Transcriptome Analysis Reveals the Symbiotic Mechanism of Ustilago esculenta-Induced Gall Formation of Zizania latifolia.

Jie Li,Shidong Zhu,Guohu Chen,Zhiyuan Lu,Jinfeng Hou,Chenggang Wang,Yang Yang,Shaoke Jia,Lingyun Yuan,Xuming Feng

doi:10.1094/mpmi-05-20-0126-r

Abstract

Zizania latifolia is a perennial aquatic vegetable, whose symbiosis with the fungus Ustilago esculenta (member of Basidiomycota, class Ustilaginaceae) results in the establishment of swollen gall formations. Here, we analyzed symbiotic relations of Z. latifolia and U. esculenta, using a triadimefon (TDF) treatment and transcriptome sequencing (RNA-seq). Specifically, accurately identify the whole growth cycle of Z. latifolia. Microstructure observations showed that the presence of U. esculenta could be clearly observed after gall formation but was absent after the TDF treatment. A total of 17,541 differentially expressed genes (DEGs) were identified, based on the transcriptome. According to gene ontology term and Kyoto Encyclopedia of Genes and Genomes pathway results, plant hormone signal transduction, and cell wall-loosening factors were all significantly enriched due to U. esculenta infecting Z. latifolia; relative expression levels of hormone-related genes were identified, of which downregulation of indole 3-acetic acid (IAA)-related DEGs was most pronounced in JB_D versus JB_B. The ultra-high performance liquid chromatography analysis revealed that IAA, zeatin+trans zeatin riboside, and gibberellin 3 were increased under U. esculenta infection. Based on our results, we proposed a hormone-cell wall loosening model to study the symbiotic mechanism of gall formation after U. esculenta infects Z. latifolia. Our study thus provides a new perspective for studying the physiological and molecular mechanisms of U. esculenta infection of Z. latifolia causing swollen gall formations as well as a theoretical basis for enhancing future yields of cultivated Z. latifolia.[Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law. 2021.

Highlights

The raw RNA-seq data used in this study were deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database, under the accession number SRP212030
The phases of Z. latifolia development and growth had not yet been determined but discerning these was crucial for using an accurate period in the experiment and its TDF treatment for subsequently experiments
We found that GA3 and indole 3-acetic acid (IAA) contents exceeded the others, suggesting the contents of IAA, Abscisic acid (ABA), and GA3 may be driven by the U. esculenta infection–plant symbiosis, which could have stimulated the plant to produce a large amount of growth hormones to cause the characteristic swollen gall formation

Summary

Introduction

The raw RNA-seq data used in this study were deposited in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database, under the accession number SRP212030. To detect the levels of hormonal response to U. esculenta infection, ultra–high performance liquid chromatography (UHPLC) was used to measure IAA, ABA (abscisic acid), Z+ZR (zeatin and trans zeatin riboside), and GA3 (gibberellin 3) contents (Fig. 3) in Z. latifolia before and after gall formation in both CK and TDF groups. The divergent expression patterns of hormone metabolism– related DEGs between the CK and TDF groups suggest that plant hormones play a key role in governing responses to U. esculenta infection in Z. latifolia hosts.

Results

Conclusion