https://doi.org/10.4081/ija.2022.1942

Durum wheat salt stress tolerance is modulated by the interaction between plant genotypes, soil microbial biomass, and enzyme activity

Vol. 17 No. 1 (2022)
Submitted: 8 July 2021
Accepted: 5 January 2022
Published: 21 January 2022
Durum wheat, enzymatic activities, growth stages, microbial biomass, salinity, yield.
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Authors

  • Khaoula Boudabbous • khaoulaboudabbous15@gmail.com Genetics and Cereal Breeding Laboratory (LR14AGR01); and Horticultural Sciences Laboratory (LR13AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Imen Bouhaouel Genetics and Cereal Breeding Laboratory (LR14AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Nadhira Benaissa Genetics and Cereal Breeding Laboratory (LR14AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Maroua Jerbi Horticultural Sciences Laboratory (LR13AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Youssef Trifa Genetics and Cereal Breeding Laboratory (LR14AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Ali Sahli Genetics and Cereal Breeding Laboratory (LR14AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Chahine Karmous Genetics and Cereal Breeding Laboratory (LR14AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.
  • Hajer S. Amara Genetics and Cereal Breeding Laboratory (LR14AGR01), National Agronomic Institute of Tunisia, University of Carthage, Tunis-Mahragene, Tunisia.

Understanding the relationship between durum wheat genotypes and soil biochemistry under salt stress plays a key role in breeding for yield superior genotypes. Thus, microbial biomass carbon (MBC) and nitrogen (MBN), the activity of three selected enzymes including dehydrogenase (D-ase), alkaline phosphatase (Alk-ase), and protease (P-ase), and available phosphorus (available P) and nitrogen (available N) were assessed. Two landraces and two improved varieties were tested under two salinity levels of water irrigation (0.3 and 12 dS m–1). Soil sampling was carried out at five durum wheat growth stages. The soil biota-genotype interaction seems to affect the biological (MBC, MBN, and enzymatic activities) and chemical (available P and N) traits. The microbial activity of rhizospheric soil was higher at the tillering and flowering stages. Under saline conditions, ‘Maali’ (improved variety) and ‘Agili Glabre’ (landrace) showed the best belowground inputs (e.g., MBC, MBN, enzymatic activities, available P and N) and grain yield (GY) performance. Under the same conditions, four soil biochemical indicators of GY of tolerant genotypes (i.e., ‘Maali’ and ‘Agili Glabre’) were determined as available N, P-ase, available P, Alkase, and D-ase. Stepwise analysis revealed that predictive variables depended on growth stages. Overall, MBC, available N, Alk-ase, and P-ase were the variables that mainly contributed to predicting GY in saline environments. In conclusion, the results suggested a specific interaction between plant genotype roots and soil microbes to overcome salt stress. Thus, soil biological components should acquire more importance in plant salinity tolerance studies.

Highlights
- Salt-tolerant durum wheat genotypes showed greater microbial activities in the rhizosphere.
- Microbial enzymatic changes depended on the interaction plant genotype x soil salinity.
- The MBC/MBN ratio and dehydrogenase strongly correlated with grain yield under salinity.
- MBC, available N, and alkaline phosphatase as predictors of grain yield at 12 dS m–1.
- Tillering and flowering could be key stages of durum wheat salinity tolerance.

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Crossref
Scopus
Google Scholar
Europe PMC
AFNOR, 1995. Quality control of soil analyzes. Methods of official analyzes-Tome 1 (in French). AFNOR-DGCCRF, Association Française de Normalisation, Paris, France.
Allison VJ, Condron LM, Peltzer DA, Richardson SJ, Turner BL, 2007. Changes in enzyme activities and soil microbial community composition along carbon and nutrient gradients at the Franz Josef chronosequence, New Zealand. Soil Biol. Biochem. 39:1770-81. DOI: https://doi.org/10.1016/j.soilbio.2007.02.006
Barraclough PB, Lopez-Bellido R, Hawkesford MJ, 2014. Genotypic variation in the uptake, partitioning and remobilisation of nitrogen during grain-filling in wheat. Field Crop Res. 156:242-8. DOI: https://doi.org/10.1016/j.fcr.2013.10.004
Bera T, Sharma S, Thind HS, Singh Y, Sidhu HS, Jat ML, 2018. Changes in soil biochemical indicators at different wheat growth stages under conservation-based sustainable intensification of rice-wheat system. J. Integr. Agric. 17:1871-80. DOI: https://doi.org/10.1016/S2095-3119(17)61835-5
Bever JD, 2015. Preferential allocation, physio‐evolutionary feedbacks, and the stability and environmental patterns of mutualism between plants and their root symbionts. New Phytol. 205:1503-14. DOI: https://doi.org/10.1111/nph.13239
Biro Turk K, Aljughaiman AS, 2020. Land use/land cover assessment as related to soil and irrigation water salinity over an oasis in arid environment. Open Geosci. 12:220-31. DOI: https://doi.org/10.1515/geo-2020-0103
Boudabbous Kh, Bouhaouel I, Karmous C, Benaissa N, Trifa Y, Sahli A, Slim Amara H, 2019. The variation of phosphorous content, grain yield, and rhizosphere microbial biomass among durum wheat cultivars under salinity stress. Arch. Agron. Soil Sci. 66:1721-34. DOI: https://doi.org/10.1080/03650340.2019.1691170
Boudabbous Kh, Ben Aissa N, Trifa Y, Sahli A, Slim Amara H, 2016. Soil microorganisms alleviates the negative effect of salinity on morphophysiological characteristics during growth stages of durum wheat genotypes. JNS 28:1622-30.
Bowles TM, Acosta-Martínez V, Calderón F, Jackson LE, 2014. Soil enzyme activities, microbial communities, and carbon and nitrogen availability in organic agroecosystems across an intensively-managed agricultural landscape. Soil Biol. Biochem. 68:252-62. DOI: https://doi.org/10.1016/j.soilbio.2013.10.004
Boyrahmadi M, Raiesi F, 2018. Plant roots and species moderate the salinity effect on microbial respiration, biomass, and enzyme activities in a sandy clay soil. Biol. Fert. Soils 54:509-21. DOI: https://doi.org/10.1007/s00374-018-1277-6
Brookes PC, Landman A, Pruden G, Jenkinson DS, 1985. Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol. Biochem. 7:837-42. DOI: https://doi.org/10.1016/0038-0717(85)90144-0
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W, 2019. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front. Plant Sci. 10:157. DOI: https://doi.org/10.3389/fpls.2019.00157
Chaabane R, Bchini H, Ouji H, Ben Salah H, Khamassi K, Khoufi S, Babay E, Ben Naceur M, 2011. Behaviour of Tunisian durum wheat (Triticum turgidum L.) varieties under saline stress. Pak. J. Nutr. 6:539-42. DOI: https://doi.org/10.3923/pjn.2011.539.542
Chen YX, Li HH, Zhou T, Chen XP, Huang W, Liu J, Zhang CC, Xu KW, 2013. Effects of phosphorus fertilization on leaf area index, biomass accumulation and allocation, and phosphorus use efficiency of intercropped maize. J. Appl. Ecol. 24:2799-806.
Corneo PE, Suenaga H, Kertesz MA, Dijkstra FA, 2016. Effect of twenty four wheat genotypes on soil biochemical and microbial properties. Plant Soil 404:141-55. DOI: https://doi.org/10.1007/s11104-016-2833-1
Devau N, Le Cadre E, Hinsinger P, Gérard F, 2010. A mechanistic model for understanding root-induced chemical changes controlling phosphorus availability. Ann. Bot. 105:1183-97. DOI: https://doi.org/10.1093/aob/mcq098
Diallo-Diagne NH, Assigbetse K, Sall S, Masse D, Bonzi M, Ndoye I, Chotte JL, 2016. Response of soil microbial properties to long-term application of organic and inorganic amendments in a tropical soil (Saria, Burkina Faso). OJSS 6:21-33. DOI: https://doi.org/10.4236/ojss.2016.62003
Elmajdoub B, Marschner P, 2015. Responses of soil microbial activity and biomass to salinity after repeated additions of plant residues. Pedosphere 25:177-85. DOI: https://doi.org/10.1016/S1002-0160(15)60002-9
Fageria NK, Gheyi HR, Moreira A, 2011. Nutrient bioavailability in salt affected soils. J. Plant Nutr. 34:945-62. DOI: https://doi.org/10.1080/01904167.2011.555578
Francois LE, Grieve CM, Maas EV, Lesch SM, 1994. Time of salt stress affects growth and yield components of irrigated wheat. Agron. J. 86:100-7. DOI: https://doi.org/10.2134/agronj1994.00021962008600010019x
Frankenberger WT, Bingham FT, 1982. Influence of salinity on soil enzyme activities. Soil Sci. Soc. Am. J. 46:1173-7. DOI: https://doi.org/10.2136/sssaj1982.03615995004600060011x
Frija I, Frija A, Chebil A, Cheikh M’Hamed H, Speelman S, Makhlouf M, 2014. Marginal water productivity of irrigated durum wheat in semi-arid Tunisia. J. Agr. Sci. 6:84-95. DOI: https://doi.org/10.5539/jas.v6n10p84
Glaser K, Hackl E, Inselsbacher E, Strauss J, Wanek W, Zechmeister-Boltenstern S, Sessitsch A, 2010. Dynamics of ammonia-oxidizing communities in barley-planted bulk soil and rhizosphere following nitrate and ammonium fertilizer amendment. FEMS Microbiol. Ecol. 74:575-91. DOI: https://doi.org/10.1111/j.1574-6941.2010.00970.x
Gransee A, Wittenmayer L, 2000. Qualitative and quantitative analysis of water-soluble root exudates in relation to plant species and development. J. Plant Nutr. Soil Sci. 163:381-5. DOI: https://doi.org/10.1002/1522-2624(200008)163:4<381::AID-JPLN381>3.0.CO;2-7
Guangming L, Xuechen Z, Xiuping W, Hongbo S, Jingsong Y, Xiangping W, 2017. Soil enzymes as indicators of saline soil fertility under various soil amendments. Agric. Ecosyst. Environ. 237:274-9. DOI: https://doi.org/10.1016/j.agee.2017.01.004
Hagemann M, 2011. Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol. Rev. 35:87-123. DOI: https://doi.org/10.1111/j.1574-6976.2010.00234.x
Harmsen J, 2007. Measuring bioavailability: from a scientific approach to standard methods. J. Environ. Qual. 36:1420-8. DOI: https://doi.org/10.2134/jeq2006.0492
Iannucci A, Canfora N, Nigro F, De Vita P, Beleggia R, 2021. Relationships between root morphology, root exudate compounds and rhizosphere microbial community in durum wheat. Appl. Soil Ecol. 158:103781. DOI: https://doi.org/10.1016/j.apsoil.2020.103781
İnceoğlu O, Salles JF, van Overbeek L, van Elsas JD, 2010. Effects of plant genotype and growth stage on the betaproteobacterial communities associated with different potato cultivars in two fields. Appl. Environ. Microbiol. 76:3675-84. DOI: https://doi.org/10.1128/AEM.00040-10
Jat HS, Choudharya M, Datta A, Yadav AK, Meena MD, Devi R, Gathala MK, Jat ML, McDonaldd A, Sharma PC, 2020. Temporal changes in soil microbial properties and nutrient dynamics under climate smart agriculture practices. Soil Till. Res. 199:104595. DOI: https://doi.org/10.1016/j.still.2020.104595
Jezierska-Tys S, Rachoń L, Rutkowska A, Szumiło G. 2012. Effect of new lines of winter wheat on microbiological activity in Luvisol. Int. Agrophys. 26:33-8. DOI: https://doi.org/10.2478/v10247-012-0005-y
Jin K, Sleutel S, Buchan D, De Neve S, Cai DX, Gabriels D, Jin JY, 2009. Changes of soil enzyme activities under different tillage practices in the Chinese Loess Plateau. Soil Till. Res. 104:115-20. DOI: https://doi.org/10.1016/j.still.2009.02.004
Jingguo W, Bakken LR, 1997. Competition for nitrogen during mineralization of plant residues in soil: microbial response to C and N availability. Soil Biol. Biochem. 29:163-70. DOI: https://doi.org/10.1016/S0038-0717(96)00292-1
Junaidi J, Kallenbach CM, Byrne PF, Fonte SJ, 2018. Root traits and root biomass allocation impact how wheat genotypes respond to organic amendments and earthworms. PLoS One 7:e0200646. DOI: https://doi.org/10.1371/journal.pone.0200646
Karasawa T, Takebe M, Sato F, Komada M, Nagaoka K, Takenaka M, Urashima Y, Nishimura S, Takahashi S, Kato N, 2015. Trends of lettuce and carrot yields and soil enzyme activities during transition from conventional to organic farming in an Andosol. Soil Sci. Plant Nutr. 61:295-311. DOI: https://doi.org/10.1080/00380768.2014.985577
Kumar S, Chaudhuri S, Maiti SK, 2013. Soil dehydrogenase activity in natural and mine soil - A review. Mid. E. J. Sci. Res. 13:898-906.
Ladd JN, Butler JHA, 1972. Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol. Biochem. 4:19-30. DOI: https://doi.org/10.1016/0038-0717(72)90038-7
Liu W, Wang J, Wang C, Ma G, Wei Q, Lu H, Xie Y, Ma D, Kang G, 2018. Root growth, water and nitrogen use efficiencies in winter wheat under different irrigation and nitrogen regimes in north China plain. Front. Plant Sci. 9:1798. DOI: https://doi.org/10.3389/fpls.2018.01798
Lu H, Lashari MS, Liu X, Ji H, Li L, Zheng J, Kibue GW, Joseph S, Pan G, 2015. Changes in soil microbial community structure and enzyme activity with amendment of biochar-manure compost and pyroligneous solution in a saline soil from Central China. Eur. J. Soil Biol. 70:67-76. DOI: https://doi.org/10.1016/j.ejsobi.2015.07.005
Mandal A, Patra AK, Singh D, Swarup A, Masto RE, 2007. Effect of long-term application of manure and fertilizer on biological and biochemical activities in soil during crop development stages. Bioresour. Technol. 98:3585-92. DOI: https://doi.org/10.1016/j.biortech.2006.11.027
Maseko ST, Dakora FD, 2013. Rhizosphere acid and alkaline phosphatase activity as a marker of Pb nutrition in nodulated Cyclopia and Aspalathus species in the Cape fynbos of South Africa. S. Afr. J. Bot. 89:289-95. DOI: https://doi.org/10.1016/j.sajb.2013.06.023
Mikanová O, Šimon T, Javůrek M, Vach M, 2012. Relationships between winter wheat yields and soil carbon under various tillage systems. Plant Soil. Environ. 58:540-4. DOI: https://doi.org/10.17221/512/2012-PSE
Munns R, James RA, Läuchli A, 2006. Approaches to increasing the salt tolerance of wheat and other cereals. J. Exp. Bot. 57:1025-43. DOI: https://doi.org/10.1093/jxb/erj100
Olsen SR, Cole CV, Watanabe FS, Dean LA, 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. Circular 939. U.S. Dept of Agriculture, Washington, DC, USA.
Petard J, 1993. Soil analysis methods-Tome I (in French). IRD. ORSTOM, Nouméa, France.
Rassaa N, Bnejdi F, Chalh A, El Gazzah M, 2012. The validity of using juvenile stages for evaluation of salt stress tolerance of Triticum durum genotypes. Afr. J. Biotechnol. 9:2178-2189. DOI: https://doi.org/10.5897/AJB11.536
Sayar R, Bchini H, Mosbahi M, Ezzine M, 2010. Effects of salt and drought stresses on germination, emergence and seedling growth of durum wheat (Triticum durum Desf.). J. Agric. Res. 5:2008-16.
Shahbaz M, Ashraf M, 2013. Improving salinity tolerance in cereals. Crit. Rev. Plant Sci. 32:237-49. DOI: https://doi.org/10.1080/07352689.2013.758544
Silva AP, Babujia LC, Franchini JC, Souza RA, Hungria M, 2010. Microbial biomass under various soil- and crop-management systems in short- and long-term experiments in Brazil. Field Crop Res. 119:20-26. DOI: https://doi.org/10.1016/j.fcr.2010.06.012
Singh K, 2016. Microbial and enzyme activities of saline and sodic soils. Land Degrad. Dev. 27:706-18. DOI: https://doi.org/10.1002/ldr.2385
Slim A, Piarulli L, Kourda HC, Rouaissi M, Robbana C, Chaabane R, Pignone D, Montemurro C, Mangini G, 2019. Genetic structure analysis of a collection of Tunisian durum wheat germoplasm. Int. J. Mol. Sci. 20:3362. DOI: https://doi.org/10.3390/ijms20133362
Tabatabai MA, Bremner JM, 1969. Use of p-nitrophenol phosphate for the assay of soil phosphatase activity. Soil Biol. Biochem. 1:301-7. DOI: https://doi.org/10.1016/0038-0717(69)90012-1
Tamilselvi SM, Chinnadurai C, Ilamurugu K, Arulmozhiselvan K, Balachandar D, 2015. Effect of long-term nutrient managements on biological and biochemical properties of semi-arid tropical Alfisol during maize crop development stages. Ecol. Indic. 48:76-87. DOI: https://doi.org/10.1016/j.ecolind.2014.08.001
USDA, 2013. Soil classification: A comprehensives system (prepared by) soil survey staff. Government Printing Office, Washington, USA.
Vance ED, Brookes PC, Jenkinson DS, 1987. An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19:703-7. DOI: https://doi.org/10.1016/0038-0717(87)90052-6
Walkley A, Black IA, 1934. An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci. 37:29-38. DOI: https://doi.org/10.1097/00010694-193401000-00003
Wang X, Tang C, 2018. The role of rhizosphere pH in regulating the rhizosphere priming effect and implications for the availability of soil-derived nitrogen to plants. Ann. Bot. 121:143-51. DOI: https://doi.org/10.1093/aob/mcx138
Waring SA, Bremner JM, 1964. Ammonium production in soil under waterlogged conditions as an index of nitrogen availability. Nature 201:951-2. DOI: https://doi.org/10.1038/201951a0
Wei T, Simko V, Levy M, Xie Y, Jin Y, Zemla J, 2017. Package ‘corrplot’. Statistician 56:316-24.
Wickham H, 2009. ggplot2: Elegant graphics for data analysis. Springer Science + Business, Media LLC, Berlin, Germany.
Zadoks JC, Chang TT, Konzak CF, 1974. A decimal code for the growth stages of cereals. Weed Res. 14:415-21. DOI: https://doi.org/10.1111/j.1365-3180.1974.tb01084.x
Zhang WW, Wang C, Xue R, Wang LJ, 2019. Effects of salinity on the soil microbial community and soil fertility. J. Integr. Agric. 18:1360-8. DOI: https://doi.org/10.1016/S2095-3119(18)62077-5
Zhou M, Butterbach-Bahl K, Vereecken H, Brüggemann N, 2017. A meta-analysis of soil salinization effects on nitrogen pools, cycles and fluxes in coastal ecosystems. Glob. Chang. Biol. 23:1338-52. DOI: https://doi.org/10.1111/gcb.13430
Zhu S, Huang X, Ho S-H, Wang L, Yang J, 2017. Effect of plant species compositions on performance of lab-scale constructed wetland through investigating photosynthesis and microbial communities. Bioresour. Technol. 229:196-203. DOI: https://doi.org/10.1016/j.biortech.2017.01.023
Zuo S, Li X, Ma Y, Yang S, 2014. Soil microbes are linked to the allelopathic potential of different wheat genotypes. Plant Soil 378:49-58. DOI: https://doi.org/10.1007/s11104-013-2020-6

How to Cite

Boudabbous, K., Bouhaouel , I., Benaissa, N. . ., Jerbi, M., Trifa, Y. ., Sahli, A. ., Karmous, C. ., & Amara, H. S. (2022). Durum wheat salt stress tolerance is modulated by the interaction between plant genotypes, soil microbial biomass, and enzyme activity. Italian Journal of Agronomy, 17(1). https://doi.org/10.4081/ija.2022.1942
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