Microbe-plant interactions to promote the restoration of desertic areas

INTRODUCTION

Desertification is a serious environmental problem all over the world. This one is defined as “land degradation in arid, semi-arid, and dry subhumid areas resulting from various factors, including climatic variations and human activities”(Reynolds et al., 2007). Due to the fact that the 21st century has been marked by global climate change (Kumar & Verma, 2018) the world’s drylands, 6.31 billion hectares (Bha) or 47% of the earth’s land area, are found in a wide range of climates. (Lal, 2001). Thus soils identified as dryland regions are rapidly increasing all over the world, “characterized by frequent drought stress, low organic matter content, low nutrient reserves, and especially low N content” (Lal, 2001). Moreover, soils in dry areas are estimated to contain more than a quarter of Earth’s total stores of organic carbon. Yet, as these lands are degraded, they release carbon into the atmosphere, accounting for about 4 percent of total global emissions each year(Lucas, 2009).

Plant growth-promoting bacteria (PGPB) are a group of bacteria communly used to increase crop yield in specific conditions. The activities of these bacteria are more important and active in rhizosphere and to lesser extent on the leaf surfaces. The beneficial effects of these rhizobacteria on plant growth can be direct or indirect. In drylands, the most important subgroup in PGPB is the growth-promoting rhizobacteria (PGPR), because its activity take place on the roots (Compant, Clément, & Sessitsch, 2010).

Figure 1. The left side is an example of a root without PGPB and the right side is an example of what the root would be like with PGPB Source: Wikiadmin, (2006), Plant Growth Promoting Bacteria, Microbewiki, https://microbewiki.kenyon.edu/index.php/Plant_Growth_Promoting_Bacteria

Microbe-plant interactions have been utilized to improve plant growth in a wide range of areas such are food, fibre, biofuels or key metabolites. This article pretends to investigate microbe-plant interactions in order to find a way of restoring deserted areas by promoting plant growth. In this review we describe the 4 mainstay results of these interactions, which are explained in the following points below.

I. Change in the surface soil properties

II. Direct plant growth promotion

      a) Increase of nutrients supply

      b) Phytohormones

      c) Stress Controllers

III. Diseases

I. CHANGE IN THE SURFACE SOIL PROPERTIES

To prevent the expansion of desertification, an effective method was shown to be the inoculation of desert cyanobacteria in soils, thus accelerating the formation of biological soil crusts (BSCs)(Xu et al., 2013).

Biological soil crusts are special structures constituted by cyanobacteria, microalgae, lichens, and fungi, usually embedded in a polysaccharidic matrix, that aggregate soil particles in arid and semiarid areas.

Cyanobacterial polysaccharides are complex anionic heteropolymers, components, such as peptidic moieties, acetyl, pyruvyl, and/or sulfate groups containing different monosaccharides, uronic acids, and non-saccharidic (De Philippis et al. 2001; Pereira et al. 2009; Xu et al., 2013).This EPS layer surrounding cyanobacterial cells is capable of creating a microenvironment that buffers the osmotic disequilibrium preventing water loss, thus maintaining a relatively high humidity available for seed germination and creating a microhabitat suitable for the viability of the residing microbial community (Vázquez et al. 1998; Xu et al., 2013).

Moreover, BSC play an important role in sand surface stabilisation. Polysaccharidic sheaths of the cyanobacteria can glue sand particles together, stabilize the soil surface, prevent water erosion, and improve the hydrological properties of crust-covered dunes (Xu et al., 2013).

Furthermore, it has been demonstrated that microbes can dissolve minerals by direct and indirect action under aerobic and anaerobic conditions (Ehrlich, 2002; Kurek, 2002). Instragating the spontaneous precipitation of metals by altering the chemistry of the microenvironment (Beveridge et al., 1997; Douglas and Beveridge, 1998).

II. DIRECT PLANT GROWTH PROMOTION

a) Increase of nutrients supply

Microorganisms are responsible for soil biochemical cycles, therefore they control the cycle of plant nutrients (Marulanda, A., Barea, J. M., & Azcón, R., 2009).PGPR can modify the soil fertility and facilitate plant establishment and development. Rhizobacteria are able to enhance absorption with different mechanisms. One way is solubilizing normally poorly soluble nutrients with secreting bacteria siderophores. The siderophores are agents iron-chelating and serving to transport iron across cell membranes. Iron is an essential nutrient, but it is scarce in soil, but PGPB produce this siderophores, which acquire ferric iron (Fe3+), root cells can then take this up by active transport mechanisms.  Other mechanism is lowering the PH by secreting acidic organic compounds.

Phosphorous is a macronutrient and is essential for plants, but isn’t easily up taken because it reacts with iron,aluminium and calcium and lead to precipitation. Some PGPR can convert phosphorus into a more plant attainable form, such as to orthophosphate. There are  a number of PGPB, which are able to fix atmosphere nitrogen (N2) such as Rhizobium and Bradyrhizobium. Their system can form nodules on roots of leguminous plants, in which they convert N2 into ammonia, which is a nitrogen source to plants. (Lugtenberg,B.,  Kamilova, F.,2009). But in some cases, the capacity for establishing the symbiosis between bacteria and the plant needs is determined in the plant genotype, some locis are needed to establish symbiosis for nutrient acquisition. ( Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009)

b) Phytohormones

PGPR can produce a range of plant growth-stimulating phytohormones (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). Phytohormones are chemical messengers produced by plants and microorganisms, which coordinate plant cellular activities (Morel, M. A., & Castro-Sowinski, S., 2013). The main groups of phytohormones are: auxins, cytokinins, gibberellins, abscisic acid, and ethylene (Morel, M. A., & Castro-Sowinski, S., 2013). The different phytohormone producers bacteria have differential capability to produce the five major phytohormones (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009).

Auxins act on root architecture increasing the number of lateral roots and root hair elongation, and they are also responsible for apical dominance (Morel, M. A., & Castro-Sowinski, S., 2013). As a result, the plant may have a larger area for nutrient and water uptake (Morel, M. A., & Castro-Sowinski, S., 2013).  The most important auxin is indole-3-acetic acid (IAA) (Morel, M. A., & Castro-Sowinski, S., 2013). Many PGPR, such as Azospirillum, Pseudomonas, Delftia, and Rhizobium species, induce root proliferation through IAA production (Morel, M. A., & Castro-Sowinski, S., 2013). For example Bacillus amyloliquefaciens and Pseudomonas putida produce and secrete significant amounts of IAA (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). However, the bacterial production of IAA may not always be beneficial for plant because a high concentration of IAA can also inhibit root cell growth (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009).

Cytokinins promote of root and shoot cell division, cell growth (Morel, M. A., & Castro-Sowinski, S., 2013), and induce stomata-opening (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009) mainly. When soil is drying, cytokinin concentration decrease to induce stomatal closure, but at the same time cell growth is effected. Bacillus subtilis is an example of cytokinin-producing bacteria. This bacteria can promote lettuce plants growth allowing them to grow under water stress conditions (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). Abscisic acid works as a cytokinin antagonism, a balance of these hormones is needed for a normal growth (Liu, F., Xing, S., Ma, H., Du, Z., & Ma, B., 2013).

Gibberellins act as chemical signals for root colonization by symbiotic arbuscular mycorrhizal fungi and inhibit shoot branching (Morel, M. A., & Castro-Sowinski, S., 2013).

Ethylene has effects on plant growth, development and modulation of responses to biotic and abiotic stresses (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). Some bacteria as Pseudomonas spp. can low the endogenous ethylene level in planta by producing a degradative enzyme 1-aminocyclopropane-1-carboxylic acid (ACC) - deaminase (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). ACC is the precursor for the production of ethylene, whose amounts are increased under stress, affecting adversely plant growth (Porcel R, Zamarreño Á, García-Mina J, Aroca R, 2014). Abscisic acid (ABA) is important for the response to environmental stresses such as desiccation, salt and cold, it controls plant growth and inhibits root elongation (Porcel, R., Zamarreño, Á. M., García-Mina, J. M., & Aroca, R., 2014). Ethylene and ABA act antagonistically to modulate development (Porcel, R., Zamarreño, Á. M., García-Mina, J. M., & Aroca, R., 2014). Normal ABA levels are required to maintain root growth (Porcel, R., Zamarreño, Á. M., García-Mina, J. M., & Aroca, R., 2014).

Although the properties of each type of hormone, these molecules work together, so it’s important to consider that different combinations of phytohormones may have different impact on plant growth (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). Therefore, the modulation of phytohormone by bacteria is very complex and needs to adapt on each plant specie and the environment where it's located.

The effect of the bacteria can be improved by adding the action of Arbuscular mycorrhiza, which can also disturb the plant hormone levels. (Marulanda, A., Barea, J. M., & Azcón, R., 2009).

c) Stress controllers

PGPR can improve plant tolerance to abiotic stresses, such as drought, salt and nutrient deficiency or excess (Yang, J., Kloepper, J. W., & Ryu, C. M.,2009). These physical and chemical changes induced by PGPR are named “induced systemic tolerance” (IST) (Yang, J., Kloepper, J. W., & Ryu, C. M.,2009).

Under stress conditions, plants start to increase ethylene level reducing plant growth. Some PGPR synthesize ACC-deaminase ,  that degrades ethylene precursor ACC. The presence of this enzyme effects on the plant increasing root growth, and improving tolerance of salt and water stress (Wu, C. H., Bernard, S. M., Andersen, G. L., & Chen, W., 2009). For example, Achromobacter piechaudii ARV8, a PGPR strain, produces ACC-deaminase and degrades ACC in pepper (Capsicum annuum L.) and tomato (Solanum lycopersicum L.) plants, so these plants although being under stress conditions can keep a normal growth  (Yang, J., Kloepper, J. W., & Ryu, C. M.,2009).

Drought stress is also being revealed to increase ABA content in leaves provoking stomata closure. But this increase induces to a normal growth alteration. So some PGPR produce cytokinin hormones, compensating the balance cytokinin-ABA and conferring resistance to the plant (Liu, F., Xing, S., Ma, H., Du, Z., & Ma, B., 2013).

PGPR also emit some volatiles that regulate “high-affinity K+ transporter 1” (HKT1) expression. HKT1 adjust Na+ and K+ levels differentially on plants, depending on the plant tissue (Yang, J., Kloepper, J. W., & Ryu, C. M.,2009). VOCs downregulate HKT1 expression in roots and upregulate it in shoot tissues, provoking lower Na+ levels in the whole plant, so bacterial VOC causes a tissue-specific regulation of HKT1 that controls Na+ homeostasis under salt stress (Yang, J., Kloepper, J. W., & Ryu, C. M.,2009).

The lack of soil nutrients causes abiotic stress too. PGPR that produces indole acetic acid (IAA) has been told to be promote root development increasing root surface area increasing the nutrient uptake sites and reducing stress (Yang, J., Kloepper, J. W., & Ryu, C. M.,2009).

Under salt stress, plants may produce reactive oxygen species (ROS), such as hydrogen peroxide (H2O2). These compounds causes oxidative damage to lipids, proteins and other cellular components. Some antioxidative enzymes and compounds can neutralize that effect (de Andrade Santos, A. et al., 2018). Some PGPR promote plant tolerance to salinity stress producing catalase, an antioxidative enzyme (de Andrade Santos, A. et al., 2018).

Figure 2. IST induced by PGPR against drought, salt and fertility stresses. Source: Rhizosphere bacteria help plants tolerate abiotic stress (2009). Trends in plant science, 14(1), 1-4.

III. DISEASES

Some of these microbial control mechanisms are based on PGPR. PGPR can protect plants against the effects of phytopathogens, competing for nutrients or for space at the root where PGPR have more affinity (Grobelak, A., Napora, A., & Kacprzak, M.,2015). For example, PGPR produce chelators (also called siderophores) which are specific for the Fe3+ ions, so these chelators have a higher affinity for iron than chelators produced by pathogenic microorganisms (Grobelak, A., Napora, A., & Kacprzak, M.,2015). Therefore, the Fe3+ becomes unavailable for pathogens preventing them from surviving.

PGPR bacteria are also capable of the production of secondary metabolites that can act as antifungal substances, as insecticides or as immunosuppressants (Grobelak, A., Napora, A., & Kacprzak, M.,2015). So the own metabolites from the bacteria act as a plant protection improving its chance to survive in desert conditions.

CONCLUSIONS

To promote the restoration of desertic areas, microbe-plant interactions are a good chance of combat. In a society where intensive human activity and global climatic change are exponentially taking place, the need of interactions which can change the surface soil properties (as BSCs) making it suitable for living will become a key factor. Summing up, the coordinated effect of the organisms by symbiotic interactions (bacterial, fungi, lichens and plants) is capable of changing soil properties, the availability of nutrient and also remediate plant stress.

This method is an alternative to usual chemicals that end up damaging the soil, thus making a significant change at a global scale.

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