Retrograde signalling protects plants in high-light environments

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Retrograde signalling protects plants in high-light environments

Chloroplast-to-nucleus signalling in rice plays distinct roles under red and blue light conditions, fine-tuning photoprotection under potentially photodamaging conditions
Rice seedlings grown in blue light (leaves in the right) induce higher NPQ levels when exposed to high light compared to red light-grown seedlings (left leaves). Violet colour indicates higher NPQ induction.
Rice seedlings grown in blue light (leaves in the right) induce higher NPQ levels when exposed to high light compared to red light-grown seedlings (left leaves). Violet colour indicates higher NPQ induction.

The evolution from single-celled organisms to complex life is undoubtedly connected to two intracellular organelles: mitochondria and plastids. Both arose from primitive bacteria through a process called endosymbiosis and transferred most of their own genetic material to the cell nucleus, which acts as the control centre. Mitochondria and chloroplasts, the major type of plastids, provide energy for the cell and can communicate with the nucleus in a process called retrograde signalling. Such signals determine how cells respond to developmental and environmental influences, so the understanding of retrograde signalling is key to elucidate cell evolution, function and regulation.

A new study carried out by the Environmental control of plant and algae growth research group, led by CSIC researcher at CRAG Elena Monte, describes for the first time the differential impact of red and blue light in retrograde signalling during rice seedling development. These findings indicate that retrograde signalling plays a key role in protecting seedlings from damage in high-light environments. The article is part of a special issue of the Philosophical Transactions of the Royal Society B, the world's longest running science journal, dedicated to retrograde signalling from endosymbiotic organelles.

Less exposition, less risk

Light is fundamental for plants both as a source of energy and as an environmental cue, especially during germination and seedling establishment. Previous studies also led by Elena Monte revealed that retrograde signalling under high-light conditions in Arabidopsis repressed normal seedling development inhibiting cotyledon separation, therefore minimizing the area exposed to potentially damaging light. Arabidopsis is a well-known dicotyledonous model plant, but the impact of retrograde signalling in monocotyledons, such as rice, had not been addressed until now. In agriculture, the majority of the biomass produced comes from monocotyledons, thus the study of processes that affect their development is especially relevant.

Activation of retrograde signalling takes place when chloroplasts are damaged under stress conditions like high light, or with the use of chemicals like lincomycin. In order to determine the retrograde signalling response in rice, researchers grew rice seedlings in the presence of lincomycin and, in clear contrast to previous studies in Arabidopsis, results showed that early development in rice seedlings remained mainly unaffected. 

To further assess the effect of excessive light, lincomycin treatment was applied in combination with monochromatic high lights of different intensities, allowing to dissect the ability of each wavelength to cause chloroplast damage and induce retrograde signalling. Interestingly, seedlings grown under red and blue monochromatic lights responded differently to lincomycin, as blue light-grown seedlings showed inhibition of the length and declination of the second leaf.

The leaf being shorter and less declined means less area exposed to light. “Together with previous results in Arabidopsis showing inhibition of cotyledon separation, our new study adds evidence that retrograde signalling plays a key role in photoprotection probably by minimizing the area of the seedling exposed to potentially damaging light, both in monocotyledonous and dicotyledonous plants”, states senior researcher in charge Elena Monte.

Differences in managing excess light

They say excess of everything is bad, and light is no exception. For plants, too much light becomes harmful and eventually leads to cell death. To avoid such damage in high light environments, plants activate a photoprotective mechanism known as non-photochemical quenching (NPQ), which allows them to dissipate the excess energy as heat.

Red light-grown seedlings showed a white phenotype indicating the disruption of the chloroplast function, while seedlings grown under blue light stayed green. To understand these pigmentation differences, researchers measured the NPQ capacity in rice seedlings grown under continuous blue or red light. 

“Our data shows that blue light-grown seedlings are able to induce higher NPQ levels, equipping them with the capacity to better withstand high light in comparison to seedlings grown under red light”, explains María Águila Ruiz, a co-author of the work. “These findings may indicate that a specific blue light signal is necessary to activate the NPQ photoprotection mechanism”, she adds.

The seed has been sown

The study now published at the Philosophical Transactions of the Royal Society B journal reveals that retrograde signalling plays different roles under red and blue light conditions, fine-tuning the seedlings’ development, morphology and NPQ capacity to photoprotect them and optimize their response under high-light damaging situations.

This research sets de ground for further studies addressing how retrograde signalling has evolved as a photoprotective mechanism for plants and which molecular players lie behind it, a relevant question in natural environments. “Understanding how rice responds to conditions of high-light intensity, which is increasing with climate change, can help us find more resilient rice and design novel ways to grow it that allow for less damage and more productivity”, adds Liu Duan, lead author of the work.

 

Reference article: Philosophical Transactions of the Royal Society B. 04 May 2020. https://doi.org/10.1098/rstb.2019.0402. Red and blue light differentially impact retrograde signalling and photoprotection in rice. Liu Duan, M. Águila Ruiz-Sola, Ana Couso, Nil Veciana and Elena Monte.