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Regulatory networks of plant stem cell systems

A team of researchers led by Prof. Jan Lohmann at the Centre for Organismal Studies (COS) Heidelberg is investigating the regulatory programmes that control the stem cell centre in the shoot meristem of the plant Arabidopsis thaliana and enable the plant to react to environmental influences. Despite the fact that animal and plant cells have developed independently from each other, the researchers have discovered unexpected similarities between the stem cell control of plants and animals.

Prof. Dr. Jan Lohmann © Universität Heidelberg

While public debate has focused on research involving embryonic stem cells from animals and humans, research involving plant stem cells appears to have been a much calmer field of work. It is an issue that receives scant coverage in the media. This is somewhat surprising considering that the growth and developmental processes of plants cannot be understood without touching on the issue of stem cells. In addition, plant breeders depend on detailed insights into the basic mechanisms of stem cell regulation in their efforts to adapt plant varieties to constantly changing environmental conditions. 

Professor Dr. Jan Lohmann and his team in the Department of Stem Cell Biology at the Centre for Organismal Studies (COS) Heidelberg are focusing on the regulatory programmes that govern stem cell control in the plant Arabidopsis thaliana, which is the most popular model plant in molecular plant research. COS is a central institution at Universität Heidelberg and is a result of the merger that took place between the Institute of Plant Sciences, including the Botanical Garden and Herbarium, and the Institute of Zoology, including the Zoological Museum, in autumn 2010. The goal of the merger is to advance research collaboration beyond the traditional borders of botany and zoology.

The appointment of Jan Lohmann as chair of the Department of Stem Cell Biology in 2008 fits perfectly into the COS concept of focusing on the entire organism, irrespective of whether it is plant or animal. Lohmann, a scientist with a great deal of experience in using the most popular stem cell research model organisms of zoologists and botanists, did his doctorate on the morphology of the freshwater polyp Hydra. He then continued his scientific career at the Salk Institute in La Jolla, California, after which he went to the Max Planck Institute for Developmental Biology in Tübingen, Germany, where he focused on the stem cell control and patterning of flowers in the plant Arabidopsis thaliana.

Plant stem cells are located in the meristems

Arabidopsis thaliana is a popular model organism amongst plant researchers. © 5th EU-Framework Programme Quality of Life

The stem cells of plants are small, undifferentiated pluripotent cells which give rise to a broad range of different organs and tissues. Stem cells are established early on in the process of embryonic development and are embedded in specialised plant tissues called meristems. The major task of plant embryogenesis is to programme the regions of meristematic tissue formation so that the shoot meristem grows towards the light and the root meristem grows downwards in the direction of gravitational pull. The stem cells divide relatively slowly. They are surrounded by so-called precursor cells, i.e. undifferentiated cells without vacuoles. The precursor cells cannot be differentiated morphologically from stem cells, but they divide more quickly and constitute the cell material for the differentiation zone located on the periphery where new organs develop.

Another cell group resides in the deeper layers of the meristem, below the stem cells. These cells serve as control centre, they very seldom divide and they secrete signalling substances that have a decisive effect on the behaviour of the stem cells. 
Lohmann pointed out (1) that a similar distribution of tasks between spatially and functionally different cell groups is also found in animal stem cell systems although animal and plant stem cells have developed independently from each other. However, there is still a major difference between animal and plant cells: animal cells are motile and move to other sites in the growing organism while plant cells are trapped inside rigid cell walls, which prevents them from moving. New plant organs can only form in a specific environment that regulates the homoeostasis between differentiation and proliferation.

Transcription factor "Wuschel" regulates the number of stem cells in plants

Arabidopsis seedling (in foreground) with intact Wuschel gene and functional meristem. The other seedling has a defective Wuschel gene, which prevents it from forming organs at the shoot tip. Statistical analysis of the gene activities regulated by Wuschel is shown in the background. © Max Planck Society

The number of stem cells in plants is controlled by a complex feedback mechanism consisting of genetic switches and free moving signalling molecules which link control cells and stem cells with each other. This control system ensures that the number of stem cells is kept as stable as possible. As far back as 14 years ago, researchers discovered a gene in the plant Arabidopsis thaliana that plays a central role in the induction and maintenance of stem cell populations in shoot and floral meristems. The protein product of this gene is a homoeodomain transcription factor known as “Wuschel”. The homoeodomain is a region of 60 amino acids that binds to specific regions in the gene promoter, thereby switching genes on and off. This particular region was initially discovered in homoeotic genes in Drosophila. 

According to Lohmann, Wuschel is the key switch by which plants regulate the number of stem cells. In collaboration with researchers from the Max Planck Institute for Developmental Biology in Tübingen and from Santa Fe University in Argentina, Lohmann and his team of researchers have identified around 700 genes whose activity depends on the Wuschel transcription factor. In addition, they also found that Wuschel is able to directly switch on and off 130 of the 700 genes (2). The genes are mainly involved in the metabolism, development and hormone balance of plants. In addition to the genetic factors, the well-known plant hormones auxin and cytokinin are also involved in regulating the number of stem cells in Arabidopsis. Lohmann and his team have now shown that both cytokinin and auxin activity are regulated by the Wuschel gene.

Further information about auxin and cytokinin:
Auxin (the name is derived from the Greek word “auxanomai” – to grow/increase) was the first plant hormone to be discovered in the tips of oat coleoptiles around 100 years ago. The Danish botanist Peter Boysen-Jensen found that if he removed the coleoptile, plant growth stopped. Prior to this in 1880, Charles Darwin and his son Francis had already investigated the light-induced growth of the coleoptile tip and concluded that the tip of the coleoptile perceived light and produced a signal that was transported to the lower part of the coleoptile where bending occurred. In 1953, indole-3-acetic acid (IAA) was found to be the main natural auxin. Cytokinins are phytohormones that promote cell division (cytokinesis) in plant roots and shoots. In 1913, Gottlieb Haberlandt, a German plant physiologist, discovered a plant compound that had the ability to stimulate cytokinesis (hence cytokinin) and which 50 years later was shown to be an adenine derivative. 

Phytohormones and stem cell adaptation

As part of the “CellNetworks” cluster of excellence at Universität Heidelberg, Lohmann and his team are investigating how the cytokinin and auxin signalling pathways interact with the Wuschel-dependent machinery that controls the maintenance and regeneration of the meristem. The researchers are mainly focused on the role of the so-called A-type “Arabidopsis response regulator” (ARR) genes, which are negative regulators of cytokinin signalling. They have already shown that two cytokinin-inducible ARR genes repress the effect of cytokinin by way of a negative feedback loop and that auxin inhibits the expression of these two genes, thereby reinforcing the effects of cytokinin (3).

The Wuschel gene ensures that the effect of hormones that circulate in the plant meristems is adjusted to the local requirements in such a way that the stem cells are maintained and able to react to environmental influences mediated by signals coming from other plant organs. According to Lohmann, the analyses have shown that Wuschel functions like animal transcription factors that are involved in the development and renewal of stem cells (4). The control gene has also been found to use identical DNA areas as an anchor point.

In September 2011, Prof. Dr. Jan Lohmann was awarded a European Research Council (ERC) Starting Grant totalling around 1.5 million euros for his “StemCellAdapt” research project which is focused on the way plant stem cell systems adapt to various environmental conditions (5). These studies are being carried out because plants, due to their immobile nature, adapt with great flexibility to the predominant environmental conditions and simultaneously adjust their growth and development based on parameters such as light and temperature. The project is also seeking to find out how these adaptation processes have contributed to the evolution of plant species.

Further reading:

(1) Paper published in "Ruperto Carlo", Universität Heidelberg research magazine, 2/2011

(2) Busch W, Miotk A, Ariel FD, Zhao Z, Forner J, Daum G, Suzaki T, Schuster C, Schultheiss SJ, Leibfried A, Haubeiß S, Ha N, Chan RL, Lohmann JU: Transcriptional Control of a Plant Stem Cell Niche, Developmental Cell 18, 849-861, 2010

(3) Press release published on www.bio-pro.de: "Plant growth hormones: antagonists cooperate"

(4) Universität Heidelberg press release, 18th May 2010

(5) Press release published on www.bio-pro.de: European research council sponsors excellent young researchers from Universität Heidelberg

Further information:
Prof. Dr. Jan Lohmann
Centre for Organismal Studies
Dept. of Stem Cell Biology
Tel.: +49 (0)6221/ 54 5656
E-mail: jlohmann(at)meristemania.org

Website address: https://www.gesundheitsindustrie-bw.de/en/article/news/regulatory-networks-of-plant-stem-cell-systems