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Fruit traits of different variants of Zanthoxylum planispinum var. dingtanensis in the karst plateau valley area of Guizhou Province, Southwest China

BMC Plant Biology volume 24, Article number: 1097 (2024) Cite this article

Abstract

Background

Many studies have shown that seed traits, which are among the most important plant traits, can be inherited stably, a finding which is of great value for the improvement of seed germination, seed propagation, seedling establishment, plant breeding, and ecological restoration. The differences in phenotype and nutritional traits and their interactions in Zanthoxylum planispinum var. dingtanensis were ascertained, and the nutrient input rule and the strategy of resource balancing were analyzed in order to provide a scientific basis for the screening of improved variants of the test plant.

Results

The nutrient distribution with in the tissues of Z. planispinum var. dingtanensis fruit was that the pericarp had adequate concentrations of N and P concentrations and the seed was also sufficient in P, but low in N concentration. Inorganic nutrients were particularly invested in the pericarp, while organic nutrients are more likely to be stored in the seed. In the economic spectrum of seed traits, the large leaf Zanthoxylum variant represented the low-investment economic type, the tufted leaf Zanthoxylum variant represented the high-investment luxury type, and the safflower Zanthoxylum and acutifoliate leaf Zanthoxylum variants represented transitional types.

Conclusions

Inorganic nutrients were more invested in the pericarp to produce secondary metabolites, while organic nutrients are more likely to be stored in the seed to ensure seed germination and seedling establishment in order to achieve inheritance. The variants of Z. planispinum var. dingtanensis differ in terms of resource allocation and balance, which could be further exploited through combining characters in breeding programs.

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Introduction

Research on fruit traits can identify individual variant plants with excellent traits, which can contribute to germplasm resource selection and the development of improved accessions. One of the functions of the fruit is to protect the seed and help it disperse, while the main function of the seed is to produce offspring. The seed is the reproductive organ of the fruit, but also the main site of endogenous hormone synthesis and accumulation in the seedling [1], which determines the development, reproduction, and survival of plants, and the formation of yield and quality improvement [2]. In addition, seed traits can be stably inherited, which is of great value in plant breeding and ecological restoration [3]. Therefore, the characteristics of seed traits are worth studying. Among many key traits, seed dispersal distance is indirectly determined by 100-seed weight, soluble sugar and crude fat concentrations provide heat and energy for seed germination, and the C: N and C: P ratios represent the ability of plants to assimilate C while taking up N and P, reflecting plant growth rate and nutrient-use efficiency [4]. The C: N and C: P ratios also effectively reflect the balance between competitive and defensive strategies, while the N: P range reflects the role of plant nutrient limitation of plant growth.

Researchers have studied the fruit traits of many crops to identify differences between variants and to screen for superior accessions. In terms of the evaluation and screening of useful germplasm resources, Ge et al. [5] selected excellent breeding material by measuring the sensory quality and primary metabolites of five Chinese cherry (Prunus persica) variants in Qingzhou. Wang et al. [6] compared the fruit and agronomic traits, texture parameters, nutritional quality, and antioxidant capacity of five different variants of okra (Abelmoschus esculentus) in detail and identified excellent germplasm accessions. Chen et al. [7] evaluated the main fruit traits of 21 variants of Chinese gooseberry or kiwifruit (Actinidia chinensis) and concluded that the different traits varied significantly. Wang et al. [8] analyzed phenological, flower, pit, and main fruit quality traits among 38 P. pseudocerasus accessions, and confirmed significant differences in all these traits. Feng et al. [9] selected the higher-producing areas of Chinese jujube (Ziziphus jujuba) according to the change rule of fruit quality. In terms of correlations among fruit traits, Zhang et al. [10] conducted a comprehensive evaluation of the botanical and quality characteristics of (Pitaya) fruits, indicating that the traits were closely interrelated. Most of the previous studies have focused on the comparison of phenotypic traits and nutritional qualities of fruits, and used correlation analysis and principal component analysis for detailed evaluation and screening of improved variants, but did not discuss nutrient input or resource trade-off strategies. Elucidating the variation law of fruit traits of specific plants in karst areas can enrich our understanding of the relationship between fruit and habitat.

Zanthoxylum planispinum var. dingtanensis is a pepper, forming a shrub or small tree, and is found in the dry-hot valley area of the Huajiang karst area, in Guizhou Province in Southwest China. The skin of the fruit is usually olive-green in color when the fruit is ripe [11]. Because of its well-developed root system, strong adaptability, and ease of management, it has important ecological functions, such as soil consolidation, water conservation, and control of rock desertification, and it is a pioneer species that has been used in ecological restoration studies. Previous studies on Z. planispinum var. dingtanensis mainly focused on growth decline [12], soil nutrients [13], leaf functional traits [14], and fruit quality [15, 16]. Due to the abundant niches in the karst area, variants exhibiting phenotypic differentiation have evolved in the process of long-term adaptation. In our study, the differences and interactions of phenotypes and nutritional traits of different variants of Z. planispinum var. dingtanensis were investigated to reveal the rules of nutrient input and resource trade-off strategies, which provided a scientific basis for screening for improved variants.

Ecological stoichiometry is a science that studies the balance, quantitative relationship, and biogeochemical cycles of various chemical elements in ecological processes [17] and is valuable in solving the problem of nutrient supply and demand in ecosystems. To understand the cycles of nutrient elements [18], ecological stoichiometry is of great significance in studies of the survival strategies that have evolved as a result of plant adaptation to environmental changes. Stoichiometric studies can reveal patterns of nutrient distribution, nutrient-utilization efficiency, and adaptability by plants to the local environment, providing, at the same time, new ideas and methods for studying nutrient constraints and cycling in ecosystems [19]. Many studies have focused on the plant organs [20], soil [21], and leaf-litter-soil interactions [22]. The effects of terrain [23], altitude [24], and nitrogen and phosphorus addition [25] on the ecological stoichiometric characteristics of plant ecology have also been investigated.

Although the ecological stoichiometric characteristics of leaves and roots have been studied, relatively little is known about the stoichiometric characteristics of reproductive plant organs. Each plant organ should be considered in the analysis of C, N, P, and K concentrations in seeds and their stoichiometric characteristics [26]. The nutrient distribution and environmental adaptation mechanism of Z. planispinum var. dingtanensis fruits need to be determined from the perspective of the ecological stoichiometry of plant reproductive organs. Determining the nutrient distribution in Z. planispinum var. dingtanensis fruit and the mechanism of environmental adaptation can also reveal the nutrient limitation rules underlying the growth of different variants of Z. planispinum var. dingtanensis, and provide a scientific basis for the control of fruit yield and quality in Z. planispinum var. dingtanensis.

Based on this model, four different variants of Z. planispinum var. dingtanensis, characterized as large, acutifoliate, safflower, and tufted leaf, were selected as experimental material in this study, and the fruit phenotypes, nutrient element concentrations, and biochemical characteristics were determined. Using analysis of variance, correlation analysis, partial least squares regression analysis, and Variable Importance in Projection (VIP) comparisons, the aim was to answer the following three scientific questions:1) do fruit traits and nutrient restriction rules differ among the different variants? 2) does Z. planispinum var. dingtanensis preferentially store nutrients in the seed? 3) what are the trade-off strategies associated with limited resources in the fruits? The aim of this research was to provide the scientific basis for the selection of improved variants of the test plant.

Materials and methods

Overview of the study area

The study area was located in Beipanjiang Town, Zhenfeng County, Qianxinan Prefecture, Guizhou Province, China, with a geographical location of 25°40 ‘16 “N and 105°38’ 11"E, and belonging to the subtropical humid monsoon climate. The region has an annual average temperature of 18.4℃, an annual maximum temperature of 32.4℃, and an annual minimum temperature of 6.6℃, with the winter and spring being warm and dry, and the summer and autumn being hot and humid. The temporal and spatial distribution of precipitation is uneven, with an average annual precipitation of 1100 mm, mainly over May-October months. The topography of the valley, with an altitude of 530–1473 m, belongs to the typical karst plateau canyon landform, the surface being broken and the terrain area being large. The rocky desertification of the soil is mainly dominated by limestone, which is the parent material of the limey soil, which is typically shallow, with a mottled appearance.

Z. planispinum var. dingtanensis has been cultivated in this study area for hundreds of years. It entered the commodity market, with the fruit having medicinal and spice values, in 1988, gradually resulting in large-scale planting in 1992, with the cultivated area exceeding 700 hm2 by 1996. In 2018, the per capita annual net income in the area exceeded 9,000 yuan for the first time. The current area under Z. planispinum var. dingtanensis is more than 10,000 hm2, with an output economic value of 700 million yuan. The functional component aspect of this crop has huge potential and cultivation of this crop is an ecological industry suitable for promotion, which has already effectively contributed to the alleviation of poverty and rural revitalization in the region.

Sample collection and pretreatment

In order to avoid the effect of varying environmental influence on the samples collected from the Zanthoxylum variants, in July 2023, fruit samples were collected from each of the four variants at the ripe fruit stage on a dry sunny day from plantations in Beipanjiang Town, Zhenfeng County, Qianxinan Prefecture, Guizhou Province, China. Identification of the different variants was based on the following parameters by Changsheng Wei, Senior Engineer of Zhengfeng County Forestry:

  • Large leaf Zanthoxylum variant: leaves of this variant occasionally have glandular points, the leaf area is large, and the leaf shape is rounder than usual. The flowers are green, the fruit cracks and falls readily, and the fruit is clustered. The plant has strong resistance to rust disease, with lower rust infection than the other variants, and lower rates of insect-feeding damage (Fig. 1A);

  • Acutifoliate leaf Zanthoxylum variant: leaves have more glandular points, a small leaf area, and pointed leaves. The leaves gradually elongate from elliptic to pointed, with the old leaves being pointed. Flowers are green and plant growth is strong. Fruits are long and slow to drop, with a strong fruit retention ability (Fig. 1B);

  • Safflower Zanthoxylum variant: leaves lack glandular points, are thick and wide, with a large area. The leaf is long and pointed, and the back of the leaf has thorns. The flowers are red and the fruits are clustered, dispersed along the stalk, and large, and the plant is high-yielding. This variant has strong disease resistance but is less frequent than the other variants in the study area (Fig. 1C);

  • Tufted leaf Zanthoxylum variant: the leaf surface is smooth without glandular points, and the leaves are clustered. The back of the leaf is spiny and approximately flat. The flowers are green and the plant exhibits moderate resistance to rust. Fruits fall readily and should not be picked late in the season (Fig. 1D).

A number of ripe fruits were collected from representative plants of each of the four variants from regions in the east, west, south, and north of the four direction. Three replicate samples were collected from each variant and kept in separate nylon mesh bags. After each replicate sample was mixed to achieve homogeneity, a subsample of about 500 g was taken. The collected fruit samples were dried in the sun for 1–2 days, and the seeds and pericarp were separated after drying for the determination of nutritional properties.

Fig. 1
figure 1

Different variants of Zanthoxylum planispinum var. dingtanensis

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Determination of fruit traits

Determination of phenotypic traits

Ten fully ripe whole fruits were selected from each replicate, and the phenotypic traits, such as fruit diameter, fruit length, and fruit width, were measured using vernier calipers (accurate to 0.01 mm) and an electronic balance (accurate to 0.01 g). Then, 100 fruits were randomly selected and 100-seed weight was determined.

Determination of nutrient element properties

The nutritional concentrations of the seed and pericarp of each variety were determined, using the following methods. Organic carbon (OC) was determined by the potassium dichromate oxidation plus heat capacity method, total nitrogen (TN) was determined by using a SEAL AA3 continuous flow analyzer (Norderstedt, Germany), total phosphorus (TP) was determined by molybdenum-antimony spectrophotometry, and total potassium (TK) by flame photometry.

Determination of organic nutrients

The soluble sugar and soluble protein concentrations in the seed and pericarp of each variant were determined by the anthrone colorimetric method, the total sugar concentration was determined by visible spectrophotometry, and the fat concentration was determined by reference to the Determination of Fat in Food [27].

Calculation of variable importance in projection (VIP)

VIP is a statistical tool, mainly used for variable screening, especially when the sample is small and there is a strong correlation between variables. The VIP value of each nutrient trait variable in the first principal component was calculated by partial.

least squares regression to quantify the input of each nutrient element in the seed and pericarp.

Table 1 Ecological connotation of fruit traits
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Data processing

Microsoft Excel 2016 and SPSS 26.0 (IBM, Armonk, NY, USA) software were used for data processing, and Origin 9.8 software (Origin Lab Corp., Northampton, MA, USA) was used for mapping. One-way ANOVA, with Duncan’s Multiple Range multiple comparison method, was used to test for significant differences in fruit characteristics and the nutritional concentrations in the fruits and seeds among the four different variants of Z. planispinum var. dingtanensis. Pearson’s correlation analysis was used to explore the relationship between ecological stoichiometric characteristics of the fruit. The VIP comparison method was used to analyze the nutrient input level of fruit, to identify the priority storage location of nutrients in the fruit of Z. planispinum var. dingtanensis. The construction of the seed economic spectrum is based on the theory of Leaf Economic Spectrum (LES), using the concept of ‘economy’, combined with the use of trait indicators (Table 1), with seed traits being quantitatively represented at either end of the spectrum [28], revealing the weighting strategies of plants on resources.

Results

Fruit trait characteristics of the four different variants of Z. planispinum var. dingtanensis

Phenotypic trait characteristics of the four different variants

There were no significant differences in the mean weight of whole fruits, seed length, and 100-seed weight among the four variants (P > 0.05; Table 2). On the other hand, there were significant differences in whole fruit diameter, fruit length, pericarp length, and 100-seed weight among the large leaf Zanthoxylum, the acutifoliate leaf Zanthoxylum, and the safflower Zanthoxylum (P ≤ 0.05), with the traits in the large leaf Zanthoxylum and acutifoliate leaf Zanthoxylum being significantly higher than in the safflower Zanthoxylum. The diameter of the seed of the safflower Zanthoxylum was the highest, while the pericarp width of this variant was the lowest.

Table 2 Phenotypic trait characteristics of the different variants of Z. planispinum var. dingtanensis
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Nutritional traits of fruits of the different variants

C, N, P, and K concentrations in fruits of the different variants

The concentrations of C and K in the pericarp of the four variants were lowest in the safflower Zanthoxylum, but the change rule of N was lowest in this variant (Fig. 2). There was no significant difference in P concentration between the pericarp of the safflower Zanthoxylum, the large leaf Zanthoxylum, and the tufted leaf Zanthoxylum, while the P concentration in the safflower Zanthoxylum and tufted leaf Zanthoxylum pericarp were significantly higher than in the acutifoliate leaf Zanthoxylum. There was no significant difference in C and K concentrations in the seed among the variants. N concentrations in the seed of the large leaf Zanthoxylum and acutifoliate leaf Zanthoxylum were significantly higher than in the safflower Zanthoxylum and tufted leaf Zanthoxylum, whereas the seed P concentration in the safflower Zanthoxylum was significantly lower (P < 0.05) than in the other three variants.

Fig. 2
figure 2

Concentrations of carbon, nitrogen, phosphorus, and potassium in seed and pericarp tissues of different variants of Zanthoxylum planispinum var. dingtanensis. Note different lowercase letters signify a significant difference (P < 0.05). The seed and pericarp were compared respectively. A: Large leaf Zanthoxylum; B: Acutifoliate leaf Zanthoxylum; C: Safflower Zanthoxylum; D: Tufted leaf Zanthoxylum

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Organic chemical characteristics of the different variants

There were no significant differences in the concentrations of crude fat, total sugar, soluble protein, and soluble sugar in the pericarp among the different variants, but there were some differences in the seed (Fig. 3). The concentrations of total sugar, soluble sugar, and soluble protein in the pericarp among the four variants were highest in the safflower Zanthoxylum, while this variant had the lowest crude fat concentration. There was no significant difference in soluble sugar concentration in the pericarp among the four variants, with the value of the safflower Zanthoxylum being higher than those of the acutifoliate leaf Zanthoxylum and tufted leaf Zanthoxylum. The crude fat and total sugar concentrations in the seed of the four variants were lowest in the safflower Zanthoxylum, which also had the highest concentrations of soluble protein and soluble sugar. There was no significant difference in the fat concentration of the seed among the large leaf Zanthoxylum, acutifoliate leaf Zanthoxylum, and tufted leaf Zanthoxylum, but the concentration in the tufted leaf Zanthoxylum was significantly higher (P < 0.05) than in the safflower Zanthoxylum.

Fig. 3
figure 3

Concentrations of crude fat, total sugar, soluble protein, and soluble sugar in seed and pericarp tissues of different variants of Zanthoxylum planispinum var. dingtanensis. Note different lowercase letters indicate significant differences (P < 0.05). The seed and pericarp were compared respectively. A: Large leaf Zanthoxylum; B: Acutifoliate leaf Zanthoxylum; C: Safflower Zanthoxylum; D: Tufted Zanthoxylum

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Ecological stoichiometric fruit characteristics of the different variants

Ecological stoichiometric characteristics of C, N, P, and K concentrations in pericarp

With the exception of C: K and P: K ratios, there were some differences in other ecological stoichiometric parameters in the pericarp among the four variants. Analysis of the N: P ratio revealed that there was no significant difference between the acutifoliate leaf Zanthoxylum, large leaf Zanthoxylum, and safflower Zanthoxylum, with the ratio in the pericarp of the tufted leaf Zanthoxylum being significantly lower (P < 0.05) than in either the large leaf Zanthoxylum or the safflower Zanthoxylum (Table 3). Analysis of the C: N ratio indicated that the ratio in the pericarp of the safflower Zanthoxylum was significantly lower than in the other three variants, whereas the N: K ratio in the safflower Zanthoxylum was significantly higher than in the other variants. The C: P ratio in the pericarp of the large leaf and acutifoliate leaf Zanthoxylum was significantly different from those of the safflower Zanthoxylum and tufted leaf Zanthoxylum, while that of the large leaf Zanthoxylum was significantly higher than those of the safflower Zanthoxylum and tufted leaf Zanthoxylum (Table 3).

Table 3 Ecological stoichiometry characteristics of pericarp of different variants of Zanthoxylum planispinum var. dingtanensis
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Ecological stoichiometric characteristics of the C, N, P, and K concentrations of the seed

There were no significant differences among the four variants with respect to either the C: P or C: K ratios in the seed, but there were complex differences in other ecological stoichiometric characteristics. There was no significant difference in the seed C: N ratio among the large leaf Zanthoxylum, acutifoliate leaf Zanthoxylum, and safflower Zanthoxylum, but the ratio in the tufted leaf Zanthoxylum was significantly higher (P < 0.05) than that in the other three variants. There were significant differences in the seed N: P ratio between the tufted leaf Zanthoxylum and the other three variants. The seed N: K ratio in the safflower Zanthoxylum and tufted leaf Zanthoxylum were significantly lower than in the large leaf Zanthoxylum and the acutifoliate leaf Zanthoxylum. There were also significant differences in the P: K ratios in the seed among the large leaf Zanthoxylum, safflower Zanthoxylum, and tufted leaf Zanthoxylum (Table 4).

Table 4 Ecological stoichiometric characteristics of seed of different variants of Zanthoxylum planispinum var. dingtanensis
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Correlation analysis of ecological stoichiometric characteristics between the pericarp and the seed

The ecological stoichiometric characteristics of the four different variants were negatively correlated. There was a significant negative correlation between the C: N of the seed and the C: P or N: P ratio of the pericarp, but not with the P: K ratio of the pericarp. There was a significant trade-off between the seed C: P ratio and both the pericarp C: N and C: P ratios, while the correlations between the seed C: K ratio and the pericarp C: N, C: P, N: K, and P: K ratios were only weak. Pericarp P: K ratio was significantly negatively correlated with the N: P, N: K, and P: K ratios of the seed. The seed P: K ratio was positively correlated with both the pericarp C: N and C: P ratios (Fig. 4).

Fig. 4
figure 4

Correlation coefficients of ecological stoichiometric characteristics between pericarp and seed

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Nutrient inputs of the different variants

Except for the safflower Zanthoxylum, the VIP for the seed for all variants was greater than 1, and they were all greater than the VIP for the pericarp, indicating that Z. planispinum var. dingtanensis was inclined to preferentially invest nutrients into the seed rather than the pericarp during the fruit development process (Table 5).

Table 5 Significance of nutrient investment into the pericarp and seed of different variants of Zanthoxylum planispinum var. dingtanensis
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Economic spectrum of seed traits

At one end of the economic spectrum, there is a class of species with low 100-seed weight, large fruit diameter, high soluble sugar and crude fat concentration in the fruit, and low C: N and C: P ratios, that is, a low-investment economy species. At the other end of the spectrum are the high-investment luxury species, which are characterized by heavier 100-seed weight, small fruit diameter, low soluble sugar and crude fat concentrations, and high C: N and C: P ratios (Fig. 5). As shown in Fig. 5; Table 6, different variants can be assessed according to their position on the economic spectrum, with the large leaf Zanthoxylum being a low-investment economy variety, and the tufted leaf Zanthoxylum being a high-input luxury variety. The acutifoliate leaf Zanthoxylum and safflower Zanthoxylum belong to transitional variants, that is, the acutifoliate leaf Zanthoxylum is being transformed from a high-investment luxury variant to a low-investment economic variant and the safflower Zanthoxylum is being transformed from a low-investment economic variety to a high-investment luxury variety.

Fig. 5
figure 5

Conceptual illustration of the economic spectrum of seed traits

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Table 6 Comparison of the relative size and characteristics of the seed of different variants of Zanthoxylum planispinum var. dingtanensis
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Discussion

Differences in fruit traits of the different variants

There were no significant differences in phenotypic traits among the four variants, indicating that thire phenotypic traits were relatively stable, partly because the plants were cultivated in the same garden in Beipanjiang Town, and exposed to the same agronomic measures, such as water and fertilizer management, shaping and pruning, and disease and pest control, thus excluding the influence of environmental factors. The large leaf variant has a higher fruit yield potential and lower diffusion capacity of the seed, because the larger leaf area of the large leaf variant can store more nutrients for later fruit development. The chemical element concentrations of the pericarp were higher than those of the seed (Fig. 2) because the pericarp is the outermost layer of the fruit and preferentially absorbs inorganic nutrients to synthesize metabolites to improve the plant organ’s ability to tolerate stresses and is also related to the different allocation strategies of plants for elements [29], which further affects the uptake capacity of the plants for elements, resulting in differences in the distribution of nutrients among the different plant organs and tissues. The concentrations of organic nutrients in the safflower variant were generally higher than those in the other three variants. The reasons for this difference may be as follows. Practical experience shows that the safflower Zanthoxylum has a lower ability to tolerate low temperatures and freezing damage, so more organic substances will be invested in this variety to improve its osmoregulatory ability [30]. Another effect of the higher organic molecule concentration would be to increase the seed germination rate to ensure the inheritance of the biological information of the variant. The specific reasons remain to be confirmed to further clarify the genetic diversity among the four different variants.

Ecological stoichiometric characteristics of different variants

The N: P ratio of plants can be used to determine the growth-limitation pattern of plants by N and P nutrients [31,32,33], reflecting plant adaptation and defense and tolerance strategies against adverse habitats. The N: P threshold hypothesis holds that there is a specific N: P threshold that determines the nutrient-limiting plant growth [34]. Koerselman and Meulemanrer (1996) reported that, at N: P < 14, growth is mainly limited by N, whereas, at N: P > 16, it is limited by P; when the ratio is between 14 and 16, growth is limited by both N and P. The N: P ratios of the pericarp and seed of the different variants were 4.82–6.47 and 5.98–6.88, respectively, indicating that the growth of the variants tends to be N-limited. The reasons for this are that Z. planispinum var. dingtanensis needs to invest a lot of N to maintain its vegetative growth, and continuously synthesize its secondary metabolites. However, soil clods are discontinuous and the landscape where the plants grow is barren, mountainous terrain, where underground cracks develop, resulting in greater loss of soil and water and associated soluble soil N nutrients. In addition, N elements form stable compounds that are difficult to mobilize in cells, resulting in insufficient recycling of the N required for plant growth [35]. N is an essential nutrient element for plant growth, coordinating the relationship between primary and secondary metabolism, and too much or too little of it is detrimental to plant growth [36]. Therefore, it is still necessary to further investigate the demand N rule of this species to achieve optimum fertilization.

From the analysis of nutrient concentrations, the mean value of pericarp N in the study area was 21.26 g/kg, which is significantly higher than the average value in plants in China (18.6 g/kg) and the global average value for land plants (20.6 g/kg) [37, 38], whereas the mean N concentration in Zanthoxylum seed (12.19 g/kg) was lower than the global and national values [37, 38]. The mean P values in Zanthoxylum pericarp and seed were 3.67 g/kg and 12.19 g/kg, respectively, which were higher than those in plants in China (1.21 g/kg) and globally (1.99 g/kg) [37, 38]. These results showed a nutrient pattern in which Z. planispinum var. dingtanensis contained adequate N and P in the pericarp and insufficient N but adequate P in the seed. The reason for this is that, during the growth and development of plants, different organs have varying demands for individual elements, and organ functions are different, resulting in different transfer capabilities of elements within plants [39]. It is also possible that, because the pericarp is often used as a spice substance, more N is needed to synthesize the pepper-related secondary metabolites during plant growth, thereby improving its flavor. The seed needs enough P to ensure the synthesis of genetic material in the form of the backbone of nucleic acids, reflecting the nutrient distribution strategy within the plant, so as to achieve functional optimization. The relative lack of seed N affected the subsequent growth and development of the seed and the accumulation of nutrients, which may be responsible for the low seed germination rate to a certain extent. Therefore, how to regulate the balanced uptake and distribution of nutrients has become a scientific problem worthy of attention.

Nutrient input of the different variants

During plant growth, due to the different functions of the various organs, the concentrations of the required nutrients also vary, resulting in the organ-specific uptake of nutrients. In general, Z. planispinum var. dingtanensis appears to be more inclined to preferentially invest nutrients into the seed (Table 5), because the Zanthoxylum seed is the reproductive organ; in order to improve the seed fertility and germination rate, the plant will preferentially invest nutrients into the seed to ensure inheritance [40], a phenomenon which is consistent with the mechanism of plant self-adaptation and self-regulation. However, the concentrations of soluble sugar and soluble protein in the seed were lower than in the pericarp (Fig. 3), probably because the peel, as the flavoring substance of this plant, is also the “gateway” to tolerate external stresses. The higher the soluble sugar, the better the plant is able to adapt to adversity and achieve a high-quality product. The distribution of the nutrients to individual organs and tissues is specific, leading to the different patterns of nutrient concentration exhibited by the pericarp and the seed. In the future, it will be necessary to analyze the rules underlying the absorption, synthesis, and transport of inorganic and organic substances in depth to improve the functions of nutrient supply and photosynthesis.

Survival strategies of the different variants

The point on the economic spectrum denoted by seed traits reflects the resource allocation strategies adopted by plants to adapt to the environment and can quantify the relationship between seed trait combinations to a certain extent, with different species/variants occupying different positions on the economic spectrum. According to the Leaf Economic Spectrum theory proposed by Wright et al. [41], seed traits, such as 100-seed weight, fruit diameter, seed soluble sugar and crude fat concentrations, and C: N and C: P ratios, are important indicators of seed resource trade-off strategies. Among the four variants, the large leaf Zanthoxylum is an economic variant with large leaf area and high photosynthetic rate, and is more inclined to choose low-input survival strategies to adapt to the prevailing arid and barren environment. The transition from the high-input economic type to the low-input type of the acutifoliate leaf Zanthoxylum is related to its low C: N ratio. Generally, species with high N concentrations have lower resistance to biotic stresses and weakened defense abilities [42] and will allocate more resources at the seedling stage to accelerate growth [43]. In the process of growth, the leaves of young acutifoliate leaf plants gradually become elongated from the initial oval shape, with the old leaves becoming pointed. The reduced leaf area and weak photosynthetic capacity of the acutifoliate leaf Zanthoxylum are conducive to reducing transpiration and nutrient storage [44] so that the old leaves can maintain their advantages under stress. The transition of the safflower Zanthoxylum variant from the economic type variant to the high-input variant is related to its weak ability to tolerate low temperature and freezing damage. During growth and development, the safflower variant is more inclined to store more substances to maintain its own advantages [45], and it will invest more nutrients to tolerate unfavorable habitats in the later period. The tufted leaf Zanthoxylum is a high-input variant, which is more inclined to select the strategy of nutrient storage in order to adapt to environmental changes.

Conclusions

1) Z. planispinum var. dingtanensis showed a nutrient pattern of adequate N and P concentrations in the pericarp and insufficient N but adequate P in the seed, and growth was mainly limited by N in general.

2) Z. planispinum var. dingtanensis is more inclined to prioritize the organic nutrients in the seed to ensure inheritance.

3) According to the economic spectrum analysis of seed traits, the large leaf Zanthoxylum was the low-investment economic-type variant, the acutifoliate leaf Zanthoxylum was the high-investment luxury-type variant, and the safflower Zanthoxylum and the tufted leaf Zanthoxylum were transitional variants.

Data availability

All data generated or analysed during this study are included in this published article.

Abbreviations

VIP:

Variable Importance in Projection

LES:

Leaf Economic Spectrum

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Acknowledgements

We thank International Science Editing (http://www.internationalscienceediting.com) for editing this manuscript.

Funding

Funding was provided by Guizhou Province Science and Technology Support Plan Project (Qian-ke-he Zhicheng) [2023] Yiban 062 and the Innovation and Entrepreneurship Training Program of Guizhou Normal University in 2023 (grant 202310663007).

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Authors and Affiliations

  1. School of Geography and Environmental Sciences, Guizhou Normal University, Guiyang, Guizhou, 550025, China

    Youyan Guo, Guangguang Yang & Shunsong Yang

  2. School of Karst Science, State Engineering Technology Institute for Karst Decertification Control, Guizhou Normal University, Guiyang, Guizhou, 550001, China

    Yurong Fu, Yanghua Yu, Mingfeng Du & Yaqi Zhou

Authors
  1. Youyan Guo
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  2. Guangguang Yang
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  3. Yurong Fu
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  4. Shunsong Yang
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  5. Yanghua Yu
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Contributions

Youyan Guo collected data, analysised mathematical, chart visualization and wrote the manuscript; Guangguang Yang assist in data collection and revised the manuscript, reviewed literature; Yurong Fu assisted in data collection and preprocessing; Shunsong Yang assisted in chart modification and optimization; Yanghua Yu conceived and designed the project, writing guidance; Mingfeng Du participate in the paper polishing work and assist in data processing; Yaqi Zhou participate in the paper polishing work and chart optimization.

Corresponding author

Correspondence to Yanghua Yu.

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Ethics approval and consent to participate

This study was conducted in accordance with the relevant guidelines and legislation of the People’s Republic of China and international authorities. Permission for collection of the four variants of Z. planispinum var. dingtanensis in the experiments was obtained from Zhenfeng County, Qianxinan Prefecture, Guizhou Province, China. The Z. planispinum var. dingtanensis used in this study was identified by Changsheng Wei, Senior Engineer of Zhengfeng County Forestry, and voucher specimens are preserved in the Zhenfeng County Ding Tan Jiao Ye Co., Ltd (voucher ID: 991005, 992003, 221007, and 222005).

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Guo, Y., Yang, G., Fu, Y. et al. Fruit traits of different variants of Zanthoxylum planispinum var. dingtanensis in the karst plateau valley area of Guizhou Province, Southwest China. BMC Plant Biol 24, 1097 (2024). https://doi.org/10.1186/s12870-024-05828-5

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Keywords

BMC Plant Biology

ISSN: 1471-2229

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