Salma Balazadeh

• PhD
• Universität Potsdam

Heat stress (HS) poses a major challenge to plants and agriculture, especially during climate change‐induced heatwaves. Plants have evolved mechanisms to combat HS and remember past stress. This memory involves lasting changes in specific stress responses, enabling plants to better anticipate and react to future heat events. HS memory is a multi‐la...

Soil water deficit (WD) significantly impacts plant survival and crop yields. Many gaps remain in our understanding of the synergistic coordination between molecular and ecophysiological responses delaying substantial drought-induced effects on plant growth. To investigate this synergism in tomato leaves, we combined molecular, ecophysiological, an...

Soil water deficit (WD) is one of the most important abiotic stresses affecting plant survival and crop yield. Despite its economic relevance, many gaps remain in our understanding of how crops respond to WD, especially concerning the synergistic coordination of molecular and ecophysiological adaptations delaying plant damage and mortality. In this...

Quinoa (Chenopodium quinoa Willd.), an Andean crop, is a facultative halophyte food crop recognized globally for its high nutritional value and plasticity to adapt to harsh conditions. We conducted a genome-wide association study on a diverse set of quinoa germplasm accessions. These accessions were evaluated for the following agronomic and biochem...

Plants can be primed to withstand otherwise lethal heat stress (HS) through exposure to a foregoing temporary and mild HS, commonly known as the ´thermopriming stimulus´. Plants can also generate memories of a previous stress encounter and reset their physiology to the original cellular state once the stress has vanished. The priming stimulus trigg...

Senescence is a highly regulated process driven by developmental age and environmental factors. Although leaf senescence is accelerated by nitrogen (N) deficiency, the underlying physiological and molecular mechanisms are largely unknown. Here, we reveal that BBX14, a previously uncharacterized BBX-type transcription factor in Arabidopsis, is cruci...

Outline The volatile phytohormone ethylene is a major regulator of plant adaptive responses to flooding. In flooded plant tissues, it quickly increases to high concentrations due to its low solubility and diffusion rates in water. The passive, quick and consistent accumulation of ethylene in submerged plant tissues makes it a reliable cue for plant...

Plants adapt to cold, non‐freezing temperatures through cold acclimation and lose acquired freezing tolerance in warmer temperatures in a process called deacclimation. This work identified a hypoxia response during early deacclimation evidenced by increased ADH activity and upregulated gene expression of hypoxia markers. Mutants defective in hypoxi...

Pre-exposing (priming) plants to mild, non-lethal elevated temperature improves their tolerance to a later higher-temperature stress (triggering stimulus), which is of great ecological importance. ‘Thermomemory’ is maintaining this tolerance for an extended period of time. NAM/ATAF1/2/CUC2 (NAC) proteins are plant-specific transcription factors (TF...

Quinoa (Chenopodium quinoa Willd.) is an herbaceous annual crop of the amaranth family (Amaranthaceae). It is increasingly cultivated for its nutritious grains, which are rich in protein and essential amino acids, lipids, and minerals. Quinoa exhibits a high tolerance towards various abiotic stresses including drought and salinity, which supports i...

Plants ´memorize´ stressful events and protect themselves from future, often more severe, stresses. To maximize growth after stress, plants ´reset´, or ´forget´, memories of stressful situations which requires an intricate balance between stress memory formation and the degree of forgetfulness. HEAT SHOCK PROTEIN 21 (HSP21) encodes a small HSP in p...

Heat stress (HS) caused by above-optimal temperatures adversely affects plants’ growth and development and diminishes crop yields. In natural and agricultural environments, these stresses are often transient but recurrent and may progressively increase in severity over time. In addition to the inherent ability to cope with a single HS event, plants...

Mitogen-activated protein kinase (MAPK) cascades transmit environmental signals and induce stress and defence responses in plants. These signalling cascades are negatively controlled by specific phosphatases of the type 2C Ser/Thr protein phosphatase (PP2C) and dual-specificity phosphatase (DSP) families that inactivate stress-induced MAPKs; howeve...

Our results suggest that the selected drought-tolerant wheat cultivar Wadielniel has a greater capacity in regulating water deficit stress than the drought-sensitive cultivar Condor. As suggested by an enhanced physiological response supported by upregulating regulatory genes and producing more sugars, organic acids, and important amino acids in sh...

The phytohormones gibberellins (GAs) play fundamental roles in almost every aspect of plant growth and development. Although there is good knowledge about GA biosynthetic and signaling pathways, factors contributing to the mechanisms homeostatically controlling GA levels remain largely unclear. Here, we demonstrate that homeobox transcription facto...

Quinoa (Chenopodium quinoa Willd.) is an herbaceous annual crop of the amaranth family (Amaranthaceae). It is increasingly cultivated for its nutritious grains, which are rich in protein and essential amino acids, lipids, and minerals. Quinoa exhibits a high tolerance towards various abiotic stresses including drought and salinity, which supports i...

Moderate and temporary heat stresses (HS) prime plants to tolerate, and survive, a subsequent severe HS. Such acquired thermotolerance can be maintained for several days under normal growth conditions, and create a HS memory. We recently demonstrated that plastid-localized small heat shock protein HSP21 is a key component of HS memory in Arabidopsi...

Mitogen-activated protein kinase (MAPK) cascades transmit environmental signals and induce stress and defence responses in plants. These signalling cascades are negatively controlled by specific phosphatases of the type 2C Ser/Thr protein phosphatase (PP2C) and dual-specificity phosphatase (DSP) families that inactivate stress-induced MAPKs; howeve...

Pre-exposing (priming) plants to mild, non-lethal elevated temperature improves their tolerance to a later higher-temperature stress (triggering stimulus), which is of great ecological importance. ‘Thermomemory’ is maintaining this tolerance for an extended period of time. NAM/ATAF1/2/CUC2 (NAC) proteins are plant-specific transcription factors (TF...

In plants, the shoot apical meristem (SAM) is essential for the growth of above-ground organs. However, little is known about its molecular responses to abiotic stresses. Here, we show that the SAM of Arabidopsis thaliana displays an autonomous heat stress (HS) memory of a previous non-lethal HS, allowing the SAM to regain growth after exposure to...

Root hairs are outgrowths of epidermal cells central for water and nutrient acquisition. Root hair growth is plastically modified by environmental cues. A frequent response to water limitation is active shortening of root hairs, involving largely unknown molecular mechanisms. A root hair-specific cis -regulatory element (RHE) integrates development...

The phytohormones gibberellins (GAs) play fundamental roles in almost every aspect of plant growth and development. Although there is good knowledge about GA biosynthetic and signaling pathways, factors contributing to the mechanisms homeostatically controlling GA levels remain largely unclear. Here, we demonstrate that homeobox transcription facto...

2020): Selective autophagy regulates heat stress memory in Arabidopsis by NBR1-mediated targeting of HSP90 and ROF1, Autophagy, 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 stres...

Although we have a good understanding of the development of shoot apical meristems (SAM) in higher plants, and the function of the stem cells (SCs) embedded in the SAM, there is surprisingly little known of its molecular responses to abiotic stresses. Here, we show that the SAM of Arabidopsis thaliana senses heat stress (HS) and retains an autonomo...

Proteogenic dipeptides are intermediates of proteolysis as well as an emerging class of small‐molecule regulators with diverse and often dipeptide‐specific functions. Herein, prompted by differential accumulation of dipeptides in a high‐density Arabidopsis thaliana time‐course stress experiment, we decided to pursue an identity of the proteolytic p...

Proteogenic dipeptides are intermediates of proteolysis as well as an emerging class of small-molecule regulators with diverse and often dipeptide-specific functions. Herein, prompted by differential accumulation of dipeptides in a high-density Arabidopsis thaliana time-course stress experiment, we decided to pursue an identity of the proteolytic p...

Calcium-regulated protein kinases are key components of are key components of intracellular signaling in plants that mediate rapid stress-induced responses to changes in the environment. To identify in vivo phosphorylation substrates of CALCIUM-DEPENDENT PROTEIN KINASE1 (CPK1), we analyzed the conditional expression of constitutively active CPK1 in...

Oxidative stress can lead to plant growth retardation, yield loss, and death. The atr7 mutant of Arabidopsis thaliana exhibits pronounced tolerance to oxidative stress. Using positional cloning, confirmed by knockout and RNA interference (RNAi) lines, we identified the atr7 mutation and revealed that ATR7 is a previously uncharacterized gene with o...

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 salini...

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)...

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.

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 NAC involved in fruit ripening is NON-RIPENING (NOR) and the non-ripening (nor) mu...

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 molecula...

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 exp...

Analysis of GRF9 promoter-driven reporter activity in ProGRF9:GUS lines. (A)–(D) Histochemical GUS staining of GRF9 expression pattern in leaves of 4-, 6-, 8-, and 12-day-old seedlings, respectively. (E) and (F) Leaves of 3-week-old plants. Note the expression of GRF9 in the cell proliferation zone of very young leaves (B, C) and the vascular tissu...

Rosette growth of GRF9 transgenic lines under different light regimes. Rosette phenotype of grf9-2 and GRF9ox1 in comparison to WT plants in (A) short day (8 h light / 16 h dark) and (B) equal day (12 h light / 12 h dark) conditions, determined using a LemnaTec phenotyping platform [67]. Note the more pronounced phenotype of the grf9 mutant in shor...

RNA in situ hybridization using the CYCLIN B1;1 (CYCB1;1) probe. In situ hybridization was done on longitudinal sections of the shoot apical meristem with leaf primordia of WT and grf9-2 plants (Scale bar 100 μm). (PDF)

List of primers used in this study. (XLS)

Expression of GRF9 determined by qRT-PCR. (A) GRF9 expression in different tissues of 40-day-old WT plants. (B) GRF9 expression in 2-week-old WT seedlings treated with different concentrations of auxin (in the form of 2,4-D) or cytokinin (in the form of zeatin). (C) Histochemical GUS staining of GRF9 expression pattern in young Arabidopsis Col-0 se...

Base substitution analysis of the GRF9 binding site. The experiment was performed to define the DNA-binding sequence specificity of GRF9 by base substitution mutagenesis. Biotin-labelled double-stranded oligonucleotides were used. Bases that were substituted are shown in bold and as lower-case letters. The values for GRF9 binding activity are shown...

Genotyping and expression analysis in GRF9- and ORG3-modified lines. Genotyping of (A) org3-1 (SALK_025676) and (B) org3-2 (SAIL_737_H11) mutants. (a) Right gene-specific primer and T-DNA left boarder primer, and (b) left and right gene-specific primers for genotyping (designed by http://signal.salk.edu/tdnaprimers.2.html). M, DNA size marker. Prim...

Petal phenotype of the org3-1 mutant. (A) Mature petals of WT and org3-1 plants. (B) Petal size and (C) petal cell area. Data represent means ± SD from at least 32 petals (i.e., 4 petals from at least 8 plants). The asterisk indicates a significant difference from WT (Student's t-test; p < 0.05). Bar = 0.5 mm. (PDF)

Genes affected in GRF9-IOE lines after EST induction and comparison with other GRF9-modified plants. (XLSX)

Data corresponding to Figures and Supplemental Figures. (XLSX)

GRF9-responsive genes in GRF9-IOE seedlings compared to differentially expressed genes in other publically available AtGRF transcriptomes. (XLSX)

Genotyping of grf9-1 and grf9-2 mutants. (A) grf9-1 (SALK_140746c) and (B) grf9-2 (SAIL_324_G07). (a) Right gene-specific primer and T-DNA left border primer, and (b) left and right gene-specific primers for genotyping (designed by http://signal.salk.edu/tdnaprimers.2.html). M, DNA size marker. Primer sequences are given in S3 Table. (PDF)

Petal phenotype of grf9 and GRF9ox plants. (A) Mature flowers and petals of WT, grf9-1, grf9-2 and GRF9ox1 plants. (B) Petal size and (C) petal cell area. Data represent means ± SD from at least 32 petals (i.e., 4 petals from at least 8 plants). Asterisks indicate a significant difference from the WT (Student's t-test; p < 0.05). Scale bars = 1 mm...

Expression of 23 GRF9 early responding genes in different GRF9-modified lines. Gene expression as determined by Affymetrix ATH1 microarray hybridizations (first two columns) or qRT-PCR (other columns). RNA for expression analysis was obtained from 2-week-old GRF9-IOE seedlings grown on MS medium and induced with 10 μM estradiol for the indicated ti...

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 descri...

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 met...

Table S1 Oligonucleotide sequences.

Figure S1 Amino acid sequence alignment of SlJUB1 with other known NAC transcription factors. Figure S2 Phenotypes of AtJUB1 expressing (OX3) and wild‐type tomato cv. Moneymaker (MM) plants under drought stress. Figure S3 Lower ROS scavenging enzyme activities in tomato plants ectopically expressing AtJUB1 (OX1). Figure S4 Ectopic expression of...

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...

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 ) RD 26 as an impo...

Orthogonal systems for heterologous protein expression as well as for the engineering of synthetic gene regulatory circuits in hosts like Saccharomyces cerevisiae depend on synthetic transcription factors (synTFs) and corresponding cis-regulatory binding sites. We have constructed and characterized a set of synTFs based on either transcription acti...

GenBank sequences for plasmids generated in this work.

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 transcr...

Senescence is the process that marks the end of leaves lifespan. As it progresses, the massive macromolecular catabolism dismantles the chloroplasts and, consequently, decreases the photosynthetic capacity of these organs. Thus, senescence manipulation is a strategy to improve plant yield by extending the leaf photosynthetically active window of ti...

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 reprog...

Since its discovery over two decades ago as an important cell death regulator in Arabidopsis thaliana, the role of LESION SIMULATING DISEASE 1 (LSD1) has been studied intensively within both biotic and abiotic stress responses as well as with respect to plant fitness regulation. However, its molecular mode of action remains enigmatic. Here we demon...

Control of gene expression by transcription factors (TFs) is central in many synthetic biology projects where tailored expression of one or multiple genes is often needed. As TFs from evolutionary distant organisms are unlikely to affect gene expression in a host of choice, they represent excellent candidates for establishing orthogonal control sys...

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 posi...

AtJUB1 transcript in transgenic tomato plants. (A) Presence of full-length AtJUB1 transcript (arrow) in leaves of transgenic plants OX1, OX2 and OX3, confirmed by PCR using primers specific for AtJUB1. (B) Presence of AtJUB1 transcript in fruits and leaves of AtJUB1-OX (= OX2) tomato plants (arrow). Samples were taken from fruits of different devel...

List of primers.

Expression of GA- and BR-associated genes.