More than photosynthesis: chloroplasts now discovered to also function as plant growth regulators

In 1967, the American biologist Lynn Margulis formulated her famous endosymbiosis theory, explaining the origin of mitochondria and chloroplast organelles inside eukaryotic cells. These organelles, once primitive bacteria, transferred most of their own genetic material to the cell nucleus. Thus, the cell nucleus, now containing most of the cell’s DNA became the cell’s "director" and supplier of most cellular proteins. Thanks to its role as "cellular director" the nucleus is constantly sending signals to other organelles to perform important cell functions such as division or differentiation.

The main function of the mitochondria and the chloroplasts as cell energy producers is well known.So is the fact that these organelles can inform the nucleus of their status and needs, through what is known as retrograde signaling. Mitochondria and chloroplasts use this retrograde signaling to request from the nucleus the proteins they need to produce energy.Furthermore, in animal cells, retrograde signaling has been shown to be important for a variety of cellular functions besides energy production.For example, in animal cells, mitochondria signaling to the nucleus modulates important processes such as cell division or tumor progression.

In the study now published in Nature Communications, the team led by the CSIC researcher at CRAG, Elena Monte, describes for the first time that the effects of retrograde signaling in plants go far beyond what had been described so far, being able to modulate the overall plant development. "We were surprised to discover that the signals coming from the chloroplasts have the ability to modify the development of the plant, circumventing the nucleus," explains Guiomar Martín, PhD student at CRAG and first author of the article. "Just as mitochondria signaling to the nucleus regulates key processes in animals, we now know that in plants the chloroplasts can regulate development through a new mechanism that we have been able to describe at the molecular level," adds the principal investigator of the study, Elena Monte.

The chloroplast: a stress sensor

CRAG’s research group used Arabidopsis thaliana seedlings under light-guided development (photomorphogenesis) and treated them with a drug that damages the chloroplasts. Surprisingly, the drug-treated plants acquired an appearance similar to the plants grown in the dark, indicating that the retrograde signaling was repressing the normal photomorphogenesis despite the presence of light. In view of this result, the researchers sought to understand the molecular mechanism underlying this effect.

Subsequent experiments indicated that the nuclear gene GLK1 is central to photomorphogenesis development, and is regulated by retrograde signaling and a group of light-sensitive proteins called PIFs. In darkness, the PIF proteins are abundant and prevent the action of GLK1, but when the seedling reaches the soil surface and is exposed to sunlight, the PIF proteins degrade, allowing GLK1 to promote the photomorphogenic development of the seedling, including for example, leaf expansion and chlorophyll (and therefore green color) acquisition. However, when the chloroplasts are damaged (e.g. when applying the drug) or detect stressful environmental conditions (e.g. when subjecting the plant to excessive illumination) the expression of GLK1 is downregulated in response to the chloroplast retrograde signaling by a mechanism independent of the PIFs. Thanks to this molecular mechanism, that temporarily suppresses development, the plant is protected from photooxidative damage while awaiting favorable growth conditions.

Thus, the article published now in Nature Communications, describes for the first time that the chloroplasts function as a stress sensor antenna, able to temporarily take the cell control from the nucleus to modify the development and protect the plant.

For Elena Monte, "this work helps to understand how endosymbiotic organelles in eukaryotic cells can change the overall development of the organism." "In plants, this knowledge can help in finding solutions to cope with the increased radiation, and therefore an excess of light, as a result of climate change," she adds.

Other researchers who participated in this work are: CRAG researchers, Pablo Leivar and Dolores Ludevid, and the researchers from the University of California, Berkeley, James M. Tepperman and Peter H. Quail. This work has count with the financial support from projects and fellowships by the Spanish Government, the Generalitat de Catalunya, and the European Comission (Marie Curie program) to Elena Monte’s research group members; and by grants from the NIH and the USDA to Peter H. Quail.

Reference article:

Guiomar Martín, Pablo Leivar, Dolores Ludevid, James M. Tepperman, Peter H. Quail & Elena Monte “Phytochrome and retrograde signalling pathways converge to antagonistically regulate a light-induced transcriptional network” Nature Communications. May, 2016

Image:

Microscopic image of cells of Arabidopsis thaliana seedling stem. Chloroplasts are shown in green and the cell nuclei in blue.