TY - JOUR

T1 - Insights into the complex role of GRAS transcription factors in the arbuscular mycorrhiza symbiosis

AU - Hartmann, Rico M.

AU - Schaepe, Sieke

AU - Nübel, Daniel

AU - Petersen, Arne C.

AU - Bertolini, Martina

AU - Vasilev, Jana

AU - Kuester, Helge

AU - Hohnjec, Natalija

N1 - Funding Information: We thank Natascha Köppens (Institute of Plant Genetics, Leibniz Universität Hannover, Hannover, Germany) for excellent technical assistance. Medicago truncatula pt4-2 and ram1-1 seeds were kindly provided by Maria Harrison (Boyce Thompson Institute, Ithaca, NY, USA) and Giles Oldroyd (John Innes Centre, Norwich, UK), respectively. We are grateful to Franziska Krajinski-Barth (Institut für Biologie, Universität Leipzig, Leipzig, Germany) for the overexpression vectors 315p9RFP-Pt4-Expr and 917p9RFP-ubi3-Expr and to Erik Limpens (Department of Plant Sciences, Wageningen University, Wageningen, The Netherlands) for the RNAi vector pK7GWIWG2(II)-Q10:DsRED. GeneChip hybridizations were carried out by João Sobral and Jörg D. Becker (Plant Genomics Lab and Gene Expression Unit, Instituto Gulbenkian de Ciência, Oeiras, Portugal). The Medicago truncatula line NF4813 utilized in this research project, which is jointly owned by the Centre National De La Recherche Scientifique, was obtained from Noble Research Institute, LLC (successor-by-conversion to The Samuel Roberts Noble Foundation, Inc., effective May 1, 2017) and was created through research funded, in part, by a grant from the National Sience Foundation, NSF-0703285. The publication of this article was funded by the Open Access Fund of the Leibniz Universität Hannover. The authors wish to thank the Deutsche Forschungsgemeinschaft (DFG) for financial support in frame of GRK1798 “Signaling at the Plant-Soil Interface”.

PY - 2019

Y1 - 2019

N2 - To improve access to limiting nutrients, the vast majority of land plants forms arbuscular mycorrhizal (AM) symbioses with Glomeromycota fungi. We show here that AM-related GRAS transcription factors from different subgroups are upregulated during a time course of mycorrhization. Based on expression studies in mutants defective in arbuscule branching (ram1-1, with a deleted MtRam1 GRAS transcription factor gene) or in the formation of functional arbuscules (pt4-2, mutated in the phosphate transporter gene MtPt4), we demonstrate that the five AM-related GRAS transcription factor genes MtGras1, MtGras4, MtGras6, MtGras7, and MtRad1 can be differentiated by their dependency on MtRAM1 and MtPT4, indicating that the network of AM-related GRAS transcription factors consists of at least two regulatory modules. One module involves the MtRAM1- and MtPT4-independent transcription factor MtGRAS4 that activates MtGras7. Another module is controlled by the MtRAM1- and MtPT4-dependent transcription factor MtGRAS1. Genome-wide expression profiles of mycorrhized MtGras1 knockdown and ram1-1 roots differ substantially, indicating different targets. Although an MtGras1 knockdown reduces transcription of AM-related GRAS transcription factor genes including MtRam1 and MtGras7, MtGras1 overexpression alone is not sufficient to activate MtGras genes. MtGras1 knockdown roots display normal fungal colonization, with a trend towards the formation of smaller arbuscules.

AB - To improve access to limiting nutrients, the vast majority of land plants forms arbuscular mycorrhizal (AM) symbioses with Glomeromycota fungi. We show here that AM-related GRAS transcription factors from different subgroups are upregulated during a time course of mycorrhization. Based on expression studies in mutants defective in arbuscule branching (ram1-1, with a deleted MtRam1 GRAS transcription factor gene) or in the formation of functional arbuscules (pt4-2, mutated in the phosphate transporter gene MtPt4), we demonstrate that the five AM-related GRAS transcription factor genes MtGras1, MtGras4, MtGras6, MtGras7, and MtRad1 can be differentiated by their dependency on MtRAM1 and MtPT4, indicating that the network of AM-related GRAS transcription factors consists of at least two regulatory modules. One module involves the MtRAM1- and MtPT4-independent transcription factor MtGRAS4 that activates MtGras7. Another module is controlled by the MtRAM1- and MtPT4-dependent transcription factor MtGRAS1. Genome-wide expression profiles of mycorrhized MtGras1 knockdown and ram1-1 roots differ substantially, indicating different targets. Although an MtGras1 knockdown reduces transcription of AM-related GRAS transcription factor genes including MtRam1 and MtGras7, MtGras1 overexpression alone is not sufficient to activate MtGras genes. MtGras1 knockdown roots display normal fungal colonization, with a trend towards the formation of smaller arbuscules.

UR - http://www.scopus.com/inward/record.url?scp=85062427877&partnerID=8YFLogxK

U2 - 10.1038/s41598-019-40214-4

DO - 10.1038/s41598-019-40214-4

M3 - Article

VL - 9

JO - Scientific reports

JF - Scientific reports

SN - 2045-2322

IS - 1

M1 - 3360

ER -