Enzymatic activity and culturable bacteria diversity in rhizosphere of amaranth, as indicators of crop phenological changes

Iván Pável Moreno-Espíndola, María Jesús Ferrara-Guerrero, Fernando de León-González, Facundo Rivera-Becerril, Lino Mayorga-Reyes, Néstor O. Pérez

Abstract


Background: Amaranth is a plant of interest in farming due to its ability to adapt into arid and semi-arid climates. Biological activity by microorganisms in rhizosphere determines plant performance and quality.

Hypothesis: The enzymatic activity is different in two types of soil, rhizosheath soil (adhered by roots) and loose soil (non-adhered by roots), in four cropping periods of amaranth.

Species study: Amaranthus hypochondriacus L.

Methods: Parameters of soil organic matter and several enzyme activities in the amaranth rhizosphere were assessed. Two types of soil, rhizosheath soil and loose soil, and four cropping periods were compared. Thirty-seven culturable bacterial isolates obtained from rhizosheath soil were molecularly identified.

Results: Rhizosheath soil had higher content of carbon and total nitrogen compared with loose soil; however, potential enzyme activity in both soil types was similar. Dehydrogenase and acid phosphatase activities were very sensitive to the crops phenological stages. Acid and alkaline phosphatases, cellulase and protease activities correlated to changes in soil moisture. The greatest diversity of culturable bacteria was found during the flowering stage.

Conclusions: In the rhizosphere of A. hypochondriacus grown in a pumiceous sandy soil, enzymatic activities in the rhizosheath and loose soils were similar, which must be considered a unique rhizosphere environment. Dehydrogenase and acid phosphatase activities were highly sensitive to changes in the crop phenology. The behavior of phosphatases and dehydrogenase activities suggests an increased dynamic soil organic matter (SOM) during the post-harvest period. In the amaranth rhizosphere, native culturable bacteria are involved in the breakdown of SOM.

Keywords


Amaranthus hypochondriacus, soil organic carbon, enzymatic activity, rhizosphere, bacteria

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References


Andrade G. 2004. Role of functional groups of microorganisms on the rhizosphere microcosm dynamics. In: Varma A, Abbott L, Werner D, Hampp R. Eds. Plant Surface Microbiology. Berlin Heidelberg: Springer-Verlag, 51-69. ISBN: 978-3-540-00923-8

Barba de la Rosa AP, Fomsgaard IS, Laursen B, Mortensen AG, Olvera-Martínez L, Silva-Sánchez C, Mendoza-Herrera A, González-Castañeda J, De León-Rodríguez A. 2009. Amaranth (Amaranthus hypochondriacus) as an alternative crop for sustainable food production: Phenolic acids and flavonoids with potential impact on its nutraceutical quality. Journal of Cereal Science 49: 117-121. DOI:10.1016/j.jcs.2008.07.012

Bencherif K, Boutekrabt A, Dalpé Y, Lounès-Hadj-Sahraoui K. 2016. Soil and season affect arbuscular mycorrhizal fungi associated with Tamarix rhizosphere in arid and semi-arid steppes. Applied Soil Ecology 107: 182-190. DOI: 10.1016/j.apsoil.2016.06.003

Bremner JM, Mulvaney CS. 1982. Nitrogen-total. In: Page AL, Miller RH, Keeney DR. Eds. Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. Madison: American Society of Agronomy, 595-622. ISBN: 0-89118-072-9

Clouse JW, Adhikary D, Page JT, Ramaraj T, Deyholos MK, Udall JA, Fairbanks DJ, Jellen EN, Maughan PJ. 2016. The amaranth genome: genome, transcriptome, and physical map assembly. The Plant Genome 9: 1-14. DOI: 10.3835/plantgenome2015.07.0062

De León-González F, Celada-Tornel E, Hidalgo-Moreno CI, Etchevers-Barra JD, Gutiérrez-Castorena MC, Flores-Macías A. 2006. Root-soil adhesion as affected by crop species in a volcanic sandy soil of Mexico. Soil & Tillage Research 90: 77-83. DOI:10.1016/j.still.2005.08.007

Francioli D, Schulz E, Buscot F, Reitz T. 2018. Dynamics of soil bacterial communities over a vegetation season relate to both soil nutrient status and plant growth phenology. Microbial Ecology 75: 216-227. DOI: 10.1007/s00248-017-1012-0

Fuentes-Ponce M, Moreno-Espíndola IP, Sánchez-Rodríguez LM, Ferrara-Guerrero MJ, López-Ordaz R. 2016. Dehydrogenase and mycorrhizal colonization: Tools for monitoring agrosystem soil quality. Applied Soil Ecology 100: 144-153. DOI: 10.1016/j.apsoil.2015.12.011

Garcia C, Roldan A, Hernandez T. 2005. Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124: 193-202. DOI: 10.1016/j.geoderma.2004.04.013

García C, Gil F, Hernández T, Trasar C. 2003. Técnicas de Análisis de Parámetros Bioquímicos en Suelos: Medida de Actividades Enzimáticas y Biomasa microbiana. Madrid: Mundi-Prensa. ISBN: 9788484761549

Gianfreda L. 2015. Enzymes of importance to rhizosphere processes. Journal of Soil Science and Plant Nutrition 2: 283-306. DOI: 10.4067/S0718-95162015005000022

Hernández T, Garcia E, García C. 2015. A strategy for marginal semiarid degraded soil restoration: a sole addition of compost at a high rate. A five-year field experiments. Soil Biology & Biochemistry 89: 61-71. DOI: 10.1016/j.soilbio.2015.06.023

Kapoor R, Mukerji KG. 2006. Rhizosphere microbial community dynamics. In: Mukerji KG, Manoharachary C, Singh J. Eds. Microbial Activity in the Rhizosphere, pp. 55-66, Springer-Verlag, Berlin Heidelberg. ISBN: 978-3-540-29182-4

Kuddus SM, Ahmad RIZ. 2013. Isolation of novel chitinolytic bacteria and production optimization of extracellular chitinase. Journal of Genetic Engineering and Biotechnology 11: 39-46. DOI: 10.1016/j.jgeb.2013.03.001

Laguerre G, Allard M-R, Revoy F, Amarger N. 1994. Rapid identification of rhizobia by restriction fragment length polymorphism analysis of PCR-amplified 16S rRNA genes. Applied and Environmental Microbiology 60: 56-63.

Lesuffleur F, Paynel F, Bataillé M-P, Le Deunff E, Cliquet JB. 2007. Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant and Soil 294: 235-246. DOI: 10.1007/s11104-007-9249-x

Moreno-Espíndola IP, Ferrara-Guerrero MJ, De León-González F, Rivera-Becerril F, González-Halphen D. 2013. Comunidad bacteriana cultivable asociada a la rizocoraza de Amaranthus hypochondriacus. Terra Latinoamericana 31: 57-69.

Moreno-Espíndola IP, Rivera-Becerril F, Ferrara-Guerrero MJ, De León-González F. 2007. Role of root-hairs and hyphae in adhesion of sand particles. Soil Biology and Biochemistry 39: 2520-2526. DOI:10.1016/j.soilbio.2007.04.021

Othman AA, Amer WM, Fayez M, Hegazi NA. 2004. Rhizosheath of Sinai desert plants is a potential repository for associative diazotrophs. Microbiological Research 159: 285-293. DOI: 10.1016/j.micres.2004.05.004

Pal SS. 1998. Interactions of an acid tolerant strain of phosphate solubilizing bacteria with a few acid tolerant crops. Plant and Soil 198: 169-177. DOI: 10.1023/A:1004318814385

Parra-Cota FI, Peña-Cabriales JJ, de los Santos-Villalobos S, Martínez-Gallardo NA, Délano-Frier JP. 2014. Burkholderia ambifaria and B. caribensis promote growth and increase yield in grain amaranth (Amaranthus cruentus and A. hypochondriacus) by improving plant nitrogen uptake. PLOS ONE 9: e88094. DOI: 10.1371/journal.pone.0088094

Philippot L, Kuffner M, Chèneby D, Depret G, Laguerre G, Martin-Laurent F. 2006. Genetic structure and activity of the nitrate-reducers community in the rhizosphere of different cultivars of maize. Plant and Soil 287: 177-186. DOI: 10.1007/s11104-006-9063-x

Schütz A, Golbik R, Tittmann K, Svergun DI, Koch MHJ, Hübner G, König S. 2003. Studies on structure–function relationships of indolepyruvate decarboxylase from Enterobacter cloacae, a key enzyme of the indole acetic acid pathway. European Journal of Biochemistry 270: 2322-2331. DOI:10.1046/j.1432-1033.2003.03602.x

Scotti R, Bonanomi G, Scelza R, Zoina A, Rao MA. 2015. Organic amendments as sustainable tool to recovery fertility in intensive agricultural systems. Journal of Soil Science and Plant Nutrition 15: 333-352. DOI: 10.4067/S0718-95162015005000031

Segura-Castruita MA, Gutiérrez-Castorena MC, Ortiz-Solorio CA, Sánchez-Guzmán P. 2005. Régimen de humedad y clasificación de suelos pomáceos del Valle Puebla-Tlaxcala. Terra Latinoamericana 23: 13-20.

Soil Survey Staff. 2003. Soil taxonomy. Natural Resources Conservation Service, Washington.

Spohn M, Kuzyakov Y. 2013. Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation – Coupling soil zymography with 14C imaging. Soil Biology and Biochemistry 67: 106-113. DOI: 10.1016/j.soilbio.2013.08.015

Vaishampayan PA, Kanekar PP, Dhakephalkar PK. 2007. Isolation and characterization of Arthrobacter sp. strain MCM B-436, an atrazine-degrading bacterium, from rhizospheric soil. International Biodeterioration & Biodegradation 60: 273-278. DOI:10.1016/j.ibiod.2007.05.001

Vance ED, Brookes PC, Jenkinson DS. 1987. An extraction method for measuring soil microbial biomass C. Soil Biology and Biochemistry 19: 703-707. DOI: 10.1016/0038-0717(87)90052-6

Walkley A, Black IA. 1934. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Science 37: 29-38. DOI: 10.1097/00010694-193401000-00003

Yang P-X, Ma L, Chen M-H, Xi J-Q, He F, Duan C-Q, Mo M-H, Fang D-H, Duan Y-Q, Yang F-X. 2012. Phosphate solubilizing ability and phylogenetic diversity of bacteria from P-rich soils around Dianchi Lake drainage area of China. Pedosphere 22: 707-716. DOI: 10.1016/S1002-0160(12)60056-3

Yaroslavtsev AM, Manucharova NA, Stepanov AL, Zvyagintsev DG, Sudnitsyn II. 2009. Microbial destruction of chitin in soils under different moisture conditions. Eurasian Soil Science 42: 797-806. DOI: 10.1134/S1064229309070114

Yasir M, Aslam Z, Kim SW, Lee S-W, Jeon CO, Chung YR. 2009. Bacterial community composition and chitinase gene diversity of vermicompost with antifungal activity. Bioresource Technology 100: 4396-4403. DOI: 10.1016/j.biortech.2009.04.015

York LM, Carminati A, Mooney SJ, Ritz K, Bennett MJ. 2016. The holistic rhizosphere: integrating zones, processes, and semantics in the soil influenced by roots. Journal of Experimental Botany 67: 3629-3643. DOI:10.1093/jxb/erw108




DOI: http://dx.doi.org/10.17129/botsci.1991

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