Publications

The John Innes Centre Publications Repository contains details of all publications resulting from our researchers.

The repository also includes Open Access publications, which can be identified by the icons found on search results.

 Green open access publications are marked by the PDF icon. Click on the publication title, or the PDF icon, and read a pre-print PDF version of the publication.  Gold open access publications have the gold open padlock icon. You can read the full version of these papers on the publishing journal’s website without a subscription. 

The creation of this publications repository was funded by BBSRC.

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Bencivenga S., Serrano A., Bush M., Fox S., Sablowski R. (2016)

Control of oriented tissue growth through repression of organ boundary genes promotes stem morphogenesis

Developmental Cell (39) 198-208

Publisher's version: 10.1016/j.devcel.2016.08.013

ID: 55030

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Abstract

The origin of the stem is a major but poorly understood aspect of plant development, partlybecause the stem initiates in a relatively inaccessible region of the shoot apical meristem, calledthe rib zone (RZ). We developed quantitative 3D image analysis and clonal analysis tools, whichrevealed that the Arabidopsis homeodomain protein REPLUMLESS (RPL) establishes distinctpatterns of oriented cell division and growth in the central and peripheral regions of the RZ. Agenome-wide screen for target genes connected RPL directly to many of the key shootdevelopment pathways, including the development of organ boundaries; accordingly, mutationof the organ boundary gene LIGHT-SENSITIVE HYPOCOTYL 4 restored RZ function and stemgrowth in the rpl mutant. Our work opens the way to study a developmental process ofimportance to crop improvement and highlights how apparently simple changes in 3D organgrowth can reflect more complex internal changes in oriented cell activities.

Abstract

Plant tissue growth requires the interdependent cellular processes of cytoplasmic growth, cell wall extension and cell division, but the feedbacks that link these processes are poorly understood. Recent papers have revealed developmentally regulated coupling between plant cell growth and progression through both mitotic cycles and endocycles. Modeling has given insight into the effects of cell geometry and tissue mechanics on the orientation of cell divisions. Developmental inputs by auxin have been highlighted in the control of cell turgor, vacuole function and the microtubule dynamics that underlies oriented growth and division. Overall, recent work emphasizes growth and proliferation as processes that are negotiated within and between cells, rather than imposed on cells across tissues.

Abstract

Plant tissue growth requires the interdependent cellular processes of cytoplasmic growth, cell wall extension and cell division, but the feedbacks that link these processes are poorly understood. Recent papers have revealed developmentally regulated coupling between plant cell growth and progression through both mitotic cycles and endocycles. Modeling has given insight into the effects of cell geometry and tissue mechanics on the orientation of cell divisions. Developmental inputs by auxin have been highlighted in the control of cell turgor, vacuole function and the microtubule dynamics that underlies oriented growth and division. Overall, recent work emphasizes growth and proliferation as processes that are negotiated within and between cells, rather than imposed on cells across tissues.

Shi B., Zhang C., Tian C., Wang J., Wang Q., Xu T., Xu Y., Ohno C., Sablowski R., Heisler M. G., Theres K., Wang Y., Jiao Y. (2016)

Two-Step Regulation of a Meristematic Cell Population Acting in Shoot Branching in Arabidopsis.

PLoS Genetics (12) e1006168

Publisher's version: 10.1371/journal.pgen.1006168

ID: 55228

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Abstract

Shoot branching requires the establishment of new meristems harboring stem cells; this phenomenon raises questions about the precise regulation of meristematic fate. In seed plants, these new meristems initiate in leaf axils to enable lateral shoot branching. Using live-cell imaging of leaf axil cells, we show that the initiation of axillary meristems requires a meristematic cell population continuously expressing the meristem marker SHOOT MERISTEMLESS (STM). The maintenance of STM expression depends on the leaf axil auxin minimum. Ectopic expression of STM is insufficient to activate axillary buds formation from plants that have lost leaf axil STM expressing cells. This suggests that some cells undergo irreversible commitment to a developmental fate. In more mature leaves, REVOLUTA (REV) directly up-regulates STM expression in leaf axil meristematic cells, but not in differentiated cells, to establish axillary meristems. Cell type-specific binding of REV to the STM region correlates with epigenetic modifications. Our data favor a threshold model for axillary meristem initiation, in which low levels of STM maintain meristematic competence and high levels of STM lead to meristem initiation.

Serrano A., Schiessl K., Sablowski R. (2015)

Active Control of Cell Size Generates Spatial Detail during Plant Organogenesis.

Current Biology (25) 2991-6

Publisher's version: 10.1016/j.cub.2015.10.008

ID: 51967

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Abstract

How cells regulate their dimensions is a long-standing question. In fission and budding yeast, cell-cycle progression depends on cell size, although it is still unclear how size is assessed. In animals, it has been suggested that cell size is modulated primarily by the balance of external signals controlling growth and the cell cycle, although there is evidence of cell-autonomous control in cell cultures. Regardless of whether regulation is external or cell autonomous, the role of cell-size control in the development of multicellular organisms remains unclear. Plants are a convenient system to study this question: the shoot meristem, which continuously provides new cells to form new organs, maintains a population of actively dividing and characteristically small cells for extended periods. Here, we used live imaging and quantitative, 4D image analysis to measure the sources of cell-size variability in the meristem and then used these measurements in computer simulations to show that the uniform cell sizes seen in the meristem likely require coordinated control of cell growth and cell cycle in individual cells. A genetically induced transient increase in cell size was quickly corrected by more frequent cell division, showing that the cell cycle was adjusted to maintain cell-size homeostasis. Genetically altered cell sizes had little effect on tissue growth but perturbed the establishment of organ boundaries and the emergence of organ primordia. We conclude that meristem cells actively control their sizes to achieve the resolution required to pattern small-scale structures.

Sablowski R. (2015)

Control of patterning, growth, and differentiation by floral organ identity genes

Journal of Experimental Botany (66(4)) 1065-1073

Publisher's version: 10.1093/jxb/eru514

ID: 49484

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Abstract

In spite of the different morphologies of sepals, petals, stamens, and carpels, all these floral organs are believed to be modified versions of a ground-state organ similar to the leaf. Modifications of the ground-state developmental programme are orchestrated by different combinations of MADS-domain transcription factors encoded by floral organ identity genes. In recent years, much has been revealed about the gene regulatory networks controlled by the floral organ identity genes and about the genetic pathways that control leaf development. This review examines how floral organ identity is connected with the control of morphogenesis and differentiation of shoot organs, focusing on the model species Arabidopsis thaliana. Direct links have emerged between floral organ identity genes and genes involved in abaxial-adaxial patterning, organ boundary formation, tissue growth, and cell differentiation. In parallel, predictive models have been developed to explain how the activity of regulatory genes can be coordinated by intercellular signalling and constrained by tissue mechanics. When combined, these advances provide a unique opportunity for revealing exactly how leaf-like organs have been ‘metamorphosed’ into floral organs during evolution and showing crucial regulatory points in the generation of plant form.

Schiessl K., Muino J. M., Sablowski R. (2014)

Arabidopsis JAGGED links floral organ patterning to tissue growth by repressing Kip-related cell cycle inhibitors

Proceedings of the National Academy of Sciences of the United States of America (111) 2830-2835

Publisher's version: 10.1073/pnas.1320457111

ID: 46264

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Abstract

Plant morphogenesis requires coordinated cytoplasmic growth, oriented cell wall extension and cell cycle progression, but it is debated which of these processes are primary drivers for tissue growth and directly targeted by developmental genes. Here, we used chromatin immunoprecipitation-high throughput sequencing (ChIP-Seq) combined with transcriptome analysis to identify global target genes of the Arabidopsis transcription factor JAGGED (JAG), which promotes growth of the distal region of floral organs. Consistent with the roles of JAG during organ initiation and subsequent distal organ growth, we found that JAG directly repressed genes involved in meristem development, such as CLAVATA1 and HANABA TARANU, and genes involved in the development of the basal region of shoot organs, such as BLADE ON PETIOLE 2 and the GROWTH REGULATORY FACTOR pathway. At the same time, JAG regulated genes involved in tissue polarity, cell wall modification and cell cycle progression. In particular, JAG directly repressed KIP RELATED PROTEIN 4 (KRP4) and KRP2, which control the transition to the DNA synthesis phase (S-phase) of the cell cycle. krp2 and krp4 mutations suppressed jag defects in organ growth and in the morphology of petal epidermal cells, showing that the interaction between JAG and KRP genes is functionally relevant. Our work reveals that JAG is a direct mediator between genetic pathways involved in organ patterning and cellular functions required for tissue growth, and shows that a regulatory gene shapes plant organs by releasing a constraint on S-phase entry. 

Sablowski R., Dornelas M. (2013)

Interplay between cell growth and cell cycle in plants

Journal of Experimental Botany (Advance online publication) 000

Publisher's version: 10.1093/jxb/ert354

ID: 46274

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Abstract

The growth of organs and whole plants depends on both cell growth and cell cycle progression, but the interaction between both processes is poorly understood. In plants, the balance between growth and cell cycle progression requires coordinated regulation of four different processes: macromolecular synthesis (cytoplasmic growth), turgor-driven cell wall extension, mitotic cycle and endocycle. Potential feedbacks between these processes include a cell size checkpoint operating before DNA synthesis and a link between DNA contents and maximum cell size. In addition, key intercellular signals and growth regulatory genes appear to target at the same time cell cycle and cell growth functions. For example, auxin, gibberellin and brassinosteroid all have parallel links to cell cycle progression (through S-phase Cyclin D/CDK and the anaphase-promoting complex), and to cell wall functions (through cell wall extensibility or microtubule dynamics). Another intercellular signal mediated by microtubule dynamics is the mechanical stress caused by growth of interconnected cells. Superimposed on developmental controls, sugar signaling through the TOR pathway has recently emerged as a central control point linking cytoplasmic growth, cell cycle and cell wall functions. Recent progress in quantitative imaging and computational modeling will facilitate analysis of the multiple interconnections between plant cell growth and cell cycle and ultimately will be required for predictive manipulation of plant growth.

Sauret-Güeto S., Schiessl K., Bangham A., Sablowski R., Coen E. (2013)

JAGGED Controls Arabidopsis Petal Growth and Shape by Interacting with a Divergent Polarity Field.

PLoS Biology (11) e1001550

Publisher's version: 10.1371/journal.pbio.1001550

ID: 41892

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Sablowski R. (2013)

Roots of beauty.

Nature Reviews Molecular Cell Biology (14) 268

Publisher's version: 10.1038/nrm3559

ID: 41891

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Schiessl K., Kausika S., Southam P., Bush M., Sablowski R. (2012)

JAGGED controls growth anisotropyand coordination between cell sizeand cell cycle during plant organogenesis.

Current Biology (22) 1739-46

Publisher's version: 10.1016/j.cub.2012.07.020

ID: 41487

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Sablowski R. (2011)

Plant stem cell niches: from signalling to execution.

Current Opinion in Plant Biology (14) 4-9

Publisher's version: 10.1016/j.pbi.2010.08.001

ID: 38746

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Doonan J. H., Sablowski R. (2010)

Walls around tumours - why plants do not develop cancer

Nature Reviews Cancer (10) 794-802

Publisher's version: 10.1038/nrc2942

ID: 38131

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Arnaud N., Girin T., Sorefan K., Fuentes S., Wood T. A., Lawrenson T., Sablowski R., Ostergaard L. (2010)

Gibberellins control fruit patterning in Arabidopsis thaliana

Genes & Development (24) 2127-2132

Publisher's version: 10.1101/gad.593410

ID: 38011

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Sablowski R. (2010)

Genes and functions controlled by floral organ identity genes

Seminars in Cell and Developmental Biology (21) 94-99

Publisher's version: 10.1016/j.semcdb.2009.08.008

ID: 19203

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Fulcher N., Sablowski R. (2009)

Hypersensitivity to DNA damage in plant stem cell niches

Proceedings of the National Academy of Sciences of the United States of America (106) 20984-20988

ID: 19647

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Sablowski R. (2009)

Cytokinin and WUSCHEL tie the knot around plant stem cells

Proceedings of the National Academy of Sciences of the United States of America (106) 16016-16017

Publisher's version: 10.1073/pnas.0909300106

ID: 19202

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Smith A., Coupland G., Dolan L., Harberd N., Jones J., Martin C., Sablowski R., Amey A. (2009)

Plant Biology

ID: 18786

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Sablowski R. (2007)

Flowering and determinacy in Arabidopsis

Journal of Experimental Botany (58) 899-907

Publisher's version: 10.1093/jxb/erm002

ID: 7524

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Sablowski R. (2007)

The dynamic plant stem cell niches

Current Opinion in Plant Biology (10) 639-644

ID: 7563

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Kerzendorfer C., Vignard J., Pedrosa-Harand A., Siwiec T., Akimcheva S., Jolivet S., Sablowski R., Armstrong S., Mercier R., Schlogelhofer P. (2006)

The Arabidopsis thaliana MND1 homologue plays a key role in meiotic homologous pairing, synapsis and recombination

Journal of Cell Science (119) 2486-2496

Publisher's version: 10.1242/jcs.02967

ID: 6325

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