Full Text:   <1590>

Summary:  <1021>

Suppl. Mater.: 

CLC number: S52

On-line Access: 2017-01-26

Received: 2015-11-03

Revision Accepted: 2016-05-02

Crosschecked: 2017-01-04

Cited: 2

Clicked: 3083

Citations:  Bibtex RefMan EndNote GB/T7714

 ORCID:

In-Jung Lee

http://orcid.org/0000-0001-7154-4820

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2017 Vol.18 No.2 P.109-124

http://doi.org/10.1631/jzus.B1500262


Additive effects due to biochar and endophyte application enable soybean to enhance nutrient uptake and modulate nutritional parameters


Author(s):  Muhammad Waqas, Yoon-Ha Kim, Abdul Latif Khan, Raheem Shahzad, Sajjad Asaf, Muhammad Hamayun, Sang-Mo Kang, Muhammad Aaqil Khan, In-Jung Lee

Affiliation(s):  School of Applied Biosciences, Kyungpook National University, Daegu 702-701, Korea; more

Corresponding email(s):   ijlee@knu.ac.kr

Key Words:  Phytohormone-producing endophytic fungi, Nutrients uptake, Assimilation, Nutritional quality, Soybean


Muhammad Waqas, Yoon-Ha Kim, Abdul Latif Khan, Raheem Shahzad, Sajjad Asaf, Muhammad Hamayun, Sang-Mo Kang, Muhammad Aaqil Khan, In-Jung Lee. Additive effects due to biochar and endophyte application enable soybean to enhance nutrient uptake and modulate nutritional parameters[J]. Journal of Zhejiang University Science B, 2017, 18(2): 109-124.

@article{title="Additive effects due to biochar and endophyte application enable soybean to enhance nutrient uptake and modulate nutritional parameters",
author="Muhammad Waqas, Yoon-Ha Kim, Abdul Latif Khan, Raheem Shahzad, Sajjad Asaf, Muhammad Hamayun, Sang-Mo Kang, Muhammad Aaqil Khan, In-Jung Lee",
journal="Journal of Zhejiang University Science B",
volume="18",
number="2",
pages="109-124",
year="2017",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1500262"
}

%0 Journal Article
%T Additive effects due to biochar and endophyte application enable soybean to enhance nutrient uptake and modulate nutritional parameters
%A Muhammad Waqas
%A Yoon-Ha Kim
%A Abdul Latif Khan
%A Raheem Shahzad
%A Sajjad Asaf
%A Muhammad Hamayun
%A Sang-Mo Kang
%A Muhammad Aaqil Khan
%A In-Jung Lee
%J Journal of Zhejiang University SCIENCE B
%V 18
%N 2
%P 109-124
%@ 1673-1581
%D 2017
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1500262

TY - JOUR
T1 - Additive effects due to biochar and endophyte application enable soybean to enhance nutrient uptake and modulate nutritional parameters
A1 - Muhammad Waqas
A1 - Yoon-Ha Kim
A1 - Abdul Latif Khan
A1 - Raheem Shahzad
A1 - Sajjad Asaf
A1 - Muhammad Hamayun
A1 - Sang-Mo Kang
A1 - Muhammad Aaqil Khan
A1 - In-Jung Lee
J0 - Journal of Zhejiang University Science B
VL - 18
IS - 2
SP - 109
EP - 124
%@ 1673-1581
Y1 - 2017
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1500262


Abstract: 
We studied the effects of hardwood-derived biochar (BC) and the phytohormone-producing endophyte Galactomyces geotrichum WLL1 in soybean (Glycine max (L.) Merr.) with respect to basic, macro- and micronutrient uptakes and assimilations, and their subsequent effects on the regulation of functional amino acids, isoflavones, fatty acid composition, total sugar contents, total phenolic contents, and 1,1-diphenyl-2-picrylhydrazyl (DPPH)-scavenging activity. The assimilation of basic nutrients such as nitrogen was up-regulated, leaving carbon, oxygen, and hydrogen unaffected in BC+G. geotrichum-treated soybean plants. In comparison, the uptakes of macro- and micronutrients fluctuated in the individual or co-application of BC and G. geotrichum in soybean plant organs and rhizospheric substrate. Moreover, the same attribute was recorded for the regulation of functional amino acids, isoflavones, fatty acid composition, total sugar contents, total phenolic contents, and DPPH-scavenging activity. Collectively, these results showed that BC+G. geotrichum-treated soybean yielded better results than did the plants treated with individual applications. It was concluded that BC is an additional nutriment source and that the G. geotrichum acts as a plant biostimulating source and the effects of both are additive towards plant growth promotion. Strategies involving the incorporation of BC and endophytic symbiosis may help achieve eco-friendly agricultural production, thus reducing the excessive use of chemical agents.

生物炭和内生菌促进大豆增加养分吸收和调节营养参数的叠加作用

目的:探讨提高大豆作物品质的方法。
创新点:研究了生物炭和植物内生菌联合使用对大豆营养吸收和营养品质的叠加作用。
方法:采用硬木生物炭和半乳糖霉菌(Galactomyces geotrichum WLL1)对大豆进行处理,按照处理方式的不同分成四组,包括对照组(无处理)、G. geotrichum处理组、生物炭处理组和生物炭与G. geotrichum联合处理组。通过对比研究生物炭和内生菌对大豆宏量营养素和微量营养素的吸收和同化的作用,并观察其对功能性氨基酸、异黄酮、脂肪酸组成、总糖含量、总酚含量和1,1-二苯基苦基苯肼(DPPH)自由基清除能力的影响。
结论:研究结果发现生物炭和内生菌单独或联合处理均能增加大豆养分的吸收,促进功能性氨基酸的合成,并提升大豆营养品质。同时,生物炭是一种额外的营养源,而内生菌能产生生物刺激效应,两者联合使用具有叠加作用,比单独使用更加有效。

关键词:植物内生菌;养分吸收;同化;营养品质;大豆

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]Ahmed, H.P., Schoenau, J.J., 2015. Effects of biochar on yield, nutrient recovery, and soil properties in a canola (Brassica napus L)-wheat (Triticum aestivum L) rotation grown under controlled environmental conditions. BioEnerg. Res., 8(3):1183-1196.

[2]Albalasmeh, A.A., Berhe, A.A., Ghezzehei, T.A., 2013. A new method for rapid determination of carbohydrate and total carbon concentrations using UV spectrophotometry. Carbohydr. Polym., 97(2):253-261.

[3]Algar, E., Gutierrez-Mañero, F.J., Garcia-Villaraco, A., et al., 2014. The role of isoflavone metabolism in plant protection depends on the rhizobacterial MAMP that triggers systemic resistance against Xanthomonas axonopodis pv. glycines in Glycine max (L.) Merr. cv. Osumi. Plant Physiol. Biochem., 82:9-16.

[4]Bayabil, H.K., Stoof, C.R., Lehmann, J.C., et al., 2015. Assessing the potential of biochar and charcoal to improve soil hydraulic properties in the humid Ethiopian Highlands: the Anjeni watershed. Geoderma, 243-244:115-123.

[5]Bellaloui, N., Ebelhar, M.W., Gillen, A.M., et al., 2011. Soybean seed protein, oil, and fatty acids are altered by S and S+N fertilizers under irrigated or non-irrigated environments. Agric. Sci., 2(4):465-476.

[6]Bellaloui, N., Bruns, H., Abbas, H.K., et al., 2015. Agricultural practices altered soybean seed protein, oil, fatty acids, sugars, and minerals in the Midsouth USA. Front. Plant Sci., 6:31.

[7]Butnan, S., Deenik, J.L., Toomsan, B., et al., 2015. Biochar characteristics and application rates affecting corn growth and properties of soils contrasting in texture and mineralogy. Geoderma, 237-238:105-116.

[8]Cheah, S., Malone, S.C., Feik, C.J., 2014. Speciation of sulfur in biochar produced from pyrolysis and gasification of oak and corn stover. Environ. Sci. Technol., 48(15):8474-8480.

[9]de Corato, U., Pane, C., Bruno, G.L., et al., 2015. Co-products from a biofuel production chain in crop disease management: a review. Crop Prot., 68:12-26.

[10]Dong, D., Feng, Q., McGrouther, K., et al., 2015. Effects of biochar amendment on rice growth and nitrogen retention in a waterlogged paddy field. J. Soils Sediments, 15(1):153-162.

[11]DuBois, M., Gilles, K.A., Hamilton, J.K., et al., 1956. Colorimetric method for determination of sugars and related substances. Anal. Chem., 28(3):350-356.

[12]Elad, Y., Cytryn, E., Harel, Y.M., et al., 2011. The biochar effect: plant resistance to biotic stresses. Phytopathol. Mediterr., 50:335-349.

[13]Evans, J.R., 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia, 78(1):9-19.

[14]Gulati, V., Harding, I.H., Palombo, E.A., 2012. Enzyme inhibitory and antioxidant activities of traditional medicinal plants: potential application in the management of hyperglycemia. BMC Complement. Altern. Med., 12(1):77.

[15]Gwenzi, W., Chaukura, N., Mukome, F.N.D., et al., 2015. Biochar production and applications in sub-Saharan Africa: opportunities, constraints, risks and uncertainties. J. Environ. Manage., 150:250-261.

[16]Haider, G., Koyro, H.W., Azam, F., et al., 2015. Biochar but not humic acid product amendment affected maize yields via improving plant-soil moisture relations. Plant Soil, 395(1):141-157.

[17]Hammer, E.C., Balogh-Brunstad, Z., Jakobsen, I., et al., 2014. A mycorrhizal fungus grows on biochar and captures phosphorus from its surfaces. Soil Biol. Biochem., 77:252-260.

[18]Hao, G., Du, X., Zhao, F., et al., 2010. Fungal endophytes-induced abscisic acid is required for flavonoid accumulation in suspension cells of Ginkgo biloba. Biotechnol. Lett., 32(2):305-314.

[19]Harel, Y.M., Elad, Y., Rav-David, D., et al., 2012. Biochar mediates systemic response of strawberry to foliar fungal pathogens. Plant Soil, 357(1):245-257.

[20]Hartley, S.E., Eschen, R., Horwood, J.M., et al., 2015. Infection by a foliar endophyte elicits novel arabidopside-based plant defence reactions in its host, Cirsium arvense. New Phytol., 205(2):816-827.

[21]Heinonsalo, J., Juurola, E., Linden, A., et al., 2015. Ectomycorrhizal fungi affect Scots pine photosynthesis through nitrogen and water economy, not only through increased carbon demand. Environ. Exp. Bot., 109:103-112.

[22]Huang, W.Y., Cai, Y.Z., Hyde, K.D., et al., 2007a. Endophytic fungi from Nerium oleander L (Apocynaceae): main constituents and antioxidant activity. World J. Microbiol. Biotechnol., 23(9):1253-1263.

[23]Huang, W.Y., Cai, Y.Z., Xing, J., et al., 2007b. A potential antioxidant resource: endophytic fungi from medicinal plants. Econ. Bot., 61(1):14-30.

[24]Iqbal, J., Siegrist, J.A., Nelson, J.A., et al., 2012. Fungal endophyte infection increases carbon sequestration potential of southeastern USA tall fescue stands. Soil Biol. Biochem., 44(1):81-92.

[25]Izuta, H., Narahara, Y., Shimazawa, M., et al., 2009. 1,1-Diphenyl-2-picrylhydrazyl radical scavenging activity of bee products and their constituents determined by ESR. Biol. Pharm. Bull., 32(12):1947-1951.

[26]Jusoh, M., Loh, S.H., Chuah, T.S., et al., 2015. Indole-3-acetic acid (IAA) induced changes in oil content, fatty acid profiles and expression of four fatty acid biosynthetic genes in Chlorella vulgaris at early stationary growth phase. Phytochemistry, 111:65-71.

[27]Khan, A.L., Lee, I.J., 2013. Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol., 13(1):86.

[28]Khan, A.L., Hamayun, M., Waqas, M., et al., 2012a. Exophiala sp. LHL08 association gives heat stress tolerance by avoiding oxidative damage to cucumber plants. Biol. Fertil. Soils, 48(5):519-529.

[29]Khan, A.L., Hamayun, M., Radhakrishnan, R., et al., 2012b. Mutualistic association of Paecilomyces formosus LHL10 offers thermotolerance to Cucumis sativus. Antonie Van Leeuwenhoek, 101(2):267-279.

[30]Khan, A.L., Kang, S.M., Dhakal, K.H., et al., 2013. Flavonoids and amino acid regulation in Capsicum annuum L. by endophytic fungi under different heat stress regimes. Sci. Hortic., 155:1-7.

[31]Khan, A.L., Waqas, M., Hussain, J., et al., 2014. Fungal endophyte Penicillium janthinellum LK5 can reduce cadmium toxicity in Solanum lycopersicum (Sitiens and Rhe). Biol. Fertil. Soils, 50(1):75-85.

[32]Lehmann, J., 2007. A handful of carbon. Nature, 447(7141):143-144.

[33]Li, M., Lou, Z., Wang, Y., et al., 2015. Alkali and alkaline earth metallic (AAEM) species leaching and Cu(II) sorption by biochar. Chemosphere, 119:778-785.

[34]Likar, M., Regvar, M., 2013. Isolates of dark septate endophytes reduce metal uptake and improve physiology of Salix caprea L. Plant Soil, 370(1):593-604.

[35]Malenčić, D., Maksimović, Z., Popović, M., et al., 2008. Polyphenol contents and antioxidant activity of soybean seed extracts. Bioresource Technol., 99(14):6688-6691.

[36]Martinsen, V., Mulder, J., Shitumbanuma, V., et al., 2014. Farmer-led maize biochar trials: effect on crop yield and soil nutrients under conservation farming. J. Plant Nutr. Soil Sci., 177(5):681-695.

[37]McGrath, S.P., Zhao, F.J., 1996. Sulphur uptake, yield responses and the interactions between nitrogen and sulphur in winter oilseed rape (Brassica napus). J. Agric. Sci., 126(1):53-62.

[38]Miret, J.A., Munné-Bosch, S., 2014. Plant amino acid-derived vitamins: biosynthesis and function. Amino Acids, 46(4):809-824.

[39]Newman, J.A., Abner, M.L., Dado, R.G., et al., 2003. Effects of elevated CO2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Global Change Biol., 9(3):425-437.

[40]Obledo, E.N., Barragán-Barragán, L.B., Gutiérrez-González, P., et al., 2003. Increased photosyntethic efficiency generated by fungal symbiosis in Agave victoria-reginae. Plant Cell Tissue Organ Cult., 74(3):237-241.

[41]Pańka, D., Piesik, D., Jeske, M., et al., 2013. Production of phenolics and the emission of volatile organic compounds by perennial ryegrass (Lolium perenne L.)/Neotyphodium lolii association as a response to infection by Fusarium poae. J. Plant Physiol., 170(11):1010-1019.

[42]Patel, D.P., Das, A., Kumar, M., et al., 2015. Continuous application of organic amendments enhances soil health, produce quality and system productivity of vegetable-based cropping systems in subtropical eastern Himalayas. Exp. Agric., 51(1):85-106.

[43]Porcel, R., Ruiz-Lozano, J.M., 2004. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J. Exp. Bot., 55(403):1743-1750.

[44]Ramos-Solano, B., Algar, E., Gutierrez-Mañero, F.J., et al., 2015. Bacterial bioeffectors delay postharvest fungal growth and modify total phenolics, flavonoids and anthocyanins in blackberries. LWT Food Sci. Technol., 61(2):437-443.

[45]Slinkard, K., Singleton, V.L., 1977. Total phenol analysis: automation and comparison with manual methods. Am. J. Enol. Vitic., 28:49-55.

[46]Steindal, A.L.H., Rødven, R., Hansen, E., et al., 2015. Effects of photoperiod, growth temperature and cold acclimatisation on glucosinolates, sugars and fatty acids in kale. Food Chem., 174:44-51.

[47]Tegeder, M., 2014. Transporters involved in source to sink partitioning of amino acids and ureides: opportunities for crop improvement. J. Exp. Bot., 65(7):1865-1878.

[48]Tzin, V., Galili, G., 2010. New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol. Plant, 3(6):956-972.

[49]Upchurch, R.G., 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol. Lett., 30(6):967-977.

[50]Waqas, M., Khan, A.L., Kamran, M., et al., 2012. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules, 17(9):10754-10773.

[51]Waqas, M., Khan, A.L., Kang, S.M., et al., 2014. Phytohormone-producing fungal endophytes and hardwood-derived biochar interact to ameliorate heavy metal stress in soybeans. Biol. Fert. Soils, 50(7):1155-1167.

[52]Waqas, M., Khan, A.L., Hamayun, M., et al., 2015. Endophytic infection alleviates biotic stress in sunflower through regulation of defence hormones, antioxidants and functional amino acids. Eur. J. Plant Pathol., 141(4):803-824.

[53]Weckopp, S.C., Kopriva, S., 2015. Are changes in sulfate assimilation pathway needed for evolution of C4 photosynthesis? Front. Plant Sci., 5:773.

[54]Zhai, L., CaiJi, Z., Liu, J., et al., 2015. Short-term effects of maize residue biochar on phosphorus availability in two soils with different phosphorus sorption capacities. Biol. Fertil. Soils, 51(1):113-122.

[55]Zhang, L., Sun, X.Y., Tian, Y., et al., 2014. Biochar and humic acid amendments improve the quality of composted green waste as a growth medium for the ornamental plant Calathea insignis. Sci. Hortic., 176:70-78.

[56]Zhang, Q., Du, Z., Lou, Y., et al., 2015. A one-year short-term biochar application improved carbon accumulation in large macroaggregate fractions. CATENA, 127:26-31.

[57]Zhao, X., Wang, J.W., Xu, H.J., et al., 2014. Effects of crop-straw biochar on crop growth and soil fertility over a wheat-millet rotation in soils of China. Soil Use Manage., 30(3):311-319.

[58]Zhou, S.L., Yan, S.Z., Liu, Q.S., et al., 2015. Diversity of endophytic fungi associated with the foliar tissue of a hemi-parasitic plant Macrosolen cochinchinensis. Curr. Microbiol., 70(1):58-66.

[59]List of electronic supplementary materials

[60]Table S1 Details of GC-MS conditions for the analysis of fatty acids

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - Journal of Zhejiang University-SCIENCE