@article{ThirumalaikumarGorkaSchulzetal.2020, author = {Thirumalaikumar, Venkatesh P. and Gorka, Michal and Schulz, Karina and Masclaux-Daubresse, Celine and Sampathkumar, Arun and Skirycz, Aleksandra and Vierstra, Richard D. and Balazadeh, Salma}, title = {Selective autophagy regulates heat stress memory in Arabidopsis by NBR1-mediated targeting of HSP90.1 and ROF1}, series = {Autophagy}, volume = {17}, journal = {Autophagy}, number = {9}, publisher = {Taylor \& Francis}, address = {Abingdon}, issn = {1554-8635}, doi = {10.1080/15548627.2020.1820778}, pages = {2184 -- 2199}, year = {2020}, abstract = {In nature, plants are constantly exposed to many transient, but recurring, stresses. Thus, to complete their life cycles, plants require a dynamic balance between capacities to recover following cessation of stress and maintenance of stress memory. Recently, we uncovered a new functional role for macroautophagy/autophagy in regulating recovery from heat stress (HS) and resetting cellular memory of HS inArabidopsis thaliana. Here, we demonstrated that NBR1 (next to BRCA1 gene 1) plays a crucial role as a receptor for selective autophagy during recovery from HS. Immunoblot analysis and confocal microscopy revealed that levels of the NBR1 protein, NBR1-labeled puncta, and NBR1 activity are all higher during the HS recovery phase than before. Co-immunoprecipitation analysis of proteins interacting with NBR1 and comparative proteomic analysis of annbr1-null mutant and wild-type plants identified 58 proteins as potential novel targets of NBR1. Cellular, biochemical and functional genetic studies confirmed that NBR1 interacts with HSP90.1 (heat shock protein 90.1) and ROF1 (rotamase FKBP 1), a member of the FKBP family, and mediates their degradation by autophagy, which represses the response to HS by attenuating the expression ofHSPgenes regulated by the HSFA2 transcription factor. Accordingly, loss-of-function mutation ofNBR1resulted in a stronger HS memory phenotype. Together, our results provide new insights into the mechanistic principles by which autophagy regulates plant response to recurrent HS.}, language = {en} } @misc{PajoroMadrigalMuinoetal.2014, author = {Pajoro, Alice and Madrigal, Pedro and Mui{\~n}o, Jose M. and Matus, Jos{\´e} Tom{\´a}s and Jin, Jian and Mecchia, Martin A. and Debernardi, Juan M. and Palatnik, Javier F. and Balazadeh, Salma and Arif, Muhammad and {\´O}'Maoil{\´e}idigh, Diarmuid S. and Wellmer, Frank and Krajewski, Pawel and Riechmann, Jos{\´e}-Luis and Angenent, Gerco C. and Kaufmann, Kerstin}, title = {Dynamics of chromatin accessibility and gene regulation by MADS-domain transcription factors in flower development}, series = {Zweitver{\"o}ffentlichungen der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe}, volume = {15}, journal = {Zweitver{\"o}ffentlichungen der Universit{\"a}t Potsdam : Mathematisch-Naturwissenschaftliche Reihe}, issn = {1866-8372}, doi = {10.25932/publishup-43113}, url = {http://nbn-resolving.de/urn:nbn:de:kobv:517-opus4-431139}, pages = {19}, year = {2014}, abstract = {Background: Development of eukaryotic organisms is controlled by transcription factors that trigger specific and global changes in gene expression programs. In plants, MADS-domain transcription factors act as master regulators of developmental switches and organ specification. However, the mechanisms by which these factors dynamically regulate the expression of their target genes at different developmental stages are still poorly understood. Results: We characterized the relationship of chromatin accessibility, gene expression, and DNA binding of two MADS-domain proteins at different stages of Arabidopsis flower development. Dynamic changes in APETALA1 and SEPALLATA3 DNA binding correlated with changes in gene expression, and many of the target genes could be associated with the developmental stage in which they are transcriptionally controlled. We also observe dynamic changes in chromatin accessibility during flower development. Remarkably, DNA binding of APETALA1 and SEPALLATA3 is largely independent of the accessibility status of their binding regions and it can precede increases in DNA accessibility. These results suggest that APETALA1 and SEPALLATA3 may modulate chromatin accessibility, thereby facilitating access of other transcriptional regulators to their target genes. Conclusions: Our findings indicate that different homeotic factors regulate partly overlapping, yet also distinctive sets of target genes in a partly stage-specific fashion. By combining the information from DNA-binding and gene expression data, we are able to propose models of stage-specific regulatory interactions, thereby addressing dynamics of regulatory networks throughout flower development. Furthermore, MADS-domain TFs may regulate gene expression by alternative strategies, one of which is modulation of chromatin accessibility.}, language = {en} } @article{ShubchynskyyBonieckaSchweighoferetal.2017, author = {Shubchynskyy, Volodymyr and Boniecka, Justyna and Schweighofer, Alois and Simulis, Justinas and Kvederaviciute, Kotryna and Stumpe, Michael and Mauch, Felix and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd and Boutrot, Freddy and Zipfel, Cyril and Meskiene, Irute}, title = {Protein phosphatase AP2C1 negatively regulates basal resistance and defense responses to Pseudomonas syringae}, series = {Journal of experimental botany}, volume = {68}, journal = {Journal of experimental botany}, number = {5}, publisher = {Oxford Univ. Press}, address = {Oxford}, issn = {0022-0957}, doi = {10.1093/jxb/erw485}, pages = {1169 -- 1183}, year = {2017}, abstract = {Mitogen-activated protein kinases (MAPKs) mediate plant immune responses to pathogenic bacteria. However, less is known about the cell autonomous negative regulatory mechanism controlling basal plant immunity. We report the biological role of Arabidopsis thaliana MAPK phosphatase AP2C1 as a negative regulator of plant basal resistance and defense responses to Pseudomonas syringae. AP2C2, a closely related MAPK phosphatase, also negatively controls plant resistance. Loss of AP2C1 leads to enhanced pathogen-induced MAPK activities, increased callose deposition in response to pathogen-associated molecular patterns or to P. syringae pv. tomato (Pto) DC3000, and enhanced resistance to bacterial infection with Pto. We also reveal the impact of AP2C1 on the global transcriptional reprogramming of transcription factors during Pto infection. Importantly, ap2c1 plants show salicylic acid-independent transcriptional reprogramming of several defense genes and enhanced ethylene production in response to Pto. This study pinpoints the specificity of MAPK regulation by the different MAPK phosphatases AP2C1 and MKP1, which control the same MAPK substrates, nevertheless leading to different downstream events. We suggest that precise and specific control of defined MAPKs by MAPK phosphatases during plant challenge with pathogenic bacteria can strongly influence plant resistance.}, language = {en} } @article{ShahnejatBushehriAlluMehterovetal.2017, author = {Shahnejat-Bushehri, Sara and Allu, Annapurna Devi and Mehterov, Nikolay and Thirumalaikumar, Venkatesh P. and Alseekh, Saleh and Fernie, Alisdair R. and Mueller-Roeber, Bernd and Balazadeh, Salma}, title = {Arabidopsis NAC Transcription Factor JUNGBRUNNEN1 Exerts Conserved Control Over Gibberellin and Brassinosteroid Metabolism and Signaling Genes in Tomato}, series = {Frontiers in plant science}, volume = {8}, journal = {Frontiers in plant science}, publisher = {Frontiers Research Foundation}, address = {Lausanne}, issn = {1664-462X}, doi = {10.3389/fpls.2017.00214}, pages = {13}, year = {2017}, abstract = {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.}, language = {en} } @article{WatanabeTohgeBalazadehetal.2018, author = {Watanabe, Mutsumi and Tohge, Takayuki and Balazadeh, Salma and Erban, Alexander and Giavalisco, Patrick and Kopka, Joachim and Mueller-Roeber, Bernd and Fernie, Alisdair R. and Hoefgen, Rainer}, title = {Comprehensive Metabolomics Studies of Plant Developmental Senescence}, series = {Plant Senescence: Methods and Protocols}, volume = {1744}, journal = {Plant Senescence: Methods and Protocols}, publisher = {Humana Press}, address = {Totowa}, isbn = {978-1-4939-7672-0}, issn = {1064-3745}, doi = {10.1007/978-1-4939-7672-0_28}, pages = {339 -- 358}, year = {2018}, abstract = {Leaf senescence is an essential developmental process that involves diverse metabolic changes associated with degradation of macromolecules allowing nutrient recycling and remobilization. In contrast to the significant progress in transcriptomic analysis of leaf senescence, metabolomics analyses have been relatively limited. A broad overview of metabolic changes during leaf senescence including the interactions between various metabolic pathways is required to gain a better understanding of the leaf senescence allowing to link transcriptomics with metabolomics and physiology. In this chapter, we describe how to obtain comprehensive metabolite profiles and how to dissect metabolic shifts during leaf senescence in the model plant Arabidopsis thaliana. Unlike nucleic acid analysis for transcriptomics, a comprehensive metabolite profile can only be achieved by combining a suite of analytic tools. Here, information is provided for measurements of the contents of chlorophyll, soluble proteins, and starch by spectrophotometric methods, ions by ion chromatography, thiols and amino acids by HPLC, primary metabolites by GC/TOF-MS, and secondary metabolites and lipophilic metabolites by LC/ESI-MS. These metabolite profiles provide a rich catalogue of metabolic changes during leaf senescence, which is a helpful database and blueprint to be correlated to future studies such as transcriptome and proteome analyses, forward and reverse genetic studies, or stress-induced senescence studies.}, language = {en} } @article{ThirumalaikumarDevkarMehterovetal.2017, author = {Thirumalaikumar, Venkatesh P. and Devkar, Vikas and Mehterov, Nikolay and Ali, Shawkat and Ozgur, Rengin and Turkan, Ismail and M{\"u}ller-R{\"o}ber, Bernd and Balazadeh, Salma}, title = {NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato}, series = {Plant Biotechnology Journal}, volume = {16}, journal = {Plant Biotechnology Journal}, number = {2}, publisher = {Wiley}, address = {Hoboken}, issn = {1467-7644}, doi = {10.1111/pbi.12776}, pages = {354 -- 366}, year = {2017}, abstract = {Water deficit (drought stress) massively restricts plant growth and the yield of crops; reducing the deleterious effects of drought is therefore of high agricultural relevance. Drought triggers diverse cellular processes including the inhibition of photosynthesis, the accumulation of cell-damaging reactive oxygen species and gene expression reprogramming, besides others. Transcription factors (TF) are central regulators of transcriptional reprogramming and expression of many TF genes is affected by drought, including members of the NAC family. Here, we identify the NAC factor JUNGBRUNNEN1 (JUB1) as a regulator of drought tolerance in tomato (Solanum lycopersicum). Expression of tomato JUB1 (SlJUB1) is enhanced by various abiotic stresses, including drought. Inhibiting SlJUB1 by virus-induced gene silencing drastically lowers drought tolerance concomitant with an increase in ion leakage, an elevation of hydrogen peroxide (H2O2) levels and a decrease in the expression of various drought-responsive genes. In contrast, overexpression of AtJUB1 from Arabidopsis thaliana increases drought tolerance in tomato, alongside with a higher relative leaf water content during drought and reduced H2O2 levels. AtJUB1 was previously shown to stimulate expression of DREB2A, a TF involved in drought responses, and of the DELLA genes GAI and RGL1. We show here that SlJUB1 similarly controls the expression of the tomato orthologs SlDREB1, SlDREB2 and SlDELLA. Furthermore, AtJUB1 directly binds to the promoters of SlDREB1, SlDREB2 and SlDELLA in tomato. Our study highlights JUB1 as a transcriptional regulator of drought tolerance and suggests considerable conservation of the abiotic stress-related gene regulatory networks controlled by this NAC factor between Arabidopsis and tomato.}, language = {en} } @article{KamranfarXueTohgeetal.2018, author = {Kamranfar, Iman and Xue, Gang-Ping and Tohge, Takayuki and Sedaghatmehr, Mastoureh and Fernie, Alisdair R. and Balazadeh, Salma and Mueller-Roeber, Bernd}, title = {Transcription factor RD26 is a key regulator of metabolic reprogramming during dark-induced senescence}, series = {New phytologist : international journal of plant science}, volume = {218}, journal = {New phytologist : international journal of plant science}, number = {4}, publisher = {Wiley}, address = {Hoboken}, issn = {0028-646X}, doi = {10.1111/nph.15127}, pages = {1543 -- 1557}, year = {2018}, abstract = {Leaf senescence is a key process in plants that culminates in the degradation of cellular constituents and massive reprogramming of metabolism for the recovery of nutrients from aged leaves for their reuse in newly developing sinks. We used molecular-biological and metabolomics approaches to identify NAC transcription factor (TF) RD26 as an important regulator of metabolic reprogramming in Arabidopsis thaliana. RD26 directly activates CHLOROPLAST VESICULATION (CV), encoding a protein crucial for chloroplast protein degradation, concomitant with an enhanced protein loss in RD26 over-expressors during senescence, but a reduced decline of protein in rd26 knockout mutants. RD26 also directly activates LKR/SDH involved in lysine catabolism, and PES1 important for phytol degradation. Metabolic profiling revealed reduced c-aminobutyric acid (GABA) in RD26 overexpressors, accompanied by the induction of respective catabolic genes. Degradation of lysine, phytol and GABA is instrumental for maintaining mitochondrial respiration in carbon-limiting conditions during senescence. RD26 also supports the degradation of starch and the accumulation of mono-and disaccharides during senescence by directly enhancing the expression of AMY1, SFP1 and SWEET15 involved in carbohydrate metabolism and transport. Collectively, during senescence RD26 acts by controlling the expression of genes across the entire spectrum of the cellular degradation hierarchy.}, language = {en} } @article{OmidbakhshfardFujikuraOlasetal.2018, author = {Omidbakhshfard, Mohammad Amin and Fujikura, Ushio and Olas, Justyna Jadwiga and Xue, Gang-Ping and Balazadeh, Salma and Mueller-Roeber, Bernd}, title = {GROWTH-REGULATING FACTOR 9 negatively regulates arabidopsis leaf growth by controlling ORG3 and restricting cell proliferation in leaf primordia}, series = {PLoS Genetics : a peer-reviewed, open-access journal}, volume = {14}, journal = {PLoS Genetics : a peer-reviewed, open-access journal}, number = {7}, publisher = {PLoS}, address = {San Fransisco}, issn = {1553-7404}, doi = {10.1371/journal.pgen.1007484}, pages = {31}, year = {2018}, abstract = {Leaf growth is a complex process that involves the action of diverse transcription factors (TFs) and their downstream gene regulatory networks. In this study, we focus on the functional characterization of the Arabidopsis thaliana TF GROWTH-REGULATING FACTOR9 (GRF9) and demonstrate that it exerts its negative effect on leaf growth by activating expression of the bZIP TF OBP3-RESPONSIVE GENE 3 (ORG3). While grf9 knockout mutants produce bigger incipient leaf primordia at the shoot apex, rosette leaves and petals than the wild type, the sizes of those organs are reduced in plants overexpressing GRF9 (GRF9ox). Cell measurements demonstrate that changes in leaf size result from alterations in cell numbers rather than cell sizes. Kinematic analysis and 5-ethynyl-2'-deoxyuridine (EdU) incorporation assay revealed that GRF9 restricts cell proliferation in the early developing leaf. Performing in vitro binding site selection, we identified the 6-base motif 5'-CTGACA-3' as the core binding site of GRF9. By global transcriptome profiling, electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation (ChIP) we identified ORG3 as a direct downstream, and positively regulated target of GRF9. Genetic analysis of grf9 org3 and GRF9ox org3 double mutants reveals that both transcription factors act in a regulatory cascade to control the final leaf dimensions by restricting cell number in the developing leaf.}, language = {en} } @article{MaZhangTureckovaetal.2018, author = {Ma, Xuemin and Zhang, Youjun and Tureckova, Veronika and Xue, Gang-Ping and Fernie, Alisdair R. and Mueller-R{\"o}ber, Bernd and Balazadeh, Salma}, title = {The NAC Transcription Factor SlNAP2 Regulates Leaf Senescence and Fruit Yield in Tomato}, series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, volume = {177}, journal = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants}, number = {3}, publisher = {American Society of Plant Physiologists}, address = {Rockville}, issn = {0032-0889}, doi = {10.1104/pp.18.00292}, pages = {1286 -- 1302}, year = {2018}, abstract = {Leaf senescence is an essential physiological process in plants that supports the recycling of nitrogen and other nutrients to support the growth of developing organs, including young leaves, seeds, and fruits. Thus, the regulation of senescence is crucial for evolutionary success in wild populations and for increasing yield in crops. Here, we describe the influence of a NAC transcription factor, SlNAP2 (Solanum lycopersicum NAC-like, activated by Apetala3/Pistillata), that controls both leaf senescence and fruit yield in tomato (S. lycopersicum). SlNAP2 expression increases during age-dependent and dark-induced leaf senescence. We demonstrate that SlNAP2 activates SlSAG113 (S. lycopersicum SENESCENCE-ASSOCIATED GENE113), a homolog of Arabidopsis (Arabidopsis thaliana) SAG113, chlorophyll degradation genes such as SlSGR1 (S. lycopersicum senescence-inducible chloroplast stay-green protein 1) and SlPAO (S. lycopersicum pheide a oxygenase), and other downstream targets by directly binding to their promoters, thereby promoting leaf senescence. Furthermore, SlNAP2 directly controls the expression of genes important for abscisic acid (ABA) biosynthesis, S. lycopersicum 9-cis-epoxycarotenoid dioxygenase 1 (SlNCED1); transport, S. lycopersicum ABC transporter G family member 40 (SlABCG40); and degradation, S. lycopersicum ABA 8′-hydroxylase (SlCYP707A2), indicating that SlNAP2 has a complex role in establishing ABA homeostasis during leaf senescence. Inhibiting SlNAP2 expression in transgenic tomato plants impedes leaf senescence but enhances fruit yield and sugar content likely due to prolonged leaf photosynthesis in aging tomato plants. Our data indicate that SlNAP2 has a central role in controlling leaf senescence and fruit yield in tomato.}, language = {en} } @misc{BalazadehMuellerRoeber2018, author = {Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd}, title = {A balance to death}, series = {Nature plants}, volume = {4}, journal = {Nature plants}, number = {11}, publisher = {Nature Publ. Group}, address = {London}, issn = {2055-026X}, doi = {10.1038/s41477-018-0279-6}, pages = {863 -- 864}, year = {2018}, abstract = {Leaf senescence plays a crucial role in nutrient recovery in late-stage plant development and requires vast transcriptional reprogramming by transcription factors such as ORESARA1 (ORE1). A proteolytic mechanism is now found to control ORE1 degradation, and thus senescence, during nitrogen starvation.}, language = {en} }