TY  - JOUR
A1  - Shahnejat-Bushehri, Sara
A1  - Allu, Annapurna Devi
A1  - Mehterov, Nikolay
A1  - Thirumalaikumar, Venkatesh P.
A1  - Alseekh, Saleh
A1  - Fernie, Alisdair R.
A1  - Mueller-Roeber, Bernd
A1  - Balazadeh, Salma
T1  - Arabidopsis NAC Transcription Factor JUNGBRUNNEN1 Exerts Conserved Control Over Gibberellin and Brassinosteroid Metabolism and Signaling Genes in Tomato
JF  - Frontiers in plant science
N2  - The Arabidopsis thaliana NAC transcription factor JUNGBRUNNEN1 (AtJUB1) regulates growth by directly repressing GA3ox1 and DWF4, two key genes involved in gibberellin (GA) and brassinosteroid (BR) biosynthesis, respectively, leading to GA and BR deficiency phenotypes. AtJUB1 also reduces the expression of PIF4, a bHLH transcription factor that positively controls cell elongation, while it stimulates the expression of DELLA genes, which are important repressors of growth. Here, we extend our previous findings by demonstrating that AtJUB1 induces similar GA and BR deficiency phenotypes and changes in gene expression when overexpressed in tomato (Solanum lycopersicum). Importantly, and in accordance with the growth phenotypes observed, AtJUB1 inhibits the expression of growth-supporting genes, namely the tomato orthologs of GA3ox1, DWF4 and PIF4, but activates the expression of DELLA orthologs, by directly binding to their promoters. Overexpression of AtJUB1 in tomato delays fruit ripening, which is accompanied by reduced expression of several ripeningrelated genes, and leads to an increase in the levels of various amino acids (mostly proline, beta-alanine, and phenylalanine), gamma-aminobutyric acid (GABA), and major organic acids including glutamic acid and aspartic acid. The fact that AtJUB1 exerts an inhibitory effect on the GA/BR biosynthesis and PIF4 genes but acts as a direct activator of DELLA genes in both, Arabidopsis and tomato, strongly supports the model that the molecular constituents of the JUNGBRUNNEN1 growth control module are considerably conserved across species.
KW  - Arabidopsis
KW  - tomato
KW  - fruit
KW  - growth
KW  - transcription factor
KW  - gibberellic acid
KW  - brassinosteroid
KW  - DELLA proteins
Y1  - 2017
U6  - https://doi.org/10.3389/fpls.2017.00214
SN  - 1664-462X
VL  - 8
PB  - Frontiers Research Foundation
CY  - Lausanne
ER  - 
TY  - JOUR
A1  - Balazadeh, Salma
A1  - Siddiqui, Hamad
A1  - Allu, Annapurna Devi
A1  - Matallana-Ramirez, Lilian Paola
A1  - Caldana, Camila
A1  - Mehrnia, Mohammad
A1  - Zanor, Maria-Inés
A1  - Koehler, Barbara
A1  - Müller-Röber, Bernd
T1  - A gene regulatory network controlled by the NAC transcription factor ANAC092/AtNAC2/ORE1 during salt-promoted senescence
N2  - P>The onset and progression of senescence are under genetic and environmental control. The Arabidopsis thaliana NAC transcription factor ANAC092 (also called AtNAC2 and ORE1) has recently been shown to control age-dependent senescence, but its mode of action has not been analysed yet. To explore the regulatory network administered by ANAC092 we performed microarray-based expression profiling using estradiol-inducible ANAC092 overexpression lines. Approximately 46% of the 170 genes up-regulated upon ANAC092 induction are known senescence-associated genes, suggesting that the NAC factor exerts its role in senescence through a regulatory network that includes many of the genes previously reported to be senescence regulated. We selected 39 candidate genes and confirmed their time-dependent response to enhanced ANAC092 expression by quantitative RT-PCR. We also found that the majority of them (24 genes) are up-regulated by salt stress, a major promoter of plant senescence, in a manner similar to that of ANAC092, which itself is salt responsive. Furthermore, 24 genes like ANAC092 turned out to be stage-dependently expressed during seed growth with low expression at early and elevated expression at late stages of seed development. Disruption of ANAC092 increased the rate of seed germination under saline conditions, whereas the opposite occurred in respective overexpression plants. We also detected a delay of salinity-induced chlorophyll loss in detached anac092-1 mutant leaves. Promoter-reporter (GUS) studies revealed transcriptional control of ANAC092 expression during leaf and flower ageing and in response to salt stress. We conclude that ANAC092 exerts its functions during senescence and seed germination through partly overlapping target gene sets.
Y1  - 2010
UR  - http://www3.interscience.wiley.com/cgi-bin/issn?DESCRIPTOR=PRINTISSN&VALUE=0960-7412
U6  - https://doi.org/10.1111/j.1365-313X.2010.04151.x
SN  - 0960-7412
ER  - 
TY  - JOUR
A1  - Wu, Anhui
A1  - Allu, Annapurna Devi
A1  - Garapati, Prashanth
A1  - Siddiqui, Hamad
A1  - Dortay, Hakan
A1  - Zanor, Maria-Ines
A1  - Asensi-Fabado, Maria Amparo
A1  - Munne-Bosch, Sergi
A1  - Antonio, Carla
A1  - Tohge, Takayuki
A1  - Fernie, Alisdair R.
A1  - Kaufmann, Kerstin
A1  - Xue, Gang-Ping
A1  - Müller-Röber, Bernd
A1  - Balazadeh, Salma
T1  - Jungbrunnen1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in arabidopsis
JF  - The plant cell
N2  - The transition from juvenility through maturation to senescence is a complex process that involves the regulation of longevity. Here, we identify JUNGBRUNNEN1 (JUB1), a hydrogen peroxide (H2O2)-induced NAC transcription factor, as a central longevity regulator in Arabidopsis thaliana. JUB1 overexpression strongly delays senescence, dampens intracellular H2O2 levels, and enhances tolerance to various abiotic stresses, whereas in jub1-1 knockdown plants, precocious senescence and lowered abiotic stress tolerance are observed. A JUB1 binding site containing a RRYGCCGT core sequence is present in the promoter of DREB2A, which plays an important role in abiotic stress responses. JUB1 transactivates DREB2A expression in mesophyll cell protoplasts and transgenic plants and binds directly to the DREB2A promoter. Transcriptome profiling of JUB1 overexpressors revealed elevated expression of several reactive oxygen species-responsive genes, including heat shock protein and glutathione S-transferase genes, whose expression is further induced by H2O2 treatment. Metabolite profiling identified elevated Pro and trehalose levels in JUB1 overexpressors, in accordance with their enhanced abiotic stress tolerance. We suggest that JUB1 constitutes a central regulator of a finely tuned control system that modulates cellular H2O2 level and primes the plants for upcoming stress through a gene regulatory network that involves DREB2A.
Y1  - 2012
U6  - https://doi.org/10.1105/tpc.111.090894
SN  - 1040-4651
VL  - 24
IS  - 2
SP  - 482
EP  - 506
PB  - American Society of Plant Physiologists
CY  - Rockville
ER  - 
TY  - JOUR
A1  - Allu, Annapurna Devi
A1  - Soja, Aleksandra Maria
A1  - Wu, Anhui
A1  - Szymanski, Jedrzej
A1  - Balazadeh, Salma
T1  - Salt stress and senescence: identification of cross-talk regulatory components
JF  - Journal of experimental botany
N2  - Leaf senescence is an active process with a pivotal impact on plant productivity. It results from extensive signalling cross-talk coordinating environmental factors with intrinsic age-related mechanisms. Although many studies have shown that leaf senescence is affected by a range of external parameters, knowledge about the regulatory systems that govern the interplay between developmental programmes and environmental stress is still vague. Salinity is one of the most important environmental stresses that promote leaf senescence and thus affect crop yield. Improving salt tolerance by avoiding or delaying senescence under stress will therefore play an important role in maintaining high agricultural productivity. Experimental evidence suggests that hydrogen peroxide (H2O2) functions as a common signalling molecule in both developmental and salt-induced leaf senescence. In this study, microarray-based gene expression profiling on Arabidopsis thaliana plants subjected to long-term salinity stress to induce leaf senescence was performed, together with co-expression network analysis for H2O2-responsive genes that are mutually up-regulated by salt induced-and developmental leaf senescence. Promoter analysis of tightly co-expressed genes led to the identification of seven cis-regulatory motifs, three of which were known previously, namely CACGTGT and AAGTCAA, which are associated with reactive oxygen species (ROS)-responsive genes, and CCGCGT, described as a stress-responsive regulatory motif, while the others, namely ACGCGGT, AGCMGNC, GMCACGT, and TCSTYGACG were not characterized previously. These motifs are proposed to be novel elements involved in the H2O2-mediated control of gene expression during salinity stress-triggered and developmental senescence, acting through upstream transcription factors that bind to these sites.
KW  - Arabidopsis
KW  - hydrogen peroxide
KW  - longevity
KW  - reactive oxygen species
KW  - salt stress
KW  - senescence
KW  - signal cross-talk
KW  - transcription factor
Y1  - 2014
U6  - https://doi.org/10.1093/jxb/eru173
SN  - 0022-0957
SN  - 1460-2431
VL  - 65
IS  - 14
SP  - 3993
EP  - 4008
PB  - Oxford Univ. Press
CY  - Oxford
ER  - 
TY  - JOUR
A1  - Ebrahimian-Motlagh, Saghar
A1  - Ribone, Pamela A.
A1  - Thirumalaikumar, Venkatesh P.
A1  - Allu, Annapurna Devi
A1  - Chan, Raquel L.
A1  - Mueller-Roeber, Bernd
A1  - Balazadeh, Salma
T1  - JUNGBRUNNEN1 Confers Drought Tolerance Downstream of the HD-Zip I Transcription Factor AtHB13
JF  - Frontiers in plant science
N2  - Low water availability is the major environmental factor limiting growth and productivity of plants and crops and is therefore considered of high importance for agriculture affected by climate change. Identifying regulatory components controlling the response and tolerance to drought stress is thus of major importance. The NAC transcription factor (TF) JUNGBRUNNEN1 (JUB1) from Arabidopsis thaliana extends leaf longevity under non-stress growth conditions, lowers cellular hydrogen peroxide (H2O2) level, and enhances tolerance against heat stress and salinity. Here, we additionally find that JUB1 strongly increases tolerance to drought stress in Arabidopsis when expressed from both, a constitutive (CaMV 35S) and an abiotic stress-induced (RD29A) promoter. Employing a yeast one-hybrid screen we identified HD-Zip class I TF AtHB13 as an upstream regulator of JUB1. AtHB13 has previously been reported to act as a positive regulator of drought tolerance. AtHB13 and JUB1 thereby establish a joint drought stress control module.
KW  - Arabidopsis
KW  - transcription factor
KW  - drought
KW  - JUB1
KW  - HB13
Y1  - 2017
U6  - https://doi.org/10.3389/fpls.2017.02118
SN  - 1664-462X
VL  - 8
PB  - Frontiers Research Foundation
CY  - Lausanne
ER  - 
TY  - JOUR
A1  - Allu, Annapurna Devi
A1  - Brotman, Yariv
A1  - Xue, Gang-Ping
A1  - Balazadeh, Salma
T1  - Transcription factor ANAC032 modulates JA/SA signalling in response to Pseudomonas syringae infection
JF  - EMBO reports
N2  - Responses to pathogens, including host transcriptional reprogramming, require partially antagonistic signalling pathways dependent on the phytohormones salicylic (SA) and jasmonic (JA) acids. However, upstream factors modulating the interplay of these pathways are not well characterized. Here, we identify the transcription factor ANAC032 from Arabidopsis thaliana as one such regulator in response to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (Pst). ANAC032 directly represses MYC2 activation upon Pst attack, resulting in blockage of coronatine-mediated stomatal reopening which restricts entry of bacteria into plant tissue. Furthermore, ANAC032 activates SA signalling by repressing NIMIN1, a key negative regulator of SA-dependent defence. Finally, ANAC032 reduces expression of JA-responsive genes, including PDF1.2A. Thus, ANAC032 enhances resistance to Pst by generating an orchestrated transcriptional output towards key SA- and JA-signalling genes coordinated through direct binding of ANAC032 to the MYC2, NIMIN1 and PDF1.2A promoters.
KW  - Arabidopsis
KW  - jasmonic acid
KW  - pathogens
KW  - salicylic acid
KW  - transcription factor
Y1  - 2016
U6  - https://doi.org/10.15252/embr.201642197
SN  - 1469-221X
SN  - 1469-3178
VL  - 17
SP  - 1578
EP  - 1589
PB  - Wiley-Blackwell
CY  - Hoboken
ER  - 
TY  - JOUR
A1  - Shahnejat-Bushehri, Sara
A1  - Nobmann, Barbara
A1  - Allu, Annapurna Devi
A1  - Balazadeh, Salma
T1  - JUB1 suppresses Pseudomonas syringae-induced defense responses through accumulation of DELLA proteins
JF  - Journal of trace elements in medicine and biology
N2  - Phytohormones act in concert to coordinate plant growth and the response to environmental cues. Gibberellins (GAs) are growth-promoting hormones that recently emerged as modulators of plant immune signaling. By regulating the stability of DELLA proteins, GAs intersect with the signaling pathways of the classical primary defense hormones, salicylic acid (SA) and jasmonic acid (JA), thereby altering the final outcome of the immune response. DELLA proteins confer resistance to necrotrophic pathogens by potentiating JA signaling and raise the susceptibility to biotrophic pathogens by attenuating the SA pathway. Here, we show that JUB1, a core element of the GA - brassinosteroid (BR) - DELLA regulatory module, functions as a negative regulator of defense responses against Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) and mediates the crosstalk between growth and immunity.
KW  - Arabidopsis
KW  - defense
KW  - DELLA proteins
KW  - gibberellin
KW  - jasmonic acid
KW  - pathogens
KW  - salicylic acid
KW  - transcription factor
Y1  - 2016
U6  - https://doi.org/10.1080/15592324.2016.1181245
SN  - 1559-2316
SN  - 1559-2324
VL  - 11
PB  - Elsevier
CY  - Philadelphia
ER  - 
TY  - JOUR
A1  - Allu, Annapurna Devi
A1  - Simancas, Barbara
A1  - Balazadeh, Salma
A1  - Munne-Bosch, Sergi
T1  - Defense-Related Transcriptional Reprogramming in Vitamin E-Deficient Arabidopsis Mutants Exposed to Contrasting Phosphate Availability
JF  - Frontiers in plant science
N2  - Vitamin E inhibits the propagation of lipid peroxidation and helps protecting photosystem II from photoinhibition, but little is known about its possible role in plant response to Pi availability. Here, we aimed at examining the effect of vitamin E deficiency in Arabidopsis thaliana vte mutants on phytohormone contents and the expression of transcription factors in plants exposed to contrasting Pi availability. Plants were subjected to two doses of Pi, either unprimed (controls) or previously exposed to low Pi (primed). In the wild type, alpha-tocopherol contents increased significantly in response to repeated periods of low Pi, which was paralleled by increased growth, indicative of a priming effect. This growth-stimulating effect was, however, abolished in vte mutants. Hormonal profiling revealed significant effects of Pi availability, priming and genotype on the contents of jasmonates and salicylates; remarkably, vte mutants showed enhanced accumulation of both hormones under low Pi. Furthermore, expression profiling of 1,880 transcription factors by qRT-PCR revealed a pronounced effect of priming on the transcript levels of 45 transcription factors mainly associated with growth and stress in wild-type plants in response to low Pi availability; while distinct differences in the transcriptional response were detected in vte mutants. We conclude that alpha-tocopherol plays a major role in the response of plants to Pi availability not only by protecting plants from photo-oxidative stress, but also by exerting a control over growth-and defense-related transcriptional reprogramming and hormonal modulation.
KW  - antioxidants
KW  - photosystem II
KW  - plastochromanol-8
KW  - priming
KW  - retrograde signaling
KW  - tocochromanols
KW  - vitamin E
Y1  - 2017
U6  - https://doi.org/10.3389/fpls.2017.01396
SN  - 1664-462X
VL  - 8
PB  - Frontiers Research Foundation
CY  - Lausanne
ER  -