Deciphering the Potential Role of Symbiotic Plant Microbiome and Amino Acid Application on Growth Performance of Chickpea Under Field Conditions
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
35646024
PubMed Central
PMC9134094
DOI
10.3389/fpls.2022.852851
Knihovny.cz E-zdroje
- Klíčová slova
- L-methionine, PGPR, Rhizobium, chickpea, plant-microbe interaction,
- Publikační typ
- časopisecké články MeSH
The unprecedented rise in the human population has increased pressure on agriculture production. To enhance the production of crops, farmers mainly rely on the use of chemical fertilizers and pesticides, which have, undoubtedly, increased the production rate but at the cost of losing sustainability of the environment in the form of genetic erosion of indigenous varieties of crops and loss of fertile land. Therefore, farming practices need to upgrade toward the use of biological agents to maintain the sustainability of agriculture and the environment. In this context, using microbial inoculants and amino acids may present a more effective, safer, economical, and sustainable alternative means of realizing higher productivity of crops. Therefore, field experiments were performed on chickpea for two succeeding years using Rhizobium and L-methionine (at three levels, i.e., 5, 10, and 15 mg L-1) separately and in combinations. The results show that the application of Rhizobium and all the three levels of L-methionine increased the growth and yield of chickpea. There was a higher response to a lower dose of L-methionine, i.e., 5 mg L-1. It has been found that maximum grain yield (39.96 and 34.5% in the first and second years, respectively) of chickpea was obtained with the combined use of Rhizobium and L-methionine (5 mg L-1). This treatment was also the most effective in enhancing nodule number (91.6 and 58.19%), leghemoglobin (161.1 and 131.3%), and protein content (45.2 and 45%) of plants in both years. Likewise, photosynthetic pigments and seed chemical composition were significantly improved by Rhizobium inoculation. However, these effects were prominent when Rhizobium inoculation was accompanied by L-methionine. In conclusion, utilizing the potential of combined use of L-methionine and microbial inoculant could be a better approach for developing sustainable agriculture production.
Agricultural Research Ltd Troubsko Czechia
Department of Botany and Microbiology College of Science King Saud University Riyadh Saudi Arabia
Department of Entomology University of Agriculture Faisalabad Pakistan
Institute for Environmental Studies Faculty of Science Charles University Prague Prague Czechia
Institute of Soil and Environmental Sciences University of Agriculture Faisalabad Pakistan
Soil Bacteriology Section Ayub Agricultural Research Institute Faisalabad Pakistan
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Abbas T., Zahir Z. A., Naveed M., Kremer R. J. (2018). Limitations of existing weed control practices necessitate development of alternative approaches based on biological techniques. Adv. Agron. 147 239–280. 10.1016/bs.agron.2017.10.005 DOI
Abd El-Aal M. (2018). Effect of foliar spray with lithovit and amino acids on growth, bioconstituents, anatomical and yield features of soybean plant. Ann. Agric. Sci. Moshtohor. 56 187–202. 10.21608/assjm.2018.65137 DOI
Abdullahi A. A., Howieson J., O’Hara G., Tepolilli J., Vivas-Marfisi A., Yusuf A. A. (2013). “History of Rhizobia inoculants use for grain legumes improvement in Nigeria—the journey so far,” in N2 Africa Project. N2013 Kampala Conference Paper, (Kampala: ).
Abere M., Heluf G., Fassil A. (2009). Symbiotic effectiveness and characterization of Rhizobium strains of faba bean (Vicia fabaL.) collected from eastern and western Hararghe highlands ofEthiopia. Ethiopian J. Nat. Resour. 11 223–244.
Ahmad M., Naseer I., Hussain A., Zahid Mumtaz M., Mustafa A., Hilger T. H., et al. (2019). Appraising endophyte–plant symbiosis for improved growth, nodulation, nitrogen fixation and abiotic stress tolerance: an experimental investigation with chickpea (Cicer arietinum L.). Agronomy 9:621. 10.3390/agronomy9100621 DOI
Alemayehu W. (2006). Symbiotic and Phenotypic Characterization of Common Bean Nodulating Rhizobia from Some Area of Southern ETHIOPIA. M.S. thesis in Biology. Addis Ababa: Addis Ababa University.
Ali M. A., Naveed M., Mustafa A., Abbas A. (2017). “The good, the bad, and the ugly of the rhizosphere microbiome,” in Probiotics and Plant Health, eds Kumar V., Kumar M., Parsad R., Choudry D. K. (Singapore: Springer; ), 253–290. 10.1007/978-981-10-3473-2_11 DOI
Anne C., Thomas S. (2015). Regulation of chloroplast development and function by cytokinin. J. Exp. Bot. 66 4999–5013. 10.1093/jxb/erv132 PubMed DOI
Arnon I. D. (1949). Copper enzymes in isolated chloroplast. Polyphenol oxidase in Beta vulgaris. Plant Physiol. 24 11–15. 10.1104/pp.24.1.1 PubMed DOI PMC
Bahari A., Pirdashti H., Yaghubi M. (2013). The effects of amino acid fertilizers spraying on photosynthetic pigments and antioxidant enzymes of wheat (Triticum aestivum L.) under salinity stress. Int. J. Agron. Plant Prod. 4 787–793.
Beck D. P., Materon L. A., Afandi F. (1993). Practical Rhizobium Legume Technology Manual, Vol. 19. Aleppo: Technical Manual International Center for Agricultural Research in the Dry Areas (ICARDA).
Calvo P., Nelson L., Kloepper J. (2014). Agricultural uses of plant biostimulants. Plant Soil 383 3–41. 10.1007/s11104-014-2131-8 DOI
Colla G., Cardarelli M., Bonini P., Rouphael Y. (2017). Foliar applications of protein hydrolysate, plant and seaweed extracts increase yield but differentially modulate fruit quality of greenhouse tomato. HortScience 52 1214–1220. 10.21273/HORTSCI12200-17 DOI
Datta C., Basu P. S. (2000). Indole acetic acid production by a Rhizobium species from root nodules of a leguminous shrub, Cajanus cajan. Microbiol. Res. 155 123–127. 10.1016/S0944-5013(00)80047-6 PubMed DOI
Davies P. J. (2004). Plant Hormones: Biosynthesis, Signal Transduction, Action!. New York, NY: Springer.
Deora G. S., Singal K. (2010). Isolation, biochemical characterization, and preparation of biofertilizers using Rhizobium strain for commercial use. Biosci. Biotech. Res. Comm. 3 132–136.
Drennan D. S. H., Norton C. (1972). The effect of ethrel on nodulation in Pisum sativum L. Plant Soil 36 53–57. 10.1007/BF01373456 DOI
du Jardin P. (2015). Plant biostimulants: definition, concept, main categories and regulation. Sci. Hortic. 196 3–14. 10.1016/j.scienta.2015.09.021 DOI
El-Azeem S. A. A., Mehana T. A., Shabayek A. A. (2007). Response of faba bean (Vicia fabaL.) to inoculation with plant growth-promoting rhizobacteria. Catrina 2 67–75.
El-sharabasy S., Fatma I., Gehan H., El-Dawayaty M. (2015). Effect of different amino acids at different concentrations on multiplication and rooting stage of in vitro propagation of strawberries (Fragaria X Ananassa Duch cv. Chandler). Egypt. J. Genet. Cytol. 44, 31–34.
Farfour A. S. (2013). Enhancement of the growth and phenolic content of faba bean (Vicia fabaL.) by applying some biofertilizer agents. J. Food Stud. 2013 20–30. 10.5296/jfs.v2i2.4425 DOI
Fawzy Z., El-Shal Z., Yunsheng L., Zhu O., Sawan O. M. (2012). Response of garlic (Allium Sativum L.) plants to foliar spraying of some bio-stimulants under sandy soil conditions. J. Appl. Sci. Res. 8 770–776.
Forde B. G., Roberts M. R. (2014). Glutamate receptor-like channels in plants: A role as amino acid sensors in plant defense? F1000Prime Rep. 6:37. 10.12703/P6-37 PubMed DOI PMC
Gebremariam A., Assefa F. (2018). The effect of inter cross-inoculation host group rhizobia on the growth and nitrogen fixation of faba Bean (Vicia faba L.) varieties in North Showa, Amhara Regional State, Ethiopia. J. Agric. Biotechnol. Sustain Dev. 10 25–33. 10.5897/JABSD2018.0307 DOI
Ghosh P. K., Saha P., Mayilraj S., Maiti T. K. (2013). Role of IAA metabolizing enzymes on production of IAA in root, nodule of Cajanus cajan and its PGP Rhizobium sp. Biocatal. Agric. Biotechnol. 2 234–239. 10.1016/j.bcab.2013.04.002 DOI
Ghosh S., Basu P. S. (2006). Production and metabolism of indole acetic acid in roots and root nodules of Phaseolus mungo. Microbiol. Res. 161 362–366. 10.1016/j.micres.2006.01.001 PubMed DOI
Gibson A. H. (1987). “Evaluation of nitrogen fixation by legumes in the greenhouse and growth chamber,” in SymbioticNitrogen Fixation Technology, ed. Gibson A. H. (New York, NY: Marcel Dekker; ), 321–363.
Giose E., de Neergaard A., Schjorring J. K. (2012). Interactions between uptake of amino acids and inorganic nitrogen in wheat plants. Biogeosciences 9 1509–1518. 10.1093/pcp/pcw131 PubMed DOI
Goodlass G., Smith K. A. (1979). Effect of ethylene on root extension and nodulation of pea (Pisum sativum L.) and white clover (Trifolium repens L.). Plant Soil 51 387–395. 10.1007/BF02197785 DOI
Graham P., Sadowsky M. J., Keyser H. H. (1991). Proposed minimal standards for the description of new genera of roots and stem nodulating bacteria. Syst. Bacteriol. 41 582–587. 10.1099/00207713-41-4-582 DOI
Graham P. H., Hungria M., Tlusty B. (2004). Breeding for better nitrogen fixation in grain legumes: where do the rhizobia fit in? Crop Manag. 3 1–6. 10.1094/CM-2004-0301-02-RV DOI
Grobbelaar N., Clarke B., Hough M. C. (1971). The nodulation and nitrogen fixation of isolated roots of Phaseolus vulgar&L. Plant Soil 35 215–223. 10.1007/BF02661852 DOI
Gwata E. T., Wofford D., Boote S. K. J., Mushoriwa H. (2003). Determination of effective nodulation in early juvenile soybean plants for genetic and biotechnology studies. Afr. J. Biotechnol. 2, 417–420. 10.5897/AJB2003.000-1083 DOI
Hajnaa A. (1945). Triple-Sugar Iron Medium for the identification of the intestinal group of bacteria. J. Bacteriol. 49 516–517. 10.1128/jb.49.5.516-517.1945 PubMed DOI PMC
Halpern M., Bar-Tal A., Ofek M., Minz D., Muller T., Yermiyahu U. (2015). “The use of biostimulants for enhancing nutrient uptake,” in Advances in Agronomy, Vol. 130 ed. Sparks D. L. (New York, NY: Academic Press; ), 141–174. 10.1016/bs.agron.2014.10.001 DOI
Herridge D. F., Peoples M. B., Boddey R. M. (2008). Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311 1–18. 10.1007/s11104-008-9668-3 DOI
Hildebrandt T. M., Nesi A. N., Araújo W. L., Braun H.-P. (2015). Amino acid catabolism in plants. Mol. Plant. 8 1563–1579. 10.1016/j.molp.2015.09.005 PubMed DOI
Hunter W. J. (1989). Indole-3-acetic acid production by bacteroid from soyabean root nodules. Plant Physiol. 76 31–36. 10.1111/j.1399-3054.1989.tb05448.x DOI
Jida M., Assefa F. (2011). Phenotypic and plant growth promoting characteristics of rhizobium leguminosarumbv. viciae from lentil growing areas of Ethiopia. Afr. J. Microbiol. Res. 5 4133–4142. 10.5897/AJMR11.400 DOI
Jida M., Assefa F. (2012). Phenotypic diversity and plant growth-promoting characteristics of Mesorhizobium species isolated from faba bean (Vicia faba L.) growing areas of Ethiopia. Afr. J. Biotechnol. 11 7483–7493.
John S. J., Guha-Mukherjee S. (1997). Plant Molecular Biology and Biotechnology, 1st Edn. New Delhi: Narosa Publishing House, 17–28.
Kakkar R., Nagar P., Ahuja P., Rai V. (2000). Polyamines and plant morphogenesis. Biol. Plant. 43 1–11. 10.1023/A:1026582308902 DOI
Kasole K. E., Kalke S. D., Kareepa S. M., Khade K. K. (2005). Response of chickpea to different fertilizer levels, plant population, and weed management on cultivators field in the northeastern part of Kohlapur, Maharashtara. Indian J. Agron. 40 217–219.
Keneni A., Assefa F., Prabu P. C. (2010). Characterization of acid and salt-tolerant rhizobial strains isolated from faba bean fields of Wollo, Northern Ethiopia. J. Agric. Sci. Technol. 12 365–376.
Khan N., Ali S., Shahid M. A., Mustafa A., Sayyed R. Z., Curá J. A. (2021). Insights into the interactions among roots, rhizosphere, and rhizobacteria for improving plant growth and tolerance to abiotic stresses: a review. Cells 10:1551. 10.3390/cells10061551 PubMed DOI PMC
Khan N., Bano A., Zandi P. (2018). Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. J. Plant Interact. 13 239–247. 10.1080/17429145.2018.1471527 DOI
Khan N. A. (2005). The influence of exogenous ethylene on growth and photosynthesis of mustard (Brassica juncea) following defoliation. Sci. Hortic. 105 499–505. 10.1016/j.scienta.2005.02.004 DOI
Khan N. A., Mir M. R., Nazar R., Singh S. (2008). The application of ethephon (an ethylene releaser) increases growth, photosynthesis and nitrogen accumulation in mustard (Brassica juncea L.) under high nitrogen levels. Plant Biol. 10 534–538. 10.1111/j.1438-8677.2008.00054.x PubMed DOI
Khan S., Yu H., Li Q., Gao Y., Sallam B. N., Wang H., et al. (2019). Exogenous application of amino acids improves the growth and yield of lettuce by enhancing photosynthetic assimilation and nutrient availability. Agronomy 9:266. 10.3390/agronomy9050266 DOI
Koskey G., Mburu S. W., Awino R., Njeru E. M., Maingi J. M. (2021). Potential use of beneficial microorganisms for soil amelioration, phytopathogen biocontrol, and sustainable crop production in smallholder agroecosystems. Front. Sustain. Food Syst. 5:606308. 10.3389/fsufs.2021.606308 DOI
Kowalczyk K., Zielony T., Gajewski M. (2008). “Effect of aminoplant and asahi on yield and quality of lettuce grown on rockwool,” in Monographs Series: Biostimulators in Modern Agriculture: Solanaceous Crops, ed. Dabrowski Z. T. (Warsaw: Editorial House Wies Jutra; ), 35–43.
Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. (1951). Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193 265–275. 10.1016/S0021-9258(19)52451-6 PubMed DOI
Maeda H., Dudareva N. (2012). The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol. 63 73–105. 10.1146/annurev-arplant-042811-105439 PubMed DOI
Makoi J. H., Bambara S., Ndakidemi P. A. (2013). Rhizobium inoculation and the supply of Molybdenum and lime affect the uptake of macro elements in common bean (P. vulgaris L.) plants. Aust. J. Crop Sci. 7 784–793.
Matse D. T., Huang C., Huang Y., Yen M. (2020). Effects of coinoculation of Rhizobium with plant growth promoting rhizobacteria on the nitrogen fixation and nutrient uptake of Trifolium repens in low phosphorus soil. J. Plant Nutr. 43 739–752. 10.1080/01904167.2019.1702205 DOI
Miller A. J., Fan X., Shen Q., Smith S. J. (2007). Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J. Exp. Bot. 59 111–119. 10.1093/jxb/erm208 PubMed DOI
Mirani Z. A., Jamil N. (2011). Effect of sub-lethal doses of vancomycin and oxacillin on biofilm formation by vancomycin intermediate resistant Staphylococcus aureus. J. Basic Microbiol. 51 191–195. 10.1002/jobm.201000221 PubMed DOI
Naseem H., Ahsan M., Shahid M. A., Khan N. (2018). Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. J. Basic Microbiol. 58 1009–1022. 10.1002/jobm.201800309 PubMed DOI
Naveed M., Mitter B., Yousaf S., Pastar M., Afzal M., Sessitsch A. (2014). The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol. Fertil. Soils 50 249–262. 10.1007/s00374-013-0854-y DOI
Nawaz M. A., Chen C., Shireen F., Zheng Z., Sohail H., Afzal M., et al. (2018). Genome-wide expression profiling of leaves and roots of watermelon in response to low nitrogen. BMC Genom. 19:456. 10.1186/s12864-018-4856-x PubMed DOI PMC
Nazli F., Mustafa A., Ahmad M., Hussain A., Jamil M., Wang X., et al. (2020). A review on practical application and potentials of phytohormone-producing plant growth-promoting rhizobacteria for inducing heavy metal tolerance in crops. Sustainability 12:9056. 10.3390/su12219056 DOI
Odee D. W., Sutherland J. M., Makatiani E. T., McInroy S. G., Sprent J. (1997). Phenotypic characteristics and composition of rhizobia associated with woody legumes growing in diverse Kenyan conditions. Plant Soil 188 65–75. 10.1023/A:1004204413140 DOI
Paciorek T., Zazímalová E., Ruthardt N., Petrásek J., Stierhof Y. D., Kleine-Vehn J., et al. (2005). Auxin inhibits endocytosis and promotes its own e_ux from cells. Nature 435 1251–1256. 10.1038/nature03633 PubMed DOI
Paulo E. M., Boffo E., Branco A., Ângela M., Valente M. P., Itamar S., et al. (2012). Production, extraction and characterization of exopolysaccharides produced by the native Leuconostoc pseudomesenteroides R2 strain. Ann. Braz. Acad. Sci. 84, 495–507. PubMed
Pikovskya R. I. (1948). Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Microbiology 17 362–370.
Price C. A. (2012). Leaf Gui: analyzing the geometry of veins and areoles using image segmentation algorithms. Methods Mol. Biol. 918 41–49. 10.1007/978-1-61779-995-2_4 PubMed DOI
Rafique M., Naveed M., Mustafa A., Akhtar S., Munawar M., Kaukab S., et al. (2021). The combined effects of gibberellic acid and rhizobium on growth, yield and nutritional status in chickpea (Cicer arietinum L.). Agronomy 11:105. 10.3390/agronomy11010105 DOI
Riccillo P. M., Muglia C. I., de Bruijn F., Booth I. R., Aguilar O. M. (2000). Aguilar Glutathione is involved in environmental stress responses in Rhizobium tropici, including acid tolerance. J. Bacteriol. 182 1748–1753. 10.1128/JB.182.6.1748-1753.2000 PubMed DOI PMC
Romero I., Téllez J., Yamanaka L. E., Steindel M., Romanha A. J., Grisard E. C. (2014). Transsulfuration is an active pathway for cysteine biosynthesis in Trypanosoma rangeli. Parasites Vectors 7:197. 10.1186/1756-3305-7-197 PubMed DOI PMC
Rosati A., Day K., DeJong T. (2000). Distribution of leaf mass per unit area and leaf nitrogen concentration determine partitioning of leaf nitrogen within tree canopies. Tree Physiol. 20 271–276. 10.1093/treephys/20.4.271 PubMed DOI
Rouphael Y., Colla G., Giordano M., El-Nakhel C., Kyriacou M. C., De Pascale S. (2017). Foliar applications of a legume-derived protein hydrolysate elicit dosedependent increases of growth, leaf mineral composition, yield and fruit quality in two greenhouse tomato cultivars. Sci. Hortic. 226 353–360. 10.1016/j.scienta.2017.09.007 DOI
Rouphael Y., Spíchal L., Panzarová K., Casa R., Colla G. (2018). High-throughput plant phenotyping for developing novel biostimulants: from lab to field or from field to lab? Front. Plant Sci. 9:1197. 10.3389/fpls.2018.01197 PubMed DOI PMC
Rudresh D. L., Shivaprakasha M. K., Prasad R. D. (2005). Effect of combined application of Rhizobium, phosphate solubilizing bacterium and Trichoderma spp. on growth, nutrient uptake and yield of chickpea (Cicer aritenium L.). Appl. Soil Ecol. 28 139–146. 10.1016/j.apsoil.2004.07.005 DOI
Sadak S. H. M., Abdelhamid M. T., Schmidhalter U. (2014). Effect of foliar application of aminoacids on plant yield and some physiological parameters in bean plants irrigated with seawater. Acta Biol. Colomb. 20 141–152. 10.15446/abc.v20n1.42865 DOI
Sadak S. H. M., Abdelhamid M. T., Schmidhalter U. (2015). Effect of foliar application of aminoacids on plant yield and physiological parameters in bean plants irrigated with seawater. Acta Biol. Colomb. 20 141–152. 10.15446/abc.v20n1.42865 DOI
Sadasivan S., Manickam A. (2008). Biochemical Methods, 3rd Edn. New Delhi: New Age International.
Saeed Q., Xiukang W., Haider F. U., Kučerik J., Mumtaz M. Z., Holatko J., et al. (2021). Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. Int. J. Mol. Sci. 22:10529. 10.3390/ijms221910529 PubMed DOI PMC
Santi C., Zamboni A., Varanini Z., Pandolfini T. (2017). Growth stimulatory effects and genome-wide transcriptional changes produced by protein hydrolysates in maize seedlings. Front. Plant Sci. 8:433. 10.3389/fpls.2017.00433 PubMed DOI PMC
Sarwar M., Arshad M., Martens W. T., Frankenberger J. R. (1992). Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147 207–215. 10.1007/BF00029072 DOI
Scheible W.-R., Morcuende R., Czechowski T., Fritz C., Osuna D., Palacios-Rojas N., et al. (2004). Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136, 2483–2499. 10.1104/pp.104.047019 PubMed DOI PMC
Sidhu G. S., Singh N., Singh R. (1967). Symbiotic nitrogen fixation by some summer legumes in Punjab. Role of leghemoglobin in nitrogen fixation. J. Res. Punjab Agric. Univ. 4 244–248.
Singh A. K., Choudry R. K., Sharma R. P. R. (2003). Effect of inoculation and fertilizer level on yield, nutrient up take and economics of summer pulses. J. Potassium Res. 9 175–178.
Skerman V. B. D. (1959). A Guide to the Identification of the Genera of Bacteria with Methods and Digests of Generic Characteristics. Baltimore, MD: TheWilliams and Wilkins.
Somasegaran P., Hoben H. J. (1994). Handbook for Rhizobia: Methods in Legume-RhizobiumTechnology. New York, NY: Springer. 10.1007/978-1-4613-8375-8 DOI
Steel R. G. D., Torrie J. H., Dicky D. A. (1997). Principles and Procedures of Statistics—A Biometrical Approach, 3rd Edn. Singapore: McGraw-Hill Book International Co.
Tariq M., Khan A., Asif M., Khan F., Ansari T., Shariq M., et al. (2020). Biological control: a sustainable and practical approach for plant disease management. Acta Agricult. Scand. Sect. B Soil Plant Sci. 70 507–524. 10.1080/09064710.2020.1784262 DOI
Tatjana M. H., Adriano N. N., Wagner L. A., Hans P. B. (2015). Amino acid catabolism in plants. Mol. Plant 8 1563–1579. 10.1016/j.molp.2015.09.005 PubMed DOI
Teixeira W. F., Fagan E. B., Soares L. H., Umburanas R. C., Reichardt K., Neto D. D. (2017). Foliar and seedapplication of amino acids affects the antioxidant metabolism of the soybean crop. Front. Plant Sci. 8:327. 10.3389/fpls.2017.00327 PubMed DOI PMC
Thilakarathna M. S., Chapagain T., Ghimire B., Pudasaini R., Tamang B. B., Gurung K., et al. (2019). Evaluating the effectiveness of Rhizobium inoculants and micronutrients as technologies for Nepalese common bean smallholder farmers in the real-world context of highly variable hillside environments and indigenous farming practices. Agriculture 9:20. 10.3390/agriculture9010020 DOI
Tsavkelova E. A., Cherdyntseva T. A., Botina S. G., Netrusov A. I. (2007). Bacteria associated with orchid roots and microbial production of auxin. Microbiol. Res. 162 69–76. 10.1016/j.micres.2006.07.014 PubMed DOI
Umar W., Ayub M. A., Rehman M. Z., Ahmad H. R., Farooqi Z. U. R., Shahzad A., et al. (2020). “Nitrogen and phosphorus use efficiency in agroecosystems,” in Resources Use Efficiency in Agriculture, eds Kumar S., Meena R. S., Jhariya M. K. (Singapore: Springer; ), 213–257.
Vincent J. M. (1970). A Manual for the Practical Study of Root-Nodule Bacteria; IBP Handbook No. 15. Oxford: Blackwell.
Vincill E. D., Bieck A. M., Spalding E. P. (2012). Ca2+ conduction by an amino acid-gated ion channel related to glutamate receptors. Plant Physiol. 159 40–46. 10.1104/pp.112.197509 PubMed DOI PMC
Voisin A. S., Salon C., Warembourg F. R. (2003). Seasonal patterns of 13C partitioning between shoot and nodulated roots of N2-or nitrate fed- Pisum sativum (L). Ann. Bot. 91 539–546. 10.1093/aob/mcg055 PubMed DOI PMC
Walch-Liu P., Forde B. G. (2007). L-Glutamate as a novel modifier of root growth and branching: what’s the sensor? Plant Signal. Behav. 2 284–286. 10.4161/psb.2.4.4016 PubMed DOI PMC
Weiland M., Mancuso S., Baluska F. (2016). Signalling via glutamate and GLRs in Arabidopsis thaliana. Funct. Plant Biol. 43 1–25. 10.1071/FP15109 PubMed DOI
Wolde-meskel E., van Heerwaarden J., Abdulkadir B., Kassa S., Aliyi I., Degefu T., et al. (2018). Additive yield response of chickpea (Cicer arietinum L.) to rhizobium inoculation and phosphorus fertilizer across smallholder farms in Ethiopia. Agric. Ecosyst. Environ. 261 144–152. 10.1016/j.agee.2018.01.035 PubMed DOI PMC
Wolf B. A. (1982). Comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commn. Soil Sci. Plant Anal. 13 1035–1059. 10.1080/00103628209367332 DOI
Yadav A. N., Kour D., Kaur T., Devi R., Yadav A., Dikilitas M., et al. (2021). Biodiversity, and biotechnological contribution of beneficial soil microbiomes for nutrient cycling, plant growth improvement and nutrient uptake. Biocatal. Agric. Biotechnol. 33:102009. 10.1016/j.bcab.2021.102009 DOI
Yong J. W. H., Letham S. D., Wong C. S., Graham D. F. (2014). Rhizobium-induced elevation in xylem cytokinin delivery in pigeon pea induces changes in shoot development and leaf physiology. Funct. Plant Biol. 41 1323–1335. 10.1071/FP14066 PubMed DOI
Yuan L., Yuan Y., Du J., Sun J., Guo S. (2012). Effects of 24-epibrassinolide on nitrogen metabolism in cucumber seedlings under Ca(NO3)2 stress. Plant Physiol. Biochem. 61 29–35. 10.1016/j.plaphy.2012.09.004 PubMed DOI
Zahran H. H. (1999). Conditions for successful Rhizobium-legume symbiosis in saline environments. Biol. Fertil. Soils 12 73–80. 10.1007/BF00369391 DOI