Available online at www.sciencedirect.com
ScienceDirect Editorial overview: Growth and development Niko Geldner and Sigal Savaldi-Goldstein Current Opinion in Plant Biology 2015, 23:iv–vi For a complete overview see the Issue Available online 20th January 2015 http://dx.doi.org/10.1016/j.pbi.2015.01.002 1369-5266/Published by Elsevier Ltd.
Niko Geldner Department of Plant Molecular Biology, University of Lausanne, UNIL–Sorge, Biophore Building, 1015 Lausanne, Switzerland e-mail: [email protected] Niko Geldner is interested in the differentiation and function of the root endodermis. His lab attempts to dissect the molecular mechanisms that lead to the precise subcellular deposition of the Casparian strips — lignin-like impregnations of the primary cell wall that surround endodermal cells like a belt. Using the endodermis as a model, they aim to obtain insights into the generation of stable membrane subdomains and localization of cell wall biosynthesis. The lab is also interested in using precise genetic manipulations of endodermal differentiation in order to obtain insights into physiological role of the endodermis.
Sigal Savaldi-Goldstein Faculty of Biology, Technion-Israel Institute of Technology, Haifa 3200003, Israel e-mail: [email protected] Sigal Savaldi-Goldstein Our lab aims to understand how coherent organ growth is achieved in plants. To this end, we focus on decoding the role of the brassinosteroid (BR) signaling pathway in the tissues and cell types composing the Arabidopsis root. We study the link between local effects of the hormone and whole organ growth. Our group also investigates how BR-mediated root growth is modulated by environmental signals. Special emphasis is placed on the interplay between BR and root response to low phosphate availability.
Current Opinion in Plant Biology 2015, 23:iv–vi
Despite the tremendous strides forward that plant research has taken in recent years, many fundamental questions about plants remain unanswered. These include seemingly simple questions, as for example, when do cells enter division and when do they stop? What determines directionality of cell division and what drives organ morphogenesis? How do cells and organs acquire their unique identity and function and how growth is regulated by the environment? In this 2015 edition of the Growth and Development section, we decided to put together snapshots, representing some of the most intriguing and promising current efforts to understand such questions. Not bounded by a common theme, this issue aims to highlight a broad spectrum of timely research, models and experimental approaches. Together, they reflect the various molecular, cellular and whole organ elements controlling this elusive, fascinating process of plant growth and development that unfolds each day under our eyes. Summarized below are the unique jigsaw pieces that each author has contributed to this remarkable puzzle.
The control of cell division: the number, the timing and the orientation Postembryonic growth and development require a controlled production of cells at the meristems. Core cell cycle components driving the proliferation process per se are established, but how they are regulated is a subject of current studies. Polyn et al. discuss advances related to three consecutive aspects of the cell cycle: entry, maintenance and exit (i.e., onset of differentiation). Current models of the RETINOBLASTOMA-RELATED1 (RBR1)-E2F/DIMERIZATION PARTNER (DP) interplay and the effectors linking nutrient availability with cell cycle progression are put forward to explain entry into the cell cycle. Maintenance of the cell cycle is highlighted by models in the root meristem. These include the role of the proteasome and a recently identified target of the APC/C E3 ubiquitin ligase, the role of metabolic compounds and newly identified effectors. Pathways controlling timing of cell cycle exit in roots and leaves are discussed, including those involved reactive oxygen species. Orientation of the division plane is essential for shaping plant tissues. van Dop et al. emphasize a major unknown — the identity of the genetic components linking development to oriented divisions. Focusing on the Arabidopsis embryo as a model system, the authors exemplify the importance of such genetic regulation. That is, symmetric division is guided by a defined structural rule and deviation from this rule was recently found to occur at specific stages in the developing embryo. The authors discuss the role of the few known potential effectors. Also discussed is the use of images www.sciencedirect.com
Editorial overview Geldner and Savaldi-Goldstein v
and computational simulations in 3D to quantify cell shape during embryogenesis. This advance sets a platform for future identification of regulatory genes.
Cell fate determination and function A meristem can be roughly defined as a stem cell population, associated with its dividing stem cell daughters. Zooming into the shoot apical meristem (SAM) reveals a colorful, structured environment, where cells acquire fates multiple times according to their position, before they eventually differentiate. Gaillochet et al. discuss the spatial organization of the SAM and its importance in guiding these unique cellular activities. Mechanisms of intercellular communication between functional subdomains in the SAM are reviewed. These include the recently identified trafficking of the stem cell-promoting transcription factors WUSCHEL (WUS) and the A-type Arabidopsis Response Regulators (ARRs). Also reviewed are current mechanisms controlling primordia initiation and the boundary region separating the emerging primordia from the SAM. The aforementioned importance of short-range signals in SAM has long been demonstrated by studies revealing peptide signaling (the most famous is that triggered by the CLV3 peptide and its cognate CLV1 receptor). Hence, stem cell decisions in the apical meristems, root phloem differentiation and lateral root initiation are examples of processes controlled by peptide signaling pathways. Grienenberger and Fletcher survey current knowledge in the field, focusing on the most established modules. Several peptide–receptor pairs have been uncovered. As over 1000 putative peptides are encoded in the Arabidopsis genome, an awe-inspiring number of studies are yet to be performed in order to decipher their role. The most impressive results of plant stem cell activities are certainly seen in trees, as the biggest organisms found on this planet. Their immense growth is only rendered possible by the initiation of two secondary meristems of which the vascular cambium produces the lion’s share of secondary tissue. Jouannet et al. discuss the regulatory networks regulating both procambium formation and cambium proliferation and provide a thoughtful discussion of how these networks are related to each other. The overwhelming part of a mature tree and a big part of any adult plant consists of one of the two products of the vascular cambium — the dead, lignified tracheary elements and their associated cell types. In two complementary reviews, Me´nard and Pesquet discuss our current knowledge of how tracheary elements differentiate and lignify and how their differentiation is dependent on a fascinating interplay with living, ‘good neighbors’ that assist in their correct lignification. Voxeur et al. also discuss this interplay between different xylem cell types, www.sciencedirect.com
but further highlight the complexity of lignification, pointing out its distinct composition in different cell types and even on a subcellular scale. In addition, the authors provide an overview of the known players that drive this complex process of cell wall impregnation in vivo. Altartouri and Geitmann present an overview of the amazing regulatory complexity and mechanics of cell walls in young, growing cells and discuss the need to monitor cell wall growth in vivo and the tools that are available to do so. Epigenetic regulation is crucial for cell fate maintenance and acquisition. In both animals and plants, switching a developmental phase relies on the activity of polycomb proteins. These proteins comprise the Polycomb Repressive Complex 1 (PRC1) and PRC2 that trigger a repressive state of the chromatin, thereby shutting off gene expression. Xiao and Wagner discuss the activity, regulation and recruitment of these complexes in plants, and compare these mechanisms to those known from mammals and insects. The authors review the role of PRC during various phase transitions, including the switch between cell differentiation and de-differentiation, a basic process allowing plant developmental plasticity.
Organ formation and differentiation Leaf formation involves two key stages: morphogenesis and differentiation. The longer duration of the former allows a morphological change, from simple to compound leaves, providing sufficient time to form leaflets. Bar and Ori summarize current mechanisms underlying compound leaf development in four species. As such, this review provides a stimulating comparison of the interplay between transcription factors and hormone involved in each species. The authors exemplify how a similar mechanism is used in a context specific manner, allowing variation in plant forms. An interesting aspect of lateral root formation relates to the ability of developing lateral root primordia that initiate deep within the primary root to pave their way out of the root, through the surrounding tissues. Vilches-Barro and Maizel discuss our recent understanding of this process, where communication between the growing primordia and its surrounding tissues (endodermis, cortex and epidermis) plays an important role in this process. Highlighted are auxin signaling, cell wall remodeling and mechanical constraints as important elements mediating this communication.
Environmental signals and differential growth In order to optimize their exposure to the environment, plant constantly adjust growth of their organs towards and away a specific environmental stimuli. In this issue, Friml and colleagues discuss our recent understanding of the intricate mechanisms that regulate the polar localization of auxin efflux carriers in response to two major stimuli, Current Opinion in Plant Biology 2015, 23:iv–vi
vi Growth and development
gravitropism and phototropism, thereby determining the differential accumulation of auxin within the growing organ, leading to differential, directional growth. Plants also use tropic responses in order to avoid high salinity, an environmental stress with high impact on plant growth and physiology. Focusing on ABA activity, the main signaling component regulating plant response to salt stress, Dinneny highlights the various approaches taken to elucidate regulatory networks involved, including the recently reported spatio-temporal gene expression profiling and interactome analyses. The architecture of plants is shaped by the growth angle of branches and lateral root relative to the main axis. When this angle is maintained over a long period of time, it can be defined as a gravitropic setpoint angle (GSA). Roychoudhry and Kepinski discuss the conceptual distinction between a mere response to gravity and GSA mechanisms. New models and hypotheses are put forward, and potential effectors reported in various species are discussed.
Evolutionary adaptations shaping growth and development Our fascination with the mechanisms driving growth and development does not only arise from the fact that it is ‘reproduced without appreciable change for generations,
Current Opinion in Plant Biology 2015, 23:iv–vi
permanent within centuries’, as Schroedinger so pointedly noted — it also stems from the seemingly endless variation that arises from modification of core developmental modules and that faces us in the distinct appearance of the more than hundred thousand plant species on our earth. Busch and Ogura discuss how the stunning increases in sequencing power and data analysis tools in recent years has enabled Genome Wide Association Studies that allow us to appreciate evolution on the micro-scale — as the sequence variation underlying differences of individuals within a species. The authors provide us with recent example illustrating how powerful this tool of comparative genotype–phenotype analysis can be for implicating currently unknown genes in various developmental processes. Navarro et al. discuss a fascinating example of a very relevant variation that has led to the deployment of the regulatory circuits underlying flowering for the regulation of tuberization in potato and how FT-like genes regulating this process have been targets during potato domestication. Lafon-Placette and Ko¨hler discuss the evidence for an epigenetic basis underlying hybrid incompatibility, an important mechanism causing reproductive isolation and thus speciation. Last but not least, plant growth and development cannot be understood without an appreciation of the ubiquitous interactions of plants with microorganisms, both beneficial and pathogenic. Yamazaki and Hayashi discuss and compare the cellular mechanisms that underlie the interactions of plant cells with various fungi and bacteria.
www.sciencedirect.com
ScienceDirect Editorial overview: Growth and development Niko Geldner and Sigal Savaldi-Goldstein Current Opinion in Plant Biology 2015, 23:iv–vi For a complete overview see the Issue Available online 20th January 2015 http://dx.doi.org/10.1016/j.pbi.2015.01.002 1369-5266/Published by Elsevier Ltd.
Niko Geldner Department of Plant Molecular Biology, University of Lausanne, UNIL–Sorge, Biophore Building, 1015 Lausanne, Switzerland e-mail: [email protected] Niko Geldner is interested in the differentiation and function of the root endodermis. His lab attempts to dissect the molecular mechanisms that lead to the precise subcellular deposition of the Casparian strips — lignin-like impregnations of the primary cell wall that surround endodermal cells like a belt. Using the endodermis as a model, they aim to obtain insights into the generation of stable membrane subdomains and localization of cell wall biosynthesis. The lab is also interested in using precise genetic manipulations of endodermal differentiation in order to obtain insights into physiological role of the endodermis.
Sigal Savaldi-Goldstein Faculty of Biology, Technion-Israel Institute of Technology, Haifa 3200003, Israel e-mail: [email protected] Sigal Savaldi-Goldstein Our lab aims to understand how coherent organ growth is achieved in plants. To this end, we focus on decoding the role of the brassinosteroid (BR) signaling pathway in the tissues and cell types composing the Arabidopsis root. We study the link between local effects of the hormone and whole organ growth. Our group also investigates how BR-mediated root growth is modulated by environmental signals. Special emphasis is placed on the interplay between BR and root response to low phosphate availability.
Current Opinion in Plant Biology 2015, 23:iv–vi
Despite the tremendous strides forward that plant research has taken in recent years, many fundamental questions about plants remain unanswered. These include seemingly simple questions, as for example, when do cells enter division and when do they stop? What determines directionality of cell division and what drives organ morphogenesis? How do cells and organs acquire their unique identity and function and how growth is regulated by the environment? In this 2015 edition of the Growth and Development section, we decided to put together snapshots, representing some of the most intriguing and promising current efforts to understand such questions. Not bounded by a common theme, this issue aims to highlight a broad spectrum of timely research, models and experimental approaches. Together, they reflect the various molecular, cellular and whole organ elements controlling this elusive, fascinating process of plant growth and development that unfolds each day under our eyes. Summarized below are the unique jigsaw pieces that each author has contributed to this remarkable puzzle.
The control of cell division: the number, the timing and the orientation Postembryonic growth and development require a controlled production of cells at the meristems. Core cell cycle components driving the proliferation process per se are established, but how they are regulated is a subject of current studies. Polyn et al. discuss advances related to three consecutive aspects of the cell cycle: entry, maintenance and exit (i.e., onset of differentiation). Current models of the RETINOBLASTOMA-RELATED1 (RBR1)-E2F/DIMERIZATION PARTNER (DP) interplay and the effectors linking nutrient availability with cell cycle progression are put forward to explain entry into the cell cycle. Maintenance of the cell cycle is highlighted by models in the root meristem. These include the role of the proteasome and a recently identified target of the APC/C E3 ubiquitin ligase, the role of metabolic compounds and newly identified effectors. Pathways controlling timing of cell cycle exit in roots and leaves are discussed, including those involved reactive oxygen species. Orientation of the division plane is essential for shaping plant tissues. van Dop et al. emphasize a major unknown — the identity of the genetic components linking development to oriented divisions. Focusing on the Arabidopsis embryo as a model system, the authors exemplify the importance of such genetic regulation. That is, symmetric division is guided by a defined structural rule and deviation from this rule was recently found to occur at specific stages in the developing embryo. The authors discuss the role of the few known potential effectors. Also discussed is the use of images www.sciencedirect.com
Editorial overview Geldner and Savaldi-Goldstein v
and computational simulations in 3D to quantify cell shape during embryogenesis. This advance sets a platform for future identification of regulatory genes.
Cell fate determination and function A meristem can be roughly defined as a stem cell population, associated with its dividing stem cell daughters. Zooming into the shoot apical meristem (SAM) reveals a colorful, structured environment, where cells acquire fates multiple times according to their position, before they eventually differentiate. Gaillochet et al. discuss the spatial organization of the SAM and its importance in guiding these unique cellular activities. Mechanisms of intercellular communication between functional subdomains in the SAM are reviewed. These include the recently identified trafficking of the stem cell-promoting transcription factors WUSCHEL (WUS) and the A-type Arabidopsis Response Regulators (ARRs). Also reviewed are current mechanisms controlling primordia initiation and the boundary region separating the emerging primordia from the SAM. The aforementioned importance of short-range signals in SAM has long been demonstrated by studies revealing peptide signaling (the most famous is that triggered by the CLV3 peptide and its cognate CLV1 receptor). Hence, stem cell decisions in the apical meristems, root phloem differentiation and lateral root initiation are examples of processes controlled by peptide signaling pathways. Grienenberger and Fletcher survey current knowledge in the field, focusing on the most established modules. Several peptide–receptor pairs have been uncovered. As over 1000 putative peptides are encoded in the Arabidopsis genome, an awe-inspiring number of studies are yet to be performed in order to decipher their role. The most impressive results of plant stem cell activities are certainly seen in trees, as the biggest organisms found on this planet. Their immense growth is only rendered possible by the initiation of two secondary meristems of which the vascular cambium produces the lion’s share of secondary tissue. Jouannet et al. discuss the regulatory networks regulating both procambium formation and cambium proliferation and provide a thoughtful discussion of how these networks are related to each other. The overwhelming part of a mature tree and a big part of any adult plant consists of one of the two products of the vascular cambium — the dead, lignified tracheary elements and their associated cell types. In two complementary reviews, Me´nard and Pesquet discuss our current knowledge of how tracheary elements differentiate and lignify and how their differentiation is dependent on a fascinating interplay with living, ‘good neighbors’ that assist in their correct lignification. Voxeur et al. also discuss this interplay between different xylem cell types, www.sciencedirect.com
but further highlight the complexity of lignification, pointing out its distinct composition in different cell types and even on a subcellular scale. In addition, the authors provide an overview of the known players that drive this complex process of cell wall impregnation in vivo. Altartouri and Geitmann present an overview of the amazing regulatory complexity and mechanics of cell walls in young, growing cells and discuss the need to monitor cell wall growth in vivo and the tools that are available to do so. Epigenetic regulation is crucial for cell fate maintenance and acquisition. In both animals and plants, switching a developmental phase relies on the activity of polycomb proteins. These proteins comprise the Polycomb Repressive Complex 1 (PRC1) and PRC2 that trigger a repressive state of the chromatin, thereby shutting off gene expression. Xiao and Wagner discuss the activity, regulation and recruitment of these complexes in plants, and compare these mechanisms to those known from mammals and insects. The authors review the role of PRC during various phase transitions, including the switch between cell differentiation and de-differentiation, a basic process allowing plant developmental plasticity.
Organ formation and differentiation Leaf formation involves two key stages: morphogenesis and differentiation. The longer duration of the former allows a morphological change, from simple to compound leaves, providing sufficient time to form leaflets. Bar and Ori summarize current mechanisms underlying compound leaf development in four species. As such, this review provides a stimulating comparison of the interplay between transcription factors and hormone involved in each species. The authors exemplify how a similar mechanism is used in a context specific manner, allowing variation in plant forms. An interesting aspect of lateral root formation relates to the ability of developing lateral root primordia that initiate deep within the primary root to pave their way out of the root, through the surrounding tissues. Vilches-Barro and Maizel discuss our recent understanding of this process, where communication between the growing primordia and its surrounding tissues (endodermis, cortex and epidermis) plays an important role in this process. Highlighted are auxin signaling, cell wall remodeling and mechanical constraints as important elements mediating this communication.
Environmental signals and differential growth In order to optimize their exposure to the environment, plant constantly adjust growth of their organs towards and away a specific environmental stimuli. In this issue, Friml and colleagues discuss our recent understanding of the intricate mechanisms that regulate the polar localization of auxin efflux carriers in response to two major stimuli, Current Opinion in Plant Biology 2015, 23:iv–vi
vi Growth and development
gravitropism and phototropism, thereby determining the differential accumulation of auxin within the growing organ, leading to differential, directional growth. Plants also use tropic responses in order to avoid high salinity, an environmental stress with high impact on plant growth and physiology. Focusing on ABA activity, the main signaling component regulating plant response to salt stress, Dinneny highlights the various approaches taken to elucidate regulatory networks involved, including the recently reported spatio-temporal gene expression profiling and interactome analyses. The architecture of plants is shaped by the growth angle of branches and lateral root relative to the main axis. When this angle is maintained over a long period of time, it can be defined as a gravitropic setpoint angle (GSA). Roychoudhry and Kepinski discuss the conceptual distinction between a mere response to gravity and GSA mechanisms. New models and hypotheses are put forward, and potential effectors reported in various species are discussed.
Evolutionary adaptations shaping growth and development Our fascination with the mechanisms driving growth and development does not only arise from the fact that it is ‘reproduced without appreciable change for generations,
Current Opinion in Plant Biology 2015, 23:iv–vi
permanent within centuries’, as Schroedinger so pointedly noted — it also stems from the seemingly endless variation that arises from modification of core developmental modules and that faces us in the distinct appearance of the more than hundred thousand plant species on our earth. Busch and Ogura discuss how the stunning increases in sequencing power and data analysis tools in recent years has enabled Genome Wide Association Studies that allow us to appreciate evolution on the micro-scale — as the sequence variation underlying differences of individuals within a species. The authors provide us with recent example illustrating how powerful this tool of comparative genotype–phenotype analysis can be for implicating currently unknown genes in various developmental processes. Navarro et al. discuss a fascinating example of a very relevant variation that has led to the deployment of the regulatory circuits underlying flowering for the regulation of tuberization in potato and how FT-like genes regulating this process have been targets during potato domestication. Lafon-Placette and Ko¨hler discuss the evidence for an epigenetic basis underlying hybrid incompatibility, an important mechanism causing reproductive isolation and thus speciation. Last but not least, plant growth and development cannot be understood without an appreciation of the ubiquitous interactions of plants with microorganisms, both beneficial and pathogenic. Yamazaki and Hayashi discuss and compare the cellular mechanisms that underlie the interactions of plant cells with various fungi and bacteria.
www.sciencedirect.com
