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 - 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 - Thirumalaikumar, Venkatesh P. A1 - Devkar, Vikas A1 - Mehterov, Nikolay A1 - Ali, Shawkat A1 - Ozgur, Rengin A1 - Turkan, Ismail A1 - Müller-Röber, Bernd A1 - Balazadeh, Salma T1 - NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato JF - Plant Biotechnology Journal N2 - 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. KW - Arabidopsis KW - tomato KW - transcription factor KW - drought KW - reactive oxygen species KW - DELLA Y1 - 2017 U6 - https://doi.org/10.1111/pbi.12776 SN - 1467-7644 SN - 1467-7652 VL - 16 IS - 2 SP - 354 EP - 366 PB - Wiley CY - Hoboken 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 - 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 - THES A1 - Thirumalaikumar, Venkatesh P. T1 - Investigating drought and heat stress regulatory networks in Arabidopsis and tomato Y1 - 2019 ER -