Publications by authors named "Jocelyn E Malamy"

8 Publications

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In vivo imaging of epithelial wound healing in the cnidarian Clytia hemisphaerica demonstrates early evolution of purse string and cell crawling closure mechanisms.

BMC Dev Biol 2017 12 19;17(1):17. Epub 2017 Dec 19.

Department of Molecular Genetics and Cell Biology, The University of Chicago, 929 East 57th Street, Chicago, IL, 60637, USA.

Background: All animals have mechanisms for healing damage to the epithelial sheets that cover the body and line internal cavities. Epithelial wounds heal either by cells crawling over the wound gap, by contraction of a super-cellular actin cable ("purse string") that surrounds the wound, or some combination of the two mechanisms. Both cell crawling and purse string closure of epithelial wounds are widely observed across vertebrates and invertebrates, suggesting early evolution of these mechanisms. Cnidarians evolved ~600 million years ago and are considered a sister group to the Bilateria. They have been much studied for their tremendous regenerative potential, but epithelial wound healing has not been characterized in detail. Conserved elements of wound healing in bilaterians and cnidarians would suggest an evolutionary origin in a common ancestor. Here we test this idea by characterizing epithelial wound healing in live medusae of Clytia hemisphaerica.

Results: We identified cell crawling and purse string-mediated mechanisms of healing in Clytia epithelium that appear highly analogous of those seen in higher animals, suggesting that these mechanisms may have emerged in a common ancestor. Interestingly, we found that epithelial wound healing in Clytia is 75 to >600 times faster than in cultured cells or embryos of other animals previously studied, suggesting that Clytia may provide valuable clues about optimized healing efficiency. Finally, in Clytia, we show that damage to the basement membrane in a wound gap causes a rapid shift between the cell crawling and purse string mechanisms for wound closure. This is consistent with work in other systems showing that cells marginal to a wound choose between a super-cellular actin cable or lamellipodia formation to close wounds, and suggests a mechanism underlying this decision.

Conclusions: 1. Cell crawling and purse string mechanisms of epithelial wound healing likely evolved before the divergence of Cnidaria from the bilaterian lineage ~ 600mya 2. In Clytia, the choice between cell crawling and purse string mechanisms of wound healing depends on interactions between the epithelial cells and the basement membrane.
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http://dx.doi.org/10.1186/s12861-017-0160-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5735930PMC
December 2017

Cell wall properties play an important role in the emergence of lateral root primordia from the parent root.

J Exp Bot 2014 May 11;65(8):2057-69. Epub 2014 Mar 11.

Department of Molecular Genetics and Cell Biology, The University of Chicago, Gordon Center for Integrative Science W519, 929 East 57th Street, Chicago, IL 60637, USA.

Plants adapt to their unique soil environments by altering the number and placement of lateral roots post-embryonic. Mutants were identified in Arabidopsis thaliana that exhibit increased lateral root formation. Eight mutants were characterized in detail and were found to have increased lateral root formation due to at least three distinct mechanisms. The causal mutation in one of these mutants was found in the XEG113 gene, recently shown to be involved in plant cell wall biosynthesis. Lateral root primordia initiation is unaltered in this mutant. In contrast, synchronization of lateral root initiation demonstrated that mutation of XEG113 increases the rate at which lateral root primordia develop and emerge to form lateral roots. The effect of the XEG113 mutation was specific to the root system and had no apparent effect on shoot growth. Screening of 17 additional cell wall mutants, altering a myriad of cell wall components, revealed that many (but not all) types of cell wall defects promote lateral root formation. These results suggest that proper cell wall biosynthesis is necessary to constrain lateral root primordia emergence. While previous reports have shown that lateral root emergence is accompanied by active remodelling of cell walls overlying the primordia, this study is the first to demonstrate that alteration of the cell wall is sufficient to promote lateral root formation. Therefore, inherent cell wall properties may play a previously unappreciated role in regulation of root system architecture.
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http://dx.doi.org/10.1093/jxb/eru056DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3991740PMC
May 2014

Dissecting the effects of nitrate, sucrose and osmotic potential on Arabidopsis root and shoot system growth in laboratory assays.

Philos Trans R Soc Lond B Biol Sci 2012 Jun;367(1595):1489-500

Department of Molecular Genetics and Cell Biology, Gordon Center for Integrative Sciences W519, University of Chicago, 929 East 57th Street, Chicago, IL 60637, USA.

Studying the specific effects of water and nutrients on plant development is difficult because changes in a single component can often trigger multiple response pathways. Such confounding issues are prevalent in commonly used laboratory assays. For example, increasing the nitrate concentration in growth media alters both nitrate availability and osmotic potential. In addition, it was recently shown that a change in the osmotic potential of media alters the plant's ability to take up other nutrients such as sucrose. It can also be difficult to identify the initial target tissue of a particular environmental cue because there are correlated changes in development of many organs. These growth changes may be coordinately regulated, or changes in development of one organ may trigger changes in development of another organ as a secondary effect. All these complexities make analyses of plant responses to environmental factors difficult to interpret. Here, we review the literature on the effects of nitrate, sucrose and water availability on root system growth and discuss the mechanisms underlying these effects. We then present experiments that examine the impact of nitrate, sucrose and water on root and shoot system growth in culture using an approach that holds all variables constant except the one under analysis. We found that while all three factors also alter root system size, changes in sucrose and osmotic potential also altered shoot system size. In contrast, we found that, when osmotic effects are controlled, nitrate specifically inhibits root system growth while having no effect on shoot system growth. This effectively decreases the root : shoot ratio. Alterations in root : shoot ratio have been widely observed in response to nitrogen starvation, where root growth is selectively increased, but the present results suggest that alterations in this ratio can be triggered across a wide spectrum of nitrate concentrations.
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http://dx.doi.org/10.1098/rstb.2011.0230DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3321681PMC
June 2012

Arabidopsis Lateral Root Development 3 is essential for early phloem development and function, and hence for normal root system development.

Plant J 2011 Nov 19;68(3):455-67. Epub 2011 Aug 19.

Department of Molecular Genetics and Cell Biology, The University of Chicago, 5812 S. Ellis Street, Chicago, IL 60637, USA.

We have identified a gene, Lateral Root Development 3 (LRD3), that is important for maintaining a balance between primary and lateral root growth. The lrd3 mutant has decreased primary root growth and increased lateral root growth. We determined that the LRD3 gene encodes a LIM-domain protein of unknown function. LRD3 is expressed only in the phloem companion cells, which suggested a role in phloem function. Indeed, while phloem loading and export from the shoot appear to be normal, delivery of phloem to the primary root tip is limited severely in young seedlings. Abnormalities in phloem morphology in these seedlings indicate that LRD3 is essential for correct early phloem development. There is a subsequent spontaneous recovery of normal phloem morphology, which is correlated tightly with increased phloem delivery and growth of the primary root. The LRD3 gene is one of very few genes described to affect phloem development, and the only one that is specific to early phloem development. Continuous growth on auxin also leads to recovery of phloem development and function in lrd3, which demonstrates that auxin plays a key role in early phloem development. The root system architecture and the pattern of phloem allocation in the lrd3 root system suggested that there may be regulated mechanisms for selectively supporting certain lateral roots when the primary root is compromised. Therefore, this study provides new insights into phloem-mediated resource allocation and its effects on plant root system architecture.
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http://dx.doi.org/10.1111/j.1365-313X.2011.04700.xDOI Listing
November 2011

Root system architecture in Arabidopsis grown in culture is regulated by sucrose uptake in the aerial tissues.

Plant Cell 2008 Oct 24;20(10):2643-60. Epub 2008 Oct 24.

Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, Illinois 60637, USA.

This article presents a detailed model for the regulation of lateral root formation in Arabidopsis thaliana seedlings grown in culture. We demonstrate that direct contact between the aerial tissues and sucrose in the growth media is necessary and sufficient to promote emergence of lateral root primordia from the parent root. Mild osmotic stress is perceived by the root, which then sends an abscisic acid-dependent signal that causes a decrease in the permeability of aerial tissues; this reduces uptake of sucrose from the culture media, which leads to a repression of lateral root formation. Osmotic repression of lateral root formation in culture can be overcome by mutations that cause the cuticle of a plant's aerial tissues to become more permeable. Indeed, we report here that the previously described lateral root development2 mutant overcomes osmotic repression of lateral root formation because of a point mutation in Long Chain Acyl-CoA Synthetase2, a gene essential for cutin biosynthesis. Together, our findings (1) impact the interpretation of experiments that use Arabidopsis grown in culture to study root system architecture; (2) identify sucrose as an unexpected regulator of lateral root formation; (3) demonstrate mechanisms by which roots communicate information to aerial tissues and receive information in turn; and (4) provide insights into the regulatory pathways that allow plants to be developmentally plastic while preserving the essential balance between aboveground and belowground organs.
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http://dx.doi.org/10.1105/tpc.107.055475DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2590740PMC
October 2008

The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues.

Proc Natl Acad Sci U S A 2005 Sep 12;102(38):13693-8. Epub 2005 Sep 12.

Department of Molecular Genetics and Cell Biology, University of Chicago, 1103 East 57th Street, Chicago, IL 60637, USA.

Lateral root initiation is strongly repressed in Arabidopsis by the combination of high external sucrose and low external nitrate. A previously isolated mutant, lin1, can overcome this repression. Here, we show that lin1 carries a missense mutation in the NRT2.1 gene. Several allelic mutants, including one in which the NRT2.1 gene is completely deleted, show similar phenotypes to lin1 and fail to complement lin1. NRT2.1 encodes a putative high-affinity nitrate transporter that functions at low external nitrate concentrations. Direct measurement of nitrate uptake and nitrate content in the lin1 mutant seedlings established that both are indeed reduced. Because repression of lateral root initiation in WT plants can be relieved by increased concentrations of external nitrate, it is surprising to find that repression is also relieved by a defect in a component of the high-affinity nitrate uptake system. Furthermore, lateral root initiation is increased in lin1 relative to WT even when seedlings are grown on nitrate-free media, suggesting that the mutant phenotype is nitrate-independent. These results indicate that NRT2.1 is a repressor of lateral root initiation and that this role is independent of nitrate uptake. We propose that Arabidopsis NRT2.1 acts either as a nitrate sensor or signal transducer to coordinate the development of the root system with nutritional cues.
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http://dx.doi.org/10.1073/pnas.0504219102DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1224627PMC
September 2005

Identification of quantitative trait loci that regulate Arabidopsis root system size and plasticity.

Genetics 2006 Jan 12;172(1):485-98. Epub 2005 Sep 12.

Molecular Genetics and Cell Biology Department, The University of Chicago, Chicago, Illinois 60637, USA.

Root system size (RSS) is a complex trait that is greatly influenced by environmental cues. Hence, both intrinsic developmental pathways and environmental-response pathways contribute to RSS. To assess the natural variation in both types of pathways, we examined the root systems of the closely related Arabidopsis ecotypes Landsberg erecta (Ler) and Columbia (Col) grown under mild osmotic stress conditions. We found that Ler initiates more lateral root primordia, produces lateral roots from a higher percentage of these primordia, and has an overall larger root system than Col under these conditions. Furthermore, although each of these parameters is reduced by osmotic stress in both ecotypes, Ler shows a decreased sensitivity to osmotica. To understand the genetic basis for these differences, QTL for RSS under mild osmotic stress were mapped in a Ler x Col recombinant inbred population. Two robust quantitative trait loci (QTL) were identified and confirmed in near-isogenic lines (NILs). The NILs also allowed us to define distinct physiological roles for the gene(s) at each locus. This study provides insight into the genetic and physiological complexity that determines RSS and begins to dissect the molecular basis for naturally occurring differences in morphology and developmental plasticity in the root system.
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http://dx.doi.org/10.1534/genetics.105.047555DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1456176PMC
January 2006

Transcriptional profile of the Arabidopsis root quiescent center.

Plant Cell 2005 Jul 3;17(7):1908-25. Epub 2005 Jun 3.

Department of Biology, Duke University, Durham, North Carolina 27708, USA.

The self-renewal characteristics of stem cells render them vital engines of development. To better understand the molecular mechanisms that determine the properties of stem cells, transcript profiling was conducted on quiescent center (QC) cells from the Arabidopsis thaliana root meristem. The AGAMOUS-LIKE 42 (AGL42) gene, which encodes a MADS box transcription factor whose expression is enriched in the QC, was used to mark these cells. RNA was isolated from sorted cells, labeled, and hybridized to Affymetrix microarrays. Comparisons with digital in situ expression profiles of surrounding tissues identified a set of genes enriched in the QC. Promoter regions from a subset of transcription factors identified as enriched in the QC conferred expression in the QC. These studies demonstrated that it is possible to successfully isolate and profile a rare cell type in the plant. Mutations in all enriched transcription factor genes including AGL42 exhibited no detectable root phenotype, raising the possibility of a high degree of functional redundancy in the QC.
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http://dx.doi.org/10.1105/tpc.105.031724DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1167541PMC
July 2005
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