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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2021-11-01
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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. |
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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 |
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