Microbial enhancement of plant nutrient acquisition

Abstract

Nutrient availability is a determining factor for crop yield and quality. While fertilization is a major approach for improving plant nutrition, its efficacy can be limited and the production and application of fertilizers frequently bring problems to the environment. A large number of soil microbes are capable of enhancing plant nutrient acquisition and thereby offer environmentally benign solutions to meet the requirements of plant nutrition. Herein we provide summations of how beneficial microbes enhance plant acquisition of macronutrients and micronutrients. We also review recent studies on nutrition-dependent plant-microbe interactions, which highlight the plant’s initiative in establishing or deterring the plant-microbe association. By dissecting complex signaling interactions between microbes within the root microbiome, a greater understanding of microbe-enhanced plant nutrition under specific biotic and abiotic stresses will be possible.

Keywords

Beneficial microbes / Plant / Macronutrient / Micronutrient / Plant-microbe interactions / Volatile organic compounds / Microbiome

References

[1] AlewellC, RingevalB, BallabioC, RobinsonDA, PanagosP, BorrelliP. Global phosphorus shortage will be aggravated by soil erosion. Nat Commun, 2020, 11(1):4546

[2] AloriET, GlickBR, BabalolaOO. Microbial phosphorus solubilization and its potential for use in sustainable agriculture. Front Microbiol, 2017, 8(971):971

[3] ÁlvarezC, NavarroJA, Molina-HerediaFP, MariscalV. Endophytic colonization of rice (Oryza sativa L.) by the symbiotic strain Nostoc punctiforme PCC 73102. Mol Plant Microbe Interact, 2020, 33(8):1040-1045

[4] AndresenE, PeiterE, KupperH. Trace metal metabolism in plants. J Exp Bot, 2018, 69(5):909-954

[5] AndrewsM, AndrewsME. Specificity in legume-rhizobia symbioses. Int J Mol Sci, 2017, 18(4):705

[6] Aziz M, Nadipalli RK, Xie X, Sun Y, Surowiec K, Zhang JL, Paré PW (2016) Augmenting sulfur metabolism and herbivore defense in arabidopsis by bacterial volatile signaling. Front Plant Sci 7(−):458. https://doi.org/10.3389/fpls.2016.00458

[7] BarberonM, DubeauxG, KolbC, IsonoE, ZelaznyE, VertG. Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. PNAS USA, 2014, 111(22):8293-8298

[8] BaslamM, GarmendiaI, GoicoecheaN. The arbuscular mycorrhizal symbiosis can overcome reductions in yield and nutritional quality in greenhouse-lettuces cultivated at inappropriate growing seasons. Sci Hortic, 2013, 164: 145-154

[9] BradyNC, WeilRR, WeilRR. The nature and properties of soils, 2008 NJ Prentice Hall Upper Saddle River

[10] BreuillinF, SchrammJ, HajirezaeiM, AhkamiA, FavreP, DruegeU, HauseB, BucherM, KretzschmarT, BossoliniE, KuhlemeierC, MartinoiaE, FrankenP, ScholzU, ReinhardtD. Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J, 2010, 64(6):1002-1017

[11] Carrillo-CastañedaG, MuñosJJ, Peralta-VideaJ, GomezE, TiemannbK, Duarte-GardeaM, et al.. Alfalfa growth promotion by bacteria grown under iron limiting conditions. Adv Environ Res, 2002, 6(3):391-399

[12] Castulo-RubioDY, Alejandre-RamírezNA, Del CarmenO-MM, SantoyoG, Macías-RodríguezLI, Valencia-CanteroE. Volatile organic compounds produced by the rhizobacterium Arthrobacter agilis UMCV2 modulate Sorghum bicolor (strategy II plant) morphogenesis and SbFRO1 transcription in vitro. J Plant Growth Regul, 2015, 34(3):611-623

[13] ChauhanS, ThakurR, SharmaG. Nickel: its availability and reactions in soil. J Ind Pollut Control, 2008, 24(1):1-8

[14] ChenJG, CrooksRM, SeefeldtLC, BrenKL, BullockRM, DarensbourgMY, HollandPL, HoffmanB, JanikMJ, JonesAK, KanatzidisMG, KingP, LancasterKM, LymarSV, PfrommP, SchneiderWF, SchrockRR. Beyond fossil fuel–driven nitrogen transformations. Science, 2018, 360(6391):eaar6611

[15] CoccinaA, CavagnaroTR, PellegrinoE, ErcoliL, MclaughlinMJ, Watts-WilliamsSJ. The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant Biol, 2019, 19(1):1-14

[16] CoronadoC, ZuanazziJS, SallaudC, QuirionJ-C, EsnaultR, HussonH-P, KondorosiA, RatetP. Alfalfa root flavonoid production is nitrogen regulated. Plant Physiol, 1995, 108(2):533-542

[17] CurieC, BriatJ-F. Iron transport and signaling in plants. Annu Rev Plant Biol, 2003, 54(1):183-206

[18] Del CarmenO-MM, Macías-RodríguezLI, SantoyoG, Farías-RodríguezR, Valencia-CanteroE. Medicago truncatula increases its iron-uptake mechanisms in response to volatile organic compounds produced by Sinorhizobium meliloti. Folia Microbiol (Praha), 2013, 58(6):579-585

[19] Del CarmenO-MM, Velázquez-BecerraC, Macías-RodríguezLI, SantoyoG, Flores-CortezI, Alfaro-CuevasR, et al.. Arthrobacter agilis UMCV2 induces iron acquisition in Medicago truncatula (strategy I plant) in vitro via dimethylhexadecylamine emission. Plant Soil, 2013, 362(1):51-66

[20] DixonRA, PostgateJR. Transfer of nitrogen-fixation genes by conjugation in Klebsiella pneumoniae. Nature, 1971, 234(5323):47-48

[21] EichhornE, Van Der PloegJR, LeisingerT. Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli. J Biol Chem, 1999, 274(38):26639-26646

[22] FabiańskaI, GerlachN, AlmarioJ, BucherM. Plant-mediated effects of soil phosphorus on the root-associated fungal microbiota in Arabidopsis thaliana. New Phytol, 2019, 221(4):2123-2137

[23] FaragMA, RyuC-M, SumnerLW, ParéPW. GC–MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry, 2006, 67(20):2262-2268

[24] FaragMA, ZhangH, RyuC-M. Dynamic chemical communication between plants and bacteria through airborne signals: induced resistance by bacterial volatiles. J Chem Ecol, 2013, 39(7):1007-1018

[25] FerrolN, TamayoE, VargasP. The heavy metal paradox in arbuscular mycorrhizas: from mechanisms to biotechnological applications. J Exp Bot, 2016, 67(22):erw403

[26] FinkelOM, Salas-GonzálezI, CastrilloG, SpaepenS, LawTF, TeixeiraPJPL, JonesCD, DanglJL. The effects of soil phosphorus content on plant microbiota are driven by the plant phosphate starvation response. PLoS Biol, 2019, 17(11):e3000534

[27] FreitasMA, MedeirosFH, CarvalhoSP, GuilhermeLR, TeixeiraWD, ZhangH, ParéPW. Augmenting iron accumulation in cassava by the beneficial soil bacterium Bacillus subtilis (GBO3). Front. Plant Sci, 2015, 6

[28] GahanJ, SchmalenbergerA. Arbuscular mycorrhizal hyphae in grassland select for a diverse and abundant hyphospheric bacterial community involved in sulfonate desulfurization. Appl. Soil Ecol, 2015, 89: 113-121

[29] GhoshS, BalB, DasA. Enhancing manganese recovery from low-grade ores by using mixed culture of indigenously isolated bacterial strains. Geomicrobiol J, 2018, 35(3):242-246

[30] GiovannettiM, TolosanoM, VolpeV, KoprivaS, BonfanteP. Identification and functional characterization of a sulfate transporter induced by both sulfur starvation and mycorrhiza formation in Lotus japonicus. New Phytol, 2014, 204(3):609-619

[31] GongZ, XiongL, ShiH, YangS, Herrera-EstrellaLR, XuG, ChaoDY, LiJ, WangPY, QinF, LiJ, DingY, ShiY, WangY, YangY, GuoY, ZhuJK. Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci, 2020, 63(5):635-674

[32] GovindarajuluM, PfefferPE, JinH, AbubakerJ, DoudsDD, AllenJW, BückingH, LammersPJ, Shachar-HillY. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature, 2005, 435(7043):819-823

[33] GuerinotML, MeidlEJ, PlessnerO. Citrate as a siderophore in Bradyrhizobium japonicum. J Bacteriol, 1990, 172(6):3298-3303

[34] Guerrero-GalánC, GarciaK, HoudinetG, ZimmermannS-D. Hc TOK1 participates in the maintenance of K+ homeostasis in the ectomycorrhizal fungus Hebeloma cylindrosporum, which is essential for the symbiotic K+ nutrition of Pinus pinaster. Plant Signal Behav, 2018, 13(6):e1480845

[35] HarperJE, NicholasJC. Nitrogen metabolism of soybeans: I. effect of tungstate on nitrate utilization, nodulation, and growth. Plant Physiol, 1978, 62(4):662-664

[36] HarrisonMJ, DewbreGR, LiuJ. A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell, 2002, 14(10):2413-2429

[37] HermansC, VuylstekeM, CoppensF, CristescuSM, HarrenFJ, InzéD, et al.. Systems analysis of the responses to long-term magnesium deficiency and restoration in Arabidopsis thaliana. New Phytol, 2010, 187(1):132-144

[38] Hernández-CalderónE, Aviles-GarciaME, Castulo-RubioDY, Macías-RodríguezL, RamírezVM, SantoyoG, López-BucioJ, Valencia-CanteroE. Volatile compounds from beneficial or pathogenic bacteria differentially regulate root exudation, transcription of iron transporters, and defense signaling pathways in Sorghum bicolor. Plant Mol Biol, 2018, 96(3):291-304

[39] HirumaK, GerlachN, SacristánS, NakanoRT, HacquardS, KracherB, NeumannU, RamírezD, BucherM, O’ConnellRJ, Schulze-LefertP. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell, 2016, 165(2):464-474

[40] JarstferA, Farmer-KoppenolP, SylviaDM. Tissue magnesium and calcium affect arbuscular mycorrhiza development and fungal reproduction. Mycorrhiza, 1998, 7(5):237-242

[41] JiangF, ZhangL, ZhouJ, GeorgeTS, FengG. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol, 2021, 230(1):304-315

[42] JingX, CuiQ, LiX, YinJ, RavichandranV, PanD, FuJ, TuQ, WangH, BianX, ZhangY. Engineering Pseudomonas protegens Pf-5 to improve its antifungal activity and nitrogen fixation. Microb Biotechnol, 2020, 13(1):118-133

[43] KabirAH, DebnathT, DasU, PritySA, HaqueA, RahmanMM, et al.. Arbuscular mycorrhizal fungi alleviate Fe-deficiency symptoms in sunflower by increasing iron uptake and its availability along with antioxidant defense. Plant Physiol. Biochem, 2020, 150: 254-262

[44] KaiserBN, GridleyKL, Ngaire BradyJ, PhillipsT, TyermanSD. The role of molybdenum in agricultural plant production. Ann Bot, 2005, 96(5):745-754

[45] KamranS, ShahidI, BaigDN, RizwanM, MalikKA, MehnazS. Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front. Microbiol, 2017, 8: 2593

[46] KanchiswamyCN, MalnoyM, MaffeiME. Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front. Plant Sci, 2015, 6: 151 Artn 151

[47] KerteszMA. Riding the sulfur cycle–metabolism of sulfonates and sulfate esters in gram-negative bacteria. FEMS Microbiol. Rev, 2000, 24(2):135-175

[48] KerteszMA, FellowsE, SchmalenbergerA. Rhizobacteria and plant sulfur supply. Adv Appl Microbiol, 2007, 62: 235-268

[49] KerteszMA, MirleauP. The role of soil microbes in plant Sulphur nutrition. J Exp Bot, 2004, 55(404):1939-1945

[50] KhaitovB. Effects of Rhizobium inoculation and magnesium application on growth and nodulation of soybean (Glycine max L.). J Plant Nutr, 2018, 41(16):2057-2068

[51] KingJ, QuinnJ. The utilization of organosulphonates by soil and freshwater bacteria. Lett Appl Microbiol, 1997, 24(6):474-478

[52] KissSA, Stefanovits-BányaiE, Takács-HájosM. Magnesium-content of rhizobium nodules in different plants: the importance of magnesium in nitrogen-fixation of nodules. J Am Coll Nutr, 2004, 23(6):751S-753S

[53] KloepperJW, LeongJ, TeintzeM, SchrothMN. Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature, 1980, 286(5776):885-886

[54] KongW-L, WangY-H, WuX-Q. Enhanced iron uptake in plants by volatile emissions of Rahnella aquatilis JZ-GX1. Front Plant Sci, 2021, 12: 704000

[55] KothariS, MarschnerH, RömheldV. Effect of a vesicular–arbuscular mycorrhizal fungus and rhizosphere micro-organisms on manganese reduction in the rhizosphere and manganese concentrations in maize (Zea mays L.). New Phytol, 1991, 117(4):649-655

[56] KrithikaS, BalachandarD. Expression of zinc transporter genes in rice as influenced by zinc-solubilizing Enterobacter cloacae strain ZSB14. Front. Plant Sci, 2016, 7: 446

[57] LeeY-J, GeorgeE. Contribution of mycorrhizal hyphae to the uptake of metal cations by cucumber plants at two levels of phosphorus supply. Plant Soil, 2005, 278(1):361-370

[58] LehnertN, DongHT, HarlandJB, HuntAP, WhiteCJ. Reversing nitrogen fixation. Nat Rev Chem, 2018, 2(10):278-289

[59] LiX, ChristieP. Changes in soil solution Zn and pH and uptake of Zn by arbuscular mycorrhizal red clover in Zn-contaminated soil. Chemosphere, 2001, 42(2):201-207

[60] Li X, Yin Y, Fan S, Xu X, Amombo E, Xie Y, Fu J (2021) Aspergillus aculeatus enhances potassium uptake and photosynthetic characteristics in perennial ryegrass by increasing potassium availability. J Appl Microbiol. https://doi.org/10.1111/jam.15186

[61] LiX-L, MarschnerH, GeorgeE. Acquisition of phosphorus and copper by VA-mycorrhizal hyphae and root-to-shoot transport in white clover. Plant Soil, 1991, 136(1):49-57

[62] LimBL, YeungP, ChengC, HillJE. Distribution and diversity of phytate-mineralizing bacteria. ISME J, 2007, 1(4):321-330

[63] LiuX-M, ZhangH. The effects of bacterial volatile emissions on plant abiotic stress tolerance. Front. Plant Sci, 2015, 6

[64] LugtenbergB, KamilovaF. Plant-growth-promoting rhizobacteria. Annu Rev. Microbiol, 2009, 63: 541-556

[65] MarastoniL, PiiY, MaverM, ValentinuzziF, CescoS, MimmoT. Role of Azospirillum brasilense in triggering different Fe chelate reductase enzymes in cucumber plants subjected to both nutrient deficiency and toxicity. Plant Physiol. Biochem, 2019, 136: 118-126

[66] Martínez-MedinaA, Van WeesSC, PieterseCM. Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ, 2017, 40(11):2691-2705

[67] Masood S, Bano A (2016) Mechanism of potassium solubilization in the agricultural soils by the help of soil microorganisms. In Potassium solubilizing microorganisms for sustainable agriculture. Springer, pp 137–147. https://doi.org/10.1007/978-81-322-2776-2_10

[68] MatthesMS, RobilJM, McsteenP. From element to development: the power of the essential micronutrient boron to shape morphological processes in plants. J Exp Bot, 2020, 71(5):1681-1693

[69] MeenaV, MauryaB, BahadurI. Potassium solubilization by bacterial strain in waste mica. Bangladesh J Bot, 2014, 43(2):235-237

[70] MeldauDG, MeldauS, HoangLH, UnderbergS, WünscheH, BaldwinIT. Dimethyl disulfide produced by the naturally associated bacterium Bacillus sp B55 promotes Nicotiana attenuata growth by enhancing sulfur nutrition. Plant Cell, 2013, 25(7):2731-2747

[71] MitchellDB, VogelK, WeimannBJ, PasamontesL, Van LoonAP. The phytase subfamily of histidine acid phosphatases: isolation of genes for two novel phytases from the fungi aspergillus terreus and Myceliophthora thermophila. Microbiology, 1997, 143(1):245-252

[72] MiwaK, KamiyaT, FujiwaraT. Homeostasis of the structurally important micronutrients. B and Si Curr Opin Plant Biol, 2009, 12(3):307-311

[73] MohantyS, GhoshS, NayakS, DasA. Isolation, identification and screening of manganese solubilizing fungi from low-grade manganese ore deposits. Geomicrobiol J, 2017, 34(4):309-316

[74] Montejano-RamírezV, García-PinedaE, Valencia-CanteroE. Bacterial compound N, N-dimethylhexadecylamine modulates expression of iron deficiency and defense response genes in Medicago truncatula independently of the jasmonic acid pathway. Plants, 2020, 9(5):624

[75] MorcilloRJ, SinghSK, HeD, AnG, VílchezJI, TangK, YuanF, SunY, ShaoC, ZhangS, YangY, LiuX, DangY, WangW, GaoJ, HuangW, LeiM, SongCP, ZhuJK, MachoAP, ParéPW, ZhangH. Rhizobacterium-derived diacetyl modulates plant immunity in a phosphate-dependent manner. EMBO J, 2020, 39(2

[76] MorcilloRJL, ManzaneraM. The effects of plant-associated bacterial exopolysaccharides on plant abiotic stress tolerance. Metabolites, 2021, 11 6):337

[77] MoreauC, GautratP, FrugierF. Nitrate-induced CLE35 signaling peptides inhibit nodulation through the SUNN receptor and miR2111 repression. Plant Physiol, 2021, 185(3):1216-1228

[78] MusF, CrookMB, GarciaK, Garcia CostasA, GeddesBA, KouriED, ParamasivanP, RyuMH, OldroydGED, PoolePS, UdvardiMK, VoigtCA, AnéJM, PetersJW. Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol, 2016, 82(13):3698-3710

[79] NagyR, DrissnerD, AmrheinN, JakobsenI, BucherM. Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol, 2009, 181(4):950-959

[80] NagyR, KarandashovV, ChagueV, KalinkevichK, TamasloukhtMB, XuG, et al.. The characterization of novel mycorrhiza-specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J, 2005, 42(2):236-250

[81] NannipieriP, GiagnoniL, LandiL, RenellaG. BunemannEK, ObersonA, FrossardE. Role of phosphatase enzymes in soil. In ‘phosphorus in action’, 2011 Berlin, Heidelberg Springer 215-243

[82] NguyenTD, CavagnaroTR, Watts-WilliamsSJ. The effects of soil phosphorus and zinc availability on plant responses to mycorrhizal fungi: a physiological and molecular assessment. Sci Rep, 2019, 9(1):1-13

[83] NogueiraMA, CardosoEJBN. Mycorrhizal effectiveness and manganese toxicity in soybean as affected by soil type and endophyte. Sci Agric, 2003, 60: 329-335

[84] PaszkowskiU, KrokenS, RouxC, BriggsSP. Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. PNAS USA, 2002, 99(20):13324-13329

[85] PengL, ShanX, YangY, WangY, DruzhininaIS, PanX, JinW, HeX, WangX, ZhangX, MartinFM, YuanZ. Facultative symbiosis with a saprotrophic soil fungus promotes potassium uptake in American sweetgum trees. Plant Cell Environ, 2021, 44(8):2793-2809

[86] PernerH, SchwarzD, BrunsC, MäderP, GeorgeE. Effect of arbuscular mycorrhizal colonization and two levels of compost supply on nutrient uptake and flowering of pelargonium plants. Mycorrhiza, 2007, 17(5):469-474

[87] PrasadD, VermaN, BakshiM, NarayanOP, SinghAK, DuaM, JohriAK. Functional characterization of a magnesium transporter of root endophytic fungus Piriformospora indica. Front Microbiol, 2019, 9: 3231

[88] PritySA, SajibSA, DasU, RahmanMM, HaiderSA, KabirAH. Arbuscular mycorrhizal fungi mitigate Fe deficiency symptoms in sorghum through phytosiderophore-mediated Fe mobilization and restoration of redox status. Protoplasma, 2020, 257(5):1373-1385

[89] QuirogaG, EriceG, ArocaR, Ruiz-LozanoJM. Elucidating the possible involvement of maize aquaporins in the plant boron transport and homeostasis mediated by Rhizophagus irregularis under drought stress conditions. Int J Mol Sci, 2020, 21(5):1748

[90] RajkumarM, AeN, PrasadMNV, FreitasH. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol, 2010, 28(3):142-149

[91] RauschC, DaramP, BrunnerS, JansaJ, LaloiM, LeggewieG, AmrheinN, BucherM. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature, 2001, 414(6862):462-465

[92] RelićB, PerretX, Estrada-GarcíaMT, KopcinskaJ, GolinowskiW, KrishnanH, et al.. Nod factors of Rhizobium are a key to the legume door. Mol Microbiol, 1994, 13(1):171-179

[93] RiazN, GuerinotML. All together now: regulation of the iron deficiency response. J Exp Bot, 2021, 72(6):2045-2055

[94] RichardsonAE, SimpsonRJ. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol, 2011, 156(3):989-996

[95] Rodrı́GuezH, FragaR. Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv, 1999, 17(4–5):319-339

[96] RoyS, LiuW, NandetyRS, CrookA, MysoreKS, PislariuCI, FrugoliJ, DicksteinR, UdvardiMK. Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation. Plant Cell, 2020, 32(1):15-41

[97] SaboorA, AliMA, DanishS, AhmedN, FahadS, DattaR, AnsariMJ, NasifO, RahmanMH, GlickBR. Effect of arbuscular mycorrhizal fungi on the physiological functioning of maize under zinc-deficient soils. Sci Rep, 2021, 11(1):1-11

[98] SaiaS, RappaV, RuisiP, AbenavoliMR, SunseriF, GiambalvoD, FrendaAS, MartinelliF. Soil inoculation with symbiotic microorganisms promotes plant growth and nutrient transporter genes expression in durum wheat. Front. Plant Sci, 2015, 6: 815

[99] SanketA, GhoshS, SahooR, NayakS, DasA. Molecular identification of acidophilic manganese (Mn)-solubilizing bacteria from mining effluents and their application in mineral beneficiation. Geomicrobiol J, 2017, 34(1):71-80

[100] SantosK, MoureV, HauerV, SantosAS, DonattiL, GalvãoC, et al.. Wheat colonization by an Azospirillum brasilense ammonium-excreting strain reveals upregulation of nitrogenase and superior plant growth promotion. Plant Soil, 2017, 415(1):245-255

[101] SharmaSB, SayyedRZ, TrivediMH, GobiTA. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus, 2013, 2(1):1-14

[102] ShiZ, ZhangJ, LuS, LiY, WangF. Arbuscular mycorrhizal fungi improve the performance of sweet sorghum grown in a Mo-contaminated soil. J Fungi, 2020, 6(2):44

[103] ShiZ, ZhangJ, WangF, LiK, YuanW, LiuJ. Arbuscular mycorrhizal inoculation increases molybdenum accumulation but decreases molybdenum toxicity in maize plants grown in polluted soil. RSC Adv, 2018, 8(65):37069-37076

[104] ShorrocksVM. The occurrence and correction of boron deficiency. Plant Soil, 1997, 193(1):121-148

[105] SmilV. Phosphorus in the environment: natural flows and human interferences. Annu Rev Energ Environ, 2000, 25(1):53-88

[106] SmithMJ, ShooleryJ, SchwynB, HoldenI, NeilandsJ. Rhizobactin, a structurally novel siderophore from Rhizobium meliloti. J Am Chem Soc, 1985, 107(6):1739-1743

[107] StringlisIA, YuK, FeussnerK, De JongeR, Van BentumS, Van VerkMC, et al.. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. PNAS USA, 2018, 115(22):E5213-E5E22

[108] SvistoonoffS, HocherV, GherbiH. Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation. Curr Opin Plant Biol, 2014, 20: 11-18

[109] TakahashiH, KoprivaS, GiordanoM, SaitoK, HellR. Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol, 2011, 62: 157-184

[110] VaidSK, KumarB, SharmaA, ShuklaA, SrivastavaP. Effect of Zn solubilizing bacteria on growth promotion and Zn nutrition of rice. J Soil Sci Plant Nutr, 2014, 14(4):889-910

[111] Van VelzenR, HolmerR, BuF, RuttenL, Van ZeijlA, LiuW, et al.. Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses. PNAS USA, 2018, 115(20):E4700-E47E9

[112] VermeijP, WietekC, KahnertA, WuèestT, KerteszMA. Genetic organization of Sulphur-controlled aryl desulphonation in Pseudomonas putida S-313. Mol Microbiol, 1999, 32(5):913-926

[113] VílchezJI, YangY, HeD, ZiH, PengL, LvS, KaushalR, WangW, HuangW, LiuR, LangZ, MikiD, TangK, ParéPW, SongCP, ZhuJK, ZhangH. DNA demethylases are required for myo-inositol-mediated mutualism between plants and beneficial rhizobacteria. Nat Plants, 2020, 6(8):983-995

[114] WangS, ChenA, XieK, YangX, LuoZ, ChenJ, ZengD, RenY, YangC, WangL, FengH, López-ArredondoDL, Herrera-EstrellaLR, XuG. Functional analysis of the OsNPF4. 5 nitrate transporter reveals a conserved mycorrhizal pathway of nitrogen acquisition in plants. PNAS USA, 2020, 117(28):16649-16659

[115] Watts-WilliamsSJ, CavagnaroTR. Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar. Plant Sci, 2018, 274: 163-170

[116] Watts-WilliamsSJ, PattiAF, CavagnaroTR. Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil, 2013, 371(1):299-312

[117] WeisskopfL, SchulzS, GarbevaP. Microbial volatile organic compounds in intra-kingdom and inter-kingdom interactions. Nat Rev Microbiol, 2021, 19(6):391-404

[118] WhitelawM, HardenT, HelyarK. Phosphate solubilisation in solution culture by the soil fungus Penicillium radicum. Soil Biol Biochem, 1999, 31(5):655-665

[119] XuG-H, ChagueV, Melamed-BessudoC, KapulnikY, JainA, RaghothamaKG, LevyAA, SilberA. Functional characterization of LePT4: a phosphate transporter in tomato with mycorrhiza-enhanced expression. J Exp Bot, 2007, 58(10):2491-2501

[120] YuP, HeX, BaerM, BeirinckxS, TianT, MoyaYA, et al.. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nat Plants, 2021, 7(4):481-499

[121] ZamioudisC, KortelandJ, Van PeltJA, Van HamersveldM, DombrowskiN, BaiY, et al.. Rhizobacterial volatiles and photosynthesis-related signals coordinate MYB 72 expression in Arabidopsis roots during onset of induced systemic resistance and iron-deficiency responses. Plant J, 2015, 84(2):309-322

[122] ZhangF, DuP, SongC-X, WuQ-S. Alleviation of mycorrhiza to magnesium deficiency in trifoliate orange: changes in physiological activity. Emir J Food Agric, 2015, 27: 763-769

[123] ZhangH, SunY, XieX, KimMS, DowdSE, ParéPW. A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J, 2009, 58(4):568-577

[124] ZhangH, XieX, KimMS, KornyeyevDA, HoladayS, ParéPW. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J, 2008, 56(2):264-273

[125] ZhaoF, LehmannJ, SolomonD, FoxM, McgrathS. Sulphur speciation and turnover in soils: evidence from Sulphur K-edge XANES spectroscopy and isotope dilution studies. Soil Biol Biochem, 2006, 38(5):1000-1007

[126] ZhouC, GuoJ, ZhuL, XiaoX, XieY, ZhuJ, et al.. Paenibacillus polymyxa BFKC01 enhances plant iron absorption via improved root systems and activated iron acquisition mechanisms. Plant Physiol Biochem, 2016, 105: 162-173

Funding

Chinese Academy of Sciences