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

Abstract

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.

Root Type-Specific Reprogramming of Maize Pericycle Transcriptomes by Local High Nitrate Results in Disparate Lateral Root Branching Patterns

“…It was previously demonstrated that anticlinal and periclinal divisions of pericycle cells were significantly induced in response to local high nitrate in aboveground shoot-borne brace roots (Yu et al, 2015a). In contrast, no significant induction of cell divisions in phloem pole pericycle cells were detected in this study in any region of the three seedling root types, primary, seminal, and crown roots of 80 mm length, by local high nitrate induction 24 h after treatment (Fig.…”

“…Lateral root initiation is preceded by auxin response maxima in differentiating xylem cells and in cells surrounding the protophloem vessels in maize (Jansen et al, 2012;Yu et al, 2015a). The maize root system is an ideal model to study organ-specific similarity and diversity because of its spatio-temporal complexity and distinct genetic control of different root types (Hochholdinger and Zimmermann, 2008;Rogers and Benfey, 2015).…”

“…Transcriptome analyses have provided novel insights in lateral root initiation in maize roots by identifying candidate genes associated with early cell divisions (Woll et al, 2005;Dembinsky et al, 2007;Yu et al, 2015a). To obtain an in-depth understanding of nitrate sensing during lateral root branching, this study surveyed the transcriptomic complexity of pericycle cells in the four major root types of maize in response to heterogeneous nitrate application using laser capture microdissection in combination with RNA-sequencing (LCM-RNAseq).…”

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

“…Intimate links between cell cycle progression and auxin have been demonstrated. Specifically, auxin promotes cell cycle progression in the pericycle as an early step of lateral root formation in Arabidopsis (Himanen et al, 2002) and maize (von Behrens et al, 2011;Yu et al, 2016Yu et al, , 2015. In the developing maize leaf, increased concentrations of auxins and cytokinins were found in the rapidly dividing zone of the leaf in regions prior to cell expansion (Nelissen et al, 2012).…”

The Physiology of Adventitious Roots

“…In rice, phosphate or nitrate deficiency results in longer roots with fewer lateral roots on the seminal roots (Rose et al, 2013;Sun et al, 2014), whereas zinc deficiency reduced the number on crown roots but had little effect on root length (Widodo et al, 2010). Using split-root experiments, Yu et al (2014Yu et al ( , 2015 demonstrated that, although lateral root density increased on maize crown roots that were exposed to locally high concentrations of nitrate, lateral root density was not affected on seminal roots (Yu et al, 2014). This difference in lateral root initiation between seminal and crown roots further highlights the complex differences between the different root classes in maize.…”