Abstract
Even though Jerusalem artichoke (Helianthus tuberosus L.) has strong resistance to abiotic stresses, salinity can still reduce the biomass of Jerusalem artichoke. The purpose of this study was to elucidate the differences in the development of Jerusalem artichoke and the dynamics of sugar throughout the growth period under high (7.23–8.15 g/kg) and low (3.20–4.32 g/kg) salinity stress in the field in Jiangsu Province, China. This study confirmed that high salinity promoted the conversion of reducing sugars to non-reducing sugars (fructans) in Jerusalem artichoke tubers, but significantly reduced the biomass of Jerusalem artichoke and advanced the peak time of the dry matter accumulation of aerial parts. In addition, in the early and late stages of tuberization, the total sugar content of tubers under low salinity conditions (786 ± 8 mg/g and 491 ± 8 mg/g) was 93.3% and 1.15 times than those under high salinity conditions, respectively. Moreover, the total sugar content in stems was consistently greater under high than low salinity conditions in the same period. The accumulation rate and the amount of dry matter were significantly higher in stems than in other tissues. Therefore, the aerial parts of “Nanyu No. 1” could be harvested before mid-to-early October, and the tubers after mid-November. This study revealed the internal reasons for the decreased yield of Jerusalem artichoke under salt stress, and provided theoretical basis and guidance for the cultivation and utilization of Jerusalem artichoke in saline-alkali soil.
Keywords: Jerusalem artichoke, Soil salinization, Yield, Tuber, Fructans, Dry matter
1. Introduction
Soil salinization is one of the most important abiotic stresses limiting crop yield worldwide [3,9,12,13,36,46]. About 1/3 of the agricultural land in the world is saline [1,25,32]. Over the past few decades, soil salinization has reduced the yields of major global crops [5,29,45]. It is predicted that the area of agricultural land affected by salinization in the world will be 2–3 times the current size by 2050 [43,44].
It is well known that salt stress can not only inhibit the photosynthesis, resulting in plant growth retardation, but also cause osmotic stress and ion toxicity, leading to the metabolic disorders [15,16,19,39,42]. Jerusalem artichoke (Helianthus tuberosus L., family Asteraceae) is a perennial tuberous plant with a wide environmental adaptability. Jerusalem artichoke has strong resistance to abiotic stresses, low nutrient demand, strong ecological-restoration effect and high commercial value [6,10,20,23,47]. Due to these advantageous properties, Jerusalem artichoke is used to improve saline soils and achieve strong economic, social and ecological benefits [8,18,21,45]. Even so, some scholars showed that salt stress had a negative effect on the yield of Jerusalem artichoke, and the yield reduction of tuber was much larger than that of the aboveground part [14,20].
The tuber of Jerusalem artichoke is the main organ producing economic value and the most important reservoir. The main substance stored in tubers is fructan. It has been reported that the tuber yield of Jerusalem artichoke is closely related to fructan metabolism [4,46]. Carbohydrates are the main products of plant photosynthesis, including structural carbohydrates (lignin, cellulose, etc.) used for plant morphological construction and soluble carbohydrates (glucose, fructose, sucrose, fructan and starch, etc.) involved in plant life metabolism [7,38]. Glucose and fructose are the main energy and energy substances. Sucrose is the main form of carbohydrate transport in plants and plays an important role in regulating the accumulation and distribution of sugar in plants, while fructan is an important storage carbohydrate in plant vegetative organs [24]. The synthesis, transport and distribution of these soluble carbohydrates in plants are regulated by plant growth and development, as well as environmental factors [23,30].
Relevant studies had shown that sugars (carbohydrates) in Jerusalem artichoke were mainly produced by leaves and transported to underground tubers through stems [7]. And the accumulation and redistribution of sugars in the stem played an important role in regulating the tuberization process, as sugars were temporarily stored in the stem before being transported to Jerusalem artichoke tubers [17,38]. The assimilation products (carbohydrates) produced by photosynthesis in Jerusalem artichoke leaves were mainly transported to the underground in the form of sucrose, but stored in the tubers in the form of fructan (polyfructosylsucrose) [6,24]. Sucrose was the precursor for the synthesis of fructans, but the synthesis and storage of fructans (particularly inulin) were mainly carried out in the tubers of Jerusalem artichoke [7,23,30]. In addition, fructan as an osmotic regulator, plays an important role in improving plant resistance to cold, drought and salinity [35,40,41].
Various environmental factors can affect the synthesis, transport and distribution of the photoassimilates [14,21,37]. In particular, saline-alkali stress can significantly affect the total biomass and dry matter accumulation in different tissues of Jerusalem artichoke [4,7,17,33,46], but the underlying mechanisms are still unclear.
Therefore, we hypothesized that the reduction of tuber yield caused by salt stress should be related to sugar metabolism, which affects the accumulation of dry matter in tubers by changing the synthesis and distribution of sugar in plants. Most of the reported studies on Jerusalem artichoke have focused on its physiology, ecological benefits and by-product processing, with very few studies on sugar metabolism. The aim of this study was to elucidate the dynamic changes in sugar content throughout the Jerusalem artichoke growth period to provide a theoretical basis for the cultivation and utilization of Jerusalem artichoke in the saline alkali soil.
2. Materials and methods
2.1. Site description
The Jerusalem artichoke variety Nanyu No.1 (Helianthus tuberosus L., Su-jian 200901) used in the research was provided by the experimental base of Nanjing Agricultural University, Dafeng District, Yancheng City, Jiangsu Province, China. Nanyu No.1, which has strong saline-alkaline tolerance (optimum salinity <4 g/kg, tolerance salinity <9 g/kg), barren tolerance, disease resistance and ecological adaptability, was planted on two natural saline-alkali fields with different salinities. One with low salinity (3.20–4.32 g/kg) was located in Xinyang Experimental Station of Jiangsu Academy of Agricultural Sciences, Yancheng City, Jiangsu Province, China (33°53′N, 120°45′E), and the other with high salinity of 7.23–8.15 g/kg was located in Shuntai Farm, Yancheng City, Jiangsu Province, China (33°71′N, 120°39′E). The conditions of the two fields were similar except for the difference in salinity.
The grass on naturally saline soil was mowed before plowing using a conventional moldboard plow. Each field was set up with three plots (4 m × 8 m = 32 m2 each) as replicates, and 80 cm-wide guard rows are set around each plot. Jerusalem artichoke was cultivated on April 5, 2018 and April 5, 2019. Plant row spacing was 60 cm inter-row and 45 cm intra-row. Neither fertilization nor irrigation.
2.2. Sample collection
Plants were sampled monthly starting on May 6 and ending on December 6, 2018 and 2019. At each sampling, three plants were randomly selected from each plot for measuring plant height and the length of the longest root (with a tape measure) and stem diameter (at the root base just above the ground) (with a vernier caliper). The plants were separated into leaves, stems, roots and tubers [17,33]. An appropriate amount of tuber samples collected from October to December were wrapped in tin foil, marked, quick-frozen in liquid nitrogen, and then transferred to the laboratory on ice for subsequent transcriptome analysis [32].
2.3. Methods
2.3.1. Determination of biomass
The leaves, stems, roots, and tubers were dried to constant weight at 80 °C after enzyme deactivation at 105 °C for 15 min, milled into powder and stored in dry environment for further analyses. Samples of all plant parts were weighed before and after drying [17,33].
2.3.2. Determination of sugar fraction
Total soluble sugars were quantified using colorimetric method based on phenol-sulfuric acid [17,33]. The dried and milled samples (0.30 g) were mixed with deionized water (10 mL), and then extracted in water-bath at 100 °C for 30 min (extracted twice). The supernatant was filtered through a hydrophilic membrane filter with a pore size of 0.45 μM, and then the volume was fixed in a 25-mL volumetric flask. .A 1.0-mL aliquot of this crude extract was mixed with 1.0 mL of 5% v/v aqueous phenol solution and 5.0 mL of concentrated sulfuric acid at room temperature, and measured at 490 nm by a UV spectrophotometer (UV-755B, Shanghai Jingke, China) with glucose solution as standard. High performance liquid chromatography (Agilent 1260 Infinity, Agilent Technologies Inc., Santa Clara, California, USA) was used to determine the sugar composition [17,33].
2.4. Statistics
The average value of all parameters was taken from the six replicates, and the standard error was calculated. Microsoft Excel 2013 and SPSS 19.0 (IBM, Armonk, New York, USA) were used to analyze the data using a one-way analysis of variance (ANOVA) and Tukey's new multiple range test (p ≤ 0.05). Adobe Illustrator CC 2017 (Adobe Systems Inc., SAN Jose, California, USA) was used to draw figures [28,34].
3. Results
3.1. The basic growth indicators of Jerusalem artichoke in different stages
The plant height of Jerusalem artichoke (Fig. 1A) increased continuously throughout the growth period, and remained relatively stable after reaching the peak. However, different soil salinity caused the difference in the peak plant height. The plant height of Jerusalem artichoke peaked at 357 ± 23.0 cm under low salinity around October 6, and at 160 ± 20.0 cm under high salinity around August 6.
Fig. 1.
Plant height, stem diameter and root length of “Nanyu No. 1” (Mean ± SE). Note: Different lowercase letters indicate significant differences among the samples (p ≤ 0.05).
The stem diameter (Fig. 1B) of Jerusalem artichoke also increased initially, but showed a slow decline after reaching the peak. The root length of Jerusalem artichoke (Fig. 1C) varied similarly to the stem diameter. In addition, as could be seen from Fig. 1A and C, changes in plant height (R2 = 0.99, 0.98) and root length (R2 = 0.70, 0.84) of Jerusalem artichoke could be fitted by the trinomial equation (similar to the growth curve) under both low and high salinity conditions, while the change of stem diameter could be fitted by parabola (R2 = 0.88, 0.87) (Fig. 1B).
The accumulation of dry matter in leaves (Fig. 2A), stems (Fig. 2B) and roots (Fig. 2C) of Jerusalem artichoke increased gradually from May 6 to October 6, and then followed a clear downward trend. The peak dry weights (g/plant) of leaves, stems and roots of Jerusalem artichoke under low salinity conditions were 6.11-, 2.19- and 1.15-fold, respectively, greater than under high salinity.
Fig. 2.
Dry weight of different tissues of “Nanyu No. 1” (Mean ± SE). Note: Different lowercase letters indicate significant differences among the samples (p ≤ 0.05).
The tubers of Jerusalem artichoke (Fig. 2D) were first recorded on September 6 under low salinity conditions and 2 months later under the high salinity conditions. On December 6, dry weight of Jerusalem artichoke tubers was 12.7-fold greater under low than high salinity conditions. Except that dry matter in tuber was not suitable for equation fitting, the content change of dry matter in leaf (Fig. 2A), stem (Fig. 2B) and root (Fig. 2C) could be fitted by the trinomial equation under both low (R2 = 0.81, 0.79, 0.89) and high (R2 = 0.83, 0.73, 0.61) salinity conditions.
3.2. Soluble sugar content of Jerusalem artichoke at different stages
The contents of both total and reducing sugars in the leaves were generally stable from May 6 to October 6, and did not differ under different salinity conditions. However, the total sugar content in leaves increased sharply in November under the condition of low salinity conditions, while the reducing sugar content barely changed. Therefore, the content changes of total sugar (R2 = 0.80, 0.94) and reducing sugar (R2 = 0.84, 0.80) in leaves were fitted with pentoterms and trinomials respectively under both low and high salinity conditions (Fig. 3, Fig. 4A).
Fig. 3.
Total sugar content in different tissues of “Nanyu No. 1” (Mean ± SE). Note: Different lowercase letters indicate significant differences among the samples (p ≤ 0.05).
Fig. 4.
Reducing sugar content in different tissues of “Nanyu No. 1” (Mean ± SE). Note: Different lowercase letters indicate significant differences among the samples (p ≤ 0.05).
The changes in sugar content in stems were quite different from those in leaves. The total sugars in Jerusalem artichoke stems under high salinity conditions were consistently higher than those under low salinity conditions (p ≤ 0.05) after July 6. The maximum total sugar content in stems under high salinity conditions was on September 6, when it was 2.90 times that under low salinity treatment (Fig. 3B). However, from May 6 to June 6, the content of reducing sugar in the stems of Jerusalem artichoke under low salinity conditions was significantly higher than that under high salinity conditions (p ≤ 0.05), whereas the opposite was shown on September 6 (Fig. 4B). Therefore, the content changes of total sugar (R2 = 0.84, 0.86) and reducing sugar (R2 = 0.85, 0.63) in stems were fitted with trinomials under both low and high salinity conditions (Fig. 3, Fig. 4B).
In the root system of Jerusalem artichoke, the content of total and reducing sugars also showed a fluctuating trend. The total sugar content in roots was significantly higher under high compared with low salinity on June 6 and July 6, and the opposite occurred on October 6 and November 6 (Fig. 3C). By contrast, the reducing sugar content in the roots of Jerusalem artichoke was higher under low than high salinity on June 6 and October 6 (Fig. 4C). Therefore, the content changes of total sugar (R2 = 0.96, 0.95) and reducing sugar (R2 = 1.00, 1.00) in roots were fitted with pentoterms under both low and high salinity conditions (Fig. 3, Fig. 4C).
Under low salinity conditions, the total sugar content in Jerusalem artichoke tubers was 770 ± 22.7 mg/g in September and October, and dropped to 438 ± 75.2 mg/g in November and December. Under high salinity conditions, the total sugar content in tubers was 843 ± 3.78 mg/g in November, and dropped to 427 ± 6.47 mg/g in December (Fig. 3D). The content of reducing sugars in tubers (25.5 ± 1.22 mg/g) was similar under different salinity conditions in November and December (Fig. 4D). The sugar content in Jerusalem artichoke tubers was not suitable for equation fitting.
3.3. Trends in sugar composition
From May 6 to November 6, there was no significant difference in the content of Fructose (Table 1), Glucose (Table 2), Sucrose (Table 3), 1-Kestose (GF2, Table 4), Nystose (GF3, Table 5) or 1F-fructofuranosylnystose (GF4, Table 6) in different tissues of Jerusalem artichoke. There was also no significant difference under different salinity conditions in the same tissue. Thus, their average contents (mg/g) in different tissues were 2.65 ± 0.36, 7.67 ± 0.49, 1.55 ± 0.04, 1.69 ± 0.17, 2.86 ± 0.11 and 2.99 ± 0.20, respectively.
Table 1.
Fructose in different tissues of “Nanyu No. 1” (Mean ± SE).
| Sugar content (mg/g) | May 6th | Jun. 6th | Jul. 6th | Aug. 6th | Sept. 6th | Oct. 6th | Nov. 6th | Dec. 6th | ||
|---|---|---|---|---|---|---|---|---|---|---|
| Fructose | Leaves | L | 2.50 ± 0.16b | 2.61 ± 0.01b | 2.59 ± 0.04b | 2.60 ± 0.01b | 2.60 ± 0.03b | 2.56 ± 0.02b | 2.66 ± 0.01 ab | – |
| H | 2.59 ± 0.02b | 2.60 ± 0.02b | 2.56 ± 0.01b | 2.59 ± 0.02b | 2.56 ± 0.02b | 2.59 ± 0.02b | 2.88 ± 0.27a | – | ||
| Stems | L | 2.63 ± 0.01 ab | 2.6 ± 0.01 ab | 2.60 ± 0.04 ab | 2.58 ± 0.04b | 2.56 ± 0.02b | 2.65 ± 0.06 ab | 2.72 ± 0.06 ab | – | |
| H | 2.59 ± 0.01b | 2.56 ± 0.01b | 2.70 ± 0.08 ab | 2.64 ± 0.03 ab | 2.69 ± 0.15 ab | 2.69 ± 0.03 ab | 2.80 ± 0.16a | – | ||
| Tubers | L | – | – | – | – | 2.80 ± 0.01b | 2.66 ± 0.09b | 3.15 ± 0.20b | 6.03 ± 0.10a | |
| H | – | – | – | – | – | – | 2.92 ± 0.41b | 5.62 ± 0.37a | ||
Note: L: low salinity, H: high salinity. For a given tissue and a specific sugar compound, different lowercase letters indicate significant differences among the sampling times and salinity treatments (p ≤ 0.05).
Table 2.
Glucose in different tissues of “Nanyu No. 1” (Mean ± SE).
| Sugar content (mg/g) | May 6th | Jun. 6th | Jul. 6th | Aug. 6th | Sept. 6th | Oct. 6th | Nov. 6th | Dec. 6th | ||
|---|---|---|---|---|---|---|---|---|---|---|
| Glucose | Leaves | L | 7.08 ± 0.45b | 7.39 ± 0.01b | 7.33 ± 0.11b | 7.35 ± 0.02b | 7.35 ± 0.09b | 7.30 ± 0.09b | 8.23 ± 0.01a | – |
| H | 7.35 ± 0.06b | 7.36 ± 0.04b | 7.25 ± 0.00b | 7.33 ± 0.05b | 7.24 ± 0.07b | 7.33 ± 0.04b | 8.23 ± 0.77a | – | ||
| Stems | L | 7.32 ± 0.10bc | 7.54 ± 0.26abc | 7.57 ± 0.07abc | 7.28 ± 0.07c | 7.21 ± 0.06c | 7.50 ± 0.17abc | 7.56 ± 0.13abc | – | |
| H | 7.34 ± 0.01bc | 7.25 ± 0.01c | 8.00 ± 0.24a | 7.34 ± 0.06bc | 7.71 ± 0.49abc | 7.87 ± 0.32 ab | 7.48 ± 0.06abc | – | ||
| Tubers | L | – | – | – | – | 7.42 ± 0.01a | 7.35 ± 0.17a | 7.46 ± 0.06a | 7.50 ± 0.01a | |
| H | – | – | – | – | – | – | 7.55 ± 0.07a | 7.38 ± 0.05a | ||
Note: L: low salinity, H: high salinity. For a given tissue and a specific sugar compound, different lowercase letters indicate significant differences among the sampling times and salinity treatments (p ≤ 0.05).
Table 3.
Sucrose in different tissues of “Nanyu No. 1” (Mean ± SE).
| Sugar content (mg/g) | May 6th | Jun. 6th | Jul. 6th | Aug. 6th | Sept. 6th | Oct. 6th | Nov. 6th | Dec. 6th | ||
|---|---|---|---|---|---|---|---|---|---|---|
| Sucrose | Leaves | L | 1.50 ± 0.10b | 1.56 ± 0.01b | 1.55 ± 0.02b | 1.56 ± 0.01b | 1.56 ± 0.02b | 1.55 ± 0.02b | 1.61 ± 0.01 ab | – |
| H | 1.55 ± 0.01b | 1.56 ± 0.01b | 1.53 ± 0.01b | 1.55 ± 0.01b | 1.54 ± 0.01b | 1.57 ± 0.02b | 1.73 ± 0.16a | – | ||
| Stems | L | 1.55 ± 0.00b | 1.56 ± 0.01a | 1.54 ± 0.02b | 1.54 ± 0.01b | 1.52 ± 0.01b | 1.56 ± 0.02 ab | 1.57 ± 0.02 ab | – | |
| H | 1.55 ± 0.01b | 1.54 ± 0.01b | 1.54 ± 0.01b | 1.55 ± 0.01b | 1.53 ± 0.01b | 1.60 ± 0.04a | 1.57 ± 0.01 ab | – | ||
| Tubers | L | – | – | – | – | 1.56 ± 0.01b | 1.55 ± 0.03b | 1.55 ± 0.01b | 1.61 ± 0.02a | |
| H | – | – | – | – | – | – | 1.59 ± 0.02 ab | 1.57 ± 0.01 ab | ||
Note: L: low salinity, H: high salinity. For a given tissue and a specific sugar compound, different lowercase letters indicate significant differences among the sampling times and salinity treatments (p ≤ 0.05).
Table 4.
1-Kestose (GF2) in different tissues of “Nanyu No. 1” (Mean ± SE).
| Sugar content (mg/g) | May 6th | Jun. 6th | Jul. 6th | Aug. 6th | Sept. 6th | Oct. 6th | Nov. 6th | Dec. 6th | ||
|---|---|---|---|---|---|---|---|---|---|---|
| 1-Kestose | Leaves | L | 1.49 ± 0.10c | 1.57 ± 0.01bc | 1.57 ± 0.03bc | 1.59 ± 0.01bc | 1.56 ± 0.01bc | 1.55 ± 0.02c | 1.65 ± 0.00b | – |
| H | 1.57 ± 0.01bc | 1.59 ± 0.03bc | 1.55 ± 0.00c | 1.58 ± 0.03bc | 1.54 ± 0.01c | 1.56 ± 0.01bc | 1.75 ± 0.16a | – | ||
| Stems | L | 1.55 ± 0.01c | 1.60 ± 0.01abc | 1.64 ± 0.04abc | 1.66 ± 0.07abc | 1.70 ± 0.10 ab | 1.59 ± 0.02abc | 1.58 ± 0.01bc | – | |
| H | 1.6 ± 0.01abc | 1.58 ± 0.01abc | 1.71 ± 0.07a | 1.64 ± 0.04abc | 1.69 ± 0.02 ab | 1.60 ± 0.02abc | 1.61 ± 0.04abc | – | ||
| Tubers | L | – | – | – | – | 1.67 ± 0.01d | 1.66 ± 0.06d | 2.03 ± 0.14c | 2.88 ± 0.07a | |
| H | – | – | – | – | – | – | 1.83 ± 0.17cd | 2.48 ± 0.00b | ||
Note: L: low salinity, H: high salinity. For a given tissue and a specific sugar compound, different lowercase letters indicate significant differences among the sampling times and salinity treatments (p ≤ 0.05).
Table 5.
Nystose (GF3) in different tissues of “Nanyu No. 1” (Mean ± SE).
| Sugar content (mg/g) | May 6th | Jun. 6th | Jul. 6th | Aug. 6th | Sept. 6th | Oct. 6th | Nov. 6th | Dec. 6th | ||
|---|---|---|---|---|---|---|---|---|---|---|
| Nystose | Leaves | L | 2.67 ± 0.17c | 2.82 ± 0.01bc | 2.78 ± 0.06bc | 2.79 ± 0.01bc | 2.8 ± 0.04bc | 2.77 ± 0.02bc | 2.82 ± 0.01bc | – |
| H | 2.78 ± 0.01bc | 2.86 ± 0.05b | 2.74 ± 0.01bc | 2.77 ± 0.02bc | 2.76 ± 0.03bc | 2.78 ± 0.01bc | 3.08 ± 0.29a | – | ||
| Stems | L | 2.77 ± 0.01a | 2.83 ± 0.01a | 2.87 ± 0.10a | 2.87 ± 0.09a | 2.95 ± 0.16a | 2.84 ± 0.04a | 2.81 ± 0.02a | – | |
| H | 2.87 ± 0.01a | 2.84 ± 0.04a | 2.86 ± 0.02a | 2.89 ± 0.05a | 2.91 ± 0.01a | 2.89 ± 0.06a | 2.84 ± 0.03a | – | ||
| Tubers | L | – | – | – | – | 2.95 ± 0.01c | 3.03 ± 0.15c | 3.80 ± 0.29b | 4.41 ± 0.14a | |
| H | – | – | – | – | – | – | 3.32 ± 0.16c | 4.19 ± 0.10 ab | ||
Note: L: low salinity, H: high salinity. For a given tissue and a specific sugar compound, different lowercase letters indicate significant differences among the sampling times and salinity treatments (p ≤ 0.05).
Table 6.
1F-fructofuranosylnystose (GF4) in different tissues of “Nanyu No. 1” (Mean ± SE).
| Sugar content (mg/g) | May 6th | Jun. 6th | Jul. 6th | Aug. 6th | Sept. 6th | Oct. 6th | Nov. 6th | Dec. 6th | ||
|---|---|---|---|---|---|---|---|---|---|---|
| 1F-fructofuranosylnystose | Leaves | L | 2.85 ± 0.20b | 3.06 ± 0.01b | 2.93 ± 0.03b | 2.98 ± 0.09b | 2.94 ± 0.04b | 3.15 ± 0.10b | 3.12 ± 0.34b | – |
| H | 2.94 ± 0.02b | 2.99 ± 0.11b | 2.95 ± 0.08b | 2.94 ± 0.08b | 2.95 ± 0.00b | 2.90 ± 0.03b | 3.79 ± 0.10a | – | ||
| Stems | L | 2.93 ± 0.01b | 3.06 ± 0.10 ab | 2.99 ± 0.03 ab | 3.04 ± 0.11 ab | 2.93 ± 0.01b | 3.11 ± 0.03 ab | 2.97 ± 0.04b | – | |
| H | 3.20 ± 0.01a | 3.05 ± 0.04 ab | 3.07 ± 0.09 ab | 2.93 ± 0.03b | 2.94 ± 0.02b | 3.13 ± 0.18 ab | 2.96 ± 0.03b | – | ||
| Tubers | L | – | – | – | – | 3.13 ± 0.02b | 3.31 ± 0.20a | 4.15 ± 0.32b | 4.54 ± 0.17a | |
| H | – | – | – | – | – | – | 3.60 ± 0.08b | 4.58 ± 0.12a | ||
Note: L: low salinity, H: high salinity. For a given tissue and a specific sugar compound, different lowercase letters indicate significant differences among the sampling times and salinity treatments (p ≤ 0.05).
On December 6, the content of Fructose, 1-Kestose, Nystose and 1F-fructofuranosylnystose in Jerusalem artichoke tubers all increased considerably. Among them, the content of Fructose in Jerusalem artichoke tubers reached 6.03 ± 0.10 mg/g and 5.62 ± 0.37 mg/g under low and high salinity conditions, respectively, and the content of 1-Kestose reached 2.88 ± 0.07 mg/g and 2.48 ± 0.01 mg/g, respectively. In addition, the content of Nystose also reached 4.41 ± 0.14 mg/g and 4.19 ± 0.10 mg/g, and the content of 1F-fructofuranosylnystose also reached 4.54 ± 0.17 mg/g and 4.58 ± 0.12 mg/g, respectively.
4. Discussion
Dry matter in plants is mainly derived from photosynthesis [6,17]. Some studies suggested that salt stress and drought stress could change the distribution of dry matter in various organs of plants [22,26,31]. And we all know that plant growth and development or external environmental factors can affect the synthesis, transport and distribution of these photoassimilates in plants [21,24]. Here, the results showed that high salinity stress advanced the peak time of the dry matter accumulation of aerial parts (Fig. 2). Moreover, the total sugar content in Jerusalem artichoke stems under high salinity conditions were consistently higher than that under low salinity conditions in the same period, especially after July 6th (Fig. 3). Additionally, the accumulation of dry matter in leaves (Fig. 2A), stems (Fig. 2B) and roots (Fig. 2C) of Jerusalem artichoke increased gradually from May 6 to October 6, and then followed by a clear downward trend. Previous studies observed that the peak yield of above-ground biomass was in October, and followed by significant decreases afterwards [11,17], which was consistent with the results of this study. The results proved that soil salinity had a great influence on the total biomass and dry matter accumulation of different tissues of Jerusalem artichoke [17,33].
In addition, we found that the decrease in the dry matter mass of the aerial part was accompanied by an increase in the dry matter mass of the underground tuber (Fig. 2). In other words, the peak of dry matter accumulation in Jerusalem artichoke stems appeared later than that in leaves and roots, and in the early stage of tuberization, the dry matter accumulation rate and content of Jerusalem artichoke stems were significantly higher in other tissues (Fig. 2). This was mainly due to the fact that the dry matter in Jerusalem artichoke tubers was mainly derived from its aerial parts, which were transported through the stems and accumulated in the tubers [7,21].
And relevant studies had shown that sugars (carbohydrates) in Jerusalem artichoke were mainly produced by leaves and transported to underground tubers through stems [7]. And the accumulation and redistribution of sugars in the stem played an important role in regulating the tuberization process, as sugars were temporarily stored in the stem before being transported to Jerusalem artichoke tubers [17,38]. So the amount of dry matter in the stems and roots of Jerusalem artichoke changed synchronously, and the dry weight of the stems was much higher than that of the leaves from September 6 to October 6 (Fig. 2). The above results indicated that in the early stage of tuberization, the photosynthetic assimilation products of Jerusalem artichoke were temporarily stored in the stem of Jerusalem artichoke, and the tuberization of Jerusalem artichoke changed the storage pool of photosynthetic products of Jerusalem artichoke from stems to tubers [2,17,38]. Hence, we could harvest Jerusalem artichoke “Nanyu No. 1” in different periods according to different needs. For example, to harvest the aerial parts before mid-to-early October, and to harvest the underground tubers after mid-November.
Reports also had shown that the assimilation products produced by photosynthesis in Jerusalem artichoke leaves were mainly transported to the underground in the form of sucrose, but stored in the tubers in the form of fructan (polyfructosylsucrose) [17,24,33]. Sucrose was the precursor for the synthesis of fructans, but the synthesis and storage of fructans (particularly inulin) were mainly carried out in the tubers of Jerusalem artichoke [7,23,30]. In this study, the reducing sugar content in Jerusalem artichoke tubers was 40.66 ± 2.00 mg/g under low salinity conditions on September 6, and it was reduced to half of the original content (25.5 ± 1.22 mg/g) after a month (Fig. 4D). The reduction of reducing sugars in Jerusalem artichoke tubers should be due to the formation of highly polymerized fructans, so the reduction of reducing sugar content in Jerusalem artichoke tubers could also be considered as a marker of tuber maturity [17,35,40]. Fructan could not only act as a storage carbohydrate, but also could maintain the water potential (osmotic regulation) and downregulate the freezing point of water in plant tissues [35,40,41]. Therefore, Jerusalem artichoke had the ability to convert nutrients into fructans, which indicated that it had a certain ability to resist chilling injury and drought [27,40].
Some scholars had found that the juice from Jerusalem artichoke tubers contains about 15% free sugar (wet weight), of which 70% was in the form of inulin (fructan) and the rest were fructose, sucrose and glucose [4,24]. Importantly, salinity did not affect the total free sugar or inulin content of the tubers [4]. This was the reason why the content of total sugar in tubers had no obvious difference under different salinity conditions at the early stage or the end stage of tuberization. Under low- and high-salinity conditions, the total sugar content in Jerusalem artichoke tubers were 770 ± 22.7 mg/g and 843 ± 3.78 mg/g in the early stage of tuberization, and dropped to 438 ± 75.2 mg/g and 427 ± 6.47 mg/g at the end of tuberization, while the ratio of reducing sugar to total sugar was very different (Fig. 3, Fig. 4D). Therefore, we believed that soil salinity had a significant positive effect on the synthesis rate of non-reducing sugars (fructans) in Jerusalem artichoke tubers.
5. Conclusion
The biomass of Jerusalem artichoke tuber depended on the accumulation of sugar in the tuber and photosynthesis in leaves, and stem tissue played a regulatory role in it. This study confirmed that the high salinity soil environment promoted the conversion of reducing sugars to non-reducing sugars (fructans) in Jerusalem artichoke tubers, but significantly reduced the biomass of Jerusalem artichoke. Beaides, the tuberization of Jerusalem artichoke changed the storage pool of photosynthetic products of Jerusalem artichoke from stems to tubers, so we could harvest the aerial parts of “Nanyu No. 1” before mid-to-early October, and to harvest the underground tubers after mid-November in Jiangsu Province, China. This study revealed the reasons for the decreased yield of Jerusalem artichoke under salt stress, and provided theoretical basis and guidance for the cultivation and utilization of Jerusalem artichoke in saline-alkali land.
Author contribution statement
Tianyun Shao, Xiaohua Long: Conceived and designed the experiments, Wrote the paper.
Tianyuan Shao, Yongwen Chen, Xiumei Gao: Performed the experiments.
Tianyun Shao, Zhaosheng Zhou, Zed Rengel: Analyzed and interpreted the data, Wrote the paper.
Tianyun Shao, Yongwen Chen: Contributed reagents, materials, analysis tools or data.
Funding statement
This work was financially supported by the National Key Project of Scientific and Technical Supporting Programs funded by the Ministry of Science & Technology of Jiangsu Province (BE2022304), the Programs funded by the Ministry of Science & Technology of Inner Mongolia (2020CG0057), and Forestry Science and Technology Innovation and Extension Project in Jiangsu Province (LYKJ[2019]07).
Data availability statement
The data that has been used is confidential.
Additional information
No additional information is available for this paper.
Declaration of interest's statement
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was financially supported by the National Key Project of Scientific and Technical Supporting Programs funded by the Ministry of Science & Technology of Jiangsu Province (BE2022304), the Programs funded by the Ministry of Science & Technology of Inner Mongolia (2020CG0057), and Forestry Science and Technology Innovation and Extension Project in Jiangsu Province (LYKJ[2019]07).
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.heliyon.2023.e14107.
Appendix A. Supplementary data
The following is the Supplementary data to this article:
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Data Availability Statement
The data that has been used is confidential.