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...

Full description

Bibliographic Details
Main Authors: Zhi-Ping Zhang, Si-Xiao Song, Yan-Cheng Liu, Xin-Rui Zhu, Yi-Feng Jiang, Ling-Tong Shi, Jie-Zeng Jiang, Min-Min Miao
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/22/22/12258
_version_ 1797510033069572096
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
collection DOAJ
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.
first_indexed 2024-03-10T05:27:08Z
format Article
id doaj.art-f46c3208c8134f9e8273999cced71860
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-10T05:27:08Z
publishDate 2021-11-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-f46c3208c8134f9e8273999cced718602023-11-22T23:39:31ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-11-0122221225810.3390/ijms222212258Mixed Transcriptome Analysis Revealed the Possible Interaction Mechanisms between <i>Zizania latifolia</i> and <i>Ustilago esculenta</i> Inducing Jiaobai Stem-Gall FormationZhi-Ping Zhang0Si-Xiao Song1Yan-Cheng Liu2Xin-Rui Zhu3Yi-Feng Jiang4Ling-Tong Shi5Jie-Zeng Jiang6Min-Min Miao7College of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaCollege of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, ChinaThe 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.https://www.mdpi.com/1422-0067/22/22/12258<i>Zizania latifolia</i><i>Ustilago esculenta</i>stem-gall formationtranscriptomeauxin<i>YUCCA</i>
spellingShingle 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
International Journal of Molecular Sciences
<i>Zizania latifolia</i>
<i>Ustilago esculenta</i>
stem-gall formation
transcriptome
auxin
<i>YUCCA</i>
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_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_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_sort mixed transcriptome analysis revealed the possible interaction mechanisms between i zizania latifolia i and i ustilago esculenta i inducing jiaobai stem gall formation
topic <i>Zizania latifolia</i>
<i>Ustilago esculenta</i>
stem-gall formation
transcriptome
auxin
<i>YUCCA</i>
url https://www.mdpi.com/1422-0067/22/22/12258
work_keys_str_mv AT zhipingzhang mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT sixiaosong mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT yanchengliu mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT xinruizhu mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT yifengjiang mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT lingtongshi mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT jiezengjiang mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation
AT minminmiao mixedtranscriptomeanalysisrevealedthepossibleinteractionmechanismsbetweenizizanialatifoliaiandiustilagoesculentaiinducingjiaobaistemgallformation