Abstract
Moderate soil drying (MSD) is a promising agricultural technique that can reduce water consumption and enhance rhizosheath formation promoting drought resistance in plants. The endophytic fungus Piriformospora indica (P. indica) with high auxin production may be beneficial for rhizosheath formation. However, the integrated role of P. indica with native soil microbiome in rhizosheath formation is unclear. Here, we investigated the roles of P. indica and native bacteria on rice rhizosheath formation under MSD using high-throughput sequencing and rice mutants. Under MSD, rice rhizosheath formation was significantly increased by around 30% with P. indica inoculation. Auxins in rice roots and P. indica were responsible for the rhizosheath formation under MSD. Next, the abundance of the genus Bacillus, known as plant growth-promoting rhizobacteria, was enriched in the rice rhizosheath and root endosphere with P. indica inoculation under MSD. Moreover, the abundance of Bacillus cereus (B. cereus) with high auxin production was further increased by P. indica inoculation. After inoculation with both P. indica and B. cereus, rhizosheath formation in wild-type or auxin efflux carrier OsPIN2 complemented line rice was higher than that of the ospin2 mutant. Together, our results suggest that the interaction of the endophytic fungus P. indica with the native soil bacterium B. cereus favors rice rhizosheath formation by auxins modulation in rice and microbes under MSD. This finding reveals a cooperative contribution of P. indica and native microbiota in rice rhizosheath formation under moderate soil drying, which is important for improving water use in agriculture.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Fageria N. Yield physiology of rice. J Plant Nutr. 2007;30:843–79.
Wang Z, Zhang W, Beebout S, Zhang H, Liu L, Yang J, et al. Grain yield, water and nitrogen use efficiencies of rice as influenced by irrigation regimes and their interaction with nitrogen rates. Field Crops Res. 2016;193:54–69.
Zhang H, Xue Y, Wang Z, Yang J, Zhang J. An alternate wetting and moderate soil drying regime improves root and shoot growth in rice. Crop Sci. 2009;49:2246–60.
Bouman B, Tuong T. Field water management to save water and increase its productivity in irrigated lowland rice. Agr Water Manag. 2001;49:11–30.
Harrison M, Tardieu F, Dong Z, Messina C, Hammer G. Characterizing drought stress and trait influence on maize yield under current and future conditions. Glob Change Biol. 2014;20:867–78.
Lesk C, Rowhani P, Ramankutty N. Influence of extreme weather disasters on global crop production. Nature. 2016;529:84–87.
Thorup-Kristensen K, Kirkegaard J. Root system-based limits to agricultural productivity and efficiency: the farming systems context. Ann Bot. 2016;118:573–92.
Yao F, Huang J, Cui K, Nie L, Xiang J, Liu X, et al. Agronomic performance of high-yielding rice variety grown under alternate wetting and drying irrigation. Field Crops Res. 2012;126:16–22.
Danin A. Plant adaptations to environmental stresses in desert dunes. In: Danin A (ed). Plants of desert dunes. (Springer, Berlin, 1996), pp 133–152.
Pang J, Ryan M, Siddique K, Simpson R. Unwrapping the rhizosheath. Plant Soil. 2017;418:129–39.
Marasco R, Mosqueira M, Fusi M, Ramond J, Merlino G, Booth J, et al. Rhizosheath microbial community assembly of sympatric desert speargrasses is independent of the plant host. Microbiome. 2018;6:215.
Zhang Y, Du H, Gui Y, Xu F, Liu J, Zhang J, et al. Moderate water stress induces rice rhizosheath formation associated with ABA and auxin responses. J Exp Bot. 2020;71:2740–51.
Duell R, Peacock G. Rhizosheaths on mesophytic grasses. Crop Sci. 1985;25:880–3.
Ndour P, Gueye M, Barakat M, Ortet P, Bertrand-Huleux M, Pablo A, et al. Pearl millet genetic traits shape rhizobacterial diversity and modulate rhizosphere aggregation. Front Plant Sci. 2017;8:1288.
Philippot L, Raaijmakers J, Lemanceau P, van der Putten W. Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol. 2013;11:789–99.
Ndour P, Heulin T, Achouak W, Laplaze L, Cournac L. The rhizosheath: from desert plants adaptation to crop breeding. Plant Soil. 2020;456:1–13.
George T, Brown L, Ramsay L, White P, Newton A, Bengough A, et al. Understanding the genetic control and physiological traits associated with rhizosheath production by barley (Hordeum vulgare). N Phytol. 2014;203:195–205.
Zhang Y, Du H, Xu F, Ding Y, Gui Y, Zhang J, et al. Root-bacterial associations boost rhizosheath formation in moderately dry soil through ethylene responses. Plant Physiol. 2020;183:780–92.
Basirat M, Mousavi S, Abbaszadeh S, Ebrahimi M, Zarebanadkouki M. The rhizosheath: a potential root trait helping plants to tolerate drought stress. Plant Soil. 2019;445:565–75.
Othman A, Amer W, Fayez M, Hegazi N. Rhizosheath of sinai desert plants is a potential repository for associative diazotrophs. Microbiol Res. 2004;159:285–93.
Haling R, Richardson A, Culvenor R, Lambers H, Simpson R. Root morphology, root-hair development and rhizosheath formation on perennial grass seedlings is influenced by soil acidity. Plant Soil. 2010;335:457–68.
Delhaize E, James R, Ryan P. Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil. N Phytol.2012;195:609–19.
Liu T, Ye N, Song T, Cao Y, Gao B, Zhang D, et al. Rhizosheath formation and involvement in foxtail millet (Setaria italica) root growth under drought stress. J Integr Plant Biol. 2019;61:449–62.
Liu T, Chen M, Zhang Y, Zhu F, Liu Y, Tian Y, et al. Comparative metabolite profiling of two switchgrass ecotypes reveals differences in drought stress responses and rhizosheath weight. Planta. 2019;250:1355–69.
Brown L, George T, Neugebauer K, White P. The rhizosheath–a potential trait for future agricultural sustainability occurs in orders throughout the angiosperms. Plant Soil. 2017;418:115–28.
Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, et al. Piriformospora indica affects plant growth by auxin production. Physiol Plant. 2007;131:581–9.
Weiβ M, Waller F, Zuccaro A, Selosse M. Sebacinales-one thousand and one interactions with land plants. N Phytol. 2016;211:20–40.
Vadassery J, Ranf S, Drzewiecki C, Mithoer A, Mazars C, Scheel D, et al. A cell wall extract from the endophytic fungus Piriformospora indica promotes growth of Arabidopsis seedlings and induces intracellular calcium elevation in roots. Plant J. 2009;59:193–206.
Lee Y, Johnson J, Chien C, Sun C, Cai D, Lou B, et al. Growth promotion of Chinese cabbage and Arabidopsis by Piriformospora indica is not stimulated by mycelium-synthesized auxin. Mol Plant Microbe Interact. 2011;24:421–31.
Dong S, Tian Z, Chen P, Senthil Kumar R, Shen C, Cai D, et al. The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots. J Exp Bot. 2013;64:4529–40.
Rani M, Raj S, Dayaman V, Kumar M, Dua M, Johri A. Functional characterization of a hexose transporter from root endophyte Piriformospora indica. Front Microbiol. 2016;7:1083.
Prasad D, Verma N, Bakshi M, Narayan O, Singh A, Dua M, et al. Functional characterization of a magnesium transporter of root endophytic fungus Piriformospora indica. Front Microbiol. 2018;9:3231.
Narayan O, Verma N, Jogawat A, Dua M, Johri A. Sulfur transfer from the endophytic fungus Serendipita indica improves maize growth and requires the sulfate transporter SiSulT. Plant Cell. 2021;33:1268–85.
Baltruschat H, Fodor J, Harrach B, Niemcayk E, Barna B, Gullner G, et al. Salt tolerance of barley induced by the root endophyte Piriformospora indica is associated with a strong increase in antioxidants. N Phytol. 2008;180:501–10.
Jogawat A, Saha S, Bakshi M, Dayaman V, Kumar M, Dua M, et al. Piriformospora indica rescues growth diminution of rice seedlings during high salt stress. Plant Signal Behav. 2013;8:e26891.
Fakhro A, Andrade-Linares D, von Bargen S, Bandte M, Buttner C, Grosch R. Impact of Piriformospora indica on tomato growth and on interaction with fungal and viral pathogens. Mycorrhiza. 2010;20:191–200.
Sarma M, Kumar V, Saharan K, Srivastava R, Sharma A, Prakash A, et al. Application of inorganic carrier-based formulations of fluorescent pseudomonads and Piriformospora indica on tomato plants and evaluation of their efficacy. J Appl Microbiol. 2011;111:456–66.
Sun C, Shao Y, Vahabi K, Lu J, Bhattacharya S, Dong S, et al. The beneficial fungus Piriformospora indica protects Arabidopsis from Verticillium dahliae infection by downregulation plant defense responses. BMC Plant Biol. 2014;14:268.
Abdelaziz M, Abdelsattar M, Abdeldaym E, Atia M, Mahmoud A, Saad M, et al. Piformospora indica alters Na+/K+ homeostasis, antioxidant enzymes and LeNHX1 expression of greenhouse tomato grown under salt stress. Sci Hortic. 2019;256:108532.
Zhang W, Wang J, Xu L, Wang A, Huang L, Du H, et al. Drought stress responses in maize are diminished by Piriformospora indica. Plant Signal Behav. 2017;13:e1414121.
Pion M, Spangenberg J, Simon A, Bindschedler S, Flury C, Chatelain A, et al. Bacterial farming by the fungus Morchella crassipes. Proc R Soc B. 2013;280:20132242.
Guhr A, Borken W, Spohn M, Matzner E. Redistribution of soil water by a saprotrophic fungus enhances carbon mineralization. Proc Natl Acad Sci USA. 2015;112:14647–51.
Warmink J, Nazir R, van Elsas J. Universal and species-specific bacterial ‘fungiphiles’ in the mycospheres of different basidiomycetous fungi. Environ Microbiol. 2009;11:300–12.
Nazir R, Warmink J, Boersma H, van Elsas J. Mechanisms that promote bacterial fitness in fungal-affected soil microhabitats. FEMS Microbiol Ecol. 2010;71:169–85.
Wang L, Guo M, Li Y, Ruan W, Mo X, Wu Z, et al. LARGE ROOT ANGLE1, encoding OsPIN2, is involved in root system architecture in rice. J Exp Bot. 2018;69:385–97.
Bütehorn B, Rhody D, Franken P. Isolation and characterization of Pitef1 encoding the translation elongation factor EF-1α of the root endophyte Piriformospora indica. Plant Biol. 2008;2:687–92.
Haling R, Brown L, Bengough A, Young I, Hallett P, White P, et al. Root hairs improve root penetration, root-soil contact, and phosphorus acquisition in soils of different strength. J Exp Bot. 2013;64:3711–21.
Hou M, Luo F, Wu D, Zhang X, Lou M, Shen D, et al. OsPIN9, an auxin efflux carrier, is required for the regulation of rice tiller bud outgrowth by ammonium. N Phytol 2021;229:935–49.
Yuan J, Ruan Y, Wang B, Zhang J, Waseem R, Huang Q, et al. Plant growth-promoting rhizobacteria strain Bacillus amyloliquefaciens NJN-6-enriched bio-organic fertilizer suppressed Fusarium wilt and promoted the growth of banana plants. J Agr Food Chem. 2013;61:3774–80.
Xu F, Wang K, Yuan W, Xu W, Liu S, Kronzucker H, et al. Overexpression of aquaporin OsPIP1;2 in rice improves yield by enhancing mesophyll CO2 conductance and phloem sucrose transport. J Exp Bot. 2019;70:671–81.
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 2012;488:91–95.
Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, et al. A drought resistance-promoting microbiome is selected by root system under desert farming. PLoS One. 2012;7:e48479.
Bodenhausen N, Horton M, Bergelson J. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS One. 2013;8:e56329.
Schlaeppi K, Dombrowski N, Oter R, Themaat E, Schulze-Lefert P. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci USA. 2014;111:585–92.
Han Q, Ma Q, Chen Y, Tian B, Xu L, Bai Y, et al. Variation in rhizosphere microbial communities and its association with the symbiotic efficiency of rhizobia in soybean. ISME J. 2020;14:1915–28.
Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018;34:i884–90.
Edgar R. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1.
Edgar R. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996–8.
Wang Q, Garrity G, Tiedje J, Cole J. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microb. 2007;73:5261–7.
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.
Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb. 2009;75:7537–41.
Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, et al. Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils. 2013;49:435–46.
Turner J, Backman P. Factors relating to peanut yield increases after seed treatment with Bacillus subtilis. Plant Dis. 1991;75:347–53.
Wei Z, Gu Y, Friman V, Kowalchuk G, Xu Y, Shen Q, et al. Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv. 2019;5:eaaw0759.
Zhang W, Li X, Sun K, Tang M, Xu F, Zhang M, et al. Mycelial network-mediated rhizobial dispersal enhances legume nodulation. ISME J. 2020;14:1015–29.
Mela F, Fritsche K, de Boer W, van Veen J, de Graaff L, van den Berg M, et al. Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger. ISME J. 2011;5:1494–504.
Berendsen R, Vismans G, Yu K, Song Y, de Jonge R, Burgman W, et al. Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J. 2018;12:1496–507.
Zhang J, Liu Y, Zhang N, Hu B, Jin T, Xu H, et al. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol. 2019;37:676–84.
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, et al. The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA. 2005;102:13386–91.
Chen T, Nomura K, Wang X, Sohrabi R, Xu J, Yao L, et al. A plant genetic network for preventing dysbiosis in the phyllosphere. Nature. 2020;580:653–7.
Rolli E, Marasco R, Vigani G, Ettoumi B, Mapelli F, Deangelis M, et al. Improved plant resistance to drought is promoted by the root-associated microbiome as a water stress-dependent trait. Environ Microbiol. 2015;17:316–31.
Preece C, Peñuelas J. Rhizodeposition under drought and consequences for soil communities and ecosystem resilience. Plant Soil. 2016;409:1–17.
Bezzate S, Aymerich S, Chambert R, Czarnes S, Berge O, Heulin T. Disruption of the Paenibacillus polymyxa levansucrase gene impairs its ability to aggregate soil in the wheat rhizosphere. Environ Microbiol. 2000;2:333–42.
Alami Y, Achouak W, Marol C, Heulin T. Rhizosphere soil aggregation and plant growth promotion of sunflowers by an exopolysaccharide-producing Rhizobium sp. strain isolated from sunflower roots. Appl Environ Microbiol. 2000;66:3393–8.
Berge O, Lodhi A, Brandelet G, Santaella C, Roncato M, Christen R, et al. Rhizobium alamii sp. nov., an exopolysaccharide-producing species isolated from legume and non-legume rhizospheres. Int J Syst Evol Microbiol. 2009;59:367–72.
Moreno-EspÃndola I, Rivera-Becerril F, de Jesús F-GM, De León-González F. Role of root-hairs and hyphae in adhesion of sand particles. Soil Biol Biochem. 2007;39:2520–6.
Watt M, Mccully M, Canny M. Formation and stabilization of rhizosheaths of Zea mays L. (effect of soil water content). Plant Physiol. 1994;106:179–86.
Schafer P, Pfiffi S, Voll L, Zajic D, Chandler P, Waller F, et al. Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J. 2009;59:461–74.
Xu W, Jia L, Shi W, Liang J, Zhou F, Li Q, et al. Abscisic acid accumulation modulates auxin transport in the root tip to enhance proton secretion for maintaining root growth under moderate water stress. N Phytol. 2013;197:139–50.
Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat Genet. 2013;45:1097–102.
Luschnig C, Gaxiola R, Grisafi P, Fink G. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998;12:2175–87.
Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 1998;17:6903–11.
de Boer W, Folman R, Summerbell R, Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29:795–811.
Hogan D, Kolter R. Pseudomonas-Candida interactions: an ecological role for virulence factors. Science. 2002;296:2229–32.
Ravnskov S, Nybroe O, Jakobsen I. Influence of an arbuscular mycorrhizal fungus on Pseudomonas fluorescens DF57 in rhizosphere and hyphosphere soil. N Phytol. 1999;142:113–22.
Torsvik V, Øvreas L, Thingstad T. Prokaryotic diversity-magnitude, dynamics, and controlling factors. Science. 2002;296:1064–6.
Wamberg C, Christensen S, Jakobsen I, Müller A, Sørensen S. The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem. 2003;35:1349–57.
van Hees P, Rosling A, Essen S, Godbold D, Jones D, Finlay R. Oxalate and ferricrocin exudation by the extrametrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. N Phytol. 2006;169:367–78.
Acknowledgements
We thank Prof. Chuanzao Mao (Zhejiang University, Hangzhou, China) for donating the ospin2, Complementation lines and cv. Hei-Jing2 rice seeds, Prof. Faxing Chen (Fujian Agriculture and Forestry University, Fuzhou, China) for P. indica-GFP strain and Dr. Chengyuan Tao, Dr. Guan Pang (Nanjing Agricultural University, Nanjing, China) for sharing microbial technology. We are grateful for the financial support from the National Key Research and Development Program of China (2017YFE0118100), National Natural Science Foundation of China (31761130073 and 31872169) and Postdoctoral Science Foundation of China (2020M671920).
Author information
Authors and Affiliations
Contributions
WX and FX planned and designed the research. FX, YZ, JL, LS, XZ, JY, KW, XW, and YD conducted most of the experiments. FX, HL, YZ, MY and CL analyzed the data. FX, HL, CR, JZ, KY and WX wrote the article. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Xu, F., Liao, H., Zhang, Y. et al. Coordination of root auxin with the fungus Piriformospora indica and bacterium Bacillus cereus enhances rice rhizosheath formation under soil drying. ISME J 16, 801–811 (2022). https://doi.org/10.1038/s41396-021-01133-3
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/s41396-021-01133-3
This article is cited by
-
Nutrient and mycoremediation of a global menace ‘arsenic’: exploring the prospects of phosphorus and Serendipita indica-based mitigation strategies in rice and other crops
Plant Cell Reports (2024)
-
Auxin-producing bacteria promote barley rhizosheath formation
Nature Communications (2023)
-
Hyphosphere microorganisms facilitate hyphal spreading and root colonization of plant symbiotic fungus in ammonium-enriched soil
The ISME Journal (2023)
-
Halophyte functional groups influence seasonal variations in rhizosphere microbial necromass and enzyme activities in an inland saline ecosystem
Biology and Fertility of Soils (2023)
-
Bacillus sp. LC390B from the Maize Rhizosphere Improves Plant Biomass, Root Elongation, and Branching and Requires the Phytochromes PHYA and PHYB for Phytostimulation
Journal of Plant Growth Regulation (2023)
