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Scientists uncover a link between RNA editing and chloroplast-to-nucleus communication

What will a warmer world three degrees warmer look like? How will plants cope in more extreme climatic conditions? When under stress or damage from various sources, plants use chloroplast nucleus communication to regulate gene expression and help them adapt.

Today, researchers at the Salk Institute have discovered that the GUN1 gene - a gene that integrates many retrograde signaling pathways from chloroplast to nucleus - also plays an important role in how proteins are made in damaged chloroplasts, providing a better understanding of how plants respond to stress. The article was published in the Proceedings of the National Academy of Sciences (PNAS) on April 15, 2019 and could help biologists select plants that can better resist environmental stressors.

"Climate change is likely to affect our food system dramatically. When plants are stressed, such as in a drought, they produce lower yields. If we understand how plants respond to stress, we may be able to find a way to increase their resistance and maintain their food production at a high level," says Joanne Chory, Professor Salk, Director of the Plant Molecular and Cellular Biology Laboratory and lead author of the paper.

In plant cells, structures called chloroplasts transform solar energy into chemical energy (photosynthesis). Normally, the cell nucleus transmits the information to chloroplasts to maintain stable energy production. However, in a stressful environment, chloroplasts send an alarm to the cell nucleus using retrograde signalling (creating a chloroplast-to-nucleus communication feedback loop). This SOS triggers a response that helps regulate gene expression in chloroplasts and the nucleus to optimize energy production from sunlight.

Previously, Chory's laboratory identified a group of genes, including GUN1, that influence the expression of other genes in the cell when the plant is under stress. GUN1 accumulates under stressful conditions but the exact molecular function of GUN1 has been difficult to decipher so far.

"Plants often suffer from environmental stressors, so there must be a chloroplast core communication pathway that helps the plant know when to conserve energy in case of injury," explains Xiaobo Zhao, first author and postdoctoral fellow in Chory's laboratory. "GUN1 is proving to play a big role in all this."

To understand how GUN1 regulates chloroplast core communication, scientists observed plants with functional and non-functional GUN1 undergoing pharmacological treatment that could damage chloroplasts. In plants without GUN1, gene expression has changed, as has the modification of RNA in chloroplasts. (RNA modification is a modification of RNA that modifies the identity of nucleotides, so that the information contained in mature RNA differs from that defined in the genome, thus modifying protein manufacturing instructions.) Some areas of RNA had more editing and others had less editing - suggesting that GUN1 plays a role in regulating the edition of chloroplast RNA.

After further analysis, the team unexpectedly discovered that GUN1 associates with another protein, MORF2 (an essential component of the plant's RNA editing complex), to affect the effectiveness of RNA editing during chloroplast-to-nucleus communication in damaged chloroplasts. The increased activity of MORF2 has resulted in widespread editorial changes and defects in the development of chloroplasts and leaves, even under normal growing conditions (see image). During periods of stress and injury, the overproduction of MORF2 also disrupted chloroplast-nucleus communication.

"Taken together, these results suggest a possible link between chloroplast-to-core communication and the publication of chloroplast RNA, which are important regulatory functions for flowering plants, especially during stress," says Chory, a Howard Hughes Medical Institute researcher and Howard H. and Maryam R. Newman Chair in Plant Biology.

Next, the researchers plan to examine the mechanism of activation of signals that can be relayed to the nucleus by changes in the edition of RNA in chloroplasts, and how these changes modify the plant's ability to react to stress.