How and why tobacco cultivation depletes agricultural land| Tabaccologia

Abstract

The reason why tobacco crops deplete the soil depends on the complex balance between the plant and the soil that surrounds the roots, i.e., the rhizosphere. The rhizosphere can be defined as an actual “complex system”, and it is the part of the soil where the interactions between the roots of the plant, the microorganisms and the substances present in the soil take place. The chemical-physical characteristics of the rhizosphere are substantially different from those of the bulk soil, especially for some specific parameters such as pH, humidity, electrical conductivity, and oxidation-reduction potential. The microbial population, on the other hand, is essential for improving root growth, soil structure and quality and is likely to be conditioned by the plant’s own substances, as is the case with tobacco. In fact, the development and production of tobacco is directly proportional to the presence of macronutrients (N, P, K, S), which are solubilized and absorbed thanks to the bacterial diversity represented by the Proteobacteria and Actinobacteria present in the tobacco rhizosphere, compared to the circumscribed soil and agricultural crops. Therefore, the depletion of tobacco- growing soils poses a major problem for agricultural crops, especially in developing countries. Keywords: tobacco cultivation, rhizosphere, microbiome, soil macronutrients.

Introduction

Tobacco (Nicotiana tabacum L.) is a widespread cash crop in Asia, America, and Africa, with less land invested in Europe [1]. Tobacco cultivation is considered to be a crop that depletes soil fertility and, for this reason, it is used in rotation with other crops, such as maize and other grasses [2].

Various studies [3, 4] have tackled this phenomenon, which affects the quality and quantity of agricultural products, which for the poorest and developing countries mean poverty to the point of reaching levels of undernutrition that are even at the limit of survival. An agronomic problem that, with a global vision, also becomes ethical. Crop rotation, in fact, influences soil fertility and rhizosphere microbes [3, 5, 6].

The Rhizosphere

The rhizosphere is the fraction of soil that surrounds the roots of plants. This definition was introduced by the German agronomist Lorenz Hiltner in 1904. Today we know that a wide variety of microorganisms (microbiota), fungi, bacteria live in the rhizosphere, which can be beneficial or harmful to plant growth. Despite positive advances in science, the appearance and role of 90% of microbial species present in soil remains poorly understood.

In general, this narrow area of soil around plant roots is characterized by greater microbial activity and nutrients in the soil than the surrounding soil. The rhizosphere is undoubtedly actively influenced by the plant that continuously release a complex mixture of organic and inorganic substances capable of locally altering the soil (water content and pH, oxygen) and better capturing nutrients.

The microbiota of the tobacco rhizosphere

The rhizosphere of plants plays an important role in influencing soil fertility through a particular and modified microbial composition [7]. As shown by various studies, the cultivation of tobacco in the same soil in monoculture reduces its fertility, leading to exhaustion both from a chemical and microbiological point of view. For example, bacteria in the tobacco rhizosphere, belonging to the phyla Proteobacteria, have been shown to solubilise phosphorus (P), potassium (K) and sulphur (S), facilitating their availability for crops, but also depleting the soil for the following crops [7]. It also happens that nitrogen (N) is released in excess as the soil is depleted of nitrogen-fixing bacteria [7]. In fact, tobacco absorbs extra nutrients from the soil, which is thus depleted [4].

The tobacco rhizosphere is a complex community and usually associated with different bacteria, involved in stimulating plant growth through nutrient acquisition, resulting in heavy soil depletion for P, K, S [4, 8, 9]. P is the second essential nutrient after N that is slowly released from parent rocks and is depleted over time through plant uptake, pH-dependent immobilization, and removal with soil erosion [10, 11]. A third essential nutrient in crops is K, a limiting factor in plant production since its solubility depends on soil conditions [12, 13]. Complex fertilizers based on N-P-K are among the most widely used fertilizers in agriculture.

In fact, it is a mixture that contains the three main elements necessary for plants to grow.

The tobacco plant also requires other soil nutrients such as calcium (Ca) and magnesium (Mg) [7]. On the other hand, some studies report that tobacco harvest is associated with the increase of other nutrients such as iron (Fe) and zinc (Zn) in the rhizosphere [9, 14, 15].

Regarding the biotic component of soil, the role of bacterial and fungal diversity in the rhizosphere in the ecosystem is associated with improved fertility, however, this role is still partly being studied [16]. Bacterium phyla, which include Proteobacteria, Firmicutes, Actinomycetes, Cyanobacteria, and Bacteroidetes, are known to be beneficial for promoting plant growth [17-19]. Soil bacteria play a significant role in the rhizosphere through the solubilisation and mineralisation of nutrients/organic materials [13, 20]. Through this process, soil bacteria contribute largely to the retention, recycling, and availability of nutrients for plant growth [20].

Causes of soil depletion by tobacco

There are various and diverse possible explanations that lead to the impoverishment of tobacco-growing land.

A) Roots

The root system influences the physical fitness, health, and productivity of plants through its phenotypic traits (phens) such as root length, biomass, density, volume, and surface area. Root phens or architecture significantly alter the biophysical and edaphic properties of soil such as aggregation, structure, pH, moisture, temperature, and nutrient stoichiometry (C:N, C:P, and N:P ratios). These traits differentially affect the release of 20% to 80% of total photosynthesis as root exudates. The internal and external structures of various root types demonstrate tremendous phenotypic plasticity in their cell structure, anatomy, cell types, shapes, metabolism, and biochemical profiles. These heterogeneities in the rhizosphere and endosphere create microenvironments and ecological niches for different microbial species to foster rhizospheric interactions for the benefit of both microbe-plant parts (mutualistic symbiosis relationships).

Results from the root systems of some agricultural and forest plants suggest that root phenos selectively filter and recruit different microbial communities [21]. Some plants, however, including tobacco, emit toxic substances from the root systems, which are found to inhibit the germination of other plants, to occupy their ecological niches (natural herbicides) (reference).

This aspect limits the growth of plants in association with tobacco but also later, in crop rotation. Knowledge of these attitudes is essential in establishing proper crop rotation, both for environmental and economic reasons.

B) pH

In plots with fertile soil, after tobacco cultivation, the average pH value decreases by 5.34% (from 7.86 to 7.44); organic matter from 1.95% to 1.78%; K level from 0.46 meq/100 g to 0.32 meq/100 g; P from 13.98 ppm to 9.10 ppm; S content from 16.22 ppm to 10.89 ppm and Zn concentration from 0.70 ppm to 0.53 ppm, after two consecutive years of cultivation. It should be noted that, in plots not cultivated with tobacco, but with other crops, the average pH value decreases by 2.29% (from 7.83 to 7.65), organic matter from 1.86% to 1.79%, K from 0.42 meq/100 g to 0.36 meq/100 g, P from 14.44 ppm to 11.23 ppm, S from 14.44 ppm to 11.23 ppm, S from 14.01 ppm to 12.42 ppm and Zn from 0.74 ppm to 0.61 ppm after two consecutive years [4].

Table 1 and Figure 1 show the relative percentage values of these changes.

C) Microbiome

Soil bacteria play a significant role in the rhizosphere through the solubilization and mineralization of nutrients/organic materials [13, 20]. Through this process, soil bacteria largely contribute to the retention, recycling, and availability of nutrients for plant growth. Various studies have shown that bacterial diversity in tobacco rhizosphere soils belongs to the phylum Proteobacteria, which is significantly associated (p < 0.05) with the solubilization of P, K and S, resulting in a significant decrease in these nutrients in the media for the next crop. Thus, the diversity of bacteria in the tobacco rhizosphere affects the solubility of macronutrients and reduces some bacteria involved in N fixation, increases the total N in the soil [7], resulting in a risk of leaching and pollution of groundwater [22-24].

Why the microbiome of the tobacco rhizosphere is so different from that of plants of agricultural interest and so depleted of macronutrients is still unclear. It is likely that one or more secondary metabolites of tobacco, such as alkaloids emitted by roots, affect the pH and diversity of the microbiome [25].

In fact, it has been shown that Nicotiana tabacum has allelopathic effects in the germination of Triticum aestivum and Vigna radiata [26], emitting substances into the soil that could also inhibit the germination of common wheat and beans in the following year.

Conclusions

In conclusion, it can be said that the development and production of tobacco is directly proportional to the presence of macronutrients (N, P, K, S), which are solubilized and absorbed thanks to the bacterial diversity represented by Proteobacteria and Actinobacteria present in the tobacco rhizosphere, compared to bulk soil and agricultural crops. Therefore, the impoverishment of tobacco-growing soils poses a major problem for agricultural crops, especially in developing countries, which suffer from poor and under-fertilized agriculture but with a growing presence of tobacco-growing fields.

Figures and tables

Figure 1.The contribution of tobacco to the reduction of K, P, S, and Zn elements compared to other crops after 2 years of repetition.

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