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in Agriculture
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Publications

2020
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.
Matosevich, R. ; Cohen, I. ; Gil-Yarom, N. ; Modrego, A. ; Friedlander-Shani, L. ; Verna, C. ; Scarpella, E. ; Efroni, I. Local auxin biosynthesis is required for root regeneration after wounding. Nature Plant 2020, 6 1020 - 1030. Publisher's VersionAbstract
The root meristem can regenerate following removal of its stem-cell niche by recruitment of remnant cells from the stump. Regeneration is initiated by rapid accumulation of auxin near the injury site but the source of this auxin is unknown. Here, we show that auxin accumulation arises from the activity of multiple auxin biosynthetic sources that are newly specified near the cut site and that their continuous activity is required for the regeneration process. Auxin synthesis is highly localized while PIN-mediated transport is dispensable for auxin accumulation and tip regeneration. Roots lacking the activity of the regeneration competence factor ERF115, or that are dissected at a zone of low regeneration potential, fail to activate local auxin sources. Remarkably, restoring auxin supply is sufficient to confer regeneration capacity to these recalcitrant tissues. We suggest that regeneration competence relies on the ability to specify new local auxin sources in a precise temporal pattern.
Radhakrishnan, D. ; Shanmukhan, A. P. ; Kareem, A. ; Aiyaz, M. ; Varapparambathu, V. ; Toms, A. ; Kerstens, M. ; Valsakumar, D. ; Landge, A. N. ; Shaji, A. ; et al. A coherent feed forward loop drives vascular regeneration in damaged aerial organs growing in normal developmental-context. Development 2020.Abstract
Aerial organs of plants being highly prone to local injuries, require tissue restoration to ensure their survival. However, knowledge of the underlying mechanism is sparse. In this study, we mimicked natural injuries in growing leaf and stem to study the reunion between mechanically disconnected tissues. We show that ()/ () genes, which encodes stem cell promoting factors, are activated and contribute to vascular regeneration in response to these injuries. PLT proteins bind to and activate the CUC2 promoter. Both PLT and CUC2 regulate the transcription of the local auxin biosynthesis gene YUC4 in a coherent feed forward loop, and this process is necessary to drive vascular regeneration. In the absence of this PLT mediated regeneration response, leaf ground tissue cells can neither acquire early vascular identity marker ATHB8, nor properly polarize auxin transporters to specify new venation paths. The PLT-CUC2 module is required for vascular regeneration, but is dispensable for midvein formation in leaf. We reveal the mechanisms of vascular regeneration in plants and distinguishes the wound repair ability of the tissue from its formation during normal development.
2019
Mello, A. ; Efroni, I. ; Rahni, R. ; Birnbaum, K. D. The Selaginella rhizophore has a unique transcriptional identity compared with root and shoot meristems. New Phytologist 2019, 222, 882-894. Publisher's VersionAbstract
The genus Selaginella resides in an early branch of the land plant lineage that possesses a vasculature and roots. The majority of the Selaginella root system is shoot borne and emerges through a distinctive structure known as the rhizophore, the organ identity of which has been a long-debated question. The rhizophore of Selaginella moellendorffii – a model for the lycophytes – shows plasticity to develop into a root or shoot up until 8 d after angle meristem emergence, after which it is committed to root fate. We subsequently use morphology and plasticity to define the stage of rhizophore identity. Transcriptomic analysis of the rhizophore during its plastic stage reveals that, despite some resemblance to the root meristem, rhizophore gene expression patterns are largely distinct from both shoot and root meristems. Based on this transcriptomic analysis and on historical anatomical work, we conclude that the rhizophore is a distinct organ with unique features. © 2019, Blackwell Publishing Ltd. All rights reserved.
Lieberman-Lazarovich, M. ; Yahav, C. ; Israeli, A. ; Efroni, I. Deep conservation of cis-element variants regulating plant hormonal responses. The Plant Cell 2019. Publisher's VersionAbstract
Phytohormones regulate many aspects of plant life by activating transcription factors (TF) that bind sequence-specific response elements (RE) in regulatory regions of target genes. Despite their short length, REs are degenerate with a core of just 3-4bp. This degeneracy is paradoxical, as it reduces specificity and REs are extremely common in the genome. To study whether RE degeneracy might serve a biological function we developed an algorithm for the detection of regulatory sequence conservation and applied it to phytohormones REs in 45 angiosperms. Surprisingly, we found that specific RE variants are highly conserved in core hormone response genes. Experimental evidence showed that specific variants act to regulate the magnitude and spatial profile of hormonal response in Arabidopsis and tomato. Our results suggest that hormone-regulated TFs bind a spectrum of REs, each coding for a distinct transcriptional response profile. Our approach has implications for precise genome editing and for rational promoter design.
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.
2018
Mello, A. ; Efroni, I. ; Rahni, R. ; Birnbaum, K. D. New Phytol 2018.Abstract
The genus Selaginella resides in an early branch of the land plant lineage that possesses a vasculature and roots. The majority of the Selaginella root system is shoot borne and emerges through a distinctive structure known as the rhizophore, the organ identity of which has been a long-debated question. The rhizophore of Selaginella moellendorffii - a model for the lycophytes - shows plasticity to develop into a root or shoot up until 8 d after angle meristem emergence, after which it is committed to root fate. We subsequently use morphology and plasticity to define the stage of rhizophore identity. Transcriptomic analysis of the rhizophore during its plastic stage reveals that, despite some resemblance to the root meristem, rhizophore gene expression patterns are largely distinct from both shoot and root meristems. Based on this transcriptomic analysis and on historical anatomical work, we conclude that the rhizophore is a distinct organ with unique features.
Efroni, I. ; Prasad, K. Insights into the art of recreation. Dev Biol 2018, 442, 1-2.
Efroni, I. A Conceptual Framework for Cell Identity Transitions in Plants. Plant Cell Physiol 2018, 59, 691-701.Abstract
Multicellular organisms develop from a single cell that proliferates to form different cell types with specialized functions. Sixty years ago, Waddington suggested the 'epigenetic landscape' as a useful metaphor for the process. According to this view, cells move through a rugged identity space along genetically encoded trajectories, until arriving at one of the possible final fates. In plants in particular, these trajectories have strong spatial correlates, as cell identity is intimately linked to its relative position within the plant. During regeneration, however, positional signals are severely disrupted and differentiated cells are able to undergo rapid non-canonical identity changes. Moreover, while pluripotent properties have long been ascribed to plant cells, the introduction of induced pluripotent stem cells in animal studies suggests such plasticity may not be unique to plants. As a result, current concepts of differentiation as a gradual and hierarchical process are being reformulated across biological fields. Traditional studies of plant regeneration have placed strong emphasis on the emergence of patterns and tissue organization, and information regarding the events occurring at the level of individual cells is only now beginning to emerge. Here, I review the historical and current concepts of cell identity and identity transitions, and discuss how new views and tools may instruct the future understanding of differentiation and plant regeneration.
2016
Efroni, I. ; Birnbaum, K. D. The potential of single-cell profiling in plants. 2016, 17, 65. Publisher's VersionAbstract
Single-cell transcriptomics has been employed in a growing number of animal studies, but the technique has yet to be widely used in plants. Nonetheless, early studies indicate that single-cell RNA-seq protocols developed for animal cells produce informative datasets in plants. We argue that single-cell transcriptomics has the potential to provide a new perspective on plant problems, such as the nature of the stem cells or initials, the plasticity of plant cells, and the extent of localized cellular responses to environmental inputs. Single-cell experimental outputs require different analytical approaches compared with pooled cell profiles and new tools tailored to single-cell assays are being developed. Here, we highlight promising new single-cell profiling approaches, their limitations as applied to plants, and their potential to address fundamental questions in plant biology.
Efroni, I. ; Mello, A. ; Nawy, T. ; Ip, P. - L. ; Rahni, R. ; DelRose, N. ; Powers, A. ; Satija, R. ; Birnbaum, K. D. Root Regeneration Triggers an Embryo-like Sequence Guided by Hormonal Interactions. 2016, 165, 1721 - 1733. Publisher's VersionAbstract
SummaryPlant roots can regenerate after excision of their tip, including the stem cell niche. To determine which developmental program mediates such repair, we applied a combination of lineage tracing, single-cell RNA sequencing, and marker analysis to test different models of tissue reassembly. We show that multiple cell types can reconstitute stem cells, demonstrating the latent potential of untreated plant cells. The transcriptome of regenerating cells prior to stem cell activation resembles that of an embryonic root progenitor. Regeneration defects are more severe in embryonic than in adult root mutants. Furthermore, the signaling domains of the hormones auxin and cytokinin mirror their embryonic dynamics and manipulation of both hormones alters the position of new tissues and stem cell niche markers. Our findings suggest that plant root regeneration follows, on a larger scale, the developmental stages of embryonic patterning and is guided by spatial information provided by complementary hormone domains.
Rahni, R. ; Efroni, I. ; Birnbaum, K.  D. A Case for Distributed Control of Local Stem Cell Behavior in Plants. 2016, 38, 635 - 642. Publisher's VersionAbstract
The root meristem has a centrally located group of mitotically quiescent cells, to which current models assign a stem cell organizer function. However, evidence is emerging for decentralized control of stem cell activity, whereby self-renewing behavior emerges from the lack of cell displacement at the border of opposing differentiation gradients. We term this a “stagnation” model due to its reliance on passive mechanics. The position of stem cells is established by two opposing axes that reciprocally control each other's differentiation. Such broad tissue organization programs would allow plants, like some animal systems, to rapidly reconstitute stem cells from non-stem-cell tissues.
Alvarez, J. P. ; Furumizu, C. ; Efroni, I. ; Eshed, Y. ; Bowman, J. L. Active suppression of a leaf meristem orchestrates determinate leaf growth. eLife 2016, 5 e15023. Publisher's VersionAbstract
Leaves are flat determinate organs derived from indeterminate shoot apical meristems. The presence of a specific leaf meristem is debated, as anatomical features typical of meristems are not present in leaves. Here we demonstrate that multiple NGATHA (NGA) and CINCINNATA-class-TCP (CIN-TCP) transcription factors act redundantly, shortly after leaf initiation, to gradually restrict the activity of a leaf meristem in Arabidopsis thaliana to marginal and basal domains, and that their absence confers persistent marginal growth to leaves, cotyledons and floral organs. Following primordia initiation, the restriction of the broadly acting leaf meristem to the margins is mediated by the juxtaposition of adaxial and abaxial domains and maintained by WOX homeobox transcription factors, whereas other marginal elaboration genes are dispensable for its maintenance. This genetic framework parallels the morphogenetic program of shoot apical meristems and may represent a relic of an ancestral shoot system from which seed plant leaves evolved.