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Scientists find microRNAs regulate plant development

04.05.2005


Major aspects of root and shoot development controlled by the plant hormone auxin are linked to regulation of gene expression by microRNAs



The plant hormone indole-3-acetic acid (IAA), commonly referred to as auxin, plays a major role in regulating plant growth and development. Auxin influences development by affecting the expression of numerous genes that control the processes of cell division and cell expansion in specific plant tissues at specific stages during the plant life cycle - e.g. for leaves, roots, and floral organs to develop in the correct patterns and correct time sequence. Research reported in The Plant Cell shows that microRNAs control the accumulation of transcription factor proteins that regulate the expression of genes in the auxin response pathway.

Messenger RNA (mRNA) molecules are encoded by genes and are themselves templates for the proteins that carry the main metabolic functions in a cell. The mRNA levels in a cell are fine tuned by different mechanisms, one of which is driven by microRNA molecules. MicroRNAs are ~22 nucleotide long RNA molecules that provide substrate specificity to a protein complex known as the RNA-induced silencing complex. Within the complex, microRNAs are thought to bind to mRNA molecules containing a complementary stretch of RNA sequence. The complex then cleaves the mRNA into smaller pieces, thereby preventing translation of the protein it encodes, and thus inhibiting or "silencing" gene expression. mRNAs corresponding to several regulatory genes that mediate auxin responses contain short stretches of sequence that are complementary to microRNAs, and therefore have been considered potential targets of microRNA-mediated regulation. One of these targets is the transcription factor AUXIN RESPONSE FACTOR17 (ARF17), which is thought to repress the expression of a number of other genes involved in auxin responses.


Dr. Bonnie Bartel at Rice University in Houston, TX together with Drs. David Bartel and Allison Mallory at the Massachusetts Institute of Technology and the Whitehead Institute for Biomedical Research in Cambridge, MA report experiments using transgenic Arabidopsis plants that produce a version of ARF17 mRNA that resists microRNA-mediated cleavage. The plants showed increased accumulation of ARF17 mRNA and altered levels of mRNAs corresponding to several genes that may be regulated by ARF17. These changes were correlated with dramatic development defects in leaves, roots, and flowers, showing that microRNA-mediated regulation of ARF17 is essential for normal plant development.

Bonnie Bartel notes that "we have known for several years now that microRNAs regulate genes implicated in auxin responses; with these three reports, we are beginning to understand the consequences of this regulation for the development of the plant." David Bartel adds, "We were particularly struck by the unusual quadrilaterally symmetric seedlings we uncovered in our study. This result implies that the Arabidopsis embryo relies on microRNA restriction of ARF17 activity to achieve normal bilateral symmetry."

A second report focuses on the function of the protein ARGONAUTE1 (AGO1), a major component of the RNA-induced silencing complex in Arabidopsis. There are many AGO1-like proteins in animals and other eukaryotes as well, indicating that the RNA-induced silencing complex is of ancient evolutionary origin, and that microRNA-mediated regulation of gene expression is shared among many eukaryotes. Arabidopsis ago1 mutants lacking the AGO1 protein have numerous severe developmental defects, supporting the notion that regulation by microRNAs is critical for normal plant growth. Dr. Catherine Bellini at The Swedish University of Agricultural Sciences in Umeå, Sweden and colleagues at several other institutions noticed that the ago1 mutant failed to form adventitious roots - a type of root that develops from aerial parts of the plant and is important for propagation through cuttings. Auxin is known to be a major regulator of adventitious root formation and normal Arabidopsis plants form multiple adventitious roots on the hypocotyl (stem just above the root) when treated with auxin but the ago1 mutants do not. Dr. Bellini and her colleagues found that the mutant plants over-accumulate ARF17 mRNA within the hypocotyl, pointing to ARF17 as a major regulator of adventitious rooting and microRNA-mediated regulation as a major regulator of ARF17.

In a third report, Dr. Nam-Hai Chua of Rockefeller University in New York and scientists at the Temasek Life Science Laboratories, Singapore, and the Chinese Academy of Sciences in Beijing show that microRNA is important in the regulation of a transcription factor that is induced by auxin, called NAC1. NAC1 functions in other aspects of the auxin response, such as the formation of lateral roots (roots that grow off the main tap root below ground, as opposed to the adventitious roots that grow off of the stem or other above-ground plant parts). Like ARF17, NAC1 mRNA contains a stretch of sequence that is complementary to microRNAs, and thus shows potential for microRNA-mediated regulation. In experiments analogous to those of Bartel’s group, Chua and colleagues created transgenic Arabidopsis plants that produce a version of NAC1 that is resistant to microRNA-mediated cleavage. Compared to wild-type plants, the transgenic plants overaccumulated NAC1 mRNA and produced more lateral roots. It was also found that accumulation of the microRNA that targets NAC1 mRNA is induced by auxin. The pattern of induction suggested a model wherein auxin induction of NAC1 mRNA is later followed by induction of the microRNA responsible for NAC1 mRNA cleavage. MicroRNA-mediated regulation of gene expression therefore appears to be an important mechanism for fine-tuning auxin signaling during plant development.

These reports provide significant new information on microRNA-mediated regulation of plant development and show that microRNAs play important roles in regulating the auxin response pathway.

Nancy Eckardt | EurekAlert!
Further information:
http://www.aspb.org
http://www.plantcell.org

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