Xue FU, Yongwei FU, Min TU, Xia ZENG, Hongji ZHANG

1. College of Plant Protection, Yunnan Agricultural University, Kunming 650201, China; 2. Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, China; 3. College of Ecology and Environment, Hainan University, Haikou 570228, China

Abstract Soil is the most biologically abundant ecosystem on the earth. Soil biodiversity has significant impact on maintaining soil ecological balance and agricultural production, especially on healthy growth and disease control of plants. Therefore, it is of great significance to study soil biodiversity. This paper reviewed the role of soil biodiversity in plant growth. First of all, the history of soil biodiversity was introduced. Secondly, the composition of soil biodiversity was introduced, and the role of soil biodiversity in regulating the quantity and species of soil organisms, maintaining the balance and stability of soil system, participating in nutrient circulation and energy flow, and promoting plant health were discussed based on the interactions among microbial diversity, fauna diversity and plant diversity. Finally, combined with the background of advocating the protection of soil biodiversity in the great time, the potential factors threatening soil biodiversity were analyzed.

Key words Soil biodiversity, Plant health, Soil-borne disease, Prevention and control, Soil ecological environment

1 Introduction

Soil is a layer of loose material on the surface of the earth’s lithosphere, and it provides habitats and basic living substrates for terrestrial organisms. There are very rich organisms in the soil, including microbes, animals and plants, which constitute soil biodiversity. Microbes account for the largest proportion of soil organisms, including bacteria, fungi, archaea, viruses,etc.There are a great variety of bacteria. At present, about 3 000 soil bacteria have been found in the world, only about 10% of which can be used for culture. Fungi are also abundant, with an estimated species of 1.5 million, but about 70 000 species are identified. Archaea is a kind of ancient bacteria with strong vitality. Viruses are mainly bacteriophages that can infect bacteria. Currently, there are more than 6 000 strains of bacterial viruses that can be isolated and obtained, and 9 types of morphology have been observed. There are many kinds of soil faunas, which can be divided into 3 orders of magnitude: microfauna, mesofauna and macrofauna. About 20 000 species of nematodes have been reported, most of which live in the soil. About 3 000 species of earthworms have been reported in the world, and that reported in China account for about 10%. Soil organisms are diverse and complex. Due to the limitations of current technology, the identification and protection work is not perfect, and about 90% of soil organisms have not been recognized. Some of these species are gradually declining and even extinct due to human agricultural and industrial activities, climate change and other factors. Therefore, it is important and urgent to protect soil biodiversity. Soil organism is an important part of soil ecosystem and plays a vital role in regulating the balance and stability of the ecosystem. Studies have shown that soil organisms participate in the process of organic matter decomposition, humus decomposition and nutrient transformation, and play an irreplaceable role in soil remediation, prevention and control of soil-borne diseases, improvement of soil physical and chemical properties, and promotion of plant growth. In addition, soil biodiversity is closely related to human society and plays an important role in the fields of agricultural production, environmental protection, global climate, and public health. In recent years, soil biodiversity has become a hot topic and attracted much attention. The main purpose of World Environment Day 2021 is to further promote the biodiversity conservation of the whole society, which also demonstrates the importance of protecting soil biodiversity[1]. In April 2021, the Food and Agriculture Organization of the United Nations (FAO) held a Global Symposium on Soil Biodiversity online with the theme of "maintaining soil vitality and protecting soil biodiversity"[2]. In October of the same year, the 15thConference of the Parties to theConventiononBiologicalDiversitypointed out that global biodiversity conservation should be strengthened[3]. In conclusion, the conservation of biodiversity and soil biodiversity has become a worldwide concern, which means that soil biodiversity is an important research content of soil biology, an important research direction closely related to agricultural and forestry production, and an important research progress in the field of biodiversity science.

2 History of soil biodiversity development

In the 1980s, the extinction of some species caused by human activities had aroused extensive attention from academia and society to the terrestrial beings. The scientific term "biodiversity" was first proposed by Wilson. After the academic conference in 1986, biodiversity began to become a hot topic of research and discussion in the scientific community and society[4-5]. In 1992, the Ecological Society of America listed biodiversity as one of the three global issues in the 21stcentury[6]. In addition, the promulgation of theConventiononBiologicalDiversityin 1992 further promoted biodiversity to become a hot research field in ecology[7]. At the same time, soil biodiversity also began to attract the attention of scholars. The International Symposium on Soil Biodiversity was held in 1993, which officially kicked off the research on soil biodiversity. The theme of the conference was to discuss the significance of soil biodiversity and its regulatory role in the ecosystem. The papers submitted at the conference were edited into the bookTheSignificanceandRegulationofSoilBiodiversity, which became the first comprehensive information in the study of soil biodiversity[8]. With the convening of the symposium on soil biology, soil biodiversity became a hot field of ecological research. More and more scholars realized that soil biodiversity had important research significance, and soil biodiversity had been widely cited in the literature since then. Shi Leilei and Fu Shenglei[9]published a review titledReviewofSoilBiodiversityResearch:History,CurrentStatusandFutureChallenges, which divided the history of soil biodiversity into three stages: (i) Question and academic discussion stage, to discover the limitations and importance of soil biodiversity research through early literatures and seminars; (ii) Stage of scientific research and accumulation of new knowledge, to explore the interaction mechanism of soil biodiversity and its role in the ecosystem; (iii) Discussion stage, to explore the improvement of soil biodiversity monitoring and conservation in the future.

3 Composition of soil biodiversity

Soil biodiversity refers to soil microbial diversity, soil fauna diversity and soil plant diversity. Soil microbes include bacteria, fungi, actinomycetes, archaea, viruses,etc.Soil fauna can be divided into 3 orders of magnitude: microfauna, mesofauna and macrofauna. Soil roots are diverse, including lichen, algae, and plant root system (tap root system and fibrous root system). The present known soil biological groups are shown in Fig.1.

3.1 Soil microbial diversity

3.1.1Soil microbial diversity and plant growth and development. Soil, microbes and plants together constitute a dynamic and balanced ecosystem. Soil microbes reflect soil health status, and play an important role in plant growth and development. They participate in the regulation of plant physiological and biochemical processes through a variety of ways, and are also the driving forces of plant disease resistance. Nitrogen is an essential element for plant growth and development, and soil microbes play an important role in this process, nitrogen fixation, by absorbing nitrogen from the atmosphere and converting it into ammonia ions for plant absorption and utilization. Previous results show that the sources of nitrogen fertilizer are mainly industrial nitrogen fixation and biological nitrogen fixation, and the content of biological nitrogen fixation accounts for 75%. According to the degree of affinity between nitrogen-fixing organisms and plants, nitrogen fixation is divided into 3 forms: symbiotic nitrogen fixation, combined nitrogen fixation, and autogenous nitrogen fixation[10]. Symbiotic nitrogen fixation is the main form of biological nitrogen fixation, for example, symbiosis of legumes and rhizobia[11], Frankia and non-legumes[12], and cyanobacteria and blue-green algae[13]play a symbiotic role in nitrogen fixation. Soil organic matter (SOM) can provide certain nutrient elements for plant growth and participate in physiological and biochemical activities related to cell metabolism, and is also an important indicator reflecting soil quality[14-15]. 85%-90% of soil organic matter is humus, dominated by humic acid and fulvic acid[16]. It exists as free humic acid and humate in root soil, promoting plant growth and development. Humus formation and decomposition is also an important link to promote material circulation and energy flow. Minerals are involved in plant growth and development, and studies have shown that soil microbes are conducive to the release of nutrient elements from soil insoluble minerals. Sulfurizing bacteria can convert hydrogen sulfide and sulfur-containing amino acids in the soil into sulfate for plant absorption and utilization, and the sulfuric acid generated in the conversion process can increase the absorption and utilization of calcium, manganese, magnesium, aluminum, zinc,etc.[17]. Microbes can degrade pollutants and reduce toxic effects on soil, thereby improving soil environmental quality and plant growth quality[18-19]. At present, soil-borne diseases are widespread and harmful in agriculture, and studies have shown that soil rhizosphere microbes play an important role in improving crop disease resistance. Plant rhizosphere microbes live in the microenvironment composed of plant roots and soil, forming mutual restriction, mutual benefit, parasitism and other relations with host plants[20-21]. More and more rhizosphere microbes that can be used for disease control have been discovered successively. Rhizosphere microbes can form a natural physical barrier by parasitizing on plant roots[22], which makes it difficult for some pathogens and insect pests to cross this barrier and invade plant roots, and further reduces the occurrence of soil-borne diseases, becoming the first line of defense. It plays an important role in the biological control of crop soil-borne diseases such as bananaFusariumwilt[23], tobacco soil-borne diseases[24]and tomato bacterial wilt[25]. Furthermore, rhizosphere microbes can also guide induced systemic resistance (ISR) of plants by producing salicylic acid, antibiotics, and siderophore[26]. PGPR refers to beneficial bacteria that live freely near plant roots and can promote plant growth. At present, more than 20 species of PGPR strains have been identified, includingBacillus,Pseudomonas,PseudomonasfluorescensandAgrobacterium. The mycelia of fungi in soil microbes form a combination with roots of higher plants, which is conducive to improving plant resistance. For example, endophytic fungi and arbuscular mycorrhizal fungi can form mutual-benefit symbionts with many plants[27].

The role of soil microbes in plant health and development has been a hot spot in the field of microbiology in recent years. Effective use of growth promotion and disease control mechanism of microbes on plants will play a positive role in improving plant growth and development and disease control. In the future, the application of microbes in agricultural production research will have great application prospects. However, in the role of microbes on plants, multiple microbes are often involved in a single function. It is necessary to further explore the exact species of microbes that play the dominant role, which requires studying the relationship between soil microbial diversity and function.

3.1.2Interaction mechanism of soil microbial diversity. The interaction between soil microbes has become a hot topic for microbiologists, while plant pathologists focus on the interaction between pathogenic microbes and soil microbes[28]. Studies have shown that most soil-borne pathogenic microbes have corresponding antagonistic microbes[29]. Traditional methods of controlling soil-borne diseases often use lethal agents to eradicate the pathogen, but the side effect will increase the resistance of pathogens. Therefore, taking antagonistic microbes as the research object plays an important role in controlling soil-borne diseases. For example, arbuscular mycorrhiza (AM fungi) interact with a wide range of soil microbes, including non-bacterial soil microbes, plant growth-promoting rhizosphere bacteria, mycorrhizal auxiliary bacteria and harmful bacteria, and their interactions play an important role in plant growth and development and resistance improvement, thereby reducing the occurrence of soil-borne diseases[30].

At present, progress has been made in the research of antagonistic microbes against soil-borne pathogenic microbes, and people can extract antibiotics from antagonistic microbes. In the future, people can further screen antagonistic microbes against soil-borne pathogens of different crops and whether the same antagonistic microbe can prevent and control multiple diseases, further explore the action mechanism of antagonistic microbes on host plants and pathogenic microbes, and create soil conditions suitable for the growth and function of antagonistic microbes.

3.2 Soil fauna diversity

3.2.1Soil fauna diversity, plant health and development. Soil fauna diversity and soil microbial diversity constitute the main body of soil biodiversity. Soil fauna can be divided into 3 types: microfauna, mesofauna and macrofauna. These 3 types have different functions in the soil. Microfauna is mainly involved in the regulation of microbes and plant litter decomposition; mesofauna mainly accelerates the decomposition of plant litter, and accelerates material circulation and energy flow; macrofauna can promote organic matter decomposition by changing soil structure through their own activities[31]. Soil faunas can influence the physical and chemical environment around the soil, cooperate with the degradation of microbes, promote the material cycle in the soil ecosystem and accelerate the decomposition of organic materials[32]. Soil faunas affect the flow of carbon and nitrogen, and promote plant growth and development by feeding on microbes and releasing carbon and nitrogen[31]. Earthworms, nematodes and fungi-eating springtails in the soil play an ecological role in inhibiting plant pathogens[33], which mainly control diseases by spreading microbes that can antagonize pathogens through activities and directly eating pathogen fungi. In addition, the positive effects of soil fauna on plant production include: enhancing the mineralization of nutrients, inducing plant defense mechanism, hormone-like effect, and promoting the spread of growth-promoting microbes[34].

3.2.2Soil fauna diversity and soil microbes. As an important part of soil biodiversity, soil fauna is the medium among soil, plant roots and microbes, ensuring the smooth development of their mutual relations. Therefore, the interaction between soil fauna and soil microbes is worth exploring. Microbes provide food sources for soil faunas, and there is a complex food chain relationship between them. The activities of soil faunas affect the biomass of soil microbes and change their spatial and temporal distribution, which further adjust soil physiological and biochemical properties by regulating the absorption, decomposition and utilization of soil substances by microbes, and accumulate beneficial substances to promote plant growth and development and disease control. For example, soil faunas can accelerate the decomposition of rhizosphere litter by feeding on microbes to help carbonization and nitridation, and make the uptake of carbon and nitrogen by plants exceed the loss of rhizosphere, thereby regulating the carbon and nitrogen flow in the soil ecosystem[35-37]. Non-predatory activities of macrofauna can affect soil physical and chemical properties and biological status, and may lead to drastic changes in the density, diversity, structure and activities of soil microbes and microfauna communities[38]. Moreover, disease inhibition of soil fauna plays an indirect role in soil-borne diseases, and inhibits pathogenic bacteria by improving the structure and function of beneficial bacteria[39]. At present, most of the researches on disease control focus on the direct effect of microbes, while less efforts have been dedicated to the disease inhibition of soil fauna. In addition to eating plant fungal pathogens to reduce pathogen infection[37], earthworms can regulate organic nutrients in the soil to improve the competitiveness of beneficial microbes and reduce the viability of pathogens, and reduce the damage of pathogens to plants by carrying antagonistic microbes through its own activities[40]. Earthworm feces can promote the growth of beneficial microbes such as antagonistic microbes and prevent soil-borne diseases[41]. The indirect role of soil fauna in soil-borne diseases should not be ignored. In the future, more soil faunas should be explored for their disease-inhibiting properties and their functional diversity in different ecological environments.

3.3 Soil plant diversityFor soil plant diversity, scientists often study the diversity of underground roots of plants in the soil[42]. As the lifeblood of plants, roots communicate with the soil through various reactions to ensure the healthy growth of plants. It is very important to study the regulation of plant roots on soil rhizosphere biological activities as well as plant growth and resistance. Plant roots are divided into 2 types: tap root system (dicotyledon) and fibrous root system (monocotyledon). The tap root system has deep roots that decrease in density from above. The growth mechanism of fibrous root system leads to uniform distribution of roots, which easily accumulates organic matter to improve soil texture and structure, thus increasing soil biomass. The underground rhizosphere structure of plants in the soil regulates various physical and chemical properties of soil, thus affecting soil biodiversity, and finally promoting plant growth and regulating the balance of soil ecosystem[43]. Further studies on the diversity of plant root functions in different habitats may be needed in the future. In addition to plant underground root structure that affects the quantity and distribution of soil organisms, root exudates play a crucial role in soil biodiversity[44].

3.3.1Rhizosphere exudates, plant health and development. Rhizosphere exudates are the bridges connecting roots and soil organisms, with multiple types and functions, and they can secrete some specific substances according to physiological activities and environmental influences, playing the role of inhibition and promotion[45]. The production mechanism of root exudates can be divided into 2 types: spontaneity and induction; spontaneity refers to the secretion of metabolites according to the needs of normal plant growth to provide energy for plant growth and resist external adverse environmental factors; induction refers to the decline of some indexes in plants caused by environmental stress or element absence, which affects the permeability of root cell membrane and leaks in a non-metabolic form[46]. Some organic matters and inorganic ions in root exudates can be reabsorbed and utilized by plants to promote nutrient recycling and energy flow. Meantime, they can also decompose and absorb the hard-to-dissolve organic matter in the soil to improve the utilization rate of nutrients[47]. However, not all of them have positive effects on plants. In the ubiquitous anti-competition mechanism of plants, some components of rhizosphere exudates can inhibit the growth and development of neighboring plants, and even inhibit or poison their own growth[48], such as continuous cropping obstacle caused by self-toxicity of sesame root exudates[49].

3.3.2Rhizosphere exudates and soil microbes. There are a large number of microbes in soil roots, including beneficial microbes (plant growth promoting rhizobacteria, antagonistic microbe) and pathogenic microbes. Rhizosphere exudates are mediators of dialogue between plants and microbes. Root exudates contain carbohydrates, amino acids, vitamins and other nutrients, which provide substrate nutrients and energy materials needed for the survival and reproduction of rhizosphere microbes, and also act as signals to influence the activity and quantity of rhizosphere soil microbes[50]. Most typically, legumes establish symbiotic relationships with rhizobia, and "communicate" by secreting flavonoids from roots to induce recognition of legumes by rhizobia. Rhizosphere exudates also provide sufficient carbon and nitrogen sources for fungi to ensure their normal growth. Studies have shown that there is a symbiosis between mycorrhizal fungi and plants. Mycorrhizal fungi can improve the nutrient absorption efficiency of plants, and improve the disease resistance and stress resistance of plants[51]. For example, arbuscular mycorrhizal fungi (AM fungi) can co-exist with most higher plants, and have significant effects in enhancing abiotic stress resistance and preventing and controlling soil-borne diseases[52]. The inhibitory effect of rhizosphere exudates on pathogens can be divided into 2 categories. First, the metabolites secreted by roots are equivalent to a natural selective medium; some components will directly affect the activity of pathogens, and specific exudates are not conducive to reproduction. Second, it indirectly improves the diversity of rhizosphere microbes, the more niche they occupy and the denser the community, the smaller the living space and the weaker the competitiveness of pathogens; at the same time, the higher the activity of beneficial microbes, the stronger the ability of action, the stronger the inhibition against pathogens. The feedback effect of microbes on root secretion is manifested by changing the permeability of root cell membrane, changing the mineral composition of soil rhizosphere and changing the soil environmental conditions through physiological and biochemical activities.

Rhizosphere exudates and rhizosphere microbes co-exist and influence mutually. Rhizosphere exudates provide nutrient sources for microbes and affect the quantity and distribution of microbes, thus improving soil microbial diversity. Similarly, rhizosphere microbes can regulate the physiological and biochemical activities in plants and the physical and chemical reaction process in external soil, further affect the types of root exudates, and also play a vital role in plant growth and disease control.

3.3.3Rhizosphere exudates and soil fauna. At present, there are few reports on the effects of rhizosphere exudates on soil fauna. Studies have shown that the species and quantity of fauna in the rhizosphere soil are significantly greater than those outside the rhizosphere[53]. Obviously, rhizosphere exudates have a positive impact on the diversity of soil fauna, but it is not a direct effect, and rhizosphere exudates increase the biomass of microbes, thus benefiting the growth of soil fauna that feed on some microbes. For diseases caused by some plant nematodes, rhizosphere exudates will produce specific substances to resist, thereby reducing the quantity of harmful organisms. Soil fauna can promote plant growth by changing soil physical and chemical properties, feeding on harmful microbes, and secreting specific hormones.

4 Influencing factors of soil biodiversity

4.1 Agricultural production patternAt present, agricultural measures such as intensive agricultural management and traditional farming are important factors threatening soil biodiversity[54]. In order to pursue yield and quality, pesticides and fertilizers are often used in large quantities in the process of planting, which will lead to the decline of soil biodiversity and break the balance and stability of soil biological system. Once the dynamic balance is broken, it is conducive to the growth of pathogenic bacteria and easy to cause soil-borne diseases. Meantime, the side effects caused by long-term use of chemical fertilizers and pesticides will improve the resistance and adaptability of harmful microbes, which will undoubtedly increase their competitiveness in the microbiota.

4.2 Plant varietyAt present, modern plant varieties that have been artificially cultivated have lost the ability to recruit beneficial soil microbes, resulting in the decoupling of rhizosphere soil microbial community function from plant environmental adaptability, and weakening the disease resistance and stress resistance of their host plants. Studies have shown that transgenic plants can reduce the quantity of microbes in the soil[43].

4.3 Soil propertyThe quality of the soil affects the quantity of soil organisms. Studies have shown that the content of various nutrients is higher in soils with better soil texture and smaller particles, and the soil biodiversity is improved correspondingly[55]. Soil climate characteristics are also important factors affecting soil biodiversity. When the temperature and humidity in the soil are high, plants will accelerate their metabolic activities, which lead to the increase of rhizosphere exudates, thereby affecting the soil biodiversity.

5 Summary and prospects

Soil biodiversity, like a rich resource pool, has far-reaching research significance, especially in promoting plant growth and development and disease control. The interaction among microbes, animals and plants, as shown in the Fig.2, regulates soil nutrient circulation and energy flow, affects the types and quantities of microbes and animals and plant health, and maintains the balance and stability of the soil ecosystem. Although a lot of achievements have been accumulated in the research of soil biodiversity, there are still great potentials worth exploring. (i) The recognition, identification and cultivation mechanism of soil biodiversity should be established and improved in the future. (ii) The relationship between soil microbial diversity and function should be further clarified: Microbes are involved in plant growth and development, and many microbes are involved in one function; It is necessary to further explore which microbes play the dominant role and the functional differences among different combinations of microbes. (iii) The antagonistic microbes of pathogenic bacteria are explored for some soil-borne diseases of plants, so as to reduce the incidence of diseases. (iv) The disease inhibition of soil fauna should be studied: the specificity or preference of soil fauna to plant fungal pathogens, and the effects of organic fertilizer added with soil animal manure on plant growth and disease. However, the progress of science and technology and human activities gradually affecting soil biodiversity has attracted global attention, and it is necessary to explore the potential threats to soil biodiversity and take appropriate protection measures. Only by protecting soil biodiversity can we maintain the balance of land ecosystem. On this basis, the potential of soil biodiversity should be fully explored, so as to ensure the health of soil ecological environment and promote plant health and ultimately serve the development of human society.