The NAC transcription factor ATAF2 promotes ethylene biosynthesis and response in <i>Arabidopsis thaliana</i> seedlings

Peng, Hao; Phung, Jessica; Stowe, Evan; Dhingra, Amit; Neff, Michael M.

doi:10.1002/1873-3468.14317

Cited by 4 publications

(6 citation statements)

References 41 publications

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“…The latter is part of a signaling cascade, also involving MPK 3 and MPK6, that leads to enhanced ethylene production and signaling via phosphorylation of ACS6 and ERFs, respectively ( Liu and Zhang, 2004 ; Meng et al, 2013 ). ANAC081 also positively regulates ethylene biosynthesis ( Peng et al, 2022 ). Among the enriched GO terms for late responsive genes in cluster 6 were several related to hormone response and indole metabolism ( Figure 3G; Supplemental Data Set S4 ).…”

Section: Resultsmentioning

confidence: 99%

“…These ERFs are involved in diverse stress-signaling pathways ( Muller and Munne-Bosch, 2015 ), while CAMTA1 belongs to the ethylene-induced calmodulin binding protein family and is also involved in auxin signaling ( Reddy et al, 2000 ; Galon et al, 2010 ). ANAC081 promotes ethylene production ( Peng et al, 2022 ). Interestingly, ANAC017 was also a regulator of genes in path 3 resulting from a furcation event at 120 min, suggesting it does not exclusively regulate the highly induced genes in paths 1 and 2 but is also associated with hormonal and growth responses.…”

Section: Resultsmentioning

confidence: 99%

“…These include genes encoding the ANAC TF family members ANAC081, ANAC013, ANAC102, ANAC053, and ANAC044, which control a wide range of growth processes and stress responses, including the cell cycle, senescence, responses to photooxidative damage, and seed germination ( Christianson et al, 2009 ; Takasaki et al, 2015 ; D'Alessandro et al, 2018 ; Takahashi et al, 2019 ; Nagahage et al, 2020 ), with ANAC013 and ANAC053 also directly involved in the mitochondrial dysfunction response ( De Clercq et al, 2013 ). The most significantly enriched region was located in the promoter of ANAC081 , which promotes ethylene biosynthesis ( Supplemental Data Set S16 ; Peng et al, 2022 ). bZIP60 and bZIP53 are key regulators of the unfolded protein response of the endoplasmic reticulum (UPR ER ) and metabolic reprogramming under low energy stress, respectively ( Iwata et al, 2008 ; Dietrich et al, 2011 ).…”

Section: Resultsmentioning

confidence: 99%

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The retrograde signaling regulator ANAC017 recruits the MKK9–MPK3/6, ethylene, and auxin signaling pathways to balance mitochondrial dysfunction with growth

Liew

Yin

et al. 2022

The Plant Cell

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In plant cells, mitochondria are ideally positioned to sense and balance changes in energy metabolism in response to changing environmental conditions. Retrograde signalling from mitochondria to the nucleus is crucial for adjusting the required transcriptional responses. We show that ANAC017, the master regulator of mitochondrial stress, directly recruits a signalling cascade involving the plant hormones ethylene and auxin as well as the MAP KINASE KINASE (MKK) 9 - MAP KINASE (MPK) 3/6 pathway in Arabidopsis thaliana. Chromatin immunoprecipitation followed by sequencing (ChIP-seq) and overexpression demonstrated that ANAC017 directly regulates several genes of the ethylene and auxin pathways, including MKK9, 1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 2 and YUCCA 5, in addition to genes encoding transcription factors regulating plant growth and stress responses such as BASIC REGION/LEUCINE ZIPPER MOTIF (bZIP) 60, bZIP53, ANAC081/ATAF2 and RADICAL-INDUCED CELL DEATH1. A time-resolved RNA-seq experiment established that ethylene signalling precedes the stimulation of auxin signalling in the mitochondrial stress response, with a large part of the transcriptional regulation dependent on ETHYLENE INSENSITIVE 3. These results were confirmed by mutant analyses. Our findings identify the molecular components controlled by ANAC017, which integrates the primary stress responses to mitochondrial dysfunction with whole plant growth via the activation of regulatory and partly antagonistic feedback loops.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

The retrograde signaling regulator ANAC017 recruits the MKK9–MPK3/6, ethylene, and auxin signaling pathways to balance mitochondrial dysfunction with growth

Liew

Yin

et al. 2022

The Plant Cell

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show abstract

“…Tartary Buckwheat plants overexpressing FtNAC70 showed greater salt and drought tolerance resistance [ 56 ]. Arabidopsis thaliana ATAF2 promotes ethylene biosynthesis and response through the activation of related genes [ 57 ]. Plant secondary metabolites are nonessential small molecule compounds for the proper functioning of plant growth and development, which are usually not directly involved in growth and development and have an important role in plant ecological adaptation [ 58 ].…”

Section: Discussionmentioning

confidence: 99%

Identification of the NAC Transcription Factor Family during Early Seed Development in Akebia trifoliata (Thunb.) Koidz

Liu

Chen

et al. 2023

Plants

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This study aimed to gain an understanding of the possible function of NACs by examining their physicochemical properties, structure, chromosomal location, and expression. Being a family of plant-specific transcription factors, NAC (petunia no apical meristem and Arabidopsis thaliana ATAF1, ATAF2, and CUC2) is involved in plant growth and development. None of the NAC genes has been reported in Akebia trifoliata (Thunb.) Koidz (A. trifoliata). In this study, we identified 101 NAC proteins (AktNACs) in the A. trifoliata genome by bioinformatic analysis. One hundred one AktNACs were classified into the following twelve categories based on the phylogenetic analysis of NAC protein: NAC-a, NAC-b, NAC-c, NAC-d, NAC-e, NAC-f, NAC-g, NAC-h, NAC-i, NAC-j, NAC-k, and NAC-l. The accuracy of the clustering results was demonstrated based on the gene structure and conserved motif analysis of AktNACs. In addition, we identified 44 pairs of duplication genes, confirming the importance of purifying selection in the evolution of AktNACs. The morphology and microstructure of early A. trifoliata seed development showed that it mainly underwent rapid cell division, seed enlargement, embryo formation and endosperm development. We constructed AktNACs co-expression network and metabolite correlation network based on transcriptomic and metabolomic data of A. trifoliata seeds. The results of the co-expression network showed that 25 AtNAC genes were co-expressed with 233 transcription factors. Metabolite correlation analysis showed that 23 AktNACs were highly correlated with 28 upregulated metabolites. Additionally, 25 AktNACs and 235 transcription factors formed co-expression networks with 141 metabolites, based on correlation analysis involving AktNACs, transcription factors, and metabolites. Notably, AktNAC095 participates in the synthesis of 35 distinct metabolites. Eight of these metabolites, strongly correlated with AktNAC095, were upregulated during early seed development. These studies may provide insight into the evolution, possible function, and expression of AktNACs genes.

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“…It has also been reported that ANAC102 localizes in chloroplast nucleoids and regulates gene expression in chloroplasts (Xin et al, 2021 ). ATAF2 is involved in various processes such as biotic stress responses (Delessert et al, 2005 ), brassinosteroid catabolism (Peng et al, 2015 ; Peng & Neff, 2020 , 2021 ), auxin biosynthesis (Huh et al, 2012 ), photomorphogenesis (Peng et al, 2015 , 2020 ), circadian clock (Peng et al, 2015 , 2020 ; Peng & Neff, 2020 , 2021 ), and ethylene biosynthesis and responses (Peng et al, 2022 ). Recently, we found that ATAF2 upregulates several senescence regulators such as ORE1 , ORS1 , VNI2 , and ANAC046 (Nagahage et al, 2018 , 2020 ).…”

Section: Introductionmentioning

confidence: 99%

NAC domain transcription factors VNI2 and ATAF2 form protein complexes and regulate leaf senescence

Nagahage,

Matsuda,

Miyashita

et al. 2023

Plant Direct

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The NAM, ATAF1/2, and CUC2 (NAC) domain transcription factor VND‐INTERACTING2 (VNI2) negatively regulates xylem vessel formation by interacting with another NAC domain transcription factor, VASCULAR‐RELATED NAC‐DOMAIN7 (VND7), a master regulator of xylem vessel formation. Here, we screened interacting proteins with VNI2 using yeast two‐hybrid assay and isolated two NAC domain transcription factors, Arabidopsis thaliana ACTIVATION FACTOR 2 (ATAF2) and NAC DOMAIN CONTAINING PROTEIN 102 (ANAC102). A transient gene expression assay showed that ATAF2 upregulates the expression of genes involved in leaf senescence, and VNI2 effectively inhibits the transcriptional activation activity of ATAF2. vni2 mutants accelerate leaf senescence, whereas ataf2 mutants delay leaf senescence. In addition, the accelerated leaf senescence phenotype of the vni2 mutant is recovered by simultaneous mutation of ATAF2. Our findings strongly suggest that VNI2 interacts with and inhibits ATAF2, resulting in negatively regulating leaf senescence.

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The NAC transcription factor ATAF2 promotes ethylene biosynthesis and response in Arabidopsis thaliana seedlings

Cited by 4 publications

References 41 publications

The retrograde signaling regulator ANAC017 recruits the MKK9–MPK3/6, ethylene, and auxin signaling pathways to balance mitochondrial dysfunction with growth

The retrograde signaling regulator ANAC017 recruits the MKK9–MPK3/6, ethylene, and auxin signaling pathways to balance mitochondrial dysfunction with growth

Identification of the NAC Transcription Factor Family during Early Seed Development in Akebia trifoliata (Thunb.) Koidz

NAC domain transcription factors VNI2 and ATAF2 form protein complexes and regulate leaf senescence

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