Heat Stress Modulates Mycelium Growth, Heat Shock Protein Expression, Ganoderic Acid Biosynthesis, and Hyphal Branching of Ganoderma lucidum via Cytosolic Ca2+

被引:106
|
作者
Zhang, Xue
Ren, Ang
Li, Meng-Jiao
Cao, Peng-Fei
Chen, Tian-Xi
Zhang, Guang
Shi, Liang
Jiang, Ai-Liang
Zhao, Ming-Wen [1 ]
机构
[1] Nanjing Agr Univ, Minist Agr, Key Lab Microbiol Engn Agr Environm, Nanjing, Jiangsu, Peoples R China
基金
中国国家自然科学基金;
关键词
SACCHAROMYCES-CEREVISIAE; FUNCTIONAL-ANALYSIS; NEUROSPORA-CRASSA; METHYL JASMONATE; OXIDATIVE-STRESS; PLASMA-MEMBRANE; IN-VITRO; THERMOTOLERANCE; YEAST; FUNGUS;
D O I
10.1128/AEM.01036-16
中图分类号
Q81 [生物工程学(生物技术)]; Q93 [微生物学];
学科分类号
071005 ; 0836 ; 090102 ; 100705 ;
摘要
Heat stress (HS) influences the growth and development of organisms. Thus, a comprehensive understanding of how organisms sense HS and respond to it is required. Ganoderma lucidum, a higher basidiomycete with bioactive secondary metabolites, has become a potential model system due to the complete sequencing of its genome, transgenic systems, and reliable reverse genetic tools. In this study, we found that HS inhibited mycelium growth, reduced hyphal branching, and induced the accumulation of ganoderic acid biosynthesis and heat shock proteins (HSPs) in G. lucidum. Our data showed that HS induced a significant increase in cytosolic Ca2+ concentration. Further evidence showed that Ca2+ might be a factor in the HS-mediated regulation of hyphal branching, ganoderic acid (GA) biosynthesis, and the accumulation of HSPs. Our results further showed that the calcium-permeable channel gene (cch)-silenced and phosphoinositide-specific phospholipase gene (plc)-silenced strains reduced the HS-induced increase in HSP expression compared with that observed for the wild type (WT). This study demonstrates that cytosolic Ca2+ participates in heat shock signal transduction and regulates downstream events in filamentous fungi. IMPORTANCE Ganoderma lucidum, a higher basidiomycete with bioactive secondary metabolites, has become a potential model system for evaluating how environmental factors regulate the development and secondary metabolism of basidiomycetes. Heat stress (HS) is an important environmental challenge. In this study, we found that HS inhibited mycelium growth, reduced hyphal branching, and induced HSP expression and ganoderic acid biosynthesis in G. lucidum. Further evidence showed that Ca2+ might be a factor in the HS-mediated regulation of hyphal branching, GA biosynthesis, and the accumulation of HSPs. This study demonstrates that cytosolic Ca2+ participates in heat shock signal transduction and regulates downstream events in filamentous fungi. Our research offers a new way to understand the mechanism underlying the physiological and metabolic responses to other environmental factors in G. lucidum. This research may also provide the basis for heat shock signal transduction studies of other fungi.
引用
收藏
页码:4112 / 4125
页数:14
相关论文
共 25 条
  • [1] Heat stress-induced reactive oxygen species participate in the regulation of HSP expression, hyphal branching and ganoderic acid biosynthesis in Ganoderma lucidum
    Liu, Rui
    Zhang, Xue
    Ren, Ang
    Shi, Deng-Ke
    Shi, Liang
    Zhu, Jing
    Yu, Han-Shou
    Zhao, Ming-Wen
    MICROBIOLOGICAL RESEARCH, 2018, 209 : 43 - 54
  • [2] 14-3-3 proteins are involved in growth, hyphal branching, ganoderic acid biosynthesis, and response to abiotic stress in Ganoderma lucidum
    Tian-Jun Zhang
    Liang Shi
    Dong-Dong Chen
    Rui Liu
    Deng-Ke Shi
    Chen-Gao Wu
    Ze-Hua Sun
    Ang Ren
    Ming-Wen Zhao
    Applied Microbiology and Biotechnology, 2018, 102 : 1769 - 1782
  • [3] 14-3-3 proteins are involved in growth, hyphal branching, ganoderic acid biosynthesis, and response to abiotic stress in Ganoderma lucidum
    Zhang, Tian-Jun
    Shi, Liang
    Chen, Dong-Dong
    Liu, Rui
    Shi, Deng-Ke
    Wu, Chen-Gao
    Sun, Ze-Hua
    Ren, Ang
    Zhao, Ming-Wen
    APPLIED MICROBIOLOGY AND BIOTECHNOLOGY, 2018, 102 (04) : 1769 - 1782
  • [4] Cross Talk between Calcium and Reactive Oxygen Species Regulates Hyphal Branching and Ganoderic Acid Biosynthesis in Ganoderma lucidum under Copper Stress
    Gao, Tan
    Shi, Liang
    Zhang, Tianjun
    Ren, Ang
    Jiang, Ailiang
    Yu, Hanshou
    Zhao, Mingwen
    APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2018, 84 (13)
  • [5] Abscisic acid-mediated cytosolic Ca2+ modulates triterpenoid accumulation of Ganoderma lucidum
    Cui, Meilin
    Zhao, Yitao
    Zhang, Xiuhong
    Zhao, Wei
    JOURNAL OF ZHEJIANG UNIVERSITY-SCIENCE B, 2023, 24 (12): : 1174 - 1179
  • [6] Heat stress promotes the conversion of putrescine to spermidine and plays an important role in regulating ganoderic acid biosynthesis in Ganoderma lucidum
    Yongxin Tao
    Xiaofei Han
    Ang Ren
    Jian Li
    Hanbing Song
    Baogui Xie
    Mingwen Zhao
    Applied Microbiology and Biotechnology, 2021, 105 : 5039 - 5051
  • [7] Heat stress promotes the conversion of putrescine to spermidine and plays an important role in regulating ganoderic acid biosynthesis in Ganoderma lucidum
    Tao, Yongxin
    Han, Xiaofei
    Ren, Ang
    Li, Jian
    Song, Hanbing
    Xie, Baogui
    Zhao, Mingwen
    APPLIED MICROBIOLOGY AND BIOTECHNOLOGY, 2021, 105 (12) : 5039 - 5051
  • [8] Cross Talk between Nitric Oxide and Calcium-Calmodulin Regulates Ganoderic Acid Biosynthesis in Ganoderma lucidum under Heat Stress
    Liu, Rui
    Shi, Liang
    Zhu, Ting
    Yang, Tao
    Ren, Ang
    Zhu, Jing
    Zhao, Ming-wen
    APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2018, 84 (10)
  • [9] Phospholipase D and phosphatidic acid mediate regulation in the biosynthesis of spermidine and ganoderic acids by activating GlMyb in Ganoderma lucidum under heat stress
    Han, Xiaofei
    Wang, Zi
    Shi, Lingyan
    Zhu, Jing
    Shi, Liang
    Ren, Ang
    Zhao, Mingwen
    ENVIRONMENTAL MICROBIOLOGY, 2022, 24 (11) : 5345 - 5361
  • [10] Heme Oxygenase/Carbon Monoxide Participates in the Regulation of Ganoderma lucidum Heat-Stress Response, Ganoderic Acid Biosynthesis, and Cell-Wall Integrity
    Wu, Tao
    Liu, Xiaotian
    Wang, Ting
    Tian, Li
    Qiu, Hao
    Ge, Feng
    Zhu, Jing
    Shi, Liang
    Jiang, Ailiang
    Yu, Hanshou
    Ren, Ang
    INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 2022, 23 (21)