The Aux/IAA gene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays L.) primary roots

Zhang, Yanxiang; Paschold, Anja; Marcon, Caroline; Liu, Sanzhen; Tai, Huanhuan; Nestler, Josefine; Yeh, Cheng‐Ting; Opitz, Nina; Lanz, Christa; Schnable, Patrick S.; Hochholdinger, Frank

doi:10.1093/jxb/eru249

Cited by 67 publications

(51 citation statements)

References 51 publications

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“…S3). Recently, we have also shown that the rootless with undetectable meristem1 mutant, which is defective in lateral root formation, displays significant inhibition of ubiquitindependent protein degradation and cell cycle/division processes (Zhang et al, 2014). Thus, our RNA-Seq results, together with the finding that SKP2B overexpression promotes KRP1 degradation in Arabidopsis (Ren et al, Figure 5.…”

Section: Local High Nitrate Promotes Auxin-mediated Cell Cycle Activasupporting

confidence: 77%

Cell Type-Specific Gene Expression Analyses by RNA Sequencing Reveal Local High Nitrate-Triggered Lateral Root Initiation in Shoot-Borne Roots of Maize by Modulating Auxin-Related Cell Cycle Regulation

Eggert

Wirén

et al. 2015

Plant Physiol.

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Plants have evolved a unique plasticity of their root system architecture to flexibly exploit heterogeneously distributed mineral elements from soil. Local high concentrations of nitrate trigger lateral root initiation in adult shoot-borne roots of maize (Zea mays) by increasing the frequency of early divisions of phloem pole pericycle cells. Gene expression profiling revealed that, within 12 h of local high nitrate induction, cell cycle activators (cyclin-dependent kinases and cyclin B) were up-regulated, whereas repressors (Kip-related proteins) were down-regulated in the pericycle of shoot-borne roots. In parallel, a ubiquitin protein ligase S-Phase Kinase-Associated Protein1-cullin-F-box protein S-Phase Kinase-Associated Protein 2B -related proteasome pathway participated in cell cycle control. The division of pericycle cells was preceded by increased levels of free indole-3-acetic acid in the stele, resulting in DR5-red fluorescent protein-marked auxin response maxima at the phloem poles. Moreover, laser-capture microdissectionbased gene expression analyses indicated that, at the same time, a significant local high nitrate induction of the monocot-specific PIN-FORMED9 gene in phloem pole cells modulated auxin efflux to pericycle cells. Time-dependent gene expression analysis further indicated that local high nitrate availability resulted in PIN-FORMED9-mediated auxin efflux and subsequent cell cycle activation, which culminated in the initiation of lateral root primordia. This study provides unique insights into how adult maize roots translate information on heterogeneous nutrient availability into targeted root developmental responses.

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Section: Local High Nitrate Promotes Auxin-mediated Cell Cycle Activasupporting

confidence: 77%

Cell Type-Specific Gene Expression Analyses by RNA Sequencing Reveal Local High Nitrate-Triggered Lateral Root Initiation in Shoot-Borne Roots of Maize by Modulating Auxin-Related Cell Cycle Regulation

Eggert

Wirén

et al. 2015

Plant Physiol.

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“…In line with the differentiation status of the stele, several GO terms involved in lignin biosynthesis (related to the bins cell wall and secondary metabolism) were overrepresented in this tissue (Supplemental Table S1). Lignin is deposited in the xylem elements of the stele to provide structural support (Vermerris et al, 2010;Zhang et al, 2014). In line with the overrepresentation of lignin biosynthesisrelated GO terms, six laccases (GRMZM2G146152_P01, GRMZM2G164467_P01, GRMZM5G814718_P01, GRMZM-2G367668_P01, GRMZM2G388587_P01, and GRMZM2-G305526_P01) were accumulated exclusively in the stele (Supplemental Data Sets S1 and S3).…”

Section: Discussionmentioning

confidence: 91%

A High-Resolution Tissue-Specific Proteome and Phosphoproteome Atlas of Maize Primary Roots Reveals Functional Gradients along the Root Axes

et al. 2015

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A high-resolution proteome and phosphoproteome atlas of four maize (Zea mays) primary root tissues, the cortex, stele, meristematic zone, and elongation zone, was generated. High-performance liquid chromatography coupled with tandem mass spectrometry identified 11,552 distinct nonmodified and 2,852 phosphorylated proteins across the four root tissues. Two gradients reflecting the abundance of functional protein classes along the longitudinal root axis were observed. While the classes RNA, DNA, and protein peaked in the meristematic zone, cell wall, lipid metabolism, stress, transport, and secondary metabolism culminated in the differentiation zone. Functional specialization of tissues is underscored by six of 10 cortex-specific proteins involved in flavonoid biosynthesis. Comparison of this data set with high-resolution seed and leaf proteome studies revealed 13% (1,504/11,552) root-specific proteins. While only 23% of the 1,504 root-specific proteins accumulated in all four root tissues, 61% of all 11,552 identified proteins accumulated in all four root tissues. This suggests a much higher degree of tissue-specific functionalization of root-specific proteins. In summary, these data illustrate the remarkable plasticity of the proteomic landscape of maize primary roots and thus provide a starting point for gaining a better understanding of their tissue-specific functions.

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“…DII responded to both exogenous IAA applied to leaf pieces and roots as well as endogenous auxin signaling in leaves, roots, and developing tassels. The important role of auxin in maize development (Forestan and Varotto, 2012;Galli et al, 2015;McSteen, 2010;von Behrens et al, 2011;Yu et al, 2016;Zhang et al, 2014) and during the cell cycle (Del Pozo and Manzano, 2014;Himanen et al, 2002) highlights the utility of the DII marker.…”

Section: Discussionmentioning

confidence: 99%

“…In maize (Zea mays), auxin contributes to inflorescence development (Galli et al, 2015), tassel branching (Gallavotti et al, 2008a), and root structure (Jansen et al, 2012;Zhang et al, 2014). The currently available auxin reporter in maize uses the synthetic promoter element DR5 to drive the expression of an endoplasmic reticulum retained Red Fluorescent Protein (DR5rev::mRFP-er, DR5) in response to increased auxin.…”

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confidence: 99%

A DII Domain-Based Auxin Reporter Uncovers Low Auxin Signaling during Telophase and Early G1

Mir¹,

Aranda²,

Biaocchi

et al. 2016

Plant Physiol.

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A sensitive and dynamically responsive auxin signaling reporter based on the DII domain of the INDOLE-3-ACETIC ACID28 (IAA28, DII) protein from Arabidopsis (Arabidopsis thaliana) was modified for use in maize (Zea mays). The DII domain was fused to a yellow fluorescent protein and a nuclear localization sequence to simplify quantitative nuclear fluorescence signal. DII degradation dynamics provide an estimate of input signal into the auxin signaling pathway that is influenced by both auxin accumulation and F-box coreceptor concentration. In maize, the DII-based marker responded rapidly and in a dose-dependent manner to exogenous auxin via proteasome-mediated degradation. Low levels of DII-specific fluorescence corresponding to high endogenous auxin signaling occurred near vasculature tissue and the outer layer and glume primordia of spikelet pair meristems and floral meristems, respectively. In addition, high DII levels were observed in cells during telophase and early G1, suggesting that low auxin signaling at these stages may be important for cell cycle progression.

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The Aux/IAA gene rum1 involved in seminal and lateral root formation controls vascular patterning in maize (Zea mays L.) primary roots

Abstract: SummaryRNA-Seq of RUM1-dependent gene expression in maize primary roots, in combination with histological analyses, highlighted the regulation of auxin signal transduction by RUM1 and its role in vascular development.

Cited by 67 publications

References 51 publications

Cell Type-Specific Gene Expression Analyses by RNA Sequencing Reveal Local High Nitrate-Triggered Lateral Root Initiation in Shoot-Borne Roots of Maize by Modulating Auxin-Related Cell Cycle Regulation

Cell Type-Specific Gene Expression Analyses by RNA Sequencing Reveal Local High Nitrate-Triggered Lateral Root Initiation in Shoot-Borne Roots of Maize by Modulating Auxin-Related Cell Cycle Regulation

A High-Resolution Tissue-Specific Proteome and Phosphoproteome Atlas of Maize Primary Roots Reveals Functional Gradients along the Root Axes

A DII Domain-Based Auxin Reporter Uncovers Low Auxin Signaling during Telophase and Early G1

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