC determination was done using Folin-Ciocalteu reagent, as outlined by Sun et al.¹¹ Chlorogenic acid (0.01-0.10 mg/mL) was used to calculate the amount of TPC. The results were calculated as chlorogenic acid equivalents (CAE) on a DW basis (CAE mg/100 g DW).

Total Flavonoid Content

TFC was assessed by following the colorimetric assay method published by Zhishen et al.³² Quercetin (0.01-0.10 mg/mL) was used to determine flavonoid content. TFC was presented as quercetin equivalents (QE) per 100 g DW (QE mg/100 g DW).

Total Anthocyanin Content

TAC was evaluated based on the differential pH method as explained by Sun et al,³³ with a slight modification. Briefly, a 10 µL aliquot of sample was separately mixed with 290 µL of potassium chloride (0.025 M) and sodium acetate (0.4 M) solutions. The pH of the 2 solutions was set at 1.0 and 4.5 using potassium chloride (0.025 M) and sodium acetate (0.4 M), respectively. Absorbance readings were recorded at 520 nm and 700 nm using a spectrophotometer. TAC was calculated as cyanidin 3-glucoside equivalents using an extinction coefficient (ε) of 26 900 L/cm mol and a molecular weight of 432.

Antioxidant Activity

FRAP assay

The FRAP assay was performed as described by Benzie and Strain.³⁴ A standard curve made of Trolox (10-200 µg/mL) was employed as a control to determine the assay results, which are recorded as Trolox equivalents (TE) per 100 g of sample on a DW basis (TE mg/100 g DW).

DPPH Radical Scavenging Activity

The procedure used for the DPPH assay was that described by Brand-Williams et al,³⁵ with slight modifications. Briefly, 0.1 mM of DPPH solution (3 mL) was prepared and reacted with 200 µL of sample extract. The reaction was kept in a dark room for 30 minutes at room temperature. Absorbance readings were recorded using a spectrophotometer at 517 nm. The results were expressed as ascorbic acid equivalents (AAE) on a DW basis (AAE mg/100 g DW).

ABTS Radical Scavenging Capacity Assay

The ABTS assay followed the procedure illustrated by Thaipong et al,³⁶ with little modification. Briefly, ABTS solution (7.4 mM) and potassium persulfate (2.6 mM) were mixed together in equal proportions and allowed to react for 16 hours in the dark. Subsequently, the working solution obtained was diluted in ethanol to achieve an absorbance of 0.7 ± 0.05 at 734 nm before use. The activity was recorded as AAE mg/100 g DW.

Individual Phenolic Composition

Qualitative and quantitative analysis of phenolic acids by HPLC

Extraction of sweet potato phenolic acids: Phenolic acids present in sweet potatoes were extracted as explained earlier, that is, polyphenol extraction. The obtained extracts were diluted in methanol (80%) and filtered through 0.45 µm syringe filters before HPLC analysis.^11,23

HPLC determination of sweet potato phenolic acids: Reversed phase-HPLC (Shimadzu LC20A HPLC system, Kyoto, Japan) was used to analyze the individual phenolic acids using a method described by Sun et al.¹¹ Separations were conducted at 30°C on a C18 column (150 mm × 4.6 mm; 5 µm particle size) using phosphoric acid (0.1% v/v) and acetonitrile (100%) as mobile phases A and B, respectively. The analyzed compounds were detected at 326 nm and the peak identities of the phenolic compounds were established by the retention times of phenolic acid standards. Results were presented as mg/100 g DW (Table 5).

Table 5

Retention Time and Detection Wavelength of Polyphenol Compounds Found in Sweet Potato Edible Parts.

Polyphenol compound	Peak	Retention time (min)	Detection wavelength (nm)	Identity
Phenolic acids	1	1.73	326	5-O-Caffeoylquinic acid
	2	2.56	326	3-O-Caffeoylquinic acid
	3	3.18	326	4-O-Caffeoylquinic acid
	4	5.41	326	Caffeic acid
	5	8.04	326	4,5-Di-O-caffeoylquinic acid
	6	8.62	326	3,5-Di-O-caffeoylquinic acid
	7	9.02	326	3,4-Di-O-caffeoylquinic acid
	8	10.31	326	3,4,5-Tri-O-caffeoylquinic acid
Flavonoids	1	7.35	326	Myricetrin
	2	8.11	326	Isoquercitrin
	3	8.63	326	Astragalin
	4	9.09	326	Quercitrin
	5	9.68	326	Tiliroside
	6	10.23	326	Quercetin
	7	11.25	326	Apigenin
	8	12.28	326	Kaempferol
Anthocyanins	1	15.25	530	Cyanidin
	2	16.93	530	Pelargonidin
	3	17.42	530	Peonidin

Extraction of sweet potato flavonoids: Sweet potato flavonoids were extracted following the procedure published by Liu et al.¹⁴

HPLC determination of sweet potato flavonoids: HPLC analysis of sweet potato flavonoids was also done as outlined by Liu et al.¹⁴ Briefly, the analysis was carried out at 30°C on a C18 column with 0.5% phosphoric acid and 100% acetonitrile as mobile phases A and B, respectively. The ﬂow rate was set at 1.0 mL/minute; the injection volume at 20 µL, and 326 nm was the detection wavelength. Results were described as mg/100 g DW.

Acid hydrolysis of anthocyanins: The crude polyphenol extract was hydrolyzed as described by Truong et al.²⁴Briefly, 5 mL of crude polyphenol extract was mixed with 7.5 mL of 6 N hydrochloric acid (HCl), and the contents were hydrolyzed at 100°C for 60 minutes. Hydrolysis was stopped by cooling the samples in an ice bath. Finally, the samples were redissolved in 5 mL 1% formic acid solution and acidified with 0.12 N HCl after vacuum drying in an evaporator. Additionally, the samples were filtered through 0.45 µm syringe filters before HPLC analysis.

HPLC determination of anthocyanidins: HPLC analysis of anthocyanidins was performed as outlined by Truong et al.²⁴The conditions used were as follows: column, C18; oven temperature, 30°C; ﬂow rate, 1 mL/minute; injection volume, 20 µL; and detection wavelength, 530 nm. Formic acid (1%) and acetonitrile (containing 1% formic acid) were used as mobile phases A and B, respectively. Anthocyanidin standards were used to identify the respective anthocyanidin compounds. Results were recorded as mg/100 g DW.

Statistical Analysis

The obtained data were reported as mean values ± SD of triplicate experiments. One-way analysis of variance followed by Duncan’s multiple range test was performed using SAS 8.1 (SAS Institute Inc., Cary, NC, USA). Significant differences between means were reported at P < 0.05. The relationship between TPC, TFC, TAC, and AA (FRAP, DPPH, and ABTS assays) was studied by Pearson’s coefficients of correlation.

Footnotes

Acknowledgements

The authors are grateful to Beijing Haileda Food Co., Ltd. (Beijing, China) for supplying the sweet potato samples.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: this work was supported by the Natural Science Funding of China (31701614), the National Key R&D Program of China (2016YFE0133600), and the Earmarked Fund for China Agriculture Research System (CARS-10-B21).

ORCID iD

Hong-Nan Sun

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