Influence of Rhizosphereic Biogeochemical Processes on Plant Nutrition

Available online at www.ijpab.com Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 DOI: http://dx.doi.org/10.18782/2320-7051.6728 ISSN: 2320 – 7051 Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ReviewArticle

Lokesh Patil1*, Hamsa, N.1, Adiveppa, M. Asangi and Harimohan Meena1 1Ph. D scholar, Department of Soil Science and Agricultural Chemistry, University of Agricultural Sciences, GKVK, Bengaluru 560065, India *Corresponding Author E-mail: [email protected] Received: 17.07.2018 | Revised: 22.08.2018 | Accepted: 29.08.2018

ABSTRACT The rhizosphere is the soil zone adjacent to plant roots. A number of processes takes place at rhizosphreic region like interaction between bio molecules and clay minerals, interaction between abiotic components and sorption and desorption processes. Plants exude a variety of organic compounds and inorganic ions which are involved in interaction processes. Micro- orgnisms present in the rhizosphere also are involved in the rhizosphreic proceses. All these processes lead to physical, chemical and biological change that indirectly affect solubilization, mobilisation of nutrient elements and their uptake by plants. As, nutrient availability to plants is influenced by the rhizospheric processes and their root-development system, improving plant root growth and proper management of rhizosphere region can improve nutrient availability. At this point of time, though the studies on influence of rhizosphereic biogeochemical processes on plant nutrition is limited, we try to review the studies on the concept.

Key words: Rhizosphere, Biotic and abiotic components, Interaction, Plant exudates, Nutrient availability.

INTRODUCTION complex mixture of organic acid anions, Plant developmental processes are controlled phytosiderophores, sugars, vitamins, amino by internal signals that depend on the adequate acids, purines, nucleosides, inorganic ions (e.g. 3- - + supply of mineral nutrients by soil to root and HCO , OH , H ), gaseous molecules (CO2, root to shoot. Thus, the availability of plant H2), enzymes and root border cells which have nutrients can be a major constraint to plant major direct or indirect effects on the growth in many environments of the world, acquisition of mineral nutrients required for especially the tropics where soils are plant growth. Rhizosphere was described for extremely low in nutrients thus limiting the the first time by Lorenz Hiltner in 1904. It crop productivity. Plants take up most of varies with the plant species and the soil, mineral nutrients through the rhizosphere generally considered at 2 mm distance from where microorganisms interact with root the root surface known as rhizoplane. exudates. Plant root exudates consists of a

Cite this article: Patil, L., Hamsa, N., Adiveppa, Asangi, M. and Meena, H., Influence of Rhizosphereic Biogeochemical Processes on Plant Nutrition, Int. J. Pure App. Biosci. 6(4): 506-515 (2018). doi:

http://dx.doi.org/10.18782/2320-7051.6728

Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 Biogeochemical processes at rhizosphere indirectly with a metabolically produced A number of processes take place at ligand that form a highly soluble product with rhizosphere as it is the most active region in a mineral component12. Clay minerals, pH, soil. Some of those processes that influence organic ligands are the most important factors plant nutrition directly or indirectly are given which influence the release and phase below- transformation of Al and Fe at soil plant 1. Interactions between biomolecules and clay interface and the mineralogy, order, particle minerals- Rhizosphere soil exhibits differences size, specific surface area and reactivity of the in physicochemical properties and mineralogy metal precipitation products towards nutrients compared with bulk soil. It is a major active and pollutants. The increased weathering of microsite where interactions among roots, minerals in the rhizosphere induces changes in symbiotic microorganisms, bacteria, soil the abundance and the forms of metals at soil- constituents like minerals and organic root interface, as compared to the bulk soil. substances, and soil solution take place and are 2. Interaction between abiotic and biotic soil involved in solubilization and insolubilization components in the rhizosphere and formation processes. Plant exsudes OH- or H+ to of organo-mineral complexes- Root exudates equilibrate the anion-cation balance, mineral like low molecular mass organic ligands and weathering will be increased in the biopolymers such as proteins (enzymes), rhizosphere. Chelating root exudates and nucleotides, polysaccharides and lipids interact organic compounds released by with clay minerals, OH-Al and OH-Fe species microorganisms as well as organic acids are and/or microorganisms form organo-mineral involved in the weathering of minerals and in complexes at rhizosphere43. Microorganisms- the subsequent release and transformations of mineral complexes formed by electrostatic or Fe and Al at root-soil interface. Their hydrophobic interaction between solubilisation capabilities depend on their microorganisms and minerals are other chemical composition, nature of clay minerals common complexes at soil-plant interface. and the mineral element considered20. Such Microorganisms participate in the formation of processes of acid dissolution and complexation organo-mineral complexes which these of minerals due to metabolites are considered complexes provide substrates and protection. as indirect weathering processes. Some They contribute to the formation of organo- bacteria, including anaerobic species and fungi mineral complexes excreting polysaccharides can attack mineral surfaces and thereby and proteins. mobilize constituents of the mineral or

Fig. 1: Rhizosphereic Interactions of root exudates with soil components

Source: Violante and Caporale, 2015

Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 3. Sorption and desorption processes at Cd, Co, Ca) may be strongly adsorbed on the rhizosphere- Mobility of elements at edge sites of phyllosilicates due to the rhizosphere is affected by sorption-desorption presence of –SiOH or –AlOH groups capable reactions that play a major role in their of chemisorbing these ions. Organic matter bioavailability. Soil components responsible and variable charge minerals (metal oxides, for the sorption of nutrients and pollutants allophanes, imogolite) are much more include phyllosilicates, soil organic matter, effective scavenger of polyvalent cations, carbonates, variable charge minerals, because complexation processes are the microorganisms and organo-mineral dominant binding mechanisms21. For example, complexes. Sorption of elements onto soil Free-living bacteria and their extracellular components is influenced by many factors as macromolecular products (e.g. fibrils) can pH, nature of the sorbents, redox reactions, accumulate metal ions and may have mineral presence of foreign ions as indicated by coatings with bound metals on their surfaces5. Violante40. Polyvalent cations (e.g. Zn, Cu,

Major physical, chemical, and biological changes in the rhizosphere

Fig. 2: Major physical, chemical, and biological changes in the rhizosphere9

1. Chemical changes- This article mainly Root excretion of H+ in the rhizosphere is an emphasizes on the biological and chemical effective mechanism for improving uptake of changes that occur in the rhizosphere to make micronutrients except Mo10. nutrients available to plants. Several chemical b. Redox potential- Redox potential is a changes take place in the rhizosphere due to chemical process by which electrons are given plant root and soil environmental interactions. up or acquired. Root activity alters rhizosphere Among these changes redox potential through respiratory oxygen a. Soil pH- is one of the most important consumption and ion uptake or exudation. chemical properties that influence nutrient Lindsay24, enlisted Redox reactions occur with solubility and hence, the nutrients availability various forms of elements viz. Mn (Mn2+ and to plants. At lower pH availability of most Mn4+), Fe (Fe2+ and Fe3+) and Cu (Cu+ and micronutrients is higher, except that of Cu2+). Primary source of electrons for molybdenum and decreases with increasing biological redox reactions in soil is organic soil pH. Availability of N and P is lower at matter, but aeration, pH and root and microbial lower pH. The changes in rhizosphere pH are activities also influence these reactions. associated with differences in cation/anion c. Release of organic compounds- Plant roots uptake and release of H+ or OH− (HCO3−) by not only absorb water and nutrients to support plant roots. The pH also changes with the plant growth, but also release organic and excretion of organic acids by roots and by inorganic compounds into the rhizosphere9. microorganism activities in the rhizosphere. These compounds affect microbial population

CO2 produced by roots and microorganisms and availability of nutrients. The release may respiration can dissolve in soil solution and occur as an active exudation, a passive may form carbonic acid and lower the pH. leaking, the production of mucilage, or with Copyright © July-August, 2018; IJPAB 508

Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 the death and sloughing of root cells. Sugars Cu26. Harrier and Watson17 found that P is the and amino acids released in the rhizophere most important nutrient taken up by the extra- provide energy for microorganisms in the radical hyphae and influx of P in roots rhizosphere, which mineralize or solubilize colonized by AMF fungi that can be three to many nutrients. Acids reduce the pH and five times higher than in an non-mycorrhizal improve the availability of many micro and roots. Mycorrhizae are also involved in the macro nutrients. Release of mucilages protects nutrient cycling viz. solubilization, the root tips from injury and desiccation, as mineralization) hence found to improve well as playing a role in nutrient uptake nutrient availability in rhizosphere soil26. through the mucilages, pH-dependent cation e. Beneficial microorganisms and modes of exchange capacity22. action- Plant-beneficial microbial interactions 2. Biological changes- An important can be roughly divided into three categories32. biological change associated with the i. First, those microorganisms that in rhizosphere is root colonization by many types association with plants, are responsible for its of beneficial and harmful microorganisms. nutrition (i.e., microorganisms that can plant- beneficial microorganisms include increase the supply of mineral nutrients to the nitrogen (N2)-fixing bacteria, freeliving N- plant). Saprophytic microorganisms are fixing bacteria, plant-growth-promoting responsible for many vital soil processes, such rhizobacteria, saprophytic microorganisms, as decomposition of organic residues in soil bicontrol agents, and mycorrhizae fungi. and associated soil nutrient mineralization or a. Nitrogen (N2) fixing bacteria - Nitrogen turnover processes. fixation is defined as the conversion of ii. Second, there is a group of microorganisms molecular nitrogen (N2) to ammonia and that stimulate plant growth indirectly by subsequently to organic N utilization in preventing the growth or activity of pathogens. biological processes. Microorganisms Such microorganisms are referred as responsible for biological N fixation are biocontrol agents. symbiotically living in the roots of higher iii. A third group involves those plants and also in association with roots as microorganisms responsible for direct growth well as free-living organisms in the promotion by production of phytohormones. rhizosphere. A major portion of biological N is The modes of action of PGPR involve fixed by species of Rhizobium and complex mechanisms to promote plant growth, Bradyrhizobium living in symbiosis with development and protection. Important among legume roots. them are biofertilization (increasing the b. Nitrogen fixation by free-living and root- availability of nutrients to plant), associated bacteria phytostimulation (plant growth promoting, c. Plant growth promoting rhizobacteria- usually by the production of phytohormones) Direct influence is related to increased and biocontrol (controlling diseases, mainly by solubilization and uptake of nutrients and the production of antibiotics and antifungal production of phytohormones, whereas metabolites, lytic enzymes and induction of indirect effect is associated with pathogen plant defense responses). Example- suppression, production of Fe-chelating Pseudomonas and Bacillus genera siderophores, and antibiotics, and the Root-induced changes of ionic induction of plant resistance mechanisms33. concentrations in the rhizosphere d. Mycorrhizal Fungi- Mycorrhizae associated The major function of plant roots is the uptake with crop plants are primarily arbuscular of water and nutrients. This results in either mycorrhizal fungi (AMF). The AMF improve the accumulation or depletion of all the ions host-plant nutrition by improving the present in the soil solution in the rhizosphere. acquisition of P and other minerals, especially This process occurs both for mineral nutrients the low-mobile micronutrients Zn, Fe, and and for other, nonessential elements (e.g., Si) Copyright © July-August, 2018; IJPAB 509

Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 and possibly for toxic elements19. The nature related to the uptake of nutrient and affects in and intensity of the ionic concentrations the rhizosphere region. + − changes depend on the correspondence of the The NH 4 /NO 3 ion uptake can requirements of the plant and the supply by the change rhizosphere pH up to 2 units higher or soil. Nutrients such as Ca or Mg, which lower compared with bulk soil29. Generally, in − usually occur at large concentrations in the soil oxidized soils, NO 3 is the dominant ion and solution11, may be transferred by mass flow to under reduced soil conditions (flooded rice), + the root-soil solution interface at a greater flux NH 4 is the dominant ion. Symbiotic than required by the root. Nutrients uptake organisms such as rhizobia and to lesser extent results in a decrease in their concentration in nonsymbiotic bacteria such as Azospirillum, the soil solution near plant roots, this depletion can augment plant uptake of N via N fixation. + generates a concentration gradient and mobilization of non-exchangeable NH 4 -N in diffusion of ions toward the roots takes place. the soil-root interface may be increased by Influence of rhizosphereic processes on nitrifying and hetrotrophic microorganisms Plant Nutrient Availability – with a higher activity in the rhizosphere, In rhizosphere, competition exists among the influencing the equilibrium between non- + + roots of neighboring plant species for space, exchangeable NH 4 and NH 4 in the soil 34 + water, mineral nutrients . The rhizosphere solution, thus favoring the release of NH 4 also consists of several micro and macro from interlayer of the clay minerals3. A 2-year organisms like bacteria, fungi, virus etc and field experiment on greenhouse cucumber other insects. Root–root, root-microbe, and double-cropping systems examined the effects root-insect communications of continuous of nitrogen management in rhizosphere and occurrence in this zone Hence, rhizosphere is planting of sweet corn as a catch crop in the considered as biologically active soil zone. summer fallow period on cucumber yield and 1. Nitrogen- soil Nmin dynamics compared to conventional The rhizospheric bacteria fix atmospheric N2 practices. Cucumber fruit yields were not in the soil in organic form and it is easily used significantly affected by root zone N 39 by plants . The application of nitrogen management and catch crop planting despite a fertilizers leave residual effect on soil which decrease in N fertilizer application of 53 % modifies the rhizosphere pH through chemical compared to conventional N management. 13 reactions . Root zone N management efficiently and Dong S and Shu, 2001 found the existence of directly reduced N losses by 44 % and 45 % in strong interaction among varies nutrients in the 2005 and 2006, respectively. Sweet corn, the rhizosphere, phosphorus showd depletion in summer catch crop, depleted Nmin residue in rhizosphere and the depletion zone remains the soil profile of 1.8 m at harvest of winter– larger in (NH4)2SO4 than KNO3 applied plot. spring season cucumber by 304–333 kg N The responses of potassium, calcium, −1 ha , which contributed 19– 22 % reduction in magnesium, copper, zinc, manganese and Fe N loss. Compared to conventional N concentrations in the rhizosphere to nitrogen management, N loss was reduced by 56 % fertilizers varies with species crop and kind under root zone N management and catch crop and amount of nutrient treatments. planting14. Clayton et al.6 studied the effects of Nitrogen sources affect the rhizosphere pH via elevated CO (eCO ) and soil N status on three mechanisms as given by Marschner, 2 2 wheat rhizosphere activity and residue 1997 (i) displacement of H+/OH- adsorbed on decomposition and also N recovery from crop the solid phase; not associated with any plant residues with different N status by different activity plant treatments. They found that for wheat, (ii) nitrification/denitrification reactions; not eCO reduced the negative rhizosphere effect, associated with any plant activity and 2 + resulting in greater rates of decomposition and (iii) release/uptake of H by roots in response recovery of N from field pea residues, but only to NH4/ NO3 ratio uptake. This is directly Copyright © July-August, 2018; IJPAB 510

Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 when N fertilizer was added but not for field of P extracted by the plants in both P-fertilized pea residue. and unfertilized soils. After 6 wk of rice Phosphorus- Its deficiency mostly occurs growth, 90 % of the P taken up was drawn both in acidic and calcareous soils where P from acid-soluble pools. There was a small retention and precipitation is high, hence in accumulation of alkali-soluble organic P and these soils it is one of the major limiting no changes in the more recalcitrant soil P nutritional problems for plants. The pools. The zone of P depletion was 4-6 mm mycorrhizosphere favor the nutrient uptake, wide, increased with P addition and coincided particularly P, Cu and Zn25. with a zone of acidification. The acidification Glucose, which serves as an energy was due to H+ generated in oxidation of Fe2+ + source to microorganisms, was found to have a by root-released O2 and to H released from strong effect on phosphorus mineralization in the roots to balance excess intake of cations rhizosphere region35. According to Hamer and over anions. Marschner16, amino acids that are mainly used Potassium- The original source of K is from as N by microorganisms have a smaller effect primary minerals such as micas (biotite and on P mineralization from organic sources. The muscovite), feldspar (orthoclase and mechanism involved in the microbial microcline), and their weathering products. solubilization of P is the production of organic Availability of non-exchangeable K to plants acids and the release of protons to the soil was found to increase due to an exchange solution. The alkaline phosphatase activity reaction and mineral dissolution in the increases from 102 to 325 % and acid rhizosphere30. Increased exudation of sugars, phosphatase activity from 205 to 455 % in the organic acids, and amino acids has been found soil adhering to the root mat as compared to in maize as a response to K limitation31. the non rhizosphere soil, hence the release of P Iron- Microorganisms and plants release low is high in rhizosphere soil than the bulk soil36. molecular-weight compounds (chelators) Amending acid soils with rock phosphates has which increase the Fe availability28. There are increased available form of phosphorus and two different strategies to relese iron in soil as also enhanced their rate of dissolution by the reported by Von Wiren et al., 1993. Strategy I rhizosphere soil1. Plants, fungi, and bacteria plants (dicots and non-graminaceous have their own ways to mobilize P. Release of monocots) release organic acid anions which protons that lead to a decrease in soil pH, the chelate Fe. Iron solubility is also increased by release of organic and inorganic ligands and decreasing the rhizosphere pH, and Fe uptake chelators such as bicarbonate or carboxylic is enhanced by increased reducing capacity of anion are the important mechanisms as found the roots (Fe3+ to Fe2+). Strategy II plants by Uroz 2009, that release phosphatases that (Poaceae) release phytosiderophores that mineralize in situ P. Root exudates released in chelate Fe3+. It is taken up in the chelated form the rhizosphere contain phosphate radicals that as Fe-phytosiderophore. Guo et al.15 found that will be subject to microbial modification. the production of phytosiderophres in maize Microbial processes including mineralization, plants helped peanut for uptake of Fe during immobilization, and solubilization of inorganic deficient period. Intercropping altered phosphates also influence P availability to parameters of the rhizosphere proceses viz. plants. Enhanced secretion of acid available iron concentration and pH due to an phosphatases (APase) and phytases by plant interspecific rhizosphere effect at different roots and also by rhizosphere microorganisms stages. The significantly higher levels of ferric under P deficient conditions may contribute to reductase activity and AhFRO1 and AhYSL1 P acquisition by hydrolysis of organic P esters expression at the vegetative stage of in the rhizosphere31. Saleque and Kirk37 opined intercropped peanuts suggest roles for such that the quantity of readily plant-available P genes in Fe uptake in the particular was negligible in comparison with the quantity rhizosphere conditions under intercropping. Copyright © July-August, 2018; IJPAB 511

Patil et al Int. J. Pure App. Biosci. 6 (4): 506-515 (2018) ISSN: 2320 – 7051 Manganese- dynamics of Mn in the (1) proper land preparation, rhizosphere is similar to that of Fe. Its (2) adequate and balanced fertilization and availability in soil solution increases with liming; increasing acidic condition. In alkaline soils (3) use of good-quality seeds; where Mn usually is insoluble the rhizosphere (4) sowing cultivars of high yield potential, effect is beneficial. Availability of Mn in the (5) use of adequate seed rate and plant rhizosphere is affected by important factors spacing; like redox condition, pH, moisture, (6) seed treatment for the control of seed- temperature, other nutrients and heavy metal borne diseases; concentrations in soil solution. In rhizosphere (7) appropriate methods of fertilization, 4+ Mn in oxidized form as Mn will be reduced especially immobile nutrients; 2+ to Mn by some rhizosphere bacteria like (8) topdressing N at the right stage of crop Bacillus, Pseudomonas, and Geobacter and growth (as a general rule, the best time for fungi (Gaeumannomyces graminis) make Mn topdressing N in cereals is at about panicle 8 available for plants . initiation and in legumes, about one week Zinc- Generally, Zn deficiency can be noticed before initiation of flowering. At these growth in sandy loam and organic soils than silty or stages, plants have adequate root systems to clayey soil, but White et al., 1997 reported that absorb Zn deficiency can be reclaimed by the applied N and have N requirements to increase modification in the rhizosphere soil. They the number of grains), commonly provided Zn to plants through the (9) control of diseases, insects, and weeds; fertilization system with chelating agents (10) use of proper crop rotation; (mainly EDTA or DTPA) and obtained good (11) control of soil erosion; results. Cakmak et al., 1996 bserved that long (12) maintenance of organic matter; and fine plant roots architecture favor (13) control of allelopathy; aquisition of Zn from larger soil volume, (14) proper management of soil salinity and higher synthesis and release of Zn-mobilizing alkalinity; phytosiderophore by the roots in rhizosphere (15) avoidance or minimization water region, it promotes Zn uptake as Zn- deficiency; and phytosiderophore complex. Bar-Yosef et al.2 (16) adoption of a conservation tillage system reported that root excretion of H+ at the root surface is an effective mechanism for CONCLUSION enhancing. Zinc uptake compared with Rhizosphere effect on nutrient mobility and excretion of complexing agents. plant nutrient uptake is a key activity in crop Copper- Its dynamics is similar to that of zinc. The root exudation in the rhizosphere production. Various biogeo-chemical increases its availability and plant uptake of processes occur at rhizosphere region and are Cu23. responsible for nutrient solubility and Strategies for modifying rhizosphere availability to plants. The magnitude of bio- environment to improve nutrient chemical changes varies with plant species, availability- soil type, environmental factors and their Water and nutrient availability to plants is interactions. The manipulation of root influenced by their root-development system. activities and its exudation from the plant in Hence, improving plant root growth can nutrient deficient conditions enhances nutrient improve nutrient availability. use efficiency. Hence, rhizosphere processes By adopting the following management are very complex in nature and dynamics and practices, it is possible to modify the complete knowledge about them is still not rhizosphere environment in favor of better root available. More studies are needed to development and, consequently, higher understand the changes and their interactions nutrient availability9: with plant nutrition. Copyright © July-August, 2018; IJPAB 512

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