Sweet potato NAC transcription factor, IbNAC1, upregulates sporamin gene expression by binding the SWRE motif against mechanical wounding and herbivore attack

Abstract

SUMMARYSporamin is a tuberous storage protein with trypsin inhibitory activity in sweet potato (Ipomoea batatas Lam.), which accounts for 85% of the soluble protein in tubers. It is constitutively expressed in tuberous roots but is expressed in leaves only after wounding. Thus far, its wound-inducible signal transduction mechanisms remain unclear. In the present work, a 53-bp DNA region, sporamin wound-response ciselement (SWRE), was identified in the sporamin promoter and was determined to be responsible for the wounding response. Using yeast one-hybrid screening, a NAC domain protein, IbNAC1, that specifically bound to the 5 0 -TACAATATC-3 0 sequence in SWRE was isolated from a cDNA library from wounded leaves.IbNAC1 was constitutively expressed in root tissues and was induced earlier than sporamin following the wounding of leaves. Transgenic sweet potato plants overexpressing IbNAC1 had greatly increased sporamin expression, increased trypsin inhibitory activity, and elevated resistance against Spodoptera litura. We further demonstrated that IbNAC1 has multiple biological functions in the jasmonic acid (JA) response, including the inhibition of root formation, accumulation of anthocyanin, regulation of aging processes, reduction of abiotic tolerance, and overproduction of reactive oxygen species (ROS). Thus, IbNAC1 is a core transcription factor that reprograms the transcriptional response to wounding via the JA-mediated pathway in sweet potato.

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

“…In addition to wounding-induced activity, several wounding-related signals, including methyl jasmonate (MeJA), ethylene (ET) and reactive oxygen species (ROS), also triggered the IbNAC1 promoter (Fig 1C). These results correspond to the previously reported expression pattern of IbNAC1 [7]. Simultaneously, transgenic Arabidopsis harboring P IbNAC1 :: GUS exhibited similar results with sweet potato under wounding treatment (Fig 1D), suggesting a similar signal transduction response to wounding to activate IbNAC1 expression in sweet potato and Arabidopsis.…”

“…Sweet potato IbNAC1 is known to reprogram the defense mechanism in response to herbivory and wounding [7]. However, the mechanisms of the wound signal response in gene expression remain ambiguous.…”

“…Following binding, several transcription factors regulate the promoter activity directly by activating or repressing the domain to control gene expression. To date, wound-activated promoters including ATAF1/2 [3], PI-II [4], WIPK [5] and sporamin [6,7] have been identified. Thus, the dissection of the binding mechanism between transcription factors and the promoter region of defense genes is important for determining the defense response in plants.…”

“…A wound-inducible NAC-domain transcription factor, IbNAC1, has been found to activate the sporamin promoter by binding the specific cis -acting element, TACAATATC, immediately upon wounding in leaves. In addition to enhanced resistance against herbivory, IbNAC1 simultaneously modulates several JA responses, including growth inhibition, ROS overproduction, and precocious senescence, to influence plant physiology [7]. …”

Recent Progress in Understanding the Role of Reactive Oxygen Species in Plant Cell Signaling

“…Additional ROS-response regulatory proteins identified in recent years include the APETALA2/ethylene response transcription factor REDOX RESPONSIVE TRANSCRIP-TION FACTOR1 that is regulated by different WRKYs (Matsuo et al, 2015), different members of the NAC family of transcription factors (e.g. Fang et al, 2015;Chen et al, 2016;Zhu et al, 2016), and different zinc-finger proteins such OXIDATIVE STRESS2 (He et al, 2016).…”