Arabidopsis RING E3 Ligase XBAT32 Regulates Lateral Root Production through Its Role in Ethylene Biosynthesis

Prasad, Madhulika Esther; Schofield, Andrew Craig; Lyzenga, Wendy J.; Liu, Hongxia; Stone, Sophia L.

doi:10.1104/pp.110.156976

Cited by 97 publications

(98 citation statements)

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“…et al, 2008, Figure 5I; Li et al, 2009, Figure 2G; Effendi et al, 2011, Figures 2A and 2B;Prasad et al, 2010, Figures 1A and 3). Even when both the data on primary root length and LR (and/or LRP) number or data on LR and LRP numbers are given (Swarup et al, 2008, Supplemental Figures 1D and 1E;Li et al, 2009, Figures 2F and 2G;Jiang et al, 2010, Figure 4B; Moreno-Risueno et al, 2010, Figure 4B; Ortiz-Castro et al, 2011, Figure 1E), one cannot explicitly understand whether a mutation or a treatment affects LR initiation when the data on LRP density and on the length of branching zone are not present.…”

Section: Are Numbers Of Lrs or Lrps Per Parent Root Useful Parameters?mentioning

confidence: 93%

Quantitative Analysis of Lateral Root Development: Pitfalls and How to Avoid Them

2012

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The advent of the postgenomics era has led to increased interest in exploring the role of gene networks and signaling pathways in controlling plant development. The last two decades have seen a particular increase in the number of studies focusing on the development of the Arabidopsis thaliana root system. However, the investigation of such a seemingly simple system as an Arabidopsis root can lead to problems in quantification and errors in interpretation if knowledge of root organization is lacking. In this article, we identify a number of these problems and give examples of potentially erroneous and correct determinations of lateral root parameters. Our aim is to bring this important issue to the attention of the plant science community and to suggest ways in which the problems inherent in quantifying the process of lateral root development can be avoided.The importance of root development in plant biology arises not only from the crucial role that roots play in supporting plant growth and crop productivity but also because the root is a convenient model for studies of plant development. Root system architecture is an integrative result of lateral root (LR) initiation, morphogenesis, emergence, and growth. Thus LR development is fundamental to the way in which a plant elaborates its root system to explore the soil volume. Despite recent progress in this area (Pé ret et al., 2009;Fukaki and Tasaka, 2009;Benková and Bielach, 2010;Ingram and Malamy, 2010), we are far from understanding how the multistage process of LR development is controlled during plant ontogenesis and how its complex responses to multiple intrinsic and extrinsic factors are integrated. It is axiomatic that improving our understanding of these problems depends on the proper quantitative analysis of the process of LR development. In this Commentary, we address the problems of LR quantification solely from a developmental perspective, considering how LR formation is evaluated in an individual parent root. We do not consider studies that approach root system development from ecological, root-soil-continuum, or highthroughput phenotyping perspectives (for example, Dupuy et al., 2005Dupuy et al., , 2010Trachsel et al., 2011).We have seen greatly increasing attention directed toward root development over the past 20 years. A bibliographic search on the term "lateral roots" in Web of Science from Thomson Reuters during the period 1990 to 2010 produced a total of 2619 documents and showed a 12-fold increase in publications in the last 21 years (19 publications in 1990 compared with 238 in 2010). This enhanced number of studies of root development has involved many plant biologists whose field of expertise is not root biology or plant development. As a consequence, it is our observation that many studies suffer from one or a number of inaccuracies or elementary errors in quantification of LR formation. This prompted us to write this Commentary with the aim of illustrating how an elementary error can lead to uncertain or misleading conclusions about ro...

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Section: Are Numbers Of Lrs or Lrps Per Parent Root Useful Parameters?mentioning

confidence: 93%

Quantitative Analysis of Lateral Root Development: Pitfalls and How to Avoid Them

2012

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“…2A; . Similar to the recognition of TOE motifs by ETO/ EOL proteins, XBAT recognition of ACS7 can be reconstituted in a yeast two-hybrid assay and in vitro, and has been assayed using N-terminally tagged ACS7 constructs (Prasad et al, 2010;. Interestingly, though, turnover of a C-terminally epitopetagged ACS7 requires a motif contained within the 14 N-terminal amino acids (ACS7-N 14 ; Xiong et al, 2014).…”

Section: Phosphorylation and Proteasome-mediated Degradation: Leitmotmentioning

confidence: 99%

“…Interestingly, cell-free degradation assays show that XBAT32 not only regulates ACS7 (type 3) stability, but also promotes turnover of ACS4 (Prasad et al, 2010;, a type 2 isozyme that is a predicted ETO1 target (Chae et al, 2003;Wang et al, 2004;Gingerich et al, 2005;Yoshida et al, 2005;Christians et al, 2009). In addition to its C-terminal TOE motif (Yoshida et al, 2006;Christians et al, 2009), ACS4 also carries a destabilizing N-terminal sequence (Schlögelhofer and Bachmair, 2002).…”

Section: Newly Identified Posttranslational Mechanisms Regulate Multimentioning

confidence: 99%

Producing the Ethylene Signal: Regulation and Diversification of Ethylene Biosynthetic Enzymes

Booker

DeLong

2015

Plant Physiology

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Strictly controlled production of ethylene gas lies upstream of the signaling activities of this crucial regulator throughout the plant life cycle. Although the biosynthetic pathway is enzymatically simple, the regulatory circuits that modulate signal production are fine tuned to allow integration of responses to environmental and intrinsic cues. Recently identified posttranslational mechanisms that control ethylene production converge on one family of biosynthetic enzymes and overlay several independent reversible phosphorylation events and distinct mediators of ubiquitin-dependent protein degradation. Although the core pathway is conserved throughout seed plants, these posttranslational regulatory mechanisms may represent evolutionarily recent innovations. The evolutionary origins of the pathway and its regulators are not yet clear; outside the seed plants, numerous biochemical and phylogenetic questions remain to be addressed.

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“…By contrast, elevated numbers of lateral roots are produced by ethylene resistant 1 (etr1; also known as ein1) and Never-ripe (Nr) (Negi et al, 2008;Negi et al, 2010), which are dominantnegative ethylene receptor mutations in Arabidopsis and tomato, respectively (Hua et al, 1998;Wilkinson et al, 1995;Yen et al, 1995), and ethylene insensitive 2 (ein2), which causes a defect in an ethylene signaling protein (Alonso et al, 1999). XBAT32, an E3 ubiquitin ligase that functions in proteolysis, increases lateral root number by reducing the abundance of two ACC synthase isoenzymes that function in ethylene biosynthesis (Prasad et al, 2010). Ethylene affects root branching at the earliest stages of lateral root initiation and alters auxin transport, suggesting that cross talk with auxin might regulate ACC repression of root branching (Negi et al, 2008;Negi et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers

et al. 2011

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SUMMARYWe used genetic and molecular approaches to identify mechanisms by which the gaseous plant hormone ethylene reduces lateral root formation and enhances polar transport of the hormone auxin. Arabidopsis thaliana mutants, aux1, lax3, pin3 and pin7, which are defective in auxin influx and efflux proteins, were less sensitive to the inhibition of lateral root formation and stimulation of auxin transport following treatment with the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC). By contrast, pin2 and abcb19 mutants exhibited wild-type ACC responses. ACC and indole-3-acetic acid (IAA) increased the abundance of transcripts encoding auxin transport proteins in an ETR1 and EIN2 (ethylene signaling)-dependent and TIR1 (auxin receptor)-dependent fashion, respectively. The effects of ACC on these transcripts and on lateral root development were still present in the tir1 mutant, suggesting independent signaling networks. ACC increased auxin-induced gene expression in the root apex, but decreased expression in regions where lateral roots form and reduced free IAA in whole roots. The ethylene synthesis inhibitor aminoethoxyvinylglycine (AVG) had opposite effects on auxin-dependent gene expression. These results suggest that ACC affects root development by altering auxin distribution. PIN3-and PIN7-GFP fluorescence was increased or decreased after ACC or AVG treatment, respectively, consistent with the role of PIN3 and PIN7 in ACC-elevated transport. ACC treatment abolished a localized depletion of fluorescence of PIN3-and PIN7-GFP, normally found below the site of primordia formation. These results suggest that ACC treatment increased PIN3 and PIN7 expression, resulting in elevated auxin transport, which prevented the localized accumulation of auxin needed to drive lateral root formation.

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Arabidopsis RING E3 Ligase XBAT32 Regulates Lateral Root Production through Its Role in Ethylene Biosynthesis

Cited by 97 publications

References 69 publications

Quantitative Analysis of Lateral Root Development: Pitfalls and How to Avoid Them

Quantitative Analysis of Lateral Root Development: Pitfalls and How to Avoid Them

Producing the Ethylene Signal: Regulation and Diversification of Ethylene Biosynthetic Enzymes

Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers

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