Regulation of Nicotine Biosynthesis by an Endogenous Target Mimicry of MicroRNA in Tobacco

The interaction between noncoding endogenous target mimicry (eTM) and its corresponding microRNA (miRNA) is a newly discovered regulatory mechanism and plays pivotal roles in various biological processes in plants. Tobacco (Nicotiana tabacum) is a model plant for studying secondary metabolite alkalo...

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Bibliographic Details
Published in:Plant physiology (Bethesda) 2015-10, Vol.169 (2), p.1062-1071
Main Authors: Li, Fangfang, Wang, Weidi, Zhao, Nan, Xiao, Bingguang, Cao, Peijian, Wu, Xingfu, Ye, Chuyu, Shen, Enhui, Qiu, Jie, Zhu, Qian-Hao, Xie, Jiahua, Zhou, Xueping, Fan, Longjiang
Format: Article
Language:English
Subjects:
Alkaloids
BIOCHEMISTRY AND METABOLISM
Biosynthesis
Evolution, Molecular
Gene Expression Regulation, Plant
Genomes
MicroRNA
MicroRNAs - genetics
MicroRNAs - metabolism
Molecular Mimicry
Nicotiana - genetics
Nicotiana - metabolism
Nicotine - biosynthesis
Nicotine - genetics
Pentosyltransferases - genetics
Pentosyltransferases - metabolism
Phylogeny
Plant Proteins - genetics
Plant Proteins - metabolism
Plant roots
Plants
Plants, Genetically Modified
Polymerase chain reaction
RNA
Topping
Transgenic plants
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Summary:The interaction between noncoding endogenous target mimicry (eTM) and its corresponding microRNA (miRNA) is a newly discovered regulatory mechanism and plays pivotal roles in various biological processes in plants. Tobacco (Nicotiana tabacum) is a model plant for studying secondary metabolite alkaloids, of which nicotine accounts for approximately 90%. In this work, we identified four unique tobacco-specific miRNAs that were predicted to target key genes of the nicotine biosynthesis and catabolism pathways and an eTM, novel tobacco miRNA (nta)-eTMX27, for nta-miRX27 that targetsQUINOLINATE PHOSPHORIBOSYLTRANSFERASE2(QPT2) encoding a quinolinate phosphoribosyltransferase. The expression level of nta-miRX27 was significantly down-regulated, while that ofQPT2and nta-eTMX27 was significantly up-regulated after topping, and consequently, nicotine content increased in the topping-treated plants. The topping-induced down-regulation of nta-miRX27 and up-regulation ofQPT2were only observed in plants with a functional nta-eTMX27 but not in transgenic plants containing an RNA interference construct targeting nta-eTMX27. Our results demonstrated that enhanced nicotine biosynthesis in the topping-treated tobacco plants is achieved by nta-eTMX27-mediated inhibition of the expression and functions of nta-miRX27. To our knowledge, this is the first report about regulation of secondary metabolite biosynthesis by an miRNA-eTM regulatory module in plants.
ISSN:0032-0889
1532-2548
DOI:10.1104/pp.15.00649