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Front. Microbiol. | doi: 10.3389/fmicb.2018.00091

Arbuscular mycorrhizal fungal 14-3-3 proteins are involved in arbuscule formation and responses to abiotic stresses during AM symbiosis

 Zhongfeng Sun1, Xianan Xie2*,  Xian Xin1, Jiabin Song1 and Bin Zhao1*
  • 1State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Huazhong Agricultural University, China
  • 2College of Forestry and Landscape Architecture, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, South China Agricultural University, China

Arbuscular mycorrhizal (AM) fungi are soil-borne fungi belonging to the ancient phylum Glomeromycota and are important symbionts of the arbuscular mycorrhiza, enhancing plant nutrient acquisition and resistance to various abiotic stresses. In contrast to their significant physiological implications, the molecular basis involved is poorly understood, largely due to their obligate biotrophism and complicated genetics. Here, we identify and characterize three genes termed Fm201, Ri14-3-3 and RiBMH2 that encode 14-3-3-like proteins in the AM fungi Funneliformis mosseae and Rhizophagus irregularis, respectively. The transcriptional levels of Fm201, Ri14-3-3 and RiBMH2 are strongly induced in the pre-symbiotic and symbiotic phases, including germinating spores, intraradical hyphae- and arbuscules-enriched roots. To functionally characterize the Fm201, Ri14-3-3 and RiBMH2 genes, we took advantage of a yeast heterologous system owing to the lack of AM fungal transformation systems. Our data suggest that all three genes can restore the lethal S. cerevisiae bmh1 bmh2 double mutant on galactose-containing media. Importantly, yeast one-hybrid analysis suggests that the transcription factor RiMsn2 is able to recognize the STRE (CCCCT/AGGGG) element present in the promoter region of Fm201 gene. More importantly, Host-Induced Gene Silencing of both Ri14-3-3 and RiBMH2 in R. irregularis impairs the arbuscule formation in AM symbiosis and inhibits the expression of symbiotic PT4 and MST2 genes from plant and fungal partners, respectively. We further subjected the AM fungus-Medicago truncatula association system to drought or salinity stress. Accordingly, the expression profiles in both mycorrhizal roots and extraradical hyphae reveal that these three 14-3-3-like genes are involved in response to drought or salinity stress. Collectively, our results provide new insights into molecular functions of the AM fungal 14-3-3 proteins in abiotic stress responses and arbuscule formation during AM symbiosis.

Keywords: arbuscular mycorrhiza, abiotic stresses, Funneliformis mosseae, Rhizophagus irregularis, Fm201, host-induced gene silencing, 14-3-3 Proteins

Received: 18 Sep 2017; Accepted: 16 Jan 2018.

Edited by:

Erika Kothe, Friedrich Schiller Universität Jena, Germany

Reviewed by:

Raffaella Balestrini, Consiglio Nazionale Delle Ricerche (CNR), Italy
Maria Rapala-Kozik, Jagiellonian University, Poland  

Copyright: © 2018 Sun, Xie, Xin, Song and Zhao. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Xianan Xie, South China Agricultural University, College of Forestry and Landscape Architecture, State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangzhou, China, 30004537@scau.edu.cn
Prof. Bin Zhao, Huazhong Agricultural University, State Key Laboratory of Agricultural Microbiology, College of Life Science and Technology, Wuhan, China, binzhao@mail.hzau.edu.cn