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in Agriculture
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Publications

2020
Steiner, E. ; Israeli, A. ; Gupta, R. ; Shwartz, I. ; Nir, I. ; Leibman-Markus, M. ; Tal, L. ; Farber, M. ; Amsalem, Z. ; Ori, N. ; et al. Characterization of the cytokinin sensor TCSv2 in arabidopsis and tomato. 2020, 16, 152. Publisher's VersionAbstract
Hormones are crucial to plant life and development. Being able to follow the plants hormonal response to various stimuli and throughout developmental processes is an important and increasingly widespread tool. The phytohormone cytokinin (CK) has crucial roles in the regulation of plant growth and development.
Israeli, A. ; Ben-Herzel, O. ; Burko, Y. ; Shwartz, I. ; Ben-Gera, H. ; Harpaz-Saad, S. ; Bar, M. ; Efroni, I. ; Ori, N. Coordination of differentiation rate and local patterning in compound-leaf development. New Phytologist 2020, n/a. Publisher's VersionAbstract
Summary The variability in leaf form in nature is immense. Leaf patterning occurs by differential growth, taking place during a limited window of morphogenetic activity at the leaf marginal meristem. While many regulators have been implicated in the designation of the morphogenetic window and in leaf patterning, how these effectors interact to generate a particular form is still not well understood. We investigated the interaction among different effectors of tomato (Solanum lycopersicum) compound-leaf development, using genetic and molecular analyses. Mutations in the tomato auxin response factor SlARF5/SlMP, which normally promotes leaflet formation, suppressed the increased leaf complexity of mutants with extended morphogenetic window. Impaired activity of the NAC/CUC transcription factor GOBLET (GOB), which specifies leaflet boundaries, also reduced leaf complexity in these backgrounds. Analysis of genetic interactions showed that the patterning factors SlMP, GOB and the MYB transcription factor LYRATE (LYR) coordinately regulate leaf patterning by modulating in parallel different aspects of leaflet formation and shaping, This work places an array of developmental regulators in a morphogenetic context. It reveals how organ-level differentiation rate and local growth are coordinated to sculpture an organ. These concepts are applicable to the coordination of pattering and differentiation in other species and developmental processes.
Israeli, A. ; Reed, J. W. ; Ori, N. Genetic dissection of the auxin response network. Nature Plant 2020. Publisher's VersionAbstract
The expansion of gene families during evolution, which can generate functional overlap or specialization among their members, is a characteristic feature of signalling pathways in complex organisms. For example, families of transcriptional activators and repressors mediate responses to the plant hormone auxin. Although these regulators were identified more than 20 years ago, their overlapping functions and compensating negative feedbacks have hampered their functional analyses. Studies using loss-of-function approaches in basal land plants and gain-of-function approaches in angiosperms have in part overcome these issues but have still left an incomplete understanding. Here, we propose that renewed emphasis on genetic analysis of multiple mutants and species will shed light on the role of gene families in auxin response. Combining loss-of-function mutations in auxin-response activators and repressors can unravel complex outputs enabled by expanded gene families, such as fine-tuned developmental outcomes and robustness. Similar approaches and concepts may help to analyse other regulatory pathways whose components are also encoded by large gene families.
2019
Israeli, A. ; Capua, Y. ; Shwartz, I. ; Tal, L. ; Meir, Z. ; Levy, M. ; Bar, M. ; Efroni, I. ; Ori, N. Multiple Auxin-Response Regulators Enable Stability and Variability in Leaf Development. Curr Biol 2019.Abstract
Auxin-signal transduction is mediated by the antagonistic activity of transcriptional activators and repressors. Both activators and repressors belong to gene families, but the biological importance of this complexity is not clear. Here, we addressed this question using tomato leaf development as a model by generating and analyzing mutants in multiple auxin-response components. In developing compound tomato leaves, auxin promotes leaflet formation and blade growth, and in the intercalary regions between leaflets, auxin response is inhibited by the Aux/IAA protein ENTIRE (E). e mutants form simple leaves due to ectopic blade growth in the intercalary domain. Using this unique loss-of-function phenotype and genome editing of auxin-response factor (ARF) genes, encoding auxin-response activators, we identified the contribution of specific ARFs to the e phenotype. Mutations in the related ARFs SlMP, SlARF19A, and SlARF19B, but not SlARF7, reduced the leaf blade and suppressed the e phenotype in a dosage-dependent manner that correlated with their relative expression, leading to a continuum of shapes. While single e and slmp mutants affected blade growth in an opposite manner, leaves of e slmp double mutants were similar to those of the wild type. However, the leaf shape of e slmp was more variable than that of the wild type, and it showed increased sensitivity to auxin. Our findings demonstrate that the existence of multiple auxin-response repressors and activators stabilizes the developmental output of auxin and that tuning their activity enables shape variability. The increased complexity of the auxin response therefore balances stability and flexibility in leaf patterning.
Ori, N. Dissecting the Biological Functions of ARF and Aux/IAA Genes. Plant Cell 2019.
2018
Hu, J. ; Israeli, A. ; Ori, N. ; Sun, T. - P. The Interaction between DELLA and ARF/IAA Mediates Crosstalk between Gibberellin and Auxin Signaling to Control Fruit Initiation in Tomato. Plant Cell 2018, 30, 1710-1728.Abstract
Fruit initiation following fertilization in angiosperms is strictly regulated by phytohormones. In tomato (), auxin and gibberellin (GA) play central roles in promoting fruit initiation. Without fertilization, elevated GA or auxin signaling can induce parthenocarpy (seedless fruit production). The GA-signaling repressor SlDELLA and auxin-signaling components SlIAA9 and SlARF7 repress parthenocarpy, but the underlying mechanism is unknown. Here, we show that SlDELLA and the SlARF7/SlIAA9 complex mediate crosstalk between GA and auxin pathways to regulate fruit initiation. Yeast-two-hybrid and coimmunoprecipitation assays showed that SlARF7 and additional activator SlARFs interact with SlDELLA and SlIAA9 through distinct domains. SlARF7/SlIAA9 and SlDELLA antagonistically modulate the expression of feedback-regulated genes involved in GA and auxin metabolism, whereas SlARF7/SlIAA9 and SlDELLA coregulate the expression of fruit growth-related genes. Analysis of (), (with downregulated expression of multiple activator ), and () single and double mutants indicated that these genes additively affect parthenocarpy, supporting the notion that the SlARFs/SlIAA9 and SlDELLA interaction plays an important role in regulating fruit initiation. Analysis of the GA-deficient mutant showed that active GA biosynthesis and signaling are required for auxin-induced fruit initiation. Our study reveals how direct crosstalk between auxin- and GA-signaling components is critical for tomato fruit initiation.
Roth, O. ; Alvarez, J. P. ; Levy, M. ; Bowman, J. L. ; Ori, N. ; Shani, E. The KNOXI Transcription Factor SHOOT MERISTEMLESS Regulates Floral Fate in Arabidopsis. Plant Cell 2018, 30, 1309-1321.Abstract
Plants have evolved a unique and conserved developmental program that enables the conversion of leaves into floral organs. Elegant genetic and molecular work has identified key regulators of flower meristem identity. However, further understanding of flower meristem specification has been hampered by redundancy and by pleiotropic effects. The KNOXI transcription factor SHOOT MERISTEMLESS (STM) is a well-characterized regulator of shoot apical meristem maintenance. loss-of-function mutants arrest shortly after germination; therefore, the knowledge on later roles of STM in later processes, including flower development, is limited. Here, we uncover a role for STM in the specification of flower meristem identity. Silencing in the () expression domain in the mutant background resulted in a leafy-flower phenotype, and an intermediate allele enhanced the flower meristem identity phenotype of Transcriptional profiling of perturbation suggested that STM activity affects multiple floral fate genes, among them the F-box protein-encoding gene (). In agreement with this notion, enhanced the floral fate phenotype, and ectopic expression rescued the leafy flowers in genetic backgrounds with compromised and activities. This work suggests a genetic mechanism that underlies the activity of in the specification of flower meristem identity.
2017
Salam, B. B. ; Malka, S. K. ; Zhu, X. ; Gong, H. ; Ziv, C. ; Teper-Bamnolker, P. ; Ori, N. ; Jiang, J. ; Eshel, D. Etiolated Stem Branching Is a Result of Systemic Signaling Associated with Sucrose Level. Plant Physiology 2017, 175, 734–745. Publisher's VersionAbstract
The potato (Solanum tuberosum) tuber is a swollen stem. Sprouts growing from the tuber nodes represent loss of apical dominance and branching. Long cold storage induces loss of tuber apical dominance and results in secondary branching. Here, we show that a similar branching pattern can be induced by short heat treatment of the tubers. Detached sprouts were induced to branch by the heat treatment only when attached to a parenchyma cylinder. Grafting experiments showed that the scion branches only when grafted onto heat- or cold-treated tuber parenchyma, suggesting that the branching signal is transmitted systemically from the bud-base parenchyma to the grafted stem. Exogenous supply of sucrose (Suc), glucose, or fructose solution to detached sprouts induced branching in a dose-responsive manner, and an increase in Suc level was observed in tuber parenchyma upon branching induction, suggesting a role for elevated parenchyma sugars in the regulation of branching. However, sugar analysis of the apex and node after grafting showed no distinct differences in sugar levels between branching and nonbranching stems. Vacuolar invertase is a key enzyme in determining the level of Suc and its cleavage products, glucose and fructose, in potato parenchyma. Silencing of the vacuolar invertase-encoding gene led to increased tuber branching in combination with branching-inducing treatments. These results suggest that Suc in the parenchyma induces branching through signaling and not by excess mobilization from the parenchyma to the stem.GlossaryADapical dominanceCFDAcarboxyfluorescein diacetateRBK‘Russet Burbank’Tre6Ptrehalose 6-phosphateCFcarboxyfluorescein
Goldental-Cohen, S. ; Israeli, A. ; Ori, N. ; Yasuor, H. Auxin Response Dynamics During Wild-Type and entire Flower Development in Tomato. Plant and Cell Physiology 2017, 58, 1661-1672. Publisher's VersionAbstract
The plant hormone auxin is a major regulator of plant development and response to environmental cues. Auxin plays a particularly central role in flower development, but the knowledge of its role of flower development in crop plants with fleshy fruits, such as tomato, is still scarce. Mutations in the Aux/IAA gene ENTIRE/Indole Acetic Acid 9 (E/IAA9) lead to the precocious development of young gynoecia into parthenocarpic fruits. Here, we compared the distribution of the auxin response sensor DR5::VENUS and the auxin efflux transporter PIN1 between the wild type and entire during successive stages of flower and fruit development. Up-regulation of the DR5::VENUS signal in the shoot apical meristem (SAM) was observed upon the transition to flowering, implicating a possible role for auxin in the transition from a vegetative SAM into an inflorescence meristem. DR5::VENUS was expressed in all initiating floral organs. Additionally, DR5::VENUS was highly expressed during gametogenesis, in both male and female organs, and in the developing seeds during embryogenesis. DR5::VENUS is expressed in functional cell layers such as the anther stomium and tapetum, suggesting that auxin plays a role in flower organ development and function. The entire mutation affected DR5::VENUS expression patterns during inflorescence formation and flower organ development, which correlated with phenotypic alterations. We also show dynamic distribution and localization of the auxin transporter PIN1 during flower and fruit organ development. These results emphasize the dynamic auxin response in inflorescence and flower development and suggest multiple roles of auxin in these processes.
2016
Bar, M. ; Israeli, A. ; Levy, M. ; Gera, H. B. ; Jiménez-Gómez, J. M. ; Kouril, S. ; Tarkowski, P. ; Ori, N. CLAUSA is a MYB transcription factor that promotes leaf differentiation by attenuating cytokinin signaling. Plant Cell 2016, 28, 1602 - 1615. Publisher's Version
Shwartz, I. ; Levy, M. ; Ori, N. ; Bar, M. Hormones in tomato leaf development. Dev Biol 2016, 419, 132-142.Abstract
Leaf development serves as a model for plant developmental flexibility. Flexible balancing of morphogenesis and differentiation during leaf development results in a large diversity of leaf forms, both between different species and within the same species. This diversity is particularly evident in compound leaves. Hormones are prominent regulators of leaf development. Here we discuss some of the roles of plant hormones and the cross-talk between different hormones in tomato compound-leaf development.
Ben-Gera, H. ; Dafna, A. ; Alvarez, J. P. ; Bar, M. ; Mauerer, M. ; Ori, N. Auxin-mediated lamina growth in tomato leaves is restricted by two parallel mechanisms. Plant J 2016, 86, 443-57.Abstract
In the development of tomato compound leaves, local auxin maxima points, separated by the expression of the Aux/IAA protein SlIAA9/ENTIRE (E), direct the formation of discrete leaflets along the leaf margin. The local auxin maxima promote leaflet initiation, while E acts between leaflets to inhibit auxin response and lamina growth, enabling leaflet separation. Here, we show that a group of auxin response factors (ARFs), which are targeted by miR160, antagonizes auxin response and lamina growth in conjunction with E. In wild-type leaf primordia, the miR160-targeted ARFs SlARF10A and SlARF17 are expressed in leaflets, and SlmiR160 is expressed in provascular tissues. Leaf overexpression of the miR160-targeted ARFs SlARF10A, SlARF10B or SlARF17, led to reduced lamina and increased leaf complexity, and suppressed auxin response in young leaves. In agreement, leaf overexpression of miR160 resulted in simplified leaves due to ectopic lamina growth between leaflets, reminiscent of e leaves. Genetic interactions suggest that E and miR160-targeted ARFs act partially redundantly but are both required for local inhibition of lamina growth between initiating leaflets. These results show that different types of auxin signal antagonists act cooperatively to ensure leaflet separation in tomato leaf margins.
2015
Bar, M. ; Ben-Herzel, O. ; Kohay, H. ; Shtein, I. ; Ori, N. CLAUSA restricts tomato leaf morphogenesis and GOBLET expression. Plant J 2015, 83, 888-902.Abstract
Leaf morphogenesis and differentiation are highly flexible processes. The development of compound leaves is characterized by an extended morphogenesis stage compared with that of simple leaves. The tomato mutant clausa (clau) possesses extremely elaborate compound leaves. Here we show that this elaboration is generated by further extension of the morphogenetic window, partly via the activity of ectopic meristems present on clau leaves. Further, we propose that CLAU might negatively affect expression of the NAM/CUC gene GOBLET (GOB), an important modulator of compound-leaf development, as GOB expression is elevated in clau mutants and reducing GOB expression suppresses the clau phenotype. Expression of GOB is also elevated in the compound leaf mutant lyrate (lyr), and the remarkable enhancement of the clau phenotype by lyr suggests that clau and lyr affect leaf development and GOB in different pathways.