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The Sweet Potato NAC-Domain Transcription Factor IbNAC1 Is Dynamically Coordinated by the Activator IbbHLH3 and the Repressor IbbHLH4 to Reprogram the Defense Mechanism against Wounding.

ABSTRACT: IbNAC1 is known to activate the defense system by reprogramming a genetic network against herbivory in sweet potato. This regulatory activity elevates plant defense potential but relatively weakens plants by IbNAC1-mediated JA response. The mechanism controlling IbNAC1 expression to balance plant vitality and survival remains unclear. In this study, a wound-responsive G-box cis-element in the IbNAC1 promoter from -1484 to -1479 bp was identified. From a screen of wound-activated transcriptomic data, one transcriptional activator, IbbHLH3, and one repressor, IbbHLH4, were selected that bind to and activate or repress, respectively, the G-box motif in the IbNAC1 promoter to modulate the IbNAC1-mediated response. In the early wound response, the IbbHLH3-IbbHLH3 protein complex binds to the G-box motif to activate IbNAC1 expression. Thus, an elegant defense network is activated against wounding stress. Until the late stages of wounding, IbbHLH4 interacts with IbbHLH3, and the IbbHLH3-IbbHLH4 heterodimer competes with the IbbHLH3-IbbHLH3 complex to bind the G-box and suppress IbNAC1 expression and timely terminates the defense network. Moreover, the JAZs and IbEIL1 proteins interact with IbbHLH3 to repress the transactivation function of IbbHLH3 in non-wounded condition, but their transcription is immediately inhibited upon early wounding. Our work provides a genetic model that accurately switches the regulatory mechanism of IbNAC1 expression to adjust wounding physiology and represents a delicate defense regulatory network in plants.

SUBMITTER: Chen SP

PROVIDER: S-EPMC5079590 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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The Sweet Potato NAC-Domain Transcription Factor IbNAC1 Is Dynamically Coordinated by the Activator IbbHLH3 and the Repressor IbbHLH4 to Reprogram the Defense Mechanism against Wounding.

Chen Shi-Peng SP Kuo Chih-Hsien CH Lu Hsueh-Han HH Lo Hui-Shan HS Yeh Kai-Wun KW

PLoS genetics 20161025 10

IbNAC1 is known to activate the defense system by reprogramming a genetic network against herbivory in sweet potato. This regulatory activity elevates plant defense potential but relatively weakens plants by IbNAC1-mediated JA response. The mechanism controlling IbNAC1 expression to balance plant vitality and survival remains unclear. In this study, a wound-responsive G-box cis-element in the IbNAC1 promoter from -1484 to -1479 bp was identified. From a screen of wound-activated transcriptomic d ...[more]

PMID: 27780204

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Project description:BACKGROUND: Plants respond differently to mechanical wounding and herbivore attack, using distinct pathways for defense. The versatile sweet potato sporamin possesses multiple biological functions in response to stress. However, the regulation of sporamin gene expression that is activated upon mechanical damage or herbivore attack has not been well studied. RESULTS: Biochemical analysis revealed that different patterns of Reactive oxygen species (ROS) and antioxidant mechanism exist between mechanical wounding (MW) and herbivore attack (HA) in the sweet potato leaf. Using LC-ESI-MS (Liquid chromatography electrospray ionization mass spectrometry analysis), only the endogenous JA (jasmonic acid) level was found to increase dramatically after MW in a time-dependent manner, whereas both endogenous JA and SA (salicylic acid) increase in parallel after HA. Through yeast one-hybrid screening, two transcription factors IbNAC1 (no apical meristem (NAM), Arabidopsis transcription activation factor (ATAF), and cup-shaped cotyledon (CUC)) and IbWRKY1 were isolated, which interact with the sporamin promoter fragment of SWRE (sporamin wounding-responsive element) regulatory sequences. Exogenous application of MeJA (methyl jasmonate), SA and DIECA (diethyldithiocarbamic acid, JAs biosynthesis inhibitor) on sweet potato leaves was employed, and the results revealed that IbNAC1 mediated the expression of sporamin through a JA-dependent signaling pathway upon MW, whereas both IbNAC1 and IbWRKY1 coordinately regulated sporamin expression through JA- and SA-dependent pathways upon HA. Transcriptome analysis identified MYC2/4 and JAZ2/TIFY10A (jasmonate ZIM/tify-domain), the repressor and activator of JA and SA signaling among others, as the genes that play an intermediate role in the JA and SA pathways, and these results were further validated by qRT-PCR (quantitative real-time polymerase chain reaction). CONCLUSION: This work has improved our understanding of the differential regulatory mechanism of sporamin expression. Our study illustrates that sweet potato sporamin expression is differentially induced upon abiotic MW and biotic HA that involves IbNAC1 and IbWRKY1 and is dependent on the JA and SA signaling pathways. Thus, we established a model to address the plant-wounding response upon physical and biotic damage.

Project description:NAC (NAM, ATAF1/2, and CUC2) proteins play a pivotal role in modulating plant development and offer protection against biotic and abiotic stresses. Until now, no systematic knowledge of NAC family genes is available for the food security crop, sweet potato. Here, a comprehensive genome-wide survey of NAC domain-containing proteins identified 130 ItbNAC and 144 ItfNAC genes with full length sequences in the genomes of two diploid wild relatives of cultivated sweet potato, Ipomoea triloba and Ipomoea trifida, respectively. These genes were physically mapped onto 15 I. triloba and 16 I. trifida chromosomes, respectively. Phylogenetic analysis divided all 274 NAC proteins into 20 subgroups together with NAC transcription factors (TFs) from Arabidopsis. There were 9 and 15 tandem duplication events in the I. triloba and I. trifida genomes, respectively, indicating an important role of tandem duplication in sweet potato gene expansion and evolution. Moreover, synteny analysis suggested that most NAC genes in the two diploid sweet potato species had a similar origin and evolutionary process. Gene expression patterns based on RNA-Seq data in different tissues and in response to various hormone, biotic or abiotic treatments revealed their possible involvement in organ development and response to various biotic/abiotic stresses. The expression of 36 NAC TFs, which were upregulated in the five tissues and in response to mannitol treatment, was also determined by real-time quantitative polymerase chain reaction (RT-qPCR) in hexaploid cultivated sweet potato exposed to drought stress. Those results largely corroborated the expression profile of mannitol treatment uncovered by the RNA-Seq data. Some significantly up-regulated genes related to drought stress, such as ItbNAC110, ItbNAC114, ItfNAC15, ItfNAC28, and especially ItfNAC62, which had a conservative spatial conformation with a closely related paralogous gene, ANAC019, may be potential candidate genes for a sweet potato drought tolerance breeding program. This analysis provides comprehensive and systematic information about NAC family genes in two diploid wild relatives of cultivated sweet potato, and will provide a blueprint for their functional characterization and exploitation to improve the tolerance of sweet potato to abiotic stresses.

Dataset Information

The Sweet Potato NAC-Domain Transcription Factor IbNAC1 Is Dynamically Coordinated by the Activator IbbHLH3 and the Repressor IbbHLH4 to Reprogram the Defense Mechanism against Wounding.

Publications

The Sweet Potato NAC-Domain Transcription Factor IbNAC1 Is Dynamically Coordinated by the Activator IbbHLH3 and the Repressor IbbHLH4 to Reprogram the Defense Mechanism against Wounding.

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