Abstract
Plants colonised by dark septate endophytic (DSE) fungi show increased uptake of nutrients available in the environment. The objective of the present study was to evaluate the impact of DSE fungi on the activity of proton pumps, nitrogen (N) recovery from ammonium sulphate, and nutrient accumulation in rice plants. Treatments consisted of non-inoculated plants and plants inoculated with two isolates of DSE fungi, A101 and A103. To determine N recovery from the soil, ammonium sulphate enriched with 15N was added to a non-sterile substrate while parameters associated with the activity of proton pumps and with NO3− uptake were determined in a sterile environment. The A101 and A103 fungal isolates colonised the roots of rice plants, promoting 15N uptake, growth, and accumulation of nutrients as compared with the mock control. A103 induced the expression of the plasma membrane H+-ATPase (PM H+-ATPase) isoforms OsA5 and OsA8, the activity of the PM H+-ATPase and H+-pyrophosphatase. Our results suggest that the inoculation of rice plants with DSE fungi represents a strategy to improve the N recovery from ammonium sulphate and rice plant growth through the induction of OsA5 and OsA8 isoforms and stimulation of the PM H+-ATPase and H+-pyrophosphatase.
Similar content being viewed by others
References
Jumpponen A (2001) Dark septate endophytes-are they mycorrhizal? Mycorrhiza 11:207–211. https://doi.org/10.1007/s0057201001
Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310. https://doi.org/10.1046/j.1469-8137.1998.00265.x
Knapp DG, Kovács GM, Zajta E, Groenewald J, Crous PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35:87–100. https://doi.org/10.3767/003158515X687669
Berthelot C, Leyval C, Foulon J, Chalot M, Blaudez D (2016) Plant growth promotion, metabolite production and metal tolerance of dark septate endophytes isolated from metal-polluted poplar phytomanagement sites. FEMS Microbiol Ecol 92:fiw144. https://doi.org/10.1093/femsec/fiw144
Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773. https://doi.org/10.3390/molecules170910754
Mandyam K, Jumpponen A (2005) Abundance and possible functions of the root-colonizing dark septate endophytic fungi. Stud Mycol 53:173–190
Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11. https://doi.org/10.1007/s00572-009-0260-3
Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184. https://doi.org/10.3852/mycologia.99.2.175
Mandyam K, Loughin T, Jumpponen A (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821. https://doi.org/10.3852/09-212
Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark-septate, root endophytes. Mycologia 92:230–230. https://doi.org/10.2307/3761555
Krajinski F, Courty PE, Sieh D, Franken P, Zhang H, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M, Hause B (2014) The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell 26:1808–1817
Felle HH, Waller F, Molitor A, Kogel KH (2009) The mycorrhiza fungus Piriformospora indica induces fast root-surface pH signaling and primes systemic alkalinization of the leaf apoplast upon powdery mildew infection. Mol Plant-Microbe Interact 22:1179–1185. https://doi.org/10.1094/mpmi-22-9-1179
Lopez-Coria M, Hernandez-Mendoza JL, Sanchez-Nieto S (2016) Trichoderma asperellum induces maize seedling growth by activating the plasma membrane H+-ATPase. Mol Plant-Microbe Interact 29:797–806. https://doi.org/10.1094/mpmi-07-16-0138-r
Liu J, Liu J, Chen A, Ji M, Chen J, Yang X, Gu M, Qu H, Xu G (2016) Analysis of tomato plasma membrane H+-ATPase gene family suggests a mycorrhiza-mediated regulatory mechanism conserved in diverse plant species. Mycorrhiza 26:645–656. https://doi.org/10.1007/s00572-016-0700-9
Wang E, Yu N, Zhang X, Liu C, Miller AJ et al (2014) A H+-ATPase that energizes nutrient uptake during mycorrhizal symbioses in rice and Medicago truncatula. Plant Cell 26:1818–1830
Yuan Q, Ouyang S, Wang A, Zhu W, Maiti R, Lin H, Hamilton J, Haas B, Sultana R, Cheung F, Wortman J, Buell CR (2005) The institute for genomic research Osa1 rice genome annotation database. Plant Physiol 138:18–26. https://doi.org/10.1104/pp.104.059063
Gaxiola RA, Palmgren MG, Schumacher K (2007) Plant proton pumps. FEBS Lett 581:2204–2214
Janicka-Russak M (2011) Plant plasma membrane H+-ATPase in adaptation of plants to abiotic stresses. In: Abiotic stress response in plants-physiological, biochemical and genetic perspectives. InTech
Taiz L, Zeiger E, Møller IM, Murphy A (2017) Fisiologia e desenvolvimento vegetal. Porto Alegre: Artmed. 888–888 p
Okumura M, Inoue S, Takahashi K, Ishizaki K, Kohchi T, Kinoshita T (2012) Characterization of the plasma membrane H+-ATPase in the liverwort Marchantia polymorpha. Plant Physiol 159:826–834. https://doi.org/10.1104/pp.112.195537
Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud JL, Boutry M (2005) Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer. Proc Natl Acad Sci U S A 102:11675–11680. https://doi.org/10.1073/pnas.0504498102
Morsomme P, Boutry M (2000) The plant plasma membrane H+-ATPase: structure, function and regulation. Biochim Biophys Acta 1465:1–16. https://doi.org/10.1016/S0005-2736(00)00128-0
Morth JP, Pedersen BP, Buch-Pedersen MJ, Andersen JP, Vilsen B, Palmgren MG, Nissen P (2011) A structural overview of the plasma membrane Na+, K+-ATPase and H+-ATPase ion pumps. Nat Rev Mol Cell Biol 12:60–70. https://doi.org/10.1038/nrm3031
Sperandio MVL, Santos LA, Bucher CA, Fernandes MS, SRd S (2011) Isoforms of plasma membrane H+-ATPase in rice root and shoot are differentially induced by starvation and resupply of NO3 − or NH4 +. Plant Sci 180:251–258
Haruta M, Sussman MR (2012) The effect of a genetically reduced plasma membrane protonmotive force on vegetative growth of Arabidopsis. Plant Physiol 158:1158–1171. https://doi.org/10.1104/pp.111.189167
Haruta M, Burch HL, Nelson RB, Barrett-Wilt G, Kline KG, Mohsin SB, Young JC, Otegui MS, Sussman MR (2010) Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. J Biol Chem 285:17918–17929. https://doi.org/10.1074/jbc.M110.101733
Hayashi Y, Takahashi K, Inoue S, Kinoshita T (2014) Abscisic acid suppresses hypocotyl elongation by dephosphorylating plasma membrane H+-ATPase in Arabidopsis thaliana. Plant Cell Physiol 55:845–853. https://doi.org/10.1093/pcp/pcu028
Falhof J, Pedersen Jesper T, Fuglsang Anja T, Palmgren M (2016) Plasma membrane H+-ATPase regulation in the Center of Plant Physiology. Mol Plant 9:323–337. https://doi.org/10.1016/j.molp.2015.11.002
Morales-Cedillo F, Gonzalez-Solis A, Gutierrez-Angoa L, Cano-Ramirez DL, Gavilanes-Ruiz M (2015) Plant lipid environment and membrane enzymes: the case of the plasma membrane H+-ATPase. Plant Cell Rep 34:617–629. https://doi.org/10.1007/s00299-014-1735-z
Haruta M, Gray WM, Sussman MR (2015) Regulation of the plasma membrane proton pump (H+-ATPase) by phosphorylation. Curr Opin Plant Biol 28:68–75. https://doi.org/10.1016/j.pbi.2015.09.005
Johansson F, Sommarin M, Larsson C (1993) Fusicoccin activates the plasma membrane H+-ATPase by a mechanism involving the C-terminal inhibitory domain. Plant Cell 5:321–327. https://doi.org/10.1105/tpc.5.3.321
Korthout HA, de Boer AH (1994) A fusicoccin binding protein belongs to the family of 14-3-3 brain protein homologs. Plant Cell 6:1681–1692. https://doi.org/10.1105/tpc.6.11.1681
Gutierrez-Najera N, Munoz-Clares RA, Palacios-Bahena S, Ramirez J, Sanchez-Nieto S et al (2005) Fumonisin B1, a sphingoid toxin, is a potent inhibitor of the plasma membrane H+-ATPase. Planta 221:589–596. https://doi.org/10.1007/s00425-004-1469-1
Lupini A, Araniti F, Mauceri A, Princi MP, Sorgona A et al (2017) Coumarin enhances nitrate uptake in maize roots through modulation of plasma membrane H+ -ATPase activity. Plant Biol (Stuttg) 20:390–398. https://doi.org/10.1111/plb.12674
Lassaletta L, Billen G, Grizzetti B, Anglade J, Garnier J (2014) 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. Environ Res Lett 9:105011. https://doi.org/10.1088/1748-9326/9/10/105011
Cole J (1993) Controlling environmental nitrogen through microbial metabolism. Trends Biotechnol 11:368–372. https://doi.org/10.1016/0167-7799(93)90160-b
De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S et al (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442:939–942. https://doi.org/10.1038/nature05013
Aslam M, Travis RL, Huffaker RC (1993) Comparative induction of nitrate and nitrite uptake and reduction systems by ambient nitrate and nitrite in intact roots of barley (Hordeum vulgare L.) seedlings. Plant Physiol 102:811–819. https://doi.org/10.1104/pp.102.3.811
Krebs M, Beyhl D, Gorlich E, Al-Rasheid KA, Marten I et al (2010) Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proc Natl Acad Sci U S A 107:3251–3256. https://doi.org/10.1073/pnas.0913035107
Palmgren MG (2001) Plant plasma membrane H+-ATPases: powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol 52:817–845. https://doi.org/10.1146/annurev.arplant.52.1.817
Miller AJ, Smith SJ (1996) Nitrate transport and compartmentation in cereal root cells. J Exp Bot 47:843–854. https://doi.org/10.1093/jxb/47.7.843
Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58:2297–2306. https://doi.org/10.1093/jxb/erm066
Drechsler N, Courty PE, Brule D, Kunze R (2017) Identification of arbuscular mycorrhiza-inducible nitrate transporter 1/peptide transporter family (NPF) genes in rice. Mycorrhiza 28:93–100. https://doi.org/10.1007/s00572-017-0802-z
Hildebrandt U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 115:125–136. https://doi.org/10.1034/j.1399-3054.2002.1150115.x
Saia S, Rappa V, Ruisi P, Abenavoli MR, Sunseri F, Giambalvo D, Frenda AS, Martinelli F (2015) Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat. Front Plant Sci 6:815. https://doi.org/10.3389/fpls.2015.00815
Vergara C, Araujo KEC, Alves LS, Souza SR, Santos LA et al (2018) Contribution of dark septate fungi to the nutrient uptake and growth of rice plants. Braz J Microbiol 49:67–78. https://doi.org/10.1016/j.bjm.2017.04.010
Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343. https://doi.org/10.1146/annurev.ecolsys.29.1.319
Mandyam KG, Jumpponen A (2015) Mutualism–parasitism paradigm synthesized from results of root-endophyte models. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00776
Wilcox HE, Wang CJK (1987) Mycorrhizal and pathological associations of dematiaceous fungi in roots of 7-month-old tree seedlings. Can J For Res 17:884–899. https://doi.org/10.1139/x87-140
Diene O, Wang W, Narisawa K (2013) Pseudosigmoidea ibarakiensis sp. nov., a dark septate endophytic fungus from a cedar Forest in Ibaraki, Japan. Microbes Environ 28:381–387. https://doi.org/10.1264/jsme2.ME13002
Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793. https://doi.org/10.1111/j.1469-8137.2010.03611.x
Vergara C, Araujo KEC, Urquiaga S, Santa-Catarina C, Schultz N, da Silva Araújo E, de Carvalho Balieiro F, Xavier GR, Zilli JÉ (2018) Dark septate endophytic fungi increase green manure-(15)N recovery efficiency, N contents, and micronutrients in rice grains. Front Plant Sci 9:613. https://doi.org/10.3389/fpls.2018.00613
Freire L, Balieiro FdC, Zonta E, Anjos Ld, Pereira M, et al. (2013) Manual de calagem e adubação do Estado do Rio de Janeiro. Seropédica, RJ: Universidade Rural do Rio de Janeiro: Editora Universidade Rural. 430 p
Vergara C, Araujo KEC, Urquiaga S, Schultz N, FdC B et al (2017) Dark septate endophytic fungi help tomato to acquire nutrients from ground plant material. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02437
Ribeiro KG (2011) Fungos endofíticos dark septates em arroz silvestre Oryza glumaepatula Steund [Dissertation]. Boa Vista,RO: Universidade Federal de Roraima. 68–68 p
Andrade-Linares DR, Grosch R, Restrepo S, Krumbein A, Franken P (2011) Effects of dark septate endophytes on tomato plant performance. Mycorrhiza 21:413–422. https://doi.org/10.1007/s00572-010-0351-1
Smith J, Um MH (1990) Rapid procedures for preparing soil and KCl extracts for 15N analysis. Communications in Soil Science & Plant Analysis 21:2173–2179. https://doi.org/10.1080/00103629009368368
ISO 12914 (2012) Soil quality-microwave-assisted extraction of the aqua regia soluble fraction for the determination of elements. International Organization for Standardization, Geneva
Tedesco MJ (1982) Extração simultânea de N, P, K, Ca, e Mg em tecido de plantas por disgestão com H2O2-H2SO4. Porto Alegre, RS: UFRGS. 23–23 p
Boddey RM, Alves BJR, Urquiaga S (1994) Quantificação da fixação biológica de nitrogênio associada a plantas utilizando o isótopo 15N. In: Hungria M, Araujo RS (eds) Manual de métodos empregados em estudos de microbiologia agrícola. Embrapa-SPI, Documentos, 46, Brasília, pp 471–494
IAEA (2001) Training course series No 14. Use of isotope and radiation methods in soil and water management and crop nutrition. IAEA, Vienna
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn Bull 347:1–32
Furlani AMC, Furlani PR (1988) Composição e pH de soluções nutritivas para estudos fisiológicos e seleção de plantas em condições nutricionais adversas. Campinas
Lee RB, Rudge RA (1986) Effects of nitrogen deficiency on the absorption of nitrate and ammonium by barley plants. Ann Bot 57:471–486
Bucher CA, Santos LA, Nogueira EM, Rangel RP, de Souza SR et al (2014) The transcription of nitrate transporters in upland rice varieties with contrasting nitrate-uptake kinetics. J Plant Nutr Soil Sci 177:395–403. https://doi.org/10.1002/jpln.201300086
Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651. https://doi.org/10.1016/j.bbrc.2006.04.140
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Facanha AR, De Meis L (1995) Inhibition of maize root H+-ATPase by fluoride and fluoroaluminate complexes. Plant Physiol 108:241–246. https://doi.org/10.1104/pp.108.1.241
Santos LA, Bucher CA, Souza SR, Fernandes MS (2009) Effects of nitrogen stress on proton-pumping and nitrogen metabolism in rice. J Plant Nutr 32:549–564
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Yan F, Zhu Y, Muller C, Zorb C, Schubert S (2002) Adaptation of H+-pumping and plasma membrane H+-ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol 129:50–63. https://doi.org/10.1104/pp.010869
Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular-arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162. https://doi.org/10.1016/S0953-7562(09)80005-1
Mahmoud RS, Narisawa K (2013) A new fungal endophyte, Scolecobasidium humicola, promotes tomato growth under organic nitrogen conditions. PLoS One 8:e78746–e78746. https://doi.org/10.1371/journal.pone.0078746
(2017) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing
Santos LA, Santos WA, Sperandio MVL, Bucher CA, SRd S et al (2011) Nitrate uptake kinetics and metabolic parameters in two rice varieties grown in high and low nitrate. J Plant Nutr 34:988–1002
Souza SR, Stark EMLM, Fernandes MS (1998) Nitrogen remobilization during the reproductive period in two Brazilian rice varieties. J Plant Nutr:2049–2063
Qin Y, Pan X, Kubicek C, Druzhinina I, Chenthamara K, Labbé J, Yuan Z (2017) Diverse plant-associated pleosporalean fungi from saline areas: ecological tolerance and nitrogen-status dependent effects on plant growth. Front Microbiol 8:158. https://doi.org/10.3389/fmicb.2017.00158
Yuan ZL, Llin FC, Zhang CL, Kubicek CP (2010) A new species of Harpophora (Magnaporthaceae) recovered from healthy wild rice (Oryza granulata) roots, representing a novel member of a beneficial dark septate endophyte. FEMS Microbiol Lett 307:94–101. https://doi.org/10.1111/j.1574-6968.2010.01963.x
Santos SG, Silva PR, Garcia AC, Zilli JE, Berbara RL (2017) Dark septate endophyte decreases stress on rice plants. Braz J Microbiol 48:333–341. https://doi.org/10.1016/j.bjm.2016.09.018
Jumpponen A, Mattson KG, Trappe JM (1998) Mycorrhizal functioning of Phialocephala fortinii with Pinus contorta on glacier forefront soil: interactions with soil nitrogen and organic matter. Mycorrhiza 7:261–265. https://doi.org/10.1007/s005720050190
Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass ADM (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiol 140:1036–1046. https://doi.org/10.1104/pp.105.074385
Zhuo D, Okamoto M, Vidmar JJ, Glass ADM (1999) Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. Plant J 17:563–568. https://doi.org/10.1046/j.1365-313X.1999.00396.x
Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc Natl Acad Sci 103:19206–19211. https://doi.org/10.1073/pnas.0605275103
Volpe V, Giovannetti M, Sun XG, Fiorilli V, Bonfante P (2016) The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots. Plant Cell Environ 39:660–671
Thibaud JB, Grignon C (1981) Mechanism of nitrate uptake in corn roots. Plant Sci Lett 22:279–289. https://doi.org/10.1016/0304-4211(81)90241-8
Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482. https://doi.org/10.1104/pp.104.048231
Yoneyama T, Ito O, Engelaar WMHG (2003) Uptake, metabolism and distribution of nitrogen in crop plants traced by enriched and natural 15N: Progress over the last 30 years. Phytochem Rev 2:121–132. https://doi.org/10.1023/B:PHYT.0000004198.95836.ad
Yoneyama T, Fujita K, Yoshida T, Matsumoto T, Kambayashi I, Yazaki J (1986) Variation in natural abundance of 15N among plant parts and in 15N/14N fractionation during N2 fixation in the legume-rhizobia symbiotic system. Plant Cell Physiol 27:791–799. https://doi.org/10.1093/oxfordjournals.pcp.a077165
Tatsumi J, Kono Y (1980) Root growth of rice plants in relation to nitrogen supply from shoot. Jpn J Crop Sci 49:112–119. https://doi.org/10.1626/jcs.49.112
Valli PPS, Muthukumar T (2018) Dark septate root endophytic fungus Nectria haematococca improves tomato growth under water limiting conditions. Indian J Microbiol 58:1–7. https://doi.org/10.1007/s12088-018-0749-6
Russell DW (1973) Soil conditions and plant growth. Longman Group Ltd, New York
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Hanson JB (1984) The functions of calcium in plant nutrition. In: Tinker PB, Lauchli A (eds) Advances in plant nutrition. Praeger Publishers, New York, pp 149–208
Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155. https://doi.org/10.1105/tpc.105.032508
Hepler PK, Winship LJ (2010) Calcium at the cell wall-cytoplast interface. J Integr Plant Biol 52:147–160. https://doi.org/10.1111/j.1744-7909.2010.00923.x
Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21. https://doi.org/10.1038/35036035
Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442. https://doi.org/10.1104/pp.104.046490
Hong-Bo S, Li-Ye C, Ming-An S, Shi-Qing L, Ji-Cheng Y (2008) Bioengineering plant resistance to abiotic stresses by the global calcium signal system. Biotechnol Adv 26:503–510. https://doi.org/10.1016/j.biotechadv.2008.04.004
Kudla J, Batistič O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22:541–563. https://doi.org/10.1105/tpc.109.072686
Bartholdy B, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. BioMetals 14:33–42. https://doi.org/10.1023/A:101668702
Haselwandter K (2009) Mycorrhizal fungi: colonisation pattern of alpine plants and ecological significance of siderophore release. Asp Appl Biol:105–108
Ding Y-C, Chang C-R, Luo W, Wu Y-S, Ren X-L et al (2008) High potassium aggravates the oxidative stress induced by magnesium deficiency in rice leaves. 1 1Project supported by the Dead Sea Works Ltd. Israel Pedosphere 18:316–327. https://doi.org/10.1016/S1002-0160(08)60021-1
Shaul O (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15:309–323. https://doi.org/10.1104/pp.112.199778
Hermans C, Vuylsteke M, Coppens F, Cristescu SM, Harren FJ et al (2010) Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol 187:132–144. https://doi.org/10.1111/j.1469-8137.2010.03257.x
Li J, Yang H, Peer WA, Richter G, Blakeslee J et al (2005) Arabidopsis H+-PPase AVP1 regulates auxin-mediated organ development. Science 310:121–125. https://doi.org/10.1126/science.1115711
Li X, Guo C, Gu J, Duan W, Zhao M, Ma C, du X, Lu W, Xiao K (2014) Overexpression of VP, a vacuolar H+-pyrophosphatase gene in wheat (Triticum aestivum L.), improves tobacco plant growth under pi and N deprivation, high salinity, and drought. J Exp Bot 65:683–696. https://doi.org/10.1093/jxb/ert442
Paez-Valencia J, Sanchez-Lares J, Marsh E, Dorneles LT, Santos MP, Sanchez D, Winter A, Murphy S, Cox J, Trzaska M, Metler J, Kozic A, Facanha AR, Schachtman D, Sanchez CA, Gaxiola RA (2013) Enhanced proton translocating pyrophosphatase activity improves nitrogen use efficiency in Romaine lettuce. Plant Physiol 161:1557–1569
Park S, Li J, Pittman JK, Berkowitz GA, Yang H, Undurraga S, Morris J, Hirschi KD, Gaxiola RA (2005) Up-regulation of a H+-pyrophosphatase (H+-PPase) as a strategy to engineer drought-resistant crop plants. Proc Natl Acad Sci U S A 102:18830–18835. https://doi.org/10.1073/pnas.0509512102
Yang H, Zhang X, Gaxiola RA, Xu G, Peer WA, Murphy AS (2014) Over-expression of the Arabidopsis proton-pyrophosphatase AVP1 enhances transplant survival, root mass, and fruit development under limiting phosphorus conditions. J Exp Bot 65:3045–3053. https://doi.org/10.1093/jxb/eru149
Duby G, Boutry M (2009) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Pflugers Arch 457:645–655. https://doi.org/10.1007/s00424-008-0457-x
Arango M, Gevaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta 216:355–365. https://doi.org/10.1007/s00425-002-0856-8
Chang C, Hu Y, Sun S, Zhu Y, Ma G, Xu G (2009) Proton pump OsA8 is linked to phosphorus uptake and translocation in rice. J Exp Bot 60:557–565. https://doi.org/10.1093/jxb/ern298
Acknowledgements
We are indebted to the University Federal Rural do Rio de Janeiro (UFRRJ), especially for the Laboratory Nutrition of Plants, the state University of Norte Fluminense Darcy Ribeiro (UENF), especially for LBCT, the Brazilian Agricultural Research Corporation (Embrapa), for their help with the work. This work was supported by the Foundation for Support of Research in the State of Rio de Janeiro (FAPERJ), the Brazilian National Council for Scientific and Technological Development (CNPq), and the Coordination for the Improvement of Higher Education Personnel (CAPES).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Luiz Roesch.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Vergara, C., Araujo, K.E.C., Sperandio, M.V.L. et al. Dark septate endophytic fungi increase the activity of proton pumps, efficiency of 15N recovery from ammonium sulphate, N content, and micronutrient levels in rice plants. Braz J Microbiol 50, 825–838 (2019). https://doi.org/10.1007/s42770-019-00092-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-019-00092-4