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The Robert H. Smith Institute of
Plant Sciences and Genetics
in Agriculture
POB 12, Rehovot 76100, Israel

Administrator: Neomi Maimon 
Tel: 972-8-948-9251,
Fax: 972-8-948-9899,

Director: Prof. David Weiss
Tel: 972-8-948-9436
Fax: 972-8-948-9899



Ramon, U. ; Weiss, D. ; Illouz-Eliaz, N. Underground gibberellin activity: differential gibberellin response in tomato shoots and roots. New PhytologistNew PhytologistNew Phytol 2021, 229, 1196 - 1200. Publisher's Version
Steiner, E. ; Triana, M. R. ; Kubasi, S. ; Blum, S. ; Paz-Ares, J. ; Rubio, V. ; Weiss, D. KISS ME DEADLY F-box proteins modulate cytokinin responses by targeting the transcription factor TCP14 for degradation. Plant Physiol 2021. Publisher's Version
Illouz-Eliaz, N. ; Nissan, I. ; Nir, I. ; Ramon, U. ; Shohat, H. ; Weiss, D. Mutations in the tomato gibberellin receptors suppress xylem proliferation and reduce water loss under water-deficit conditions. J Exp Bot 2020, 71, 3603 - 3612. Publisher's VersionAbstract
Low gibberellin (GA) activity in tomato (Solanum lycopersicum) inhibits leaf expansion and reduces stomatal conductance. This leads to lower transpiration and improved water status under transient drought conditions. Tomato has three GIBBERELLIN-INSENSITIVE DWARF1 (GID1) GA receptors with overlapping activities and high redundancy. We tested whether mutation in a single GID1 reduces transpiration without affecting growth and productivity. CRISPR-Cas9 gid1 mutants were able to maintain higher leaf water content under water-deficit conditions. Moreover, while gid1a exhibited normal growth, it showed reduced whole-plant transpiration and better recovery from dehydration. Mutation in GID1a inhibited xylem vessel proliferation, which led to lower hydraulic conductance. In stronger GA mutants, we also found reduced xylem vessel expansion. These results suggest that low GA activity affects transpiration by multiple mechanisms: it reduces leaf area, promotes stomatal closure, and reduces xylem proliferation and expansion, and as a result, xylem hydraulic conductance. We further examined if gid1a performs better than the control M82 in the field. Under these conditions, the high redundancy of GID1s was lost and gid1a plants were semi-dwarf, but their productivity was not affected. Although gid1a did not perform better under drought conditions in the field, it exhibited a higher harvest index.
Shohat, H. ; Illouz-Eliaz, N. ; Kanno, Y. ; Seo, M. ; Weiss, D. The Tomato DELLA Protein PROCERA Promotes Abscisic Acid Responses in Guard Cells by Upregulating an Abscisic Acid Transporter. Plant Physiology 2020, 184, 518. Publisher's VersionAbstract
Plants reduce transpiration through stomatal closure to avoid drought stress. While abscisic acid (ABA) has a central role in the regulation of stomatal closure under water-deficit conditions, we demonstrated in tomato (Solanum lycopersicum) that a gibberellin response inhibitor, the DELLA protein PROCERA (PRO), promotes ABA-induced stomatal closure and gene transcription in guard cells. To study how PRO affects stomatal closure, we performed RNA-sequencing analysis of isolated guard cells and identified the ABA transporters ABA-IMPORTING TRANSPORTER1.1 (AIT1.1) and AIT1.2, also called NITRATE TRANSPORTER1/PTR TRANSPORTER FAMILY4.6 in Arabidopsis (Arabidopsis thaliana), as being upregulated by PRO. Tomato has four AIT1 genes, but only AIT1.1 and AIT1.2 were upregulated by PRO, and only AIT1.1 exhibited high expression in guard cells. Functional analysis of AIT1.1 in yeast (Saccharomyces cerevisiae) confirmed its activity as an ABA transporter, possibly an importer. A clustered regularly interspaced short palindromic repeats-Cas9–derived ait1.1 mutant exhibited an increased transpiration, a larger stomatal aperture, and a reduced stomatal response to ABA. Moreover, ait1.1 suppressed the promoting effects of PRO on ABA-induced stomatal closure and gene expression in guard cells, suggesting that the effects of PRO on stomatal aperture and transpiration are AIT1.1-dependent. Previous studies suggest a negative crosstalk between gibberellin and ABA that is mediated by changes in hormone biosynthesis and signaling. The results of this study suggest this crosstalk is also mediated by changes in hormone transport.
Ramon, U. ; Weiss, D. ; Illouz-Eliaz, N. Underground gibberellin activity: differential gibberellin response in tomato shoots and roots. New PhytologistNew PhytologistNew Phytol 2020, n/a. Publisher's VersionAbstract
Abstract Plant organ growth is governed and modified by developmental programs and environmental cues. In most cases, these changes are mediated by the activity of phytohormones (Bradford Verma et al., 2016). Gibberellins (GAs) are growth promoting hormones that regulate many developmental processes, including organ growth and elongation (Davière Ueguchi-Tanaka et al., 2007).
Zhu, Z. ; Kang, X. ; Lor, V. S. ; Weiss, D. ; Olszewski, N. Characterization of a semidominant dwarfing PROCERA allele identified in a screen for CRISPR/Cas9-induced suppressors of loss-of-function alleles. Plant Biotechnol J 2019, 17, 319-321.
Illouz-Eliaz, N. ; Ramon, U. ; Shohat, H. ; Blum, S. ; Livne, S. ; Mendelson, D. ; Weiss, D. Multiple gibberellin receptors contribute to phenotypic stability under changing environments. Plant Cell 2019, 31, 1506–1519. Publisher's VersionAbstract
The pleiotropic and complex gibberellin (GA) response relies on targeted proteolysis of DELLA proteins mediated by a GA-activated GIBBERELLIN-INSENSITIVE DWARF1 (GID1) receptor. The tomato (Solanum lycopersicum) genome encodes for a single DELLA protein, PROCERA (PRO), and three receptors, SlGID1a (GID1a), GID1b1 and GID1b2, that may guide specific GA responses. In this work, CRISPR-Cas9-derived gid1 mutants were generated and their effect on GA responses was studied. The gid1 triple mutant was extremely dwarf and fully insensitive to GA. Under optimal growth conditions, the three receptors function redundantly and the single gid1 mutants exhibited very mild phenotypic changes. Among the three receptors, GID1a had the strongest effects on germination and growth. Yeast two-hybrid assays suggested that GID1a has the highest affinity to PRO. Analysis of lines with a single active receptor demonstrated a unique role for GID1a in protracted response to GA that was saturated only at high doses. When the gid1 mutants were grown in the field under ambient changing environments, they showed phenotypic instability, the high redundancy was lost and gid1a exhibited dwarfism that was strongly exacerbated by the loss of another GID1b receptor gene. These results suggest that multiple GA receptors contribute to phenotypic stability under environmental extremes.
Nir, I. ; Shohat, H. ; Panizel, I. ; Olszewski, N. ; Aharoni, A. ; Weiss, D. The Tomato DELLA Protein PROCERA Acts in Guard Cells to Promote Stomatal Closure. Plant Cell 2017, 29, 3186-3197.Abstract
Plants employ stomatal closure and reduced growth to avoid water deficiency damage. Reduced levels of the growth-promoting hormone gibberellin (GA) lead to increased tolerance to water deficit, but the underlying mechanism is unknown. Here, we show that the tomato () DELLA protein PROCERA (PRO), a negative regulator of GA signaling, acts in guard cells to promote stomatal closure and reduce water loss in response to water deficiency by increasing abscisic acid (ABA) sensitivity. The loss-of-function mutant exhibited increased stomatal conductance and rapid wilting under water deficit stress. Transgenic tomato overexpressing constitutively active stable DELLA proteins (S-) displayed the opposite phenotype. The effects of S- on stomatal aperture and water loss were strongly suppressed in the ABA-deficient mutant , indicating that these effects of S- are ABA dependent. While DELLA had no effect on ABA levels, guard cell ABA responsiveness was increased in S- and reduced in plants compared with the wild type. Expressing S- under the control of a guard-cell-specific promoter was sufficient to increase stomatal sensitivity to ABA and to reduce water loss under water deficit stress but had no effect on leaf size. This result indicates that DELLA promotes stomatal closure independently of its effect on growth.
Farber, M. ; Attia, Z. ; Weiss, D. Cytokinin activity increases stomatal density and transpiration rate in tomato. Journal of Experimental Botanyjxb 2016, 67, 6351 - 6362. Publisher's VersionAbstract
Previous studies on cytokinin (CK) and drought have suggested that the hormone has positive and negative effects on plant adaptation to restrictive conditions. This study examined the effect of CK on transpiration, stomatal activity, and response to drought in tomato (Solanum lycopersicum) plants. Transgenic tomato plants overexpressing the Arabidopsis thaliana CK-degrading enzyme CK oxidase/dehydrogenase 3 (CKX3) maintained higher leaf water status under drought conditions due to reduced whole-plant transpiration. The reduced transpiration could be attributed to smaller leaf area and reduced stomatal density. CKX3-overexpressing plants contained fewer and larger pavement cells and fewer stomata per leaf area than wild-type plants. In addition, wild-type leaves treated with CK exhibited enhanced transpiration and had more pavement cells and increased numbers of stomata per leaf area than untreated leaves. Manipulation of CK levels did not affect stomatal movement or abscisic acid-induced stomatal closure. Moreover, we found no correlation between stomatal aperture and the activity of the CK-induced promoter Two-Component Signaling Sensor (TCS) in guard cells. Previous studies have shown that drought reduces CK levels, and we propose this to be a mechanism of adaptation to water deficiency: the reduced CK levels suppress growth and reduce stomatal density, both of which reduce transpiration, thereby increasing tolerance to prolonged drought conditions.
Steiner, E. ; Livne, S. ; Kobinson-Katz, T. ; Tal, L. ; Pri-Tal, O. ; Mosquna, A. ; Tarkowská, D. ; Mueller, B. ; Tarkowski, P. ; Weiss, D. The Putative O-Linked N-Acetylglucosamine Transferase SPINDLY Inhibits Class I TCP Proteolysis to Promote Sensitivity to Cytokinin. Plant Physiol 2016, 171, 1485-94.Abstract
Arabidopsis (Arabidopsis thaliana) SPINDLY (SPY) is a putative serine and threonine O-linked N-acetylglucosamine transferase (OGT). While SPY has been shown to suppress gibberellin signaling and to promote cytokinin (CK) responses, its catalytic OGT activity was never demonstrated and its effect on protein fate is not known. We previously showed that SPY interacts physically and functionally with TCP14 and TCP15 to promote CK responses. Here, we aimed to identify how SPY regulates TCP14/15 activities and how these TCPs promote CK responses. We show that SPY activity is required for TCP14 stability. Mutation in the putative OGT domain of SPY (spy-3) stimulated TCP14 proteolysis by the 26S proteasome, which was reversed by mutation in CULLIN1 (CUL1), suggesting a role for SKP, CUL1, F-box E3 ubiquitin ligase in TCP14 proteolysis. TCP14 proteolysis in spy-3 suppressed all TCP14 misexpression phenotypes, including the enhanced CK responses. The increased CK activity in TCP14/15-overexpressing flowers resulted from increased sensitivity to the hormone and not from higher CK levels. TCP15 overexpression enhanced the response of the CK-induced synthetic promoter pTCS to CK, suggesting that TCP14/15 affect early steps in CK signaling. We propose that posttranslational modification of TCP14/15 by SPY inhibits their proteolysis and that the accumulated proteins promote the activity of the CK phosphorelay cascade in developing Arabidopsis leaves and flowers.
Manela, N. ; Oliva, M. ; Ovadia, R. ; Sikron-Persi, N. ; Ayenew, B. ; Fait, A. ; Galili, G. ; Perl, A. ; Weiss, D. ; Oren-Shamir, M. Phenylalanine and tyrosine levels are rate-limiting factors in production of health promoting metabolites in Vitis vinifera cv. Gamay Red cell suspension. Front Plant Sci 2015, 6 538.Abstract
Environmental stresses such as high light intensity and temperature cause induction of the shikimate pathway, aromatic amino acids (AAA) pathways, and of pathways downstream from AAAs. The induction leads to production of specialized metabolites that protect the cells from oxidative damage. The regulation of the diverse AAA derived pathways is still not well understood. To gain insight on that regulation, we increased AAA production in red grape Vitis vinifera cv. Gamay Red cell suspension, without inducing external stress on the cells, and characterized the metabolic effect of this induction. Increased AAA production was achieved by expressing a feedback-insensitive bacterial form of 3-deoxy- D-arabino-heptulosonate 7-phosphate synthase enzyme (AroG (*)) of the shikimate pathway under a constitutive promoter. The presence of AroG(*) protein led to elevated levels of primary metabolites in the shikimate and AAA pathways including phenylalanine and tyrosine, and to a dramatic increase in phenylpropanoids. The AroG (*) transformed lines accumulated up to 20 and 150 fold higher levels of resveratrol and dihydroquercetin, respectively. Quercetin, formed from dihydroquercetin, and resveratrol, are health promoting metabolites that are induced due to environmental stresses. Testing the expression level of key genes along the stilbenoids, benzenoids, and phenylpropanoid pathways showed that transcription was not affected by AroG (*). This suggests that concentrations of AAAs, and of phenylalanine in particular, are rate-limiting in production of these metabolites. In contrast, increased phenylalanine production did not lead to elevated concentrations of anthocyanins, even though they are also phenylpropanoid metabolites. This suggests a control mechanism of this pathway that is independent of AAA concentration. Interestingly, total anthocyanin concentrations were slightly lower in AroG(*) cells, and the relative frequencies of the different anthocyanins changed as well.
Livne, S. ; Lor, V. S. ; Nir, I. ; Eliaz, N. ; Aharoni, A. ; Olszewski, N. E. ; Eshed, Y. ; Weiss, D. Uncovering DELLA-Independent Gibberellin Responses by Characterizing New Tomato procera Mutants. Plant Cell 2015, 27, 1579-94.Abstract
Gibberellin (GA) regulates plant development primarily by triggering the degradation/deactivation of the DELLA proteins. However, it remains unclear whether all GA responses are regulated by DELLAs. Tomato (Solanum lycopersicum) has a single DELLA gene named PROCERA (PRO), and its recessive pro allele exhibits constitutive GA activity but retains responsiveness to external GA. In the loss-of-function mutant pro(ΔGRAS), all examined GA developmental responses were considerably enhanced relative to pro and a defect in seed desiccation tolerance was uncovered. As pro, but not pro(ΔGRAS), elongation was promoted by GA treatment, pro may retain residual DELLA activity. In agreement with homeostatic feedback regulation of the GA biosynthetic pathway, we found that GA20oxidase1 expression was suppressed in pro(ΔGRAS) and was not affected by exogenous GA3. In contrast, expression of GA2oxidase4 was not affected by the elevated GA signaling in pro(ΔGRAS) but was strongly induced by exogenous GA3. Since a similar response was found in Arabidopsis thaliana plants with impaired activity of all five DELLA genes, we suggest that homeostatic GA responses are regulated by both DELLA-dependent and -independent pathways. Transcriptome analysis of GA-treated pro(ΔGRAS) leaves suggests that 5% of all GA-regulated genes in tomato are DELLA independent.