TY - JOUR A1 - Thirumalaikumar, Venkatesh P. A1 - Gorka, Michal A1 - Schulz, Karina A1 - Masclaux-Daubresse, Celine A1 - Sampathkumar, Arun A1 - Skirycz, Aleksandra A1 - Vierstra, Richard D. A1 - Balazadeh, Salma T1 - Selective autophagy regulates heat stress memory in Arabidopsis by NBR1-mediated targeting of HSP90.1 and ROF1 JF - Autophagy N2 - 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. KW - Arabidopsis thaliana KW - heat stress KW - HSFA2 KW - HSP90.1 KW - NBR1 KW - ROF1 KW - selective autophagy KW - stress memory KW - stress recovery Y1 - 2020 U6 - https://doi.org/10.1080/15548627.2020.1820778 SN - 1554-8635 VL - 17 IS - 9 SP - 2184 EP - 2199 PB - Taylor & Francis CY - Abingdon ER - TY - JOUR A1 - Devkar, Vikas A1 - Thirumalaikumar, Venkatesh P. A1 - Xue, Gang-Ping A1 - Vallarino, Jose G. A1 - Tureckova, Veronika A1 - Strnad, Miroslav A1 - Fernie, Alisdair R. A1 - Hoefgen, Rainer A1 - Mueller-Roeber, Bernd A1 - Balazadeh, Salma T1 - Multifaceted regulatory function of tomato SlTAF1 in the response to salinity stress JF - New phytologist : international journal of plant science N2 - Salinity stress limits plant growth and has a major impact on agricultural productivity. Here, we identify NAC transcription factor SlTAF1 as a regulator of salt tolerance in cultivated tomato (Solanum lycopersicum). While overexpression of SlTAF1 improves salinity tolerance compared with wild-type, lowering SlTAF1 expression causes stronger salinity-induced damage. Under salt stress, shoots of SlTAF1 knockdown plants accumulate more toxic Na+ ions, while SlTAF1 overexpressors accumulate less ions, in accordance with an altered expression of the Na+ transporter genes SlHKT1;1 and SlHKT1;2. Furthermore, stomatal conductance and pore area are increased in SlTAF1 knockdown plants during salinity stress, but decreased in SlTAF1 overexpressors. We identified stress-related transcription factor, abscisic acid metabolism and defence-related genes as potential direct targets of SlTAF1, correlating it with reactive oxygen species scavenging capacity and changes in hormonal response. Salinity-induced changes in tricarboxylic acid cycle intermediates and amino acids are more pronounced in SlTAF1 knockdown than wild-type plants, but less so in SlTAF1 overexpressors. The osmoprotectant proline accumulates more in SlTAF1 overexpressors than knockdown plants. In summary, SlTAF1 controls the tomato’s response to salinity stress by combating both osmotic stress and ion toxicity, highlighting this gene as a promising candidate for the future breeding of stress-tolerant crops. KW - abscisic acid (ABA) KW - ion homeostasis KW - NAC KW - proline KW - salt stress KW - SlTAF1 KW - transcription factors Y1 - 2019 U6 - https://doi.org/10.1111/nph.16247 SN - 0028-646X SN - 1469-8137 VL - 225 IS - 4 SP - 1681 EP - 1698 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Sedaghatmehr, Mastoureh A1 - Thirumalaikumar, Venkatesh P. A1 - Kamranfar, Iman A1 - Marmagne, Anne A1 - Masclaux-Daubresse, Celine A1 - Balazadeh, Salma T1 - A regulatory role of autophagy for resetting the memory of heat stress in plants JF - Plant, cell & environment : cell physiology, whole-plant physiology, community physiology N2 - As sessile life forms, plants are repeatedly confronted with adverse environmental conditions, which can impair development, growth, and reproduction. During evolution, plants have established mechanisms to orchestrate the delicate balance between growth and stress tolerance, to reset cellular biochemistry once stress vanishes, or to keep a molecular memory, which enables survival of a harsher stress that may arise later. Although there are several examples of memory in diverse plants species, the molecular machinery underlying the formation, duration, and resetting of stress memories is largely unknown so far. We report here that autophagy, a central self-degradative process, assists in resetting cellular memory of heat stress (HS) in Arabidopsis thaliana. Autophagy is induced by thermopriming (moderate HS) and, intriguingly, remains high long after stress termination. We demonstrate that autophagy mediates the specific degradation of heat shock proteins at later stages of the thermorecovery phase leading to the accumulation of protein aggregates after the second HS and a compromised heat tolerance. Autophagy mutants retain heat shock proteins longer than wild type and concomitantly display improved thermomemory. Our findings reveal a novel regulatory mechanism for HS memory in plants. KW - Arabidopsis KW - heat shock proteins KW - priming KW - resetting Y1 - 2019 U6 - https://doi.org/10.1111/pce.13426 SN - 0140-7791 SN - 1365-3040 VL - 42 IS - 3 SP - 1054 EP - 1064 PB - Wiley CY - Hoboken ER - TY - JOUR A1 - Ma, Xuemin A1 - Balazadeh, Salma A1 - Mueller-Roeber, Bernd T1 - Tomato fruit ripening factor NOR controls leaf senescence JF - Journal of experimental botany N2 - NAC transcription factors (TFs) are important regulators of expressional reprogramming during plant development, stress responses, and leaf senescence. NAC TFs also play important roles in fruit ripening. In tomato (Solanum lycopersicum), one of the best characterized NACs involved in fruit ripening is NON-RIPENING (NOR), and the non-ripening (nor) mutation has been widely used to extend fruit shelf life in elite varieties. Here, we show that NOR additionally controls leaf senescence. Expression of NOR increases with leaf age, and developmental as well as dark-induced senescence are delayed in the nor mutant, while overexpression of NOR promotes leaf senescence. Genes associated with chlorophyll degradation as well as senescence-associated genes (SAGs) show reduced and elevated expression, respectively, in nor mutants and NOR overexpressors. Overexpression of NOR also stimulates leaf senescence in Arabidopsis thaliana. In tomato, NOR supports senescence by directly and positively regulating the expression of several senescence-associated genes including, besides others, SlSAG15 and SlSAG113, SlSGR1, and SlYLS4. Finally, we find that another senescence control NAC TF, namely SlNAP2, acts upstream of NOR to regulate its expression. Our data support a model whereby NAC TFs have often been recruited by higher plants for both the control of leaf senescence and fruit ripening. KW - Aging KW - leaf KW - NAC KW - non-ripening KW - NOR KW - senescence KW - tomato KW - transcription factor Y1 - 2019 U6 - https://doi.org/10.1093/jxb/erz098 SN - 0022-0957 SN - 1460-2431 VL - 70 IS - 10 SP - 2727 EP - 2740 PB - Oxford Univ. Press CY - Oxford ER - TY - JOUR A1 - Omidbakhshfard, Mohammad Amin A1 - Fujikura, Ushio A1 - Olas, Justyna Jadwiga A1 - Xue, Gang-Ping A1 - Balazadeh, Salma A1 - Mueller-Roeber, Bernd T1 - GROWTH-REGULATING FACTOR 9 negatively regulates arabidopsis leaf growth by controlling ORG3 and restricting cell proliferation in leaf primordia JF - PLoS Genetics : a peer-reviewed, open-access journal N2 - 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. Y1 - 2018 U6 - https://doi.org/10.1371/journal.pgen.1007484 SN - 1553-7404 VL - 14 IS - 7 PB - PLoS CY - San Fransisco ER - TY - JOUR A1 - Watanabe, Mutsumi A1 - Tohge, Takayuki A1 - Balazadeh, Salma A1 - Erban, Alexander A1 - Giavalisco, Patrick A1 - Kopka, Joachim A1 - Mueller-Roeber, Bernd A1 - Fernie, Alisdair R. A1 - Hoefgen, Rainer T1 - Comprehensive Metabolomics Studies of Plant Developmental Senescence JF - Plant Senescence: Methods and Protocols N2 - 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. KW - Senescence KW - Metabolomics KW - Arabidopsis KW - GC/MS KW - LC/MS KW - HPLC KW - IC Y1 - 2018 SN - 978-1-4939-7672-0 SN - 978-1-4939-7670-6 U6 - https://doi.org/10.1007/978-1-4939-7672-0_28 SN - 1064-3745 SN - 1940-6029 VL - 1744 SP - 339 EP - 358 PB - Humana Press CY - Totowa ER - TY - JOUR A1 - Ma, Xuemin A1 - Zhang, Youjun A1 - Tureckova, Veronika A1 - Xue, Gang-Ping A1 - Fernie, Alisdair R. A1 - Mueller-Röber, Bernd A1 - Balazadeh, Salma T1 - The NAC Transcription Factor SlNAP2 Regulates Leaf Senescence and Fruit Yield in Tomato JF - Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants N2 - 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. Y1 - 2018 U6 - https://doi.org/10.1104/pp.18.00292 SN - 0032-0889 SN - 1532-2548 VL - 177 IS - 3 SP - 1286 EP - 1302 PB - American Society of Plant Physiologists CY - Rockville ER - TY - JOUR A1 - Kamranfar, Iman A1 - Xue, Gang-Ping A1 - Tohge, Takayuki A1 - Sedaghatmehr, Mastoureh A1 - Fernie, Alisdair R. A1 - Balazadeh, Salma A1 - Mueller-Roeber, Bernd T1 - Transcription factor RD26 is a key regulator of metabolic reprogramming during dark-induced senescence JF - New phytologist : international journal of plant science N2 - 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. KW - Arabidopsis KW - fatty acid KW - primary metabolism KW - protein and amino acid degradation KW - respiration KW - senescence Y1 - 2018 U6 - https://doi.org/10.1111/nph.15127 SN - 0028-646X SN - 1469-8137 VL - 218 IS - 4 SP - 1543 EP - 1557 PB - Wiley CY - Hoboken ER - TY - GEN A1 - Balazadeh, Salma A1 - Müller-Röber, Bernd T1 - A balance to death T2 - Nature plants N2 - 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. Y1 - 2018 U6 - https://doi.org/10.1038/s41477-018-0279-6 SN - 2055-026X SN - 2055-0278 VL - 4 IS - 11 SP - 863 EP - 864 PB - Nature Publ. Group CY - London ER - 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 -