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Developmental Biology - Cell Signals

How Plant Roots Harness 'Bad' Molecules

Identifying the complex molecular interactions that regulate root and stem growth...


When most people think of a plant, they picture stems, leaves, flowers, and all those parts visible above ground. But Duke biologist Philip Benfey is more interested in the hidden half of the plant buried beneath the soil. Roots! They may be out of sight, but Benfey identifies the critical roles they play, (1) anchoring the plant and (2) absorbing water and nutrients.

Now, Benfey and colleagues have pieced together new details in the cascade of events that guide root growth.

As a root tunnels through the soil, stem cells in the root tips determine whether to divide and reproduce more of the same stem cells, or differentiate into other cell types. The study published in the journal Nature, shows that cells get some of the information they need to decide from substances usually thought harmful.

Natural byproducts of cellular respiration, "reactive oxygen species" molecules have long been described as signals of stress that indicate tissue damage will begin if left unheeded. But Benfey's work shows they also play a role in signalling cell differentiation.

In a study of the small flowering plant Arabidopsis thaliana, researchers observe how root growth is partly regulated by interactions between two types of reactive oxygen species (1) superoxide and (2) hydrogen peroxide as they build up in different regions of the root tip.

"What we did was map out, from signal to response, how these supposedly toxic chemicals are harnessed for a signaling process," Benfey explains.
Roots grow longer thanks to stem cells located in a small region of each root tip. Stem cells produce a constant supply of new and identical cells, propelling the root tip deeper into the soil. The daughter cells left behind stay put and stop dividing, but begin to specialize into other parts of the plant.

How fast a root grows depends on the balance between two opposing signals. One signal that encourages stem cells to multiply and one signal that stops stem cell proliferation and initiates stem cell specialization. When the RITF1 protein is activated, it triggers that developmental switch.

The protein appears to work by controlling where these two reactive oxygen species are concentrated within the growing root tip.

These reactive oxygen signals tell surrounding cells what action to take. Cells exposed to higher amounts of superoxide keep dividing and producing new and identical stem cells. Cells receiving a heavy dose of hydrogen peroxide differentiate.

But what happens in the transition zone where the two overlap?
"We don't have all the pieces yet, but there are a lot more steps of the process now known through this work than before. Reactive oxygen species aren't just toxic chemicals. They serve important roles as regulators of a developmental process, going from a stem cell to fully differentiated tissue.

Philip N. Benfey PhD, Department of Biology and Howard Hughes Medical Institute, Duke University, Durham, North Carolina, USA.

Abstract
The stem cell niche and the size of the root meristem in plants are maintained by intercellular interactions and signalling networks involving a peptide hormone, root meristem growth factor 1 (RGF1)1. Understanding how RGF1 regulates the development of the root meristem is essential for understanding stem cell function. Although five receptors for RGF1 have been identified2,3,4, the downstream signalling mechanism remains unknown. Here we report a series of signalling events that follow RGF1 activity. We find that the RGF1-receptor pathway controls the distribution of reactive oxygen species (ROS) along the developmental zones of the Arabidopsis root. We identify a previously uncharacterized transcription factor, RGF1-INDUCIBLE TRANSCRIPTION FACTOR 1 (RITF1), that has a central role in mediating RGF1 signalling. Manipulating RITF1 expression leads to the redistribution of ROS along the root developmental zones. Changes in ROS distribution in turn enhance the stability of the PLETHORA2 protein, a master regulator of root stem cells. Our results thus clearly depict a signalling cascade that is initiated by RGF1, linking this peptide to mechanisms that regulate ROS.

Authors
Masashi Yamada, Xinwei Han and Philip N. Benfey.


Acknowledgments
The authors thank I. Taylor, J. Dickinson, E. Pierre-Jerome, K. Lehner and C. Winter for comments on the manuscript; C. Wilson for help with generating overexpression lines; G. Yang for help in identifying CRISPR mutants; K. Sugimoto for HYP2-GFP seeds; Y. Matsubayashi for rgfr1/2/3 seeds; R. Heidstra for gPLT2-YFP and pPLT2-CFP seeds; N.-H. Chua for the pMDC7 vector; The Duke Genome Sequencing Center for sequencing Illumina libraries; the Plant Tech Core Facility in the Agricultural Biotechnology Research Center for generating the CRISPR construct; and the Transgenic Plant Laboratory at Academia Sinica for transforming the CRISPR construct into plants. This work was funded by the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation (through grant GBMF3405), the US National Institutes of Health (MIRA 1R35GM131725) to P.N.B., and Academia Sinica, Taiwan, to M.Y.

This research was supported by the Howard Hughes Medical Institute, the Gordon and Betty Moore Foundation (GBMF3405), and the U.S. National Institutes of Health (MIRA 1R35GM131725).


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Dec 11 2019   Fetal Timeline   Maternal Timeline   News 



A vertical cross section of the growing tip of an Arabidopsis thaliana root tip, revealing stacks of cells at different stages of development. Stem cells are near the tip while differentiated cells are higher up.

CREDIT Duke University.


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