Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation

The smut fungus <i>Ustilago esculenta</i> infects <i>Zizania latifolia</i> and induces stem expansion to form a unique vegetable named Jiaobai. Although previous studies have demonstrated that hormonal control is essential for triggering stem swelling, the role of hormones sy...

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Autores principales: Zhi-Ping Zhang, Si-Xiao Song, Yan-Cheng Liu, Xin-Rui Zhu, Yi-Feng Jiang, Ling-Tong Shi, Jie-Zeng Jiang, Min-Min Miao
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spelling oai:doaj.org-article:f46c3208c8134f9e8273999cced718602021-11-25T17:54:48ZMixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation10.3390/ijms2222122581422-00671661-6596https://doaj.org/article/f46c3208c8134f9e8273999cced718602021-11-01T00:00:00Zhttps://www.mdpi.com/1422-0067/22/22/12258https://doaj.org/toc/1661-6596https://doaj.org/toc/1422-0067The smut fungus <i>Ustilago esculenta</i> infects <i>Zizania latifolia</i> and induces stem expansion to form a unique vegetable named Jiaobai. Although previous studies have demonstrated that hormonal control is essential for triggering stem swelling, the role of hormones synthesized by <i>Z. latifolia</i> and <i>U. esculenta</i> and the underlying molecular mechanism are not yet clear. To study the mechanism that triggers swollen stem formation, we analyzed the gene expression pattern of both interacting organisms during the initial trigger of culm gall formation, at which time the infective hyphae also propagated extensively and penetrated host stem cells. Transcriptional analysis indicated that abundant genes involving fungal pathogenicity and plant resistance were reprogrammed to maintain the subtle balance between the parasite and host. In addition, the expression of genes involved in auxin biosynthesis of <i>U. esculenta</i> obviously decreased during stem swelling, while a large number of genes related to the synthesis, metabolism and signal transduction of hormones of the host plant were stimulated and showed specific expression patterns, particularly, the expression of <i>ZlYUCCA9</i> (a flavin monooxygenase, the key enzyme in indole-3-acetic acid (IAA) biosynthesis pathway) increased significantly. Simultaneously, the content of IAA increased significantly, while the contents of cytokinin and gibberellin showed the opposite trend. We speculated that auxin produced by the host plant, rather than the fungus, triggers stem swelling. Furthermore, from the differently expressed genes, two candidate Cys2-His2 (C2H2) zinc finger proteins, GME3058_g and GME5963_g, were identified from <i>U. esculenta</i>, which may conduct fungus growth and infection at the initial stage of stem-gall formation.Zhi-Ping ZhangSi-Xiao SongYan-Cheng LiuXin-Rui ZhuYi-Feng JiangLing-Tong ShiJie-Zeng JiangMin-Min MiaoMDPI AGarticle<i>Zizania latifolia</i><i>Ustilago esculenta</i>stem-gall formationtranscriptomeauxin<i>YUCCA</i>Biology (General)QH301-705.5ChemistryQD1-999ENInternational Journal of Molecular Sciences, Vol 22, Iss 12258, p 12258 (2021)
institution DOAJ
collection DOAJ
language EN
topic <i>Zizania latifolia</i>
<i>Ustilago esculenta</i>
stem-gall formation
transcriptome
auxin
<i>YUCCA</i>
Biology (General)
QH301-705.5
Chemistry
QD1-999
spellingShingle <i>Zizania latifolia</i>
<i>Ustilago esculenta</i>
stem-gall formation
transcriptome
auxin
<i>YUCCA</i>
Biology (General)
QH301-705.5
Chemistry
QD1-999
Zhi-Ping Zhang
Si-Xiao Song
Yan-Cheng Liu
Xin-Rui Zhu
Yi-Feng Jiang
Ling-Tong Shi
Jie-Zeng Jiang
Min-Min Miao
Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation
description The smut fungus <i>Ustilago esculenta</i> infects <i>Zizania latifolia</i> and induces stem expansion to form a unique vegetable named Jiaobai. Although previous studies have demonstrated that hormonal control is essential for triggering stem swelling, the role of hormones synthesized by <i>Z. latifolia</i> and <i>U. esculenta</i> and the underlying molecular mechanism are not yet clear. To study the mechanism that triggers swollen stem formation, we analyzed the gene expression pattern of both interacting organisms during the initial trigger of culm gall formation, at which time the infective hyphae also propagated extensively and penetrated host stem cells. Transcriptional analysis indicated that abundant genes involving fungal pathogenicity and plant resistance were reprogrammed to maintain the subtle balance between the parasite and host. In addition, the expression of genes involved in auxin biosynthesis of <i>U. esculenta</i> obviously decreased during stem swelling, while a large number of genes related to the synthesis, metabolism and signal transduction of hormones of the host plant were stimulated and showed specific expression patterns, particularly, the expression of <i>ZlYUCCA9</i> (a flavin monooxygenase, the key enzyme in indole-3-acetic acid (IAA) biosynthesis pathway) increased significantly. Simultaneously, the content of IAA increased significantly, while the contents of cytokinin and gibberellin showed the opposite trend. We speculated that auxin produced by the host plant, rather than the fungus, triggers stem swelling. Furthermore, from the differently expressed genes, two candidate Cys2-His2 (C2H2) zinc finger proteins, GME3058_g and GME5963_g, were identified from <i>U. esculenta</i>, which may conduct fungus growth and infection at the initial stage of stem-gall formation.
format article
author Zhi-Ping Zhang
Si-Xiao Song
Yan-Cheng Liu
Xin-Rui Zhu
Yi-Feng Jiang
Ling-Tong Shi
Jie-Zeng Jiang
Min-Min Miao
author_facet Zhi-Ping Zhang
Si-Xiao Song
Yan-Cheng Liu
Xin-Rui Zhu
Yi-Feng Jiang
Ling-Tong Shi
Jie-Zeng Jiang
Min-Min Miao
author_sort Zhi-Ping Zhang
title Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation
title_short Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation
title_full Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation
title_fullStr Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation
title_full_unstemmed Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall Formation
title_sort mixed transcriptome analysis revealed the possible interaction mechanisms between <i>zizania latifolia</i> and <i>ustilago esculenta</i> inducing jiaobai stem-gall formation
publisher MDPI AG
publishDate 2021
url https://doaj.org/article/f46c3208c8134f9e8273999cced71860
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