Iron-Dependent Callose Deposition Adjusts Root Meristem Maintenance to Phosphate AvailabilityDevelopmental Cell

About

Authors
Jens Müller, Theresa Toev, Marcus Heisters, Janine Teller, Katie L. Moore, Gerd Hause, Dhurvas Chandrasekaran Dinesh, Katharina Bürstenbinder, Steffen Abel
Year
2015
DOI
10.1016/j.devcel.2015.02.007
Subject
Developmental Biology

Text

Article

Iron-Dependent Callose Deposition Adjusts Root

Phosphate Availability

Highlights d Primary root growth inhibition under low-phosphate conditions needs iron availability d Phosphate limitation triggers apoplastic iron and callose deposition in root meristems d Callose deposition inhibits symplastic communication in the root stem cell niche d Root meristem-specific LOW PHOSPHATE ROOT1 encodes

Authors

Jens Mu¨ller, Theresa Toev, ...,

Katharina Bu¨rstenbinder, Steffen Abel

Correspondence sabel@ipb-halle.de

In Brief

Edaphic (soil-derived) cues inform root development. Mu¨ller et al. show that antagonistic interactions between phosphate and iron availabilities adjust root growth via meristem-specific callose deposition, which regulates cell-to-cell communication in the stem cell niche.Mu¨ller et al., 2015, Developmental Cell 33, 216–230

April 20, 2015 ª2015 Elsevier Inc. http://dx.doi.org/10.1016/j.devcel.2015.02.007a cell-wall-targeted ferroxidaseGraphical AbstractMeristem Maintenance toLPR1 ferroxidase-dependent redox signaling, initiated in the root apoplast, is central to local phosphate sensing. p in r ,1 t a y

Cdopsis thaliana (Petricka et al., 2012). The simple anatomy of its root, comprising the vascular cylinder and three radial cell layers (endodermis, cortex, and epidermis), is maintained by the stem

In root development, PD and, possibly, callose turnover are essential for SHR movement (Vate´n et al., 2011) or for determining the pattern of lateral root formation (Benitez-Alfonsocell niche (SCN) of the root apical meristem (RAM). The SCN is patterned during embryogenesis and includes the quiescent center (QC) and contacting pluripotent cells. These initials are et al., 2013). However, the mechanisms that connect calloseregulated cell-to-cell signaling in the RAM to the perception of soil-borne cues are elusive.as demonstrated by impaired SHORT-ROOT movement. Antagonistic interactions of Pi and Fe availability control primary root growth via meristem-specific callose formation, likely triggered by LPR1-dependent redox signaling. Our results link callose-regulated cell-to-cell signaling in root meristems to the perception of an abiotic cue.

INTRODUCTION

Vigorous development of the seed radicle into an elaborate root system is critical for plant survival and performance because roots provide an extensive interface for water uptake, mineral nutrition, and chemical interactions with the rhizosphere.

Root development, which is highly plastic and responsive to numerous edaphic cues, has been studied extensively in Arabiroutes of cell-to-cell communication are known in plants. Intercellular translocation of cargo is facilitated by exo- and endocytosis (Contento and Bassham, 2012) or by direct symplastic transport via specialized channels, called plasmodesmata (PD) (Burch-Smith and Zambryski, 2012). Metabolites, small proteins, and RNAs may transverse PD by diffusion, whereas other macromolecules interact with PD and move by a targeted mechanism. Symplastic trafficking can be tuned by modification of PD structure or deposition of callose (a b-1,3 glucan) at the

PD neck region (Benitez-Alfonso et al., 2013; Zavaliev et al., 2011). During numerous developmental processes or environmental responses, callose production controls PD conductivity, which is counteracted by specific PD-localized b-1,3 glucanases (Burch-Smith and Zambryski, 2012). There is growing evidence that reactive oxygen species (ROS) and redox signaling regulate callose deposition and symplastic permeability (Benitez-Alfonso et al., 2011; Stonebloom et al., 2009).Iron-Dependent Callose De

Adjusts Root Meristem Ma to Phosphate Availability

Jens Mu¨ller,1 Theresa Toev,1 Marcus Heisters,1 Janine Telle

Dhurvas Chandrasekaran Dinesh,1 Katharina Bu¨rstenbinder 1Department of Molecular Signal Processing, Leibniz Institute of Plan 2Department of Materials, University of Oxford, Oxford OX1 3PH, UK 3Biocenter, Martin Luther University Halle-Wittenberg, 06120 Halle (S 4Institute of Biochemistry and Biotechnology, Martin Luther Universit 5Department of Plant Sciences, University of California, Davis, Davis, *Correspondence: sabel@ipb-halle.de http://dx.doi.org/10.1016/j.devcel.2015.02.007

SUMMARY

Plant root development is informed by numerous edaphic cues. Phosphate (Pi) availability impacts the root system architecture by adjusting meristem activity. However, the sensory mechanisms monitoring external Pi status are elusive. Two functionally interacting Arabidopsis genes, LPR1 (ferroxidase) and PDR2 (P5-type ATPase), are key players in root

Pi sensing, which is modified by iron (Fe) availability.

We show that the LPR1-PDR2 module facilitates, upon Pi limitation, cell-specific apoplastic Fe and callose deposition in the meristem and elongation zone of primary roots. Expression of cell-wall-targeted LPR1 determines the sites of Fe accumulation as well as callose production, which interferes with symplastic communication in the stem cell niche,216 Developmental Cell 33, 216–230, April 20, 2015 ª2015 Elsevier IDevelopmental Cell

Article osition tenance ,1 Katie L. Moore,2 Gerd Hause,3 and Steffen Abel1,4,5,*

Biochemistry, 06120 Halle (Saale), Germany ale), Germany

Halle-Wittenberg, 06120 Halle (Saale), Germany

A 95616, USA perpetual sources of daughter cells that generate the lineages of transit-amplifying (TA) cells of the proximal meristem (Dolan et al., 1993; Scheres, 2007). At the boundary to the elongation zone (transition zone), TA cells exit the cell cycle, expand, and differentiate by acquiring tissue-specific characteristics (Perilli et al., 2012). The position of the transition zone determines

RAM size and is directly related to the root growth rate (Baum et al., 2002).

Cell-to-cell signaling is a key organizing principle in metazoan development. RAM and SCN maintenance require the precise coordination of cell division and differentiation, which depends on the directional intercellular transport of mobile signals (Gallagher et al., 2014; Perilli et al., 2012). For example, the QC maintains adjacent stem cells via unknown short-range signals that prevent their differentiation (Scheres, 2007; van den Berg et al., 1997). The transcription factor SHORT-ROOT (SHR) moves from the stele into the QC and endodermis to determine cell fate, partly by interaction with SCARECROW (Cui et al., 2007; Nakajima et al., 2001; Sabatini et al., 2003). Two majornc.