DNA-binding specificity and molecular functions of NAC transcription factors

Olsen, Addie Nina; Ernst, Heidi A.; Leggio, Leila Lo; Skriver, Karen

doi:10.1016/j.plantsci.2005.05.035

Cited by 174 publications

(214 citation statements)

References 35 publications

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“…S7E) to the LUC reporter gene and used the construct as a senescence-responsive reporter. The 788-bp SAG12 promoter contains the 9-mer sequence T(TAG)(GA)CGT(GA)(TCA)(TAG), which is the preferred binding site of ORE1 (28). All PP2Cs decreased SAG12-LUC expression in the presence of ABA (Fig.…”

Section: Resultsmentioning

confidence: 99%

ABA receptor PYL9 promotes drought resistance and leaf senescence

Zhao

Chan

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

499

402

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Drought stress is an important environmental factor limiting plant productivity. In this study, we screened drought-resistant transgenic plants from 65 promoter-pyrabactin resistance 1-like (PYL) abscisic acid (ABA) receptor gene combinations and discovered that pRD29A::PYL9 transgenic lines showed dramatically increased drought resistance and drought-induced leaf senescence in both Arabidopsis and rice. Previous studies suggested that ABA promotes senescence by causing ethylene production. However, we found that ABA promotes leaf senescence in an ethylene-independent manner by activating sucrose nonfermenting 1-related protein kinase 2s (SnRK2s), which subsequently phosphorylate ABA-responsive element-binding factors (ABFs) and Related to ABA-Insensitive 3/VP1 (RAV1) transcription factors. The phosphorylated ABFs and RAV1 up-regulate the expression of senescence-associated genes, partly by up-regulating the expression of Oresara 1. The pyl9 and ABA-insensitive 1-1 single mutants, pyl8-1pyl9 double mutant, and snrk2.2/3/6 triple mutant showed reduced ABA-induced leaf senescence relative to the WT, whereas pRD29A::PYL9 transgenic plants showed enhanced ABA-induced leaf senescence. We found that leaf senescence may benefit drought resistance by helping to generate an osmotic potential gradient, which is increased in pRD29A::PYL9 transgenic plants and causes water to preferentially flow to developing tissues. Our results uncover the molecular mechanism of ABA-induced leaf senescence and suggest an important role of PYL9 and leaf senescence in promoting resistance to extreme drought stress.drought stress | abscisic acid | PYL | dormancy | Arabidopsis C ell and organ senescence causes programmed cell death to regulate the growth and development of organisms. In plants, leaf senescence increases the transfer of nutrients to developing and storage tissues. Recently, studies on transgenic tobacco showed that delayed leaf senescence increases plant resistance to drought stress (1). However, the senescence and abscission of older leaves and subsequent transfer of nutrients are known to increase plant survival under abiotic stresses, including drought, low or high temperatures, and darkness (2, 3). Senescence mainly develops in an age-dependent manner and is also triggered by environmental stresses and phytohormones, such as abscisic acid (ABA), ethylene, salicylic acid, and jasmonic acid, but delayed by cytokinin (4).Senescence-associated genes (SAGs) are induced by leaf senescence. The expression of SAGs is tightly controlled by several senescence-promoting, plant-specific NAC (NAM, ATAF1, and CUC2) transcription factors, such as Oresara 1 (ORE1) (5), Oresara 1 sister 1 (ORS1) (6), and AtNAP (7). Environmental stimuli and phytohormones may regulate leaf senescence through NACs. Phytochrome-interacting factor 4 (PIF4) and PIF5 transcription factors promote dark-induced senescence by activating ORE1 expression (8). The expression of ORE1, AtNAP, and OsNAP (ortholog of AtNAP) is up-regulated by ABA by an unknown molecular m...

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Section: Resultsmentioning

confidence: 99%

ABA receptor PYL9 promotes drought resistance and leaf senescence

Zhao

Chan

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

499

402

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“…In a contrast, mutagenesis studies of ANAC showed that two areas of the ANAC NAC domain, which contain the positively charged residues Lys123 and Lys126 (ANAC) positioned between β4 and 5 on a turn protruding from the surface of the domain in addition to Lys79 and Arg85 (ANAC) positioned in a loop between β1 and β2, as well as Arg88, the first residue in β2, take the responsibility of ANAC DNA binding. While K123A/K126A mutants did not impair the DNA binding of ANAC, both K79A/R85A/R88A triple mutants and R85A/R88A double mutants abolished the DNA binding (Olsen et al, 2005). As size-exclusion chromatography showed proper folding of all these mutant domains, Arg85, Arg88 or both are therefore biochemically important for binding.…”

Section: Dimeric Assembly Of Snac1 Nac Domainmentioning

confidence: 86%

A structural view of the conserved domain of rice stress-responsive NAC1

et al. 2011

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The importance of NAC (named as NAM, ATAF1, 2, and CUC2) proteins in plant development, transcription regulation and regulatory pathways involving proteinprotein interactions has been increasingly recognized. We report here the high resolution crystal structure of SNAC1 (stress-responsive NAC) NAC domain at 2.5 Å. Although the structure of the SNAC1 NAC domain shares a structural similarity with the reported structure of the ANAC NAC1 domain, some key features, especially relating to two loop regions which potentially take the responsibility for DNA-binding, distinguish the SNAC1 NAC domain from other reported NAC structures. Moreover, the dimerization of the SNAC1 NAC domain is demonstrated by both soluble and crystalline conditions, suggesting this dimeric state should be conserved in this type of NAC family. Additionally, we discuss the possible NAC-DNA binding model according to the structure and reported biological evidences.

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“…Previous work defined the 4-bp core sequence of the NAC binding motif as CACG (Olsen et al, 2005). Moreover, studies using binding motif analysis tools and promoter binding assays have identified the specific binding motifs of NAC TFs, and these assays indicate that each NAC TF likely has a specific and different binding motif (Olsen et al, 2005;Yabuta et al, 2010;De Clercq et al, 2013).…”

Section: Nac016 Binds To a Unique Motif That Differs From The Core Namentioning

confidence: 99%

“…Moreover, studies using binding motif analysis tools and promoter binding assays have identified the specific binding motifs of NAC TFs, and these assays indicate that each NAC TF likely has a specific and different binding motif (Olsen et al, 2005;Yabuta et al, 2010;De Clercq et al, 2013). To find the specific binding motif for NAC016, we used the MEME motif discovery tool (http://meme-suite.org) (Bailey et al, 2006) and our microarray data; we identified an 11-bp consensus sequence, GATTGGAT[A/T]CA, present in 14 of the 15 genes most downregulated at 0 HDT in nac016-1 mutants (Figures 4A and 4B; Supplemental Figure 6 and Supplemental Table 2).…”

Section: Nac016 Binds To a Unique Motif That Differs From The Core Namentioning

confidence: 99%

The Arabidopsis Transcription Factor NAC016 Promotes Drought Stress Responses by Repressing AREB1 Transcription through a Trifurcate Feed-Forward Regulatory Loop Involving NAP

et al. 2015

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Drought and other abiotic stresses negatively affect plant growth and development and thus reduce productivity. The plantspecific NAM/ATAF1/2/CUC2 (NAC) transcription factors have important roles in abiotic stress-responsive signaling. Here, we show that Arabidopsis thaliana NAC016 is involved in drought stress responses; nac016 mutants have high drought tolerance, and NAC016-overexpressing (NAC016-OX) plants have low drought tolerance. Using genome-wide gene expression microarray analysis and MEME motif searches, we identified the NAC016-specific binding motif (NAC16BM), GATTGGAT[AT]CA, in the promoters of genes downregulated in nac016-1 mutants. The NAC16BM sequence does not contain the core NAC binding motif CACG (or its reverse complement CGTG). NAC016 directly binds to the NAC16BM in the promoter of ABSCISIC ACID-RESPONSIVE ELEMENT BINDING PROTEIN1 (AREB1), which encodes a central transcription factor in the stress-responsive abscisic acid signaling pathway and represses AREB1 transcription. We found that knockout mutants of the NAC016 target gene NAC-LIKE, ACTIVATED BY AP3/PI (NAP) also exhibited strong drought tolerance; moreover, NAP binds to the AREB1 promoter and suppresses AREB1 transcription. Taking these results together, we propose that a trifurcate feed-forward pathway involving NAC016, NAP, and AREB1 functions in the drought stress response, in addition to affecting leaf senescence in Arabidopsis.

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DNA-binding specificity and molecular functions of NAC transcription factors

Cited by 174 publications

References 35 publications

ABA receptor PYL9 promotes drought resistance and leaf senescence

ABA receptor PYL9 promotes drought resistance and leaf senescence

A structural view of the conserved domain of rice stress-responsive NAC1

The Arabidopsis Transcription Factor NAC016 Promotes Drought Stress Responses by Repressing AREB1 Transcription through a Trifurcate Feed-Forward Regulatory Loop Involving NAP

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