Abstract
Biochar amendment is a management strategy to alleviate drought stress in plants. However, in-depth assessments are needed to elucidate how biochar amendment affects root growth by modulating various physiological and biochemical changes under drought stress. In this study, we investigated ion fluxes, metabolic levels, and physiological traits of maize roots in biochar-amended soil under drought stress using noninvasive micro-test technology, metabolomics profiling, and ratiometric fluorescence. The results revealed that the biochar treatment increased soil K+ supply and root sap K+ concentration, but decreased root Ca2+ efflux under moderate drought stress, compared to the no biochar treatment. Root apoplastic pH and abscisic acid content increased significantly in the biochar treatment under severe drought stress. Consequently, root osmolality and root malonaldehyde content decreased, whereas root water potential, root ascorbate peroxidase activity, and plant fresh weight increased in the biochar treatment under severe drought stress. In addition, the biochar treatment enhanced the accumulation of trehalose and 3-hydroxyanthranilic acid in response to moderate and severe drought stress while reducing the levels of uridine, cytidine, guanosine, l-tryptophan, and l-glutamine in maize roots. These results indicate that the biochar-mediated improvements in plant drought tolerance were associated with increased K+ concentration, less Ca2+ efflux, and an increase in apoplastic pH in maize roots.
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References
Abideen Z, Koyro H-W, Huchzermeyer B, Gul B, Khan MA (2020) Impact of a biochar or a biochar-compost mixture on water relation, nutrient uptake and photosynthesis of Phragmites karka. Pedosphere 30(4):466–477. https://doi.org/10.1016/S1002-0160(17)60362-X
Armengaud P, Sulpice R, Miller AJ, Stitt M, Amtmann A, Gibon Y (2009) Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiol 150(2):772–785. https://doi.org/10.1104/pp.108.133629
Aroca R (2012) Plant responses to drought stress. Departamento de Microbiología del Suelo ySistemas Simbióticos, Spain
Barbez E, Dünser K, Gaidora A, Lendl T, Busch W (2017) Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. Proc Natl Acad Sci USA 114(24):E4884–E4893. https://doi.org/10.1073/pnas.1613499114
Biederman LA, Harpole WS (2013) Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. GCB Bioenergy 5(2):202–214. https://doi.org/10.1111/gcbb.12037
Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40(1):4–10. https://doi.org/10.1111/pce.12800
Bose J, Pottosin I, Shabala S, Palmgren M, Shabala S (2011) Calcium efflux systems in stress signaling and adaptation in plants. Front Plant Sci. https://doi.org/10.3389/fpls.2011.00085
Bose J, Shabala L, Pottosin I, Zeng F, Velarde-Buendia A-M, Massart A, Poschenrieder C, Hariadi Y, Shabala S (2014) Kinetics of xylem loading, membrane potential maintenance, and sensitivity of K+-permeable channels to reactive oxygen species: physiological traits that differentiate salinity tolerance between pea and barley. Plant Cell Environ 37(3):589–600. https://doi.org/10.1111/pce.12180
Castro B, Citterico M, Kimura S, Stevens DM, Wrzaczek M, Coaker G (2021) Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nat Plants 7(4):403–412. https://doi.org/10.1038/s41477-021-00887-0
Chen Z, Pottosin II, Cuin TA, Fuglsang AT, Tester M, Jha D, Zepeda-Jazo I, Zhou M, Palmgren MG, Newman IA, Shabala S (2007) Root plasma membrane transporters controlling K+/Na+ homeostasis in salt-stressed barley. Plant Physiol 145(4):1714–1725. https://doi.org/10.1104/pp.107.110262
Chen J, Wang W-H, Wu F-H, He E-M, Liu X, Shangguan Z-P, Zheng H-L (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5(1):12516. https://doi.org/10.1038/srep12516
Dakora FD, Matiru VN, Kanu AS (2015) Rhizosphere ecology of lumichrome and riboflavin, two bacterial signal molecules eliciting developmental changes in plants. Front Plant Sci 6:700. https://doi.org/10.3389/fpls.2015.00700
Dang X, Chen B, Liu F, Ren H, Liu X, Zhou J, Qin Y, Lin D (2020) Auxin signaling-mediated apoplastic pH modification functions in petal conical cell sha**. Cell Rep 30(11):3904–3916. https://doi.org/10.1016/j.celrep.2020.02.087
Demidchik V (2014) Mechanisms and physiological roles of K+ efflux from root cells. J Plant Physiol 171(9):696–707. https://doi.org/10.1016/j.jplph.2014.01.015
Demidchik V, Cuin TA, Svistunenko D, Smith SJ, Miller AJ, Shabala S, Sokolik A, Yurin V (2010) Arabidopsis root K+-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J Cell Sci 123(Pt 9):1468–1479. https://doi.org/10.1242/jcs.064352
Fàbregas N, Lozano-Elena F, Blasco-Escámez D, Tohge T, Martínez-Andújar C, Albacete A, Osorio S, Bustamante M, Riechmann JL, Nomura T, Yokota T, Conesa A, Alfocea FP, Fernie AR, Caño-Delgado AI (2018) Overexpression of the vascular brassinosteroid receptor BRL3 confers drought resistance without penalizing plant growth. Nat Commun 9(1):4680. https://doi.org/10.1038/s41467-018-06861-3
Farhangi-Abriz S, Torabian S (2017) Antioxidant enzyme and osmotic adjustment changes in bean seedlings as affected by biochar under salt stress. Ecotoxicol Environ Saf 137:64–70. https://doi.org/10.1016/j.ecoenv.2016.11.029
Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and Management. In: Lichtfouse E, Navarrete M, Debaeke P, Véronique S, Alberola C (eds) Sustainable agriculture. Springer Netherlands, Dordrecht, pp 153–188. https://doi.org/10.1007/978-90-481-2666-8_12
Felle HH, Hanstein S (2002) The apoplastic pH of the substomatal cavity of Vicia faba leaves and its regulation responding to different stress factors. J Exp Bot 53(366):73–82. https://doi.org/10.1093/jxb/53.366.73
Feng X, Liu W, Zeng F, Chen Z, Zhang G, Wu F (2016) K+ uptake, H+-ATPase pum** activity and Ca2+ efflux mechanism are involved in drought tolerance of barley. Environ Exp Bot 129:57–66. https://doi.org/10.1016/j.envexpbot.2015.11.006
Fernandez O, Béthencourt L, Quero A, Sangwan R, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417. https://doi.org/10.1016/j.tplants.2010.04.004
Fischer BMC, Manzoni S, Morillas L, Garcia M, Johnson MS, Lyon SW (2019) Improving agricultural water use efficiency with biochar—a synthesis of biochar effects on water storage and fluxes across scales. Sci Total Environ 657:853–862. https://doi.org/10.1016/j.scitotenv.2018.11.312
Geilfus C-M (2017) The pH of the apoplast: dynamic factor with functional impact under stress. Mol Plant 10(11):1371–1386. https://doi.org/10.1016/j.molp.2017.09.018
Gharibi S, Tabatabaei BES, Saeidi G, Goli SAH (2016) Effect of drought stress on total phenolic, lipid peroxidation, and antioxidant activity of Achillea species. Appl Biochem Biotechnol 178(4):796–809. https://doi.org/10.1007/s12010-015-1909-3
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171(3):1606–1615. https://doi.org/10.1104/pp.16.00434
Gong D-S, **ong Y-C, Ma B-L, Wang T-M, Ge J-P, Qin X-L, Li P-F, Kong H-Y, Li Z-Z, Li F-M (2010) Early activation of plasma membrane H+-ATPase and its relation to drought adaptation in two contrasting oat (Avena sativa L.) genotypes. Environ Exp Bot 69(1):1–8. https://doi.org/10.1016/j.envexpbot.2010.02.011
Graether SP, Boddington KF (2014) Disorder and function: a review of the dehydrin protein family. Front Plant Sci 5:576. https://doi.org/10.3389/fpls.2014.00576
Griesser M, Weingart G, Schoedl-Hummel K, Neumann N, Becker M, Varmuza K, Liebner F, Schuhmacher R, Forneck A (2015) Severe drought stress is affecting selected primary metabolites, polyphenols, and volatile metabolites in grapevine leaves (Vitis vinifera cv. Pinot noir). Plant Physiol Biochem 88:17–26. https://doi.org/10.1016/j.plaphy.2015.01.004
Han S, Fang L, Ren X, Wang W, Jiang J (2015) MPK6 controls H2O2-induced root elongation by mediating Ca2+ influx across the plasma membrane of root cells in Arabidopsis seedlings. New Phytol 205(2):695–706. https://doi.org/10.1111/nph.12990
Hayashi Y, Takahashi K, Inoue S-i, Kinoshita T (2014) Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H+-ATPase in Arabidopsis thaliana. Plant Cell Physiol 55(4):845–853. https://doi.org/10.1093/pcp/pcu028
Hossain MA, Wani SH, Bhattacharjee S, Burritt DJ, Tran L-SP (2016) Drought stress tolerance in plants, vol 2. Springer, Switzerland
Huda KM, Banu MS, Garg B, Tula S, Tuteja R, Tuteja N (2013) OsACA6, a P-type IIB Ca2+ ATPase promotes salinity and drought stress tolerance in tobacco by ROS scavenging and enhancing the expression of stress-responsive genes. Plant J 76(6):997–1015. https://doi.org/10.1111/tpj.12352
Kammann CI, Linsel S, Gößling JW, Koyro H-W (2011) Influence of biochar on drought tolerance of Chenopodium quinoa Willd and on soil–plant relations. Plant Soil 345(1):195–210. https://doi.org/10.1007/s11104-011-0771-5
Kang Z, Babar MA, Khan N, Guo J, Khan J, Islam S, Shrestha S, Shahi D (2019) Comparative metabolomic profiling in the roots and leaves in contrasting genotypes reveals complex mechanisms involved in post-anthesis drought tolerance in wheat. PLoS ONE 14(3):e0213502. https://doi.org/10.1371/journal.pone.0213502
Khan N, Bano A, Rahman MA, Rathinasabapathi B, Babar MA (2019) UPLC-HRMS-based untargeted metabolic profiling reveals changes in chickpea (Cicer arietinum) metabolome following long-term drought stress. Plant Cell Environ 42(1):115–132. https://doi.org/10.1111/pce.13195
Kubicova L, Hadacek F, Chobot V (2013) Quinolinic acid: neurotoxin or oxidative stress modulator? Int J Mol Sci 14(11):21328–21338. https://doi.org/10.3390/ijms141121328
Lehmann J (2007) A handful of carbon. Nature 447(7141):143–144. https://doi.org/10.1038/447143a
Li L, Verstraeten I, Roosjen M, Takahashi K, Rodriguez L, Merrin J, Chen J, Shabala L, Smet W, Ren H, Vanneste S, Shabala S, De Rybel B, Weijers D, Kinoshita T, Gray WM, Friml J (2021) Cell surface and intracellular auxin signalling for H+ fluxes in root growth. Nature 599(7884):273–277. https://doi.org/10.1038/s41586-021-04037-6
Limwikran T, Kheoruenromne I, Suddhiprakarn A, Prakongkep N, Gilkes RJ (2018) Dissolution of K, Ca, and P from biochar grains in tropical soils. Geoderma 312:139–150. https://doi.org/10.1016/j.geoderma.2017.10.022
Lyons DJ, Lynch PJ (1985) Determination of exchangeable cations (Ca, Mg, Na, K) in aqueous and alcoholic NH4Cl extracts of soils using ICPES. Commun Soil Sci Plant Anal 16(1):15–26. https://doi.org/10.1080/00103628509367584
Ma X, Sun M, Sa G, Zhang Y, Li J, Sun J, Shen X, Polle A, Chen S (2014) Ion fluxes in Paxillus involutus-inoculated roots of Populus×canescens under saline stress. Environ Exp Bot 108:99–108. https://doi.org/10.1016/j.envexpbot.2013.11.016
Mak M, Babla M, Xu S-C, O’Carrigan A, Liu X-H, Gong Y-M, Holford P, Chen Z-H (2014) Leaf mesophyll K+, H+ and Ca2+ fluxes are involved in drought-induced decrease in photosynthesis and stomatal closure in soybean. Environ Exp Bot 98:1–12. https://doi.org/10.1016/j.envexpbot.2013.10.003
Martínez J, Schanck A, Bajji M, Kinet J-M (2004) Is osmotic adjustment required for water stress resistance in the Mediterranean shrub Atriplex halimus L.? J Plant Physiol. J Plant Physiol 161:1041–1051. https://doi.org/10.1016/j.jplph.2003.12.009
Michaletti A, Naghavi MR, Toorchi M, Zolla L, Rinalducci S (2018) Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Sci Rep 8:5710. https://doi.org/10.1038/s41598-018-24012-y
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58(1):459–481. https://doi.org/10.1146/annurev.arplant.58.032806.103946
Muhling KH, Lauchli A (1999) Effect of K+ nutrition, leaf age and light intensity on apoplastic K+ in leaves of Vicia faba. J Plant Nutr Soil Sci 162(6):571–576
Muhling KH, Sattelmacher B (1997) Determination of apoplastic K+ in intact leaves by ratio imaging of PBFI fluorescence. J Exp Bot 48(313):1609–1614. https://doi.org/10.1093/jexbot/48.313.1609
Müller J, Wiemken A, Aeschbacher R (1999) Trehalose metabolism in sugar sensing and plant development. Plant Sci 147(1):37–47. https://doi.org/10.1016/S0168-9452(99)00094-1
Peng X, Ye LL, Wang CH, Zhou H, Sun B (2011) Temperature- and duration-dependent rice straw-derived biochar: characteristics and its effects on soil properties of an ultisol in southern China. Soil Tillage Res 112(2):159–166. https://doi.org/10.1016/j.still.2011.01.002
Pérez-González A, Alvarez-Idaboy J, Galano A (2017) Dual antioxidant/pro-oxidant behavior of the tryptophan metabolite 3-hydroxyanthranilic acid: a theoretical investigation on reaction mechanisms and kinetics. New J Chem. https://doi.org/10.1039/C6NJ03980D
Shabala S, Bose J, Fuglsang AT, Pottosin I (2015) On a quest for stress tolerance genes: membrane transporters in sensing and adapting to hostile soils. J Exp Bot 67(4):1015–1031. https://doi.org/10.1093/jxb/erv465
Shabala S, Newman IA, Morris J (1997) Oscillations in H+ and Ca2+ ion fluxes around the elongation region of corn roots and effects of external pH. Plant Physiol 113:111–118. https://doi.org/10.1104/pp.113.1.111
Shen B, Yi X, Sun Y, Bi X, Du J, Zhang C, Quan S, Zhang F, Sun R, Qian L, Ge W, Liu W, Liang S, Chen H, Zhang Y, Li J, Xu J, He Z, Chen B, Wang J, Yan H, Zheng Y, Wang D, Zhu J, Kong Z, Kang Z, Liang X, Ding X, Ruan G, **ang N, Cai X, Gao H, Li L, Li S, **ao Q, Lu T, Zhu Y, Liu H, Chen H, Guo T (2020) Proteomic and metabolomic characterization of COVID-19 patient sera. Cell 182(1):59-72e15. https://doi.org/10.1016/j.cell.2020.05.032
Silber A, Levkovitch I, Graber ER (2010) pH-dependent mineral release and surface properties of cornstraw biochar: agronomic implications. Environ Sci Technol 44(24):9318–9323. https://doi.org/10.1021/es101283d
Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS ONE 7(6):e38554. https://doi.org/10.1371/journal.pone.0038554
Slade WO, Werth EG, McConnell EW, Alvarez S, Hicks LM (2015) Quantifying reversible oxidation of protein thiols in photosynthetic organisms. J Am Soc Mass Spectrom 26(4):631–640. https://doi.org/10.1007/s13361-014-1073-y
Staff SS (2015) Illustrated guide to soil taxonomy. U.S. Department of Agriculture, Natural Resources Conservation Service, National Soil Survey Center, Lincoln
Sun Z, Zhang Z, Zhu K, Wang Z, Zhao X, Lin Q, Li G (2020) Biochar altered native soil organic carbon by changing soil aggregate size distribution and native SOC in aggregates based on an 8-year field experiment. Sci Total Environ 708:134829. https://doi.org/10.1016/j.scitotenv.2019.134829
Tavakol E, Jákli B, Cakmak I, Dittert K, Karlovsky P, Pfohl K, Senbayram M (2018) Optimized potassium nutrition improves plant-water-relations of barley under PEG-induced osmotic stress. Plant Soil 430(1):23–35. https://doi.org/10.1007/s11104-018-3704-8
Turski MP, Kamiński P, Zgrajka W, Turska M, Turski WA (2012) Potato- an important source of nutritional kynurenic acid. Plant Foods Hum Nutr 67(1):17–23. https://doi.org/10.1007/s11130-012-0283-3
Veronika Z, Břendová K, Pavlíková D, Kubátová P, Tlustoš P (2017) Effect of biochar application on the content of nutrients (Ca, Fe, K, Mg, Na, P) and amino acids in subsequently growing spinach and mustard. Plant Soil Environ. https://doi.org/10.17221/318/2017-PSE
Viger M, Hancock RD, Miglietta F, Taylor G (2015) More plant growth but less plant defence? First global gene expression data for plants grown in soil amended with biochar. GCB Bioenergy 7(4):658–672. https://doi.org/10.1111/gcbb.12182
Villiers F, Kwak JM (2013) Rapid apoplastic pH measurement in Arabidopsis leaves using a fluorescent dye. Plant Signal Behav 8(1):e22587. https://doi.org/10.4161/psb.22587
Wang Y, Pan F, Wang G, Zhang G, Wang Y, Chen X, Mao Z (2014) Effects of biochar on photosynthesis and antioxidative system of Malus hupehensis Rehd. seedlings under replant conditions. Sci Hort 175:9–15. https://doi.org/10.1016/j.scienta.2014.05.029
Wegner LH, Shabala S (2020) Biochemical pH clamp: the forgotten resource in membrane bioenergetics. New Phytol 225(1):37–47. https://doi.org/10.1111/nph.16094
Wilkinson S, Davies WJ (1997) Xylem sap pH increase: a drought signal received at the apoplastic face of the guard cell that involves the suppression of saturable abscisic acid uptake by the epidermal symplast. Plant Physiol 113(2):559–573. https://doi.org/10.1104/pp.113.2.559
Woolf D, Amonette JE, Street-Perrott FA, Lehmann J, Joseph S (2010) Sustainable biochar to mitigate global climate change. Nat Commun 1(1):56. https://doi.org/10.1038/ncomms1053
**ang Y, Deng Q, Duan H, Guo Y (2017) Effects of biochar application on root traits: a meta-analysis. GCB Bioenergy 9(10):1563–1572. https://doi.org/10.1111/gcbb.12449
Zeng F, Konnerup D, Shabala L, Zhou M, Colmer TD, Zhang G, Shabala S (2014) Linking oxygen availability with membrane potential maintenance and K+ retention of barley roots: implications for waterlogging stress tolerance. Plant Cell Environ 37(10):2325–2338. https://doi.org/10.1111/pce.12422
Zhou K, Sui Y-y, Xu X, Zhang J-y, Chen Y-m, Hou M, Jiao X-g (2018) The effects of biochar addition on phosphorus transfer and water utilization efficiency in a vegetable field in Northeast China. Agric Water Manag 210:324–329. https://doi.org/10.1016/j.agwat.2018.08.007
Acknowledgements
We thank Professor Li Pu at Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, China for supplying the seeds of B73 and technical assistance.
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This study was funded by National Key Research and Development Program of China (Grant No. 2023YFD1500900).
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RR: Investigation, Formal analysis, Data curation, Software, Writing—original draft. YY: Investigation. CW: Investigation. YW: Funding acquisition, Writing—original draft, Writing—review & editing.
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Ruan, R., Yuan, Y., Wang, C. et al. Biochar effects on drought tolerance in maize roots are linked to K+ concentration, Ca2+ efflux, and apoplastic pH. Plant Growth Regul 103, 307–320 (2024). https://doi.org/10.1007/s10725-023-01104-y
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DOI: https://doi.org/10.1007/s10725-023-01104-y