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Start Over Author "Bennett, Malcolm J" Publisher american society of plant biologists
42 results on '"Bennett, Malcolm J"'

1. Modeling root loss reveals impacts on nutrient uptake and crop development

Author

Owen, Markus R, Band, Leah R, Farcot, Etienne, Bennett, Malcolm J, and Lynch, Jonathan P

Subjects
Physiology, Genetics, Plant Science
Abstract

Despite the widespread prevalence of root loss in plants, its effects on crop productivity are not fully understood. While root loss reduces the capacity of plants to take up water and nutrients from the soil, it may provide benefits by decreasing the resources required to maintain the root system. Here, we simulated a range of root phenotypes in different soils and root loss scenarios for barley (Hordeum vulgare), common bean (Phaseolus vulgaris) and maize (Zea mays) using and extending the open-source, functional-structural root/soil simulation model OpenSimRoot. The model enabled us to quantify the impact of root loss on shoot dry weight in these scenarios and identify in which scenarios root loss is beneficial, detrimental, or has no effect. The simulations showed that root loss is detrimental for phosphorus uptake in all tested scenarios whereas nitrogen uptake was relatively insensitive to root loss unless main root axes were lost. Loss of axial roots reduced shoot dry weight for all phenotypes in all species and soils, whereas lateral root loss had a smaller impact. In barley and maize plants with high lateral branching density that were not phosphorus-stressed, loss of lateral roots increased shoot dry weight. The fact that shoot dry weight increased due to root loss in these scenarios indicates that plants overproduce roots for some environments, such as those found in high-input agriculture. We conclude that a better understanding of the effects of root loss on plant development is an essential part of optimizing root system phenotypes for maximizing yield.

Published
2022

2. Systems approaches reveal that ABCB and PIN proteins mediate co-dependent auxin efflux

Author

Mellor, Nathan L, Ware, Alexander, Janes, George, Barrack, Duncan, Bishopp, Anthony, Bennett, Malcolm J, Geisler, Markus, Wells, Darren M, and Band, Leah R

Subjects
Cell Biology, Plant Science
Abstract

Members of the B family of membrane-bound ATP-binding cassette (ABC) transporters represent key components of the auxin-efflux machinery in plants. Over the last two decades experimental studies have shown that modifying ABCB expression affects auxin distribution and plant phenotypes. However, precisely how ABCB proteins transport auxin in conjunction with the more widely studied family of PIN-formed (PIN) auxin efflux transporters is unclear, and studies using heterologous systems have produced conflicting results.Here, we integrate ABCB localization data into a multicellular model of auxin transport in the Arabidopsis thaliana root tip to predict how ABCB-mediated auxin transport impacts organ-scale auxin distribution. We use our model to test five potential ABCB–PIN regulatory interactions, simulating the auxin dynamics for each interaction and quantitatively comparing the predictions with experimental images of the DII-VENUS auxin reporter in wild type and abcb single and double loss-of-function mutants. Only specific ABCB–PIN regulatory interactions result in predictions that recreate the experimentally observed DII-VENUS distributions and long-distance auxin transport. Our results suggest that ABCBs enable auxin efflux independently of PINs; however, PIN-mediated auxin efflux is predominantly through a co-dependent efflux where co-localised with ABCBs.

Published
2022

3. High-throughput quantification of root growth using a novel image-analysis tool

Author

French, Andrew, Ubeda-Tomas, Susana, Holman, Tara J., Bennett, Malcolm J., and Pridmore, Tony

Subjects
Algorithms -- Research, Arabidopsis thaliana -- Growth, Arabidopsis thaliana -- Physiological aspects, Growth (Plants) -- Research, Roots (Botany) -- Research, Algorithm, Company growth, Biological sciences, Science and technology
Published
2009

4. The binding of auxin to the arabidopsis auxin influx transporter aux1

Author

Carrier, David J., Bakar, Norliza Tendot Abu, Swarup, Ranjan, Callaghan, Richard, Napier, Richard M., Bennett, Malcolm J., and Kerr, Ian D.

Subjects
Organic acids -- Chemical properties, Arabidopsis thaliana -- Chemical properties, Biological sciences, Science and technology
Published
2008

5. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation [W]

Author

Swarup, Ranjan, Perry, Paula, Hagenbeek, Dik, Van Der Straeten, Dominique, Beemster, Gerrit T.S., Sandberg, Goran, Bhalerao, Rishikesh, Ljung, Karin, and Bennett, Malcolm J.

Subjects
Arabidopsis thaliana -- Physiological aspects, Auxin -- Physiological aspects, Biosynthesis -- Research, Ethylene -- Properties, Plant cells and tissues -- Growth, Roots (Botany) -- Growth, Company growth, Biological sciences, Science and technology
Published
2007

6. Structure-function analysis of the presumptive arabidopsis auxin permease aux1 ([W])

Author

Swarup, Ranjan, Kargul, Joanna, Marchant, Alan, Zadik, Daniel, Rahman, Abidur, Mills, Rebecca, Yemm, Anthony, May, Sean, Williams, Lorriane, Millner, Paul, Tsurumi, Seiji, Moore, Ian, Napier, Richard, Kerr, Ian D., and Bennett, Malcolm J.

Subjects
Auxin -- Structure, Arabidopsis thaliana -- Genetic aspects, Fluorescence spectroscopy -- Analysis, Biological sciences, Science and technology
Published
2004

7. Emergent Protective Organogenesis in Date Palms: A Morpho-devo-dynamic Adaptive Strategy During Early Development

Author

Xiao, Tingting, Kirschner, Gwendolyn, Deng, Yanming, Atkinson, Brian, Sturrock, Craig, Lube, Vinicius, Wang, Jian You, Lubineau, Gilles, Al-Babili, Salim, Bennett, Malcolm J., and Blilou, Ikram

Abstract

Desert plants have developed mechanisms for adapting to hostile desert conditions, yet these mechanisms remain poorly understood. Here, we describe two unique modes used by desert date palms (Phoenix dactylifera L.) to protect their meristematic tissues during early organogenesis. We used X-ray micro-computed tomography combined with high-resolution tissue imaging to reveal that, after germination, development of the embryo pauses while it remains inside a dividing and growing cotyledonary petiole. Transcriptomic and hormone analyses show that this developmental arrest is associated with the low expression of development-related genes and accumulation of hormones that promote dormancy and confer resistance to stress. Furthermore, organ-specific cell type mapping demonstrates that organogenesis occurs inside the cotyledonary petiole, with identifiable root and shoot meristems and their respective stem cells. The plant body emerges from the surrounding tissues with developed leaves and a complex root system that maximizes efficient nutrient and water uptake. We further show that, similar to its role in Arabidopsis thaliana, the SHORT-ROOT (SHR) homologue from date palms functions in maintaining stem cell activity and promoting formative divisions in the root ground tissue. Our findings provide insight into developmental programs that confer adaptive advantages in desert plants that thrive in hostile habitats.

Published
2019

8. MtLAX2, a Functional Homologue of the Arabidopsis Auxin Influx Transporter AUX1, Is Required for Nodule Organogenesis1[CC-BY]

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Subjects
Indoleacetic Acids, fungi, food and beverages, Membrane Transport Proteins, Biological Transport, Articles, biochemical phenomena, metabolism, and nutrition, Plants, Genetically Modified, Plant Root Nodulation, Plant Roots, Gravitropism, Gene Expression Regulation, Plant, Medicago truncatula, Mutation, Root Nodules, Plant, Symbiosis, Plant Proteins, Rhizobium
Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of

Published
2017

9. Tonoplast Aquaporins Facilitate Lateral Root Emergence

Author

UCL - SST/ISV - Institut des sciences de la vie, Reinhardt, Hagen, Hachez, Charles, Bienert, Manuela Désirée, Beebo, Azeez, Swarup, Kamal, Voss, Ute, Bouhidel, Karim, Frigerio, Lorenzo, Schjoerring, Jan K., Bennett, Malcolm J., Chaumont, François, UCL - SST/ISV - Institut des sciences de la vie, Reinhardt, Hagen, Hachez, Charles, Bienert, Manuela Désirée, Beebo, Azeez, Swarup, Kamal, Voss, Ute, Bouhidel, Karim, Frigerio, Lorenzo, Schjoerring, Jan K., Bennett, Malcolm J., and Chaumont, François

Abstract

Aquaporins (AQPs) are water channels allowing fast and passive diffusion of water across cell membranes. It was hypothesized that AQPs contribute to cell elongation processes by allowing water influx across the plasma membrane and the tonoplast to maintain adequate turgor pressure. Here, we report that, in Arabidopsis (Arabidopsis thaliana), the highly abundant tonoplast AQP isoforms AtTIP1;1, AtTIP1;2, and AtTIP2;1 facilitate the emergence of new lateral root primordia (LRPs). The number of lateral roots was strongly reduced in the triple tip mutant, whereas the single, double, and triple tip mutants showed no or minor reduction in growth of the main root. This phenotype was due to the retardation of LRP emergence. Live cell imaging revealed that tight spatiotemporal control of TIP abundance in the tonoplast of the different LRP cells is pivotal to mediating this developmental process. While lateral root emergence is correlated to a reduction of AtTIP1;1 and AtTIP1;2 protein levels in LRPs, expression of AtTIP2;1 is specifically needed in a restricted cell population at the base, then later at the flanks, of developing LRPs. Interestingly, the LRP emergence phenotype of the triple tip mutants could be fully rescued by expressing AtTIP2;1 under its native promoter. We conclude that TIP isoforms allow the spatial and temporal fine-tuning of cellular water transport, which is critically required during the highly regulated process of LRP morphogenesis and emergence.

Published
2016

10. Branching Out in Roots: Uncovering Form, Function, and Regulation1

Author

Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voß, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., and Bennett, Malcolm J.

Subjects
Terminology as Topic, Arabidopsis, Morphogenesis, food and beverages, Edible Grain, human activities, Plant Roots, UPDATES - FOCUS ISSUE
Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.

Published
2014

11. The ASH1-RELATED3 SET-Domain Protein Controls Cell Division Competence of the Meristem and the Quiescent Center of the Arabidopsis Primary Root1[W][OPEN]

Author

Kumpf, Robert, Thorstensen, Tage, Rahman, Mohummad Aminur, Heyman, Jefri, Nenseth, H. Zeynep, Lammens, Tim, Herrmann, Ullrich, Swarup, Ranjan, Veiseth, Silje Veie, Emberland, Gitika, Bennett, Malcolm J., De Veylder, Lieven, and Aalen, Reidunn B.

Subjects
DNA Replication, DNA, Plant, Arabidopsis Proteins, Research Articles - Focus Issue, Meristem, Mutation, Arabidopsis, Plant Roots, Cell Division, S Phase
Abstract

The stem cell niche of the Arabidopsis (Arabidopsis thaliana) primary root apical meristem is composed of the quiescent (or organizing) center surrounded by stem (initial) cells for the different tissues. Initial cells generate a population of transit-amplifying cells that undergo a limited number of cell divisions before elongating and differentiating. It is unclear whether these divisions occur stochastically or in an orderly manner. Using the thymidine analog 5-ethynyl-2'-deoxyuridine to monitor DNA replication of cells of Arabidopsis root meristems, we identified a pattern of two, four, and eight neighboring cells with synchronized replication along the cortical, epidermal, and endodermal cell files, suggested to be daughters, granddaughters, and great-granddaughters of the direct progeny of each stem cell. Markers of mitosis and cytokinesis were not present in the region closest to the transition zone where the cells start to elongate, suggesting that great-granddaughter cells switch synchronously from the mitotic cell cycle to endoreduplication. Mutations in the stem cell niche-expressed ASH1-RELATED3 (ASHR3) gene, encoding a SET-domain protein conferring histone H3 lysine-36 methylation, disrupted this pattern of coordinated DNA replication and cell division and increased the cell division rate in the quiescent center. E2Fa/E2Fb transcription factors controlling the G1-to-S-phase transition regulate ASHR3 expression and bind to the ASHR3 promoter, substantiating a role for ASHR3 in cell division control. The reduced length of the root apical meristem and primary root of the mutant ashr3-1 indicate that synchronization of replication and cell divisions is required for normal root growth and development.

Published
2014

12. Root Systems Biology: Integrative Modeling across Scales, from Gene Regulatory Networks to the Rhizosphere1

Author

Hill, Kristine, Porco, Silvana, Lobet, Guillaume, Zappala, Susan, Mooney, Sacha, Draye, Xavier, and Bennett, Malcolm J.

Subjects
Systems Biology, Rhizosphere, Gene Regulatory Networks, Topical Review, Models, Biological, Plant Roots
Abstract

Genetic and genomic approaches in model organisms have advanced our understanding of root biology over the last decade. Recently, however, systems biology and modeling have emerged as important approaches, as our understanding of root regulatory pathways has become more complex and interpreting pathway outputs has become less intuitive. To relate root genotype to phenotype, we must move beyond the examination of interactions at the genetic network scale and employ multiscale modeling approaches to predict emergent properties at the tissue, organ, organism, and rhizosphere scales. Understanding the underlying biological mechanisms and the complex interplay between systems at these different scales requires an integrative approach. Here, we describe examples of such approaches and discuss the merits of developing models to span multiple scales, from network to population levels, and to address dynamic interactions between plants and their environment.

Published
2013

13. RootNav: Navigating Images of Complex Root Architectures1[C][W]

Author

Pound, Michael P., French, Andrew P., Atkinson, Jonathan A., Wells, Darren M., Bennett, Malcolm J., and Pridmore, Tony

Subjects
User-Computer Interface, Brassica napus, Meristem, Seeds, ComputingMethodologies_IMAGEPROCESSINGANDCOMPUTERVISION, Arabidopsis, Image Processing, Computer-Assisted, Oryza, Breakthrough Technologies, Plant Roots, Algorithms, Software, Triticum
Abstract

We present a novel image analysis tool that allows the semiautomated quantification of complex root system architectures in a range of plant species grown and imaged in a variety of ways. The automatic component of RootNav takes a top-down approach, utilizing the powerful expectation maximization classification algorithm to examine regions of the input image, calculating the likelihood that given pixels correspond to roots. This information is used as the basis for an optimization approach to root detection and quantification, which effectively fits a root model to the image data. The resulting user experience is akin to defining routes on a motorist's satellite navigation system: RootNav makes an initial optimized estimate of paths from the seed point to root apices, and the user is able to easily and intuitively refine the results using a visual approach. The proposed method is evaluated on winter wheat (Triticum aestivum) images (and demonstrated on Arabidopsis [Arabidopsis thaliana], Brassica napus, and rice [Oryza sativa]), and results are compared with manual analysis. Four exemplar traits are calculated and show clear illustrative differences between some of the wheat accessions. RootNav, however, provides the structural information needed to support extraction of a wider variety of biologically relevant measures. A separate viewer tool is provided to recover a rich set of architectural traits from RootNav's core representation.

Published
2013

14. SHORT-ROOT and SCARECROW Regulate Leaf Growth in Arabidopsis by Stimulating S-Phase Progression of the Cell Cycle1[W][OA]

Author

Dhondt, Stijn, Coppens, Frederik, De Winter, Freya, Swarup, Kamal, Merks, Roeland M.H., Inzé, Dirk, Bennett, Malcolm J., and Beemster, Gerrit T.S.

Subjects
Plant Leaves, Arabidopsis Proteins, Gene Expression Regulation, Plant, RNA, Plant, Development and Hormone Action, Mutation, Arabidopsis, behavioral disciplines and activities, Plant Roots, Cell Division, Oligonucleotide Array Sequence Analysis, S Phase, Transcription Factors
Abstract

SHORT-ROOT (SHR) and SCARECROW (SCR) are required for stem cell maintenance in the Arabidopsis (Arabidopsis thaliana) root meristem, ensuring its indeterminate growth. Mutation of SHR and SCR genes results in disorganization of the quiescent center and loss of stem cell activity, resulting in the cessation of root growth. This paper reports on the role of SHR and SCR in the development of leaves, which, in contrast to the root, have a determinate growth pattern and lack a persistent stem cell niche. Our results demonstrate that inhibition of leaf growth in shr and scr mutants is not a secondary effect of the compromised root development but is caused by an effect on cell division in the leaves: a reduced cell division rate and early exit of the proliferation phase. Consistent with the observed cell division phenotype, the expression of SHR and SCR genes in leaves is closely associated with cell division activity in most cell types. The increased cell cycle duration is due to a prolonged S-phase duration, which is mediated by up-regulation of cell cycle inhibitors known to restrain the activity of the transcription factor, E2Fa. Therefore, we conclude that, in contrast to their specific roles in cortex/endodermis differentiation and stem cell maintenance in the root, SHR and SCR primarily function as general regulators of cell proliferation in leaves.

Published
2010

15. PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root

Author

Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes, Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia, Ministerio de Ciencia e Innovación, European Regional Development Fund, Consejo Superior de Investigaciones Científicas, Antoni-Alandes, Regina, González Guzmán, Miguel, Rodriguez, Lesia, Peirats-Llobet, Marta, Pizzio Bianchi, Gaston Alfredo, Fernández, Maria A., De Winne, Nancy, De Jaeger, Geert, Dietrich, Daniela, Bennett, Malcolm J., Rodríguez Egea, Pedro Luís, Universitat Politècnica de València. Instituto Universitario Mixto de Biología Molecular y Celular de Plantas - Institut Universitari Mixt de Biologia Molecular i Cel·lular de Plantes, Universitat Politècnica de València. Departamento de Biotecnología - Departament de Biotecnologia, Ministerio de Ciencia e Innovación, European Regional Development Fund, Consejo Superior de Investigaciones Científicas, Antoni-Alandes, Regina, González Guzmán, Miguel, Rodriguez, Lesia, Peirats-Llobet, Marta, Pizzio Bianchi, Gaston Alfredo, Fernández, Maria A., De Winne, Nancy, De Jaeger, Geert, Dietrich, Daniela, Bennett, Malcolm J., and Rodríguez Egea, Pedro Luís

Abstract

[EN] Abscisic acid (ABA) signaling plays a critical role in regulating root growth and root system architecture. ABA-mediated growth promotion and root tropic response under water stress are key responses for plant survival under limiting water conditions. In this work, we have explored the role of Arabidopsis (Arabidopsis thaliana) PYRABACTIN RESISTANCE1 (PYR1)/PYR1-LIKE (PYL)/REGULATORY COMPONENTS OF ABA RECEPTORS for root ABA signaling. As a result, we discovered that PYL8 plays a nonredundant role for the regulation of root ABA sensitivity. Unexpectedly, given the multigenic nature and partial functional redundancy observed in the PYR/PYL family, the single pyl8 mutant showed reduced sensitivity to ABA-mediated root growth inhibition. This effect was due to the lack of PYL8-mediated inhibition of several clade A phosphatases type 2C (PP2Cs), since PYL8 interacted in vivo with at least five PP2Cs, namely HYPERSENSITIVE TO ABA1 (HAB1), HAB2, ABA-INSENSITIVE1 (ABI1), ABI2, and PP2CA/ABA-HYPERSENSITIVE GERMINATION3 as revealed by tandem affinity purification and mass spectrometry proteomic approaches. We also discovered that PYR/PYL receptors and clade A PP2Cs are crucial for the hydrotropic response that takes place to guide root growth far from regions with low water potential. Thus, an ABA-hypersensitive pp2c quadruple mutant showed enhanced hydrotropism, whereas an ABA-insensitive sextuple pyr/pyl mutant showed reduced hydrotropic response, indicating that ABA-dependent inhibition of PP2Cs by PYR/PYLs is required for the proper perception of a moisture gradient.

Published
2013

16. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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17. Systems analysis of auxin transport in the Arabidopsis root apex

Author

Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., Bennett, Malcolm J., Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., and Bennett, Malcolm J.

Abstract

Auxin is a key regulator of plant growth and development. Within the root tip, auxin distribution plays a crucial role specifying developmental zones and coordinating tropic responses. Determining how the organ-scale auxin pattern is regulated at the cellular scale is essential to understanding how these processes are controlled. In this study, we developed an auxin transport model based on actual root cell geometries and carrier subcellular localizations. We tested model predictions using the DII-VENUS auxin sensor in conjunction with state-of-the-art segmentation tools. Our study revealed that auxin efflux carriers alone cannot create the pattern of auxin distribution at the root tip and that AUX1/LAX influx carriers are also required. We observed that AUX1 in lateral root cap (LRC) and elongating epidermal cells greatly enhance auxin’s shootward flux, with this flux being predominantly through the LRC, entering the epidermal cells only as they enter the elongation zone. We conclude that the nonpolar AUX1/LAX influx carriers control which tissues have high auxin levels, whereas the polar PIN carriers control the direction of auxin transport within these tissues.

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18. Branching out in roots: uncovering form, function, and regulation

Author

Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., Bennett, Malcolm J., Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., and Bennett, Malcolm J.

Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.

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19. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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20. Systems analysis of auxin transport in the Arabidopsis root apex

Author

Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., Bennett, Malcolm J., Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., and Bennett, Malcolm J.

Abstract

Auxin is a key regulator of plant growth and development. Within the root tip, auxin distribution plays a crucial role specifying developmental zones and coordinating tropic responses. Determining how the organ-scale auxin pattern is regulated at the cellular scale is essential to understanding how these processes are controlled. In this study, we developed an auxin transport model based on actual root cell geometries and carrier subcellular localizations. We tested model predictions using the DII-VENUS auxin sensor in conjunction with state-of-the-art segmentation tools. Our study revealed that auxin efflux carriers alone cannot create the pattern of auxin distribution at the root tip and that AUX1/LAX influx carriers are also required. We observed that AUX1 in lateral root cap (LRC) and elongating epidermal cells greatly enhance auxin’s shootward flux, with this flux being predominantly through the LRC, entering the epidermal cells only as they enter the elongation zone. We conclude that the nonpolar AUX1/LAX influx carriers control which tissues have high auxin levels, whereas the polar PIN carriers control the direction of auxin transport within these tissues.

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21. Branching out in roots: uncovering form, function, and regulation

Author

Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., Bennett, Malcolm J., Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., and Bennett, Malcolm J.

Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.

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22. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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23. Systems analysis of auxin transport in the Arabidopsis root apex

Author

Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., Bennett, Malcolm J., Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., and Bennett, Malcolm J.

Abstract

Auxin is a key regulator of plant growth and development. Within the root tip, auxin distribution plays a crucial role specifying developmental zones and coordinating tropic responses. Determining how the organ-scale auxin pattern is regulated at the cellular scale is essential to understanding how these processes are controlled. In this study, we developed an auxin transport model based on actual root cell geometries and carrier subcellular localizations. We tested model predictions using the DII-VENUS auxin sensor in conjunction with state-of-the-art segmentation tools. Our study revealed that auxin efflux carriers alone cannot create the pattern of auxin distribution at the root tip and that AUX1/LAX influx carriers are also required. We observed that AUX1 in lateral root cap (LRC) and elongating epidermal cells greatly enhance auxin’s shootward flux, with this flux being predominantly through the LRC, entering the epidermal cells only as they enter the elongation zone. We conclude that the nonpolar AUX1/LAX influx carriers control which tissues have high auxin levels, whereas the polar PIN carriers control the direction of auxin transport within these tissues.

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24. Branching out in roots: uncovering form, function, and regulation

Author

Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., Bennett, Malcolm J., Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., and Bennett, Malcolm J.

Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.

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25. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

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26. Systems analysis of auxin transport in the Arabidopsis root apex

Author

Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., Bennett, Malcolm J., Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., and Bennett, Malcolm J.

Abstract

Auxin is a key regulator of plant growth and development. Within the root tip, auxin distribution plays a crucial role specifying developmental zones and coordinating tropic responses. Determining how the organ-scale auxin pattern is regulated at the cellular scale is essential to understanding how these processes are controlled. In this study, we developed an auxin transport model based on actual root cell geometries and carrier subcellular localizations. We tested model predictions using the DII-VENUS auxin sensor in conjunction with state-of-the-art segmentation tools. Our study revealed that auxin efflux carriers alone cannot create the pattern of auxin distribution at the root tip and that AUX1/LAX influx carriers are also required. We observed that AUX1 in lateral root cap (LRC) and elongating epidermal cells greatly enhance auxin’s shootward flux, with this flux being predominantly through the LRC, entering the epidermal cells only as they enter the elongation zone. We conclude that the nonpolar AUX1/LAX influx carriers control which tissues have high auxin levels, whereas the polar PIN carriers control the direction of auxin transport within these tissues.

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27. Branching out in roots: uncovering form, function, and regulation

Author

Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., Bennett, Malcolm J., Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., and Bennett, Malcolm J.

Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.

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28. MtLAX2, a functional homologue of the Arabidopsis auxin influx transporter AUX1, is required for nodule organogenesis

Author

Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, Murray, Jeremy D., Roy, Sonali, Robson, Fran, Lilley, Jodi, Liu, Cheng-Wu, Cheng, Xiaofei, Wen, Jiangqi, Walker, Simon, Sun, Jongho, Cousins, Donna, Bone, Caitlin, Bennett, Malcolm J., Downie, J. Allan, Swarup, Ranjan, Oldroyd, Giles, and Murray, Jeremy D.

Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a. Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

Full Text
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29. Systems analysis of auxin transport in the Arabidopsis root apex

Author

Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., Bennett, Malcolm J., Band, Leah R., Wells, Darren M., Fozard, John A., Ghetiu, Teodor, French, Andrew P., Pound, Michael P., Wilson, Michael H., Yu, Lei, Li, Wenda, Hijazi, Hussein I., Oh, Jaesung, Pearce, Simon P., Perez-Amador, Miguel A., Yun, Jeonga, Kramer, Eric, Alonso, Jose M., Godin, Christophe, Vernoux, Teva, Hodgman, T. C., Pridmore, Tony P., Swarup, Ranjan, King, John R., and Bennett, Malcolm J.

Abstract

Auxin is a key regulator of plant growth and development. Within the root tip, auxin distribution plays a crucial role specifying developmental zones and coordinating tropic responses. Determining how the organ-scale auxin pattern is regulated at the cellular scale is essential to understanding how these processes are controlled. In this study, we developed an auxin transport model based on actual root cell geometries and carrier subcellular localizations. We tested model predictions using the DII-VENUS auxin sensor in conjunction with state-of-the-art segmentation tools. Our study revealed that auxin efflux carriers alone cannot create the pattern of auxin distribution at the root tip and that AUX1/LAX influx carriers are also required. We observed that AUX1 in lateral root cap (LRC) and elongating epidermal cells greatly enhance auxin’s shootward flux, with this flux being predominantly through the LRC, entering the epidermal cells only as they enter the elongation zone. We conclude that the nonpolar AUX1/LAX influx carriers control which tissues have high auxin levels, whereas the polar PIN carriers control the direction of auxin transport within these tissues.

Full Text
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30. Branching out in roots: uncovering form, function, and regulation

Author

Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., Bennett, Malcolm J., Atkinson, Jonathan A., Rasmussen, Amanda, Traini, Richard, Voss, Ute, Sturrock, Craig, Mooney, Sacha J., Wells, Darren M., and Bennett, Malcolm J.

Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research.

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31. Mechanistic insight into the role of AUXIN RESISTANCE4 in trafficking of AUXIN1 and LIKE AUX1-2.

Author

Tidy A, Abu Bakar N, Carrier D, Kerr ID, Hodgman C, Bennett MJ, and Swarup R

Subjects
Hydrolases metabolism, Indoleacetic Acids metabolism, Plant Proteins metabolism, Plant Roots genetics, Plant Roots metabolism, Arabidopsis genetics, Arabidopsis metabolism, Arabidopsis Proteins genetics, Arabidopsis Proteins metabolism
Abstract

AUXIN RESISTANCE4 (AXR4) regulates the trafficking of auxin influx carrier AUXIN1 (AUX1), a plasma-membrane protein that predominantly localizes to the endoplasmic reticulum (ER) in the absence of AXR4. In Arabidopsis (Arabidopsis thaliana), AUX1 is a member of a small multigene family comprising 4 highly conserved genes-AUX1, LIKE-AUX1 (LAX1), LAX2, and LAX3. We report here that LAX2 also requires AXR4 for correct localization to the plasma membrane. AXR4 is a plant-specific protein and contains a weakly conserved α/β hydrolase fold domain that is found in several classes of lipid hydrolases and transferases. We have previously proposed that AXR4 may either act as (i) a post-translational modifying enzyme through its α/β hydrolase fold domain or (ii) an ER accessory protein, which is a special class of ER protein that regulates targeting of their cognate partner proteins. Here, we show that AXR4 is unlikely to act as a post-translational modifying enzyme as mutations in several highly conserved amino acids in the α/β hydrolase fold domain can be tolerated and active site residues are missing. We also show that AUX1 and AXR4 physically interact with each other and that AXR4 reduces aggregation of AUX1 in a dose-dependent fashion. Our results suggest that AXR4 acts as an ER accessory protein. A better understanding of AXR4-mediated trafficking of auxin transporters in crop plants will be crucial for improving root traits (designer roots) for better acquisition of water and nutrients for sustainable and resilient agriculture., Competing Interests: Conflict of interest statement. None declared., (© The Author(s) 2023. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

Published
2023
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32. Modeling root loss reveals impacts on nutrient uptake and crop development.

Author

Schäfer ED, Owen MR, Band LR, Farcot E, Bennett MJ, and Lynch JP

Subjects
Plant Roots, Phosphorus pharmacology, Soil chemistry, Zea mays, Nutrients, Phaseolus, Hordeum genetics
Abstract

Despite the widespread prevalence of root loss in plants, its effects on crop productivity are not fully understood. While root loss reduces the capacity of plants to take up water and nutrients from the soil, it may provide benefits by decreasing the resources required to maintain the root system. Here, we simulated a range of root phenotypes in different soils and root loss scenarios for barley (Hordeum vulgare), common bean (Phaseolus vulgaris), and maize (Zea mays) using and extending the open-source, functional-structural root/soil simulation model OpenSimRoot. The model enabled us to quantify the impact of root loss on shoot dry weight in these scenarios and identify in which scenarios root loss is beneficial, detrimental, or has no effect. The simulations showed that root loss is detrimental for phosphorus uptake in all tested scenarios, whereas nitrogen uptake was relatively insensitive to root loss unless main root axes were lost. Loss of axial roots reduced shoot dry weight for all phenotypes in all species and soils, whereas lateral root loss had a smaller impact. In barley and maize plants with high lateral branching density that were not phosphorus-stressed, loss of lateral roots increased shoot dry weight. The fact that shoot dry weight increased due to root loss in these scenarios indicates that plants overproduce roots for some environments, such as those found in high-input agriculture. We conclude that a better understanding of the effects of root loss on plant development is an essential part of optimizing root system phenotypes for maximizing yield., (© The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists.)

Published
2022
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33. MtLAX2, a Functional Homologue of the Arabidopsis Auxin Influx Transporter AUX1, Is Required for Nodule Organogenesis.

Author

Roy S, Robson F, Lilley J, Liu CW, Cheng X, Wen J, Walker S, Sun J, Cousins D, Bone C, Bennett MJ, Downie JA, Swarup R, Oldroyd G, and Murray JD

Subjects
Biological Transport, Gene Expression Regulation, Plant, Gravitropism genetics, Indoleacetic Acids metabolism, Medicago truncatula metabolism, Medicago truncatula microbiology, Membrane Transport Proteins metabolism, Mutation, Plant Proteins metabolism, Plant Roots genetics, Plant Roots metabolism, Plants, Genetically Modified, Rhizobium physiology, Root Nodules, Plant metabolism, Root Nodules, Plant microbiology, Symbiosis genetics, Medicago truncatula genetics, Membrane Transport Proteins genetics, Plant Proteins genetics, Plant Root Nodulation genetics, Root Nodules, Plant genetics
Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2 , a paralogue of Arabidopsis ( Arabidopsis thaliana ) AUX1 , as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection., (© 2017 The author(s). All Rights Reserved.)

Published
2017
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34. Tonoplast Aquaporins Facilitate Lateral Root Emergence.

Author

Reinhardt H, Hachez C, Bienert MD, Beebo A, Swarup K, Voß U, Bouhidel K, Frigerio L, Schjoerring JK, Bennett MJ, and Chaumont F

Subjects
Aquaporins genetics, Arabidopsis genetics, Arabidopsis growth & development, Arabidopsis metabolism, Arabidopsis Proteins genetics, Biological Transport genetics, Gene Expression Profiling methods, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Meristem genetics, Meristem growth & development, Meristem metabolism, Microscopy, Confocal, Mutation, Plant Roots genetics, Plant Roots growth & development, Plants, Genetically Modified, Protein Isoforms genetics, Protein Isoforms metabolism, Reverse Transcriptase Polymerase Chain Reaction, Vacuoles genetics, Water metabolism, Aquaporins metabolism, Arabidopsis Proteins metabolism, Plant Roots metabolism, Vacuoles metabolism
Abstract

Aquaporins (AQPs) are water channels allowing fast and passive diffusion of water across cell membranes. It was hypothesized that AQPs contribute to cell elongation processes by allowing water influx across the plasma membrane and the tonoplast to maintain adequate turgor pressure. Here, we report that, in Arabidopsis (Arabidopsis thaliana), the highly abundant tonoplast AQP isoforms AtTIP1;1, AtTIP1;2, and AtTIP2;1 facilitate the emergence of new lateral root primordia (LRPs). The number of lateral roots was strongly reduced in the triple tip mutant, whereas the single, double, and triple tip mutants showed no or minor reduction in growth of the main root. This phenotype was due to the retardation of LRP emergence. Live cell imaging revealed that tight spatiotemporal control of TIP abundance in the tonoplast of the different LRP cells is pivotal to mediating this developmental process. While lateral root emergence is correlated to a reduction of AtTIP1;1 and AtTIP1;2 protein levels in LRPs, expression of AtTIP2;1 is specifically needed in a restricted cell population at the base, then later at the flanks, of developing LRPs. Interestingly, the LRP emergence phenotype of the triple tip mutants could be fully rescued by expressing AtTIP2;1 under its native promoter. We conclude that TIP isoforms allow the spatial and temporal fine-tuning of cellular water transport, which is critically required during the highly regulated process of LRP morphogenesis and emergence., (© 2016 American Society of Plant Biologists. All Rights Reserved.)

Published
2016
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35. The ASH1-RELATED3 SET-domain protein controls cell division competence of the meristem and the quiescent center of the Arabidopsis primary root.

Author

Kumpf R, Thorstensen T, Rahman MA, Heyman J, Nenseth HZ, Lammens T, Herrmann U, Swarup R, Veiseth SV, Emberland G, Bennett MJ, De Veylder L, and Aalen RB

Subjects
Arabidopsis cytology, Arabidopsis Proteins genetics, DNA Replication, DNA, Plant biosynthesis, Mutation, S Phase, Arabidopsis physiology, Arabidopsis Proteins physiology, Cell Division physiology, Meristem cytology, Plant Roots cytology
Abstract

The stem cell niche of the Arabidopsis (Arabidopsis thaliana) primary root apical meristem is composed of the quiescent (or organizing) center surrounded by stem (initial) cells for the different tissues. Initial cells generate a population of transit-amplifying cells that undergo a limited number of cell divisions before elongating and differentiating. It is unclear whether these divisions occur stochastically or in an orderly manner. Using the thymidine analog 5-ethynyl-2'-deoxyuridine to monitor DNA replication of cells of Arabidopsis root meristems, we identified a pattern of two, four, and eight neighboring cells with synchronized replication along the cortical, epidermal, and endodermal cell files, suggested to be daughters, granddaughters, and great-granddaughters of the direct progeny of each stem cell. Markers of mitosis and cytokinesis were not present in the region closest to the transition zone where the cells start to elongate, suggesting that great-granddaughter cells switch synchronously from the mitotic cell cycle to endoreduplication. Mutations in the stem cell niche-expressed ASH1-RELATED3 (ASHR3) gene, encoding a SET-domain protein conferring histone H3 lysine-36 methylation, disrupted this pattern of coordinated DNA replication and cell division and increased the cell division rate in the quiescent center. E2Fa/E2Fb transcription factors controlling the G1-to-S-phase transition regulate ASHR3 expression and bind to the ASHR3 promoter, substantiating a role for ASHR3 in cell division control. The reduced length of the root apical meristem and primary root of the mutant ashr3-1 indicate that synchronization of replication and cell divisions is required for normal root growth and development., (© 2014 American Society of Plant Biologists. All Rights Reserved.)

Published
2014
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36. Branching out in roots: uncovering form, function, and regulation.

Author

Atkinson JA, Rasmussen A, Traini R, Voß U, Sturrock C, Mooney SJ, Wells DM, and Bennett MJ

Subjects
Arabidopsis growth & development, Arabidopsis physiology, Edible Grain growth & development, Edible Grain physiology, Morphogenesis, Plant Roots growth & development, Terminology as Topic, Plant Roots physiology
Abstract

Root branching is critical for plants to secure anchorage and ensure the supply of water, minerals, and nutrients. To date, research on root branching has focused on lateral root development in young seedlings. However, many other programs of postembryonic root organogenesis exist in angiosperms. In cereal crops, the majority of the mature root system is composed of several classes of adventitious roots that include crown roots and brace roots. In this Update, we initially describe the diversity of postembryonic root forms. Next, we review recent advances in our understanding of the genes, signals, and mechanisms regulating lateral root and adventitious root branching in the plant models Arabidopsis (Arabidopsis thaliana), maize (Zea mays), and rice (Oryza sativa). While many common signals, regulatory components, and mechanisms have been identified that control the initiation, morphogenesis, and emergence of new lateral and adventitious root organs, much more remains to be done. We conclude by discussing the challenges and opportunities facing root branching research., (© 2014 American Society of Plant Biologists. All Rights Reserved.)

Published
2014
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37. Root systems biology: integrative modeling across scales, from gene regulatory networks to the rhizosphere.

Author

Hill K, Porco S, Lobet G, Zappala S, Mooney S, Draye X, and Bennett MJ

Subjects
Gene Regulatory Networks genetics, Models, Biological, Plant Roots genetics, Rhizosphere, Systems Biology
Abstract

Genetic and genomic approaches in model organisms have advanced our understanding of root biology over the last decade. Recently, however, systems biology and modeling have emerged as important approaches, as our understanding of root regulatory pathways has become more complex and interpreting pathway outputs has become less intuitive. To relate root genotype to phenotype, we must move beyond the examination of interactions at the genetic network scale and employ multiscale modeling approaches to predict emergent properties at the tissue, organ, organism, and rhizosphere scales. Understanding the underlying biological mechanisms and the complex interplay between systems at these different scales requires an integrative approach. Here, we describe examples of such approaches and discuss the merits of developing models to span multiple scales, from network to population levels, and to address dynamic interactions between plants and their environment.

Published
2013
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38. RootNav: navigating images of complex root architectures.

Author

Pound MP, French AP, Atkinson JA, Wells DM, Bennett MJ, and Pridmore T

Subjects
Algorithms, Arabidopsis anatomy & histology, Brassica napus anatomy & histology, Meristem anatomy & histology, Oryza anatomy & histology, Plant Roots physiology, Seeds growth & development, Triticum anatomy & histology, User-Computer Interface, Image Processing, Computer-Assisted methods, Plant Roots anatomy & histology, Software
Abstract

We present a novel image analysis tool that allows the semiautomated quantification of complex root system architectures in a range of plant species grown and imaged in a variety of ways. The automatic component of RootNav takes a top-down approach, utilizing the powerful expectation maximization classification algorithm to examine regions of the input image, calculating the likelihood that given pixels correspond to roots. This information is used as the basis for an optimization approach to root detection and quantification, which effectively fits a root model to the image data. The resulting user experience is akin to defining routes on a motorist's satellite navigation system: RootNav makes an initial optimized estimate of paths from the seed point to root apices, and the user is able to easily and intuitively refine the results using a visual approach. The proposed method is evaluated on winter wheat (Triticum aestivum) images (and demonstrated on Arabidopsis [Arabidopsis thaliana], Brassica napus, and rice [Oryza sativa]), and results are compared with manual analysis. Four exemplar traits are calculated and show clear illustrative differences between some of the wheat accessions. RootNav, however, provides the structural information needed to support extraction of a wider variety of biologically relevant measures. A separate viewer tool is provided to recover a rich set of architectural traits from RootNav's core representation.

Published
2013
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39. Short-Root regulates primary, lateral, and adventitious root development in Arabidopsis.

Author

Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, Lake D, Peret B, Zappala S, Mairhofer S, Whitworth M, Wang J, Ljung K, Marchant A, Sandberg G, Holdsworth MJ, Palme K, Pridmore T, Mooney S, and Bennett MJ

Subjects
Arabidopsis cytology, Arabidopsis ultrastructure, Arabidopsis Proteins genetics, Body Patterning, Cell Division, Germination, Indoleacetic Acids metabolism, Membrane Transport Proteins metabolism, Mutation genetics, Plant Roots cytology, Plant Roots ultrastructure, Transcription Factors genetics, Arabidopsis growth & development, Arabidopsis Proteins metabolism, Plant Roots growth & development, Transcription Factors metabolism
Abstract

Short-Root (SHR) is a well-characterized regulator of radial patterning and indeterminacy of the Arabidopsis (Arabidopsis thaliana) primary root. However, its role during the elaboration of root system architecture remains unclear. We report that the indeterminate wild-type Arabidopsis root system was transformed into a determinate root system in the shr mutant when growing in soil or agar. The root growth behavior of the shr mutant results from its primary root apical meristem failing to initiate cell division following germination. The inability of shr to reactivate mitotic activity in the root apical meristem is associated with the progressive reduction in the abundance of auxin efflux carriers, PIN-FORMED1 (PIN1), PIN2, PIN3, PIN4, and PIN7. The loss of primary root growth in shr is compensated by the activation of anchor root primordia, whose tissues are radially patterned like the wild type. However, SHR function is not restricted to the primary root but is also required for the initiation and patterning of lateral root primordia. In addition, SHR is necessary to maintain the indeterminate growth of lateral and anchor roots. We conclude that SHR regulates a wide array of Arabidopsis root-related developmental processes.

Published
2011
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40. Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules.

Author

Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Péret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, and Laplaze L

Subjects
Carrier Proteins metabolism, Computational Biology, Gene Expression Profiling, Magnoliopsida genetics, Magnoliopsida microbiology, Models, Biological, Molecular Sequence Data, Plant Proteins metabolism, Frankia, Indoleacetic Acids metabolism, Magnoliopsida metabolism, Root Nodules, Plant metabolism, Symbiosis
Abstract

Actinorhizal symbioses are mutualistic interactions between plants and the soil bacteria Frankia that lead to the formation of nitrogen-fixing root nodules. Little is known about the signaling mechanisms controlling the different steps of the establishment of the symbiosis. The plant hormone auxin has been suggested to play a role. Here we report that auxin accumulates within Frankia-infected cells in actinorhizal nodules of Casuarina glauca. Using a combination of computational modeling and experimental approaches, we establish that this localized auxin accumulation is driven by the cell-specific expression of auxin transporters and by Frankia auxin biosynthesis in planta. Our results indicate that the plant actively restricts auxin accumulation to Frankia-infected cells during the symbiotic interaction.

Published
2010
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41. SHORT-ROOT and SCARECROW regulate leaf growth in Arabidopsis by stimulating S-phase progression of the cell cycle.

Author

Dhondt S, Coppens F, De Winter F, Swarup K, Merks RM, Inzé D, Bennett MJ, and Beemster GT

Subjects
Arabidopsis metabolism, Arabidopsis Proteins genetics, Cell Division, Gene Expression Regulation, Plant, Mutation, Oligonucleotide Array Sequence Analysis, Plant Roots growth & development, RNA, Plant genetics, Transcription Factors genetics, Arabidopsis genetics, Arabidopsis Proteins metabolism, Plant Leaves growth & development, S Phase, Transcription Factors metabolism
Abstract

SHORT-ROOT (SHR) and SCARECROW (SCR) are required for stem cell maintenance in the Arabidopsis (Arabidopsis thaliana) root meristem, ensuring its indeterminate growth. Mutation of SHR and SCR genes results in disorganization of the quiescent center and loss of stem cell activity, resulting in the cessation of root growth. This paper reports on the role of SHR and SCR in the development of leaves, which, in contrast to the root, have a determinate growth pattern and lack a persistent stem cell niche. Our results demonstrate that inhibition of leaf growth in shr and scr mutants is not a secondary effect of the compromised root development but is caused by an effect on cell division in the leaves: a reduced cell division rate and early exit of the proliferation phase. Consistent with the observed cell division phenotype, the expression of SHR and SCR genes in leaves is closely associated with cell division activity in most cell types. The increased cell cycle duration is due to a prolonged S-phase duration, which is mediated by up-regulation of cell cycle inhibitors known to restrain the activity of the transcription factor, E2Fa. Therefore, we conclude that, in contrast to their specific roles in cortex/endodermis differentiation and stem cell maintenance in the root, SHR and SCR primarily function as general regulators of cell proliferation in leaves.

Published
2010
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42. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants.

Author

Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, and White PJ

Subjects
Arabidopsis metabolism, Arabidopsis Proteins genetics, Base Sequence, DNA Primers, DNA, Complementary genetics, Genetic Markers, Glucuronidase genetics, Plant Shoots metabolism, Polymerase Chain Reaction methods, Trace Elements metabolism, Arabidopsis genetics, Arabidopsis growth & development, Gene Expression Regulation, Plant, Phosphates metabolism
Abstract

Our aim was to generate and prove the concept of "smart" plants to monitor plant phosphorus (P) status in Arabidopsis. Smart plants can be genetically engineered by transformation with a construct containing the promoter of a gene up-regulated specifically by P starvation in an accessible tissue upstream of a marker gene such as beta-glucuronidase (GUS). First, using microarrays, we identified genes whose expression changed more than 2.5-fold in shoots of plants growing hydroponically when P, but not N or K, was withheld from the nutrient solution. The transient changes in gene expression occurring immediately (4 h) after P withdrawal were highly variable, and many nonspecific, shock-induced genes were up-regulated during this period. However, two common putative cis-regulatory elements (a PHO-like element and a TATA box-like element) were present significantly more often in the promoters of genes whose expression increased 4 h after the withdrawal of P compared with their general occurrence in the promoters of all genes represented on the microarray. Surprisingly, the expression of only four genes differed between shoots of P-starved and -replete plants 28 h after P was withdrawn. This lull in differential gene expression preceded the differential expression of a new group of 61 genes 100 h after withdrawing P. A literature survey indicated that the expression of many of these "late" genes responded specifically to P starvation. Shoots had reduced P after 100 h, but growth was unaffected. The expression of SQD1, a gene involved in the synthesis of sulfolipids, responded specifically to P starvation and was increased 100 h after withdrawing P. Leaves of Arabidopsis bearing a SQD1::GUS construct showed increased GUS activity after P withdrawal, which was detectable before P starvation limited growth. Hence, smart plants can monitor plant P status. Transferring this technology to crops would allow precision management of P fertilization, thereby maintaining yields while reducing costs, conserving natural resources, and preventing pollution.

Published
2003
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