Serendipita bescii promotes winter wheat growth and modulates the host root transcriptome under phosphorus and nitrogen starvation

Ray, Prasun; Guo, Yingqing; Chi, Myoung‐Hwan; Krom, Nick; Saha, Malay C.; Craven, Kelly D.

doi:10.1111/1462-2920.15242

Title: Serendipita bescii promotes winter wheat growth and modulates the host root transcriptome under phosphorus and nitrogen starvation

Journal Article · Mon Oct 05 00:00:00 EDT 2020 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.15242· OSTI ID:1670483

^[1]; Guo, Yingqing ^[1]; Chi, Myoung‐Hwan ^[1]; Krom, Nick ^[1]; Saha, Malay C. ^[1];

^[1]

Noble Research Institute, LLC Ardmore OK 73401 USA

Summary Serendipita vermifera ssp. bescii , hereafter referred to as S. bescii , is a root‐associated fungus that promotes plant growth in both its native switchgrass host and a variety of monocots and dicots. Winter wheat ( Triticum aestivum L.), a dual‐purpose crop, used for both forage and grain production, significantly contributes to the agricultural economies of the Southern Great Plains, USA. In this study, we investigated the influence of S. bescii on growth and transcriptome regulation of nitrogen (N) and phosphorus (P) metabolism in winter wheat. Serendipita bescii significantly improved lateral root growth and forage biomass under a limited N or P regime. Further, S. bescii activated sets of host genes regulating N and P starvation responses. These genes include, root‐specific auxin transport, strigolactone and gibberellin biosynthesis, degradation of phospholipids and biosynthesis of glycerolipid, downregulation of ammonium transport and nitrate assimilation, restriction of protein degradation by autophagy and subsequent N remobilization. All these genes are hypothesized to regulate acquisition, assimilation and remobilization of N and P. Based on transcriptional level gene regulation and physiological responses to N or P limitation, we suggest S. bescii plays a critical role in modulating stress imposed by limitation of these two critical nutrients in winter wheat.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1670483

Alternate ID(s):: OSTI ID: 1786954; OSTI ID: 1816289

Journal Information:: Environmental Microbiology, Journal Name: Environmental Microbiology Vol. 23 Journal Issue: 4; ISSN 1462-2912

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (60)

Global nitrogen budgets in cereals: A 50-year assessment for maize, rice and wheat production systems Ladha, J. K.; Tirol-Padre, A.; Reddy, C. K. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19355	journal	January 2016
Morphological responses of wheat ( Triticum aestivum L.) roots to phosphorus supply in two contrasting soils Yuan, H. M.; Blackwell, M.; Mcgrath, S. The Journal of Agricultural Science, Vol. 154, Issue 1 https://doi.org/10.1017/S0021859615000702	journal	July 2015
Performance of the Biocontrol Fungus Piriformospora indica on Wheat Under Greenhouse and Field Conditions Serfling, Albrecht; Wirsel, Stefan G. R.; Lind, Volker Phytopathology®, Vol. 97, Issue 4 https://doi.org/10.1094/PHYTO-97-4-0523	journal	April 2007
Yield Gap and Production Gap of Rainfed Winter Wheat in the Southern Great Plains Patrignani, Andres; Lollato, Romulo P.; Ochsner, Tyson E. Agronomy Journal, Vol. 106, Issue 4 https://doi.org/10.2134/agronj14.0011	journal	January 2014
Towards an Integrated Mycorrhizal Technology: Harnessing Mycorrhiza for Sustainable Intensification in Agriculture Rillig, Matthias C.; Sosa-Hernández, Moisés A.; Roy, Julien Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01625	journal	October 2016
Arabidopsis AIR12 influences root development Gibson, Shawn W.; Todd, Christopher D. Physiology and Molecular Biology of Plants, Vol. 21, Issue 4 https://doi.org/10.1007/s12298-015-0323-1	journal	September 2015
Anthocyanins in vegetative tissues: a proposed unified function in photoprotection Steyn, W. J.; Wand, S. J. E.; Holcroft, D. M. New Phytologist, Vol. 155, Issue 3 https://doi.org/10.1046/j.1469-8137.2002.00482.x	journal	September 2002
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Letter to the editor Dole?el, J.; Barto?, J.; Voglmayr, H. Cytometry, Vol. 51A, Issue 2 https://doi.org/10.1002/cyto.a.10013	journal	January 2003
Identification and overexpression of gibberellin 2-oxidase ( GA2ox ) in switchgrass ( Panicum virgatum L.) for improved plant architecture and reduced biomass recalcitrance Wuddineh, Wegi A.; Mazarei, Mitra; Zhang, Jiyi Plant Biotechnology Journal, Vol. 13, Issue 5 https://doi.org/10.1111/pbi.12287	journal	November 2014
Molecular and physiological aspects of nitrate uptake in plants Crawford, Nigel M.; Glass, Anthony D. M. Trends in Plant Science, Vol. 3, Issue 10 https://doi.org/10.1016/S1360-1385(98)01311-9	journal	October 1998
The transcription factor PHR1 regulates lipid remodeling and triacylglycerol accumulation in Arabidopsis thaliana during phosphorus starvation Pant, Bikram Datt; Burgos, Asdrubal; Pant, Pooja Journal of Experimental Botany, Vol. 66, Issue 7 https://doi.org/10.1093/jxb/eru535	journal	February 2015
Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency Kant, S.; Bi, Y. -M.; Rothstein, S. J. Journal of Experimental Botany, Vol. 62, Issue 4 https://doi.org/10.1093/jxb/erq297	journal	October 2010
Root colonization by Piriformospora indica enhances grain yield in barley under diverse nutrient regimes by accelerating plant development Achatz, Beate; von Rüden, Sibylle; Andrade, Diana Plant and Soil, Vol. 333, Issue 1-2 https://doi.org/10.1007/s11104-010-0319-0	journal	March 2010
Effects of phosphate availability on the root system architecture: large-scale analysis of the natural variation between Arabidopsis accessions: Phosphate and root growth in Arabidopsis accessions Chevalier, F.; Pata, M.; Nacry, P. Plant, Cell & Environment, Vol. 26, Issue 11 https://doi.org/10.1046/j.1365-3040.2003.01100.x	journal	September 2003
A Novel Phosphatidylcholine-hydrolyzing Phospholipase C Induced by Phosphate Starvation in Arabidopsis Nakamura, Yuki; Awai, Koichiro; Masuda, Tatsuru Journal of Biological Chemistry, Vol. 280, Issue 9 https://doi.org/10.1074/jbc.M408799200	journal	December 2004
A Novel Class of Gibberellin 2-Oxidases Control Semidwarfism, Tillering, and Root Development in Rice Lo, Shuen-Fang; Yang, Show-Ya; Chen, Ku-Ting The Plant Cell, Vol. 20, Issue 10 https://doi.org/10.1105/tpc.108.060913	journal	October 2008
Communities of Endophytic Sebacinales Associated with Roots of Herbaceous Plants in Agricultural and Grassland Ecosystems Are Dominated by Serendipita herbamans sp. nov Riess, Kai; Oberwinkler, Franz; Bauer, Robert PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0094676	journal	April 2014
Non-targeted Colonization by the Endomycorrhizal Fungus, Serendipita vermifera, in Three Weeds Typically Co-occurring with Switchgrass Ray, Prasun; Guo, Yingqing; Kolape, Jaydeep Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.02236	journal	January 2018
Determining the Optimal N Input to Improve Grain Yield and Quality in Winter Wheat With Reduced Apparent N Loss in the North China Plain Ma, Geng; Liu, Weixing; Li, Shasha Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00181	journal	February 2019
Sebacina vermifera: a unique root symbiont with vast agronomic potential Ray, Prasun; Craven, Kelly D. World Journal of Microbiology and Biotechnology, Vol. 32, Issue 1 https://doi.org/10.1007/s11274-015-1970-7	journal	December 2015
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
The ER Chaperone LHS1 Is Involved in Asexual Development and Rice Infection by the Blast Fungus Magnaporthe oryzae Yi, Mihwa; Chi, Myoung-Hwan; Khang, Chang Hyun The Plant Cell, Vol. 21, Issue 2 https://doi.org/10.1105/tpc.107.055988	journal	February 2009
Endophytic fungus Serendipita indica increased nutrition absorption and biomass accumulation in Cunninghamia lanceolata seedlings under low phosphate Wu, Chu; Li, Bincheng; Wei, Qiao Acta Ecologica Sinica, Vol. 39, Issue 1 https://doi.org/10.1016/j.chnaes.2018.06.005	journal	February 2019
DiVenn: An Interactive and Integrated Web-Based Visualization Tool for Comparing Gene Lists Sun, Liang; Dong, Sufen; Ge, Yinbing Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00421	journal	May 2019
Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System López-Bucio, José; Hernández-Abreu, Esmeralda; Sánchez-Calderón, Lenin Plant Physiology, Vol. 129, Issue 1 https://doi.org/10.1104/pp.010934	journal	April 2002
The Endophytic Fungus Piriformospora indica Stimulates the Expression of Nitrate Reductase and the Starch-degrading Enzyme Glucan-water Dikinase in Tobacco and Arabidopsis Roots through a Homeodomain Transcription Factor That Binds to a Conserved Motif in Their Promoters Sherameti, Irena; Shahollari, Bationa; Venus, Yvonne Journal of Biological Chemistry, Vol. 280, Issue 28 https://doi.org/10.1074/jbc.M500447200	journal	February 2005
Piriformospora indica and Sebacina vermifera increase growth performance at the expense of herbivore resistance in Nicotiana attenuata Barazani, Oz; Benderoth, Markus; Groten, Karin Oecologia, Vol. 146, Issue 2 https://doi.org/10.1007/s00442-005-0193-2	journal	July 2005
Piriformospora indica , a Cultivable Plant-Growth-Promoting Root Endophyte Varma, Ajit; Verma, Savita Applied and Environmental Microbiology, Vol. 65, Issue 6, p. 2741-2744 https://doi.org/10.1128/AEM.65.6.2741-2744.1999	journal	June 1999
Nitrate: A Crucial Signal during Lateral Roots Development Sun, Cui-Hui; Yu, Jian-Qiang; Hu, Da-Gang Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00485	journal	April 2017
Sebacinales – one thousand and one interactions with land plants Weiß, Michael; Waller, Frank; Zuccaro, Alga New Phytologist, Vol. 211, Issue 1 https://doi.org/10.1111/nph.13977	journal	February 2016
Fine-tuning by strigolactones of root response to low phosphate: Strigolactones in Root Response to Low Phosphate Kapulnik, Yoram; Koltai, Hinanit Journal of Integrative Plant Biology, Vol. 58, Issue 3 https://doi.org/10.1111/jipb.12454	journal	February 2016
Reference genes for gene expression studies in wheat flag leaves grown under different farming conditions Tenea, Gabriela N.; Peres Bota, Adrian; Cordeiro Raposo, Fernando BMC Research Notes, Vol. 4, Issue 1 https://doi.org/10.1186/1756-0500-4-373	journal	September 2011
Metabolic Adaptations of Phosphate-Starved Plants Plaxton, William C.; Tran, Hue T. Plant Physiology, Vol. 156, Issue 3 https://doi.org/10.1104/pp.111.175281	journal	May 2011
Auxin Controlled by Ethylene Steers Root Development Qin, Hua; Huang, Rongfeng International Journal of Molecular Sciences, Vol. 19, Issue 11 https://doi.org/10.3390/ijms19113656	journal	November 2018
Genome Sequence of the Plant Growth Promoting Fungus Serendipita vermifera subsp. bescii : The First Native Strain from North America Ray, Prasun; Chi, Myoung-Hwan; Guo, Yingqing Phytobiomes Journal, Vol. 2, Issue 2 https://doi.org/10.1094/PBIOMES-04-17-0017-A	journal	January 2018
A Dual Role of Strigolactones in Phosphate Acquisition and Utilization in Plants Czarnecki, Olaf; Yang, Jun; Weston, David International Journal of Molecular Sciences, Vol. 14, Issue 4 https://doi.org/10.3390/ijms14047681	journal	April 2013
Root tip contact with low-phosphate media reprograms plant root architecture Svistoonoff, Sergio; Creff, Audrey; Reymond, Matthieu Nature Genetics, Vol. 39, Issue 6 https://doi.org/10.1038/ng2041	journal	May 2007
Environmental nitrate signals through abscisic acid in the root tip Harris, Jeanne M.; Ondzighi-Assoume, Christine A. Plant Signaling & Behavior, Vol. 12, Issue 1 https://doi.org/10.1080/15592324.2016.1273303	journal	January 2017
Quantifying the Limitation to World Cereal Production Due To Soil Phosphorus Status Kvakić, Marko; Pellerin, Sylvain; Ciais, Philippe Global Biogeochemical Cycles, Vol. 32, Issue 1 https://doi.org/10.1002/2017GB005754	journal	January 2018
Nitrogen and water resources commonly limit crop yield increases, not necessarily plant genetics Sinclair, Thomas R.; Rufty, Thomas W. Global Food Security, Vol. 1, Issue 2 https://doi.org/10.1016/j.gfs.2012.07.001	journal	December 2012
Siliques Are Red1 from Arabidopsis Acts as a Bidirectional Amino Acid Transporter That Is Crucial for the Amino Acid Homeostasis of Siliques Ladwig, Friederike; Stahl, Mark; Ludewig, Uwe Plant Physiology, Vol. 158, Issue 4 https://doi.org/10.1104/pp.111.192583	journal	February 2012
Effect of nitrogen fertilizer rates on grain yield and nitrogen uptake and use efficiency of bread wheat (Triticum aestivum L.) varieties on the Vertisols of central highlands of Ethiopia Belete, Fresew; Dechassa, Nigussie; Molla, Adamu Agriculture & Food Security, Vol. 7, Issue 1 https://doi.org/10.1186/s40066-018-0231-z	journal	October 2018
Scavenging organic nitrogen and remodelling lipid metabolism are key survival strategies adopted by the endophytic fungi, Serendipita vermifera and Serendipita bescii to alleviate nitrogen and phosphorous starvation in vitro Ray, Prasun; Abraham, Paul E.; Guo, Yingqing Environmental Microbiology Reports, Vol. 11, Issue 4 https://doi.org/10.1111/1758-2229.12757	journal	May 2019
Environmentally Induced Plasticity of Root Hair Development in Arabidopsis Müller, Margarete; Schmidt, Wolfgang Plant Physiology, Vol. 134, Issue 1 https://doi.org/10.1104/pp.103.029066	journal	January 2004
StringTie enables improved reconstruction of a transcriptome from RNA-seq reads Pertea, Mihaela; Pertea, Geo M.; Antonescu, Corina M. Nature Biotechnology, Vol. 33, Issue 3 https://doi.org/10.1038/nbt.3122	journal	February 2015
Morphology and molecules: the Sebacinales, a case study Oberwinkler, Franz; Riess, Kai; Bauer, Robert Mycological Progress, Vol. 13, Issue 3 https://doi.org/10.1007/s11557-014-0983-1	journal	April 2014
A Novel Delivery System for the Root Symbiotic Fungus, Sebacina vermifera, and Consequent Biomass Enhancement of Low Lignin COMT Switchgrass Lines Ray, Prasun; Ishiga, Takako; Decker, Stephen R. BioEnergy Research, Vol. 8, Issue 3 https://doi.org/10.1007/s12155-015-9636-8	journal	June 2015
Agrobacterium-Mediated Transformation of Switchgrass and Inheritance of the Transgenes Xi, Yajun; Fu, Chunxiang; Ge, Yaxin BioEnergy Research, Vol. 2, Issue 4 https://doi.org/10.1007/s12155-009-9049-7	journal	October 2009
Novel Root-Fungus Symbiosis in Ericaceae: Sheathed Ericoid Mycorrhiza Formed by a Hitherto Undescribed Basidiomycete with Affinities to Trechisporales Vohník, Martin; Sadowsky, Jesse J.; Kohout, Petr PLoS ONE, Vol. 7, Issue 6 https://doi.org/10.1371/journal.pone.0039524	journal	June 2012
Nutrient transfer in plant–fungal symbioses Behie, Scott W.; Bidochka, Michael J. Trends in Plant Science, Vol. 19, Issue 11 https://doi.org/10.1016/j.tplants.2014.06.007	journal	November 2014
Phosphate Starvation Root Architecture and Anthocyanin Accumulation Responses Are Modulated by the Gibberellin-DELLA Signaling Pathway in Arabidopsis Jiang, Caifu; Gao, Xiuhua; Liao, Lili Plant Physiology, Vol. 145, Issue 4 https://doi.org/10.1104/pp.107.103788	journal	October 2007
The Mycorrhizal Fungus, Sebacina vermifera, Enhances Seed Germination and Biomass Production in Switchgrass (Panicum virgatum L) Ghimire, Sita R.; Charlton, Nikki D.; Craven, Kelly D. BioEnergy Research, Vol. 2, Issue 1-2 https://doi.org/10.1007/s12155-009-9033-2	journal	April 2009
KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases Xie, Chen; Mao, Xizeng; Huang, Jiaju Nucleic Acids Research, Vol. 39, Issue suppl_2 https://doi.org/10.1093/nar/gkr483	journal	June 2011
The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield Waller, F.; Achatz, B.; Baltruschat, H. Proceedings of the National Academy of Sciences, Vol. 102, Issue 38 https://doi.org/10.1073/pnas.0504423102	journal	September 2005
Variation in nutrient-acquisition patterns by mycorrhizal fungi of rare and common orchids explains diversification in a global biodiversity hotspot Nurfadilah, Siti; Swarts, Nigel D.; Dixon, Kingsley W. Annals of Botany, Vol. 111, Issue 6 https://doi.org/10.1093/aob/mct064	journal	March 2013
Mycorrhizal Fungi Respond to Resource Inequality by Moving Phosphorus from Rich to Poor Patches across Networks Whiteside, Matthew D.; Werner, Gijsbert D. A.; Caldas, Victor E. A. Current Biology, Vol. 29, Issue 12 https://doi.org/10.1016/j.cub.2019.04.061	journal	June 2019
Global imprint of mycorrhizal fungi on whole-plant nutrient economics Averill, Colin; Bhatnagar, Jennifer M.; Dietze, Michael C. Proceedings of the National Academy of Sciences, Vol. 116, Issue 46 https://doi.org/10.1073/pnas.1906655116	journal	October 2019
HISAT: a fast spliced aligner with low memory requirements Kim, Daehwan; Langmead, Ben; Salzberg, Steven L. Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3317	journal	March 2015
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Love, Michael I.; Huber, Wolfgang; Anders, Simon Genome Biology, Vol. 15, Issue 12 https://doi.org/10.1186/s13059-014-0550-8	journal	December 2014

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