Back to the past to understand the present of plant antiviral immunity

• Researchers from CRAG have discovered that Marchantia polymorpha, one of the oldest land plants, employs RNA silencing as a defense mechanism against viral infections. 

• These findings provide scientists with deeper insights into the evolution of plant immunity and suggest new strategies for tackling plant pathogens.

• These knowledge could lead to the development of crops with stronger immune systems, contributing to global food security in the context of climate crisis.

In the ongoing quest to improve crop resilience and ensure global food security, understanding how plants defend themselves against threats is crucial and often, to address the problems of the present, we must take a look to the past. Scientists from CRAG have uncovered new insights into how some of the oldest plants on Earth respond to viral infections. In a groundbreaking study published in the prestigious journal Nature Communications, the researchers explored how the liverwort Marchantia polymorpha, a non-vascular plant that has been around for hundreds of millions of years, developed defense mechanisms against viruses. The findings could help scientists better understand the evolution of plant immunity and offer new strategies to combat plant pathogens, which are responsible for significant agricultural losses worldwide.

Ancient plants, modern challenges

Marchantia polymorpha is a member of the liverwort family, one of the earliest groups of plants to colonize land more than 450 million years ago. It belongs to the group of bryophytes, which also includes mosses. These plants evolved in a time when Earth’s landscapes were barren, and they had to adapt to survive on land without the sophisticated vascular systems that modern plants possess. While liverworts may not be as well-known as crops like wheat or rice, they offer valuable clues about how plants have historically dealt with environmental stressors—like viral infections.

"Studying these ancient plants allows us to trace the evolutionary roots of plant defense mechanisms", said Ignacio Rubio-Somoza, CSIC researcher at CRAG and the study's lead author. "It’s fascinating to see how some immune responses that evolved in non-vascular plants like liverworts are still present in today’s crops and how they have been fine-tuned over evolution″.

Viral infections in ancient plants

While we know a great deal about how modern plants like corn or tomatoes respond to viruses, much less is known about how ancient plants like Marchantia deal with these invaders. Viruses are a major threat to plants; they hijack the plant’s cellular machinery to replicate, often causing significant damage. In crops, viral infections can lead to reduced yields and poor-quality products, making this research highly relevant to global agriculture.

In this study, CRAG researchers took a closer look at how Marchantia interacts with viruses. By using modern techniques based on massive sequencing they were able to determine that Marchantia primarily interacts with a completely different class of viruses, RNA viruses, compared to plant lineages that had diverged earlier, what seems to indicate that shortly after land colonization plant viromes were fully reshaped. Additionally, when particularly focusing in their interaction with Tobacco Mosaic Virus (TMV), one of the most studied plant viruses that primarily infects vascular plants like tobacco and tomatoes, the researchers observed that Marchantia employed similar immune programs as response to viral attacks. Specifically, researchers found that Marchantia employs a defense strategy known as "RNA silencing", where the plant's immune system recognizes viral RNA (the genetic material of many viruses) and breaks it down. This RNA silencing response is one of plants' most crucial defenses against viral infections. Intriguingly, that general immune response found in this non-vascular plant, had been previously reported to happen uniquely in the vasculature of crops like tobacco.

″That is very exciting since it suggests that at least some antiviral programs have been rerouted during evolution to newly acquired tissues, such as in the case of the vascular system″, Ignacio Rubio-Somoza says.

However, the researchers also uncovered some unexpected differences. For instance, Marchantia seems to have a sustained wound response that helps limit viral spread. When the virus attacks, the plant's cells around the infection site remain on high alert, preventing the virus from moving to other parts of the plant. This unique feature suggests that Marchantia evolved specific adaptations to survive in its ancient environment, which was likely filled with various microbial threats.

"One of the most exciting aspects of this research is that Marchantia has retained some ancient immune responses while also developing unique strategies that we don’t see in crop plants", Rubio-Somoza explains.

Implications for modern agriculture

The findings of this study go beyond academic interest. Understanding how plants like Marchantia defend themselves against viruses could have significant implications for agriculture. As climate change leads to more extreme weather patterns, plants are becoming increasingly vulnerable to stressors, including pathogens like viruses. Crops with stronger immune systems are more likely to survive in challenging environments, making this kind of research essential for food security.

Understanding the evolutionary dynamics of immune programs may help identify new targets for developing plant varieties with enhanced performance against pathogen threats, ultimately leading to plants with more robust immune systems.

Reference article

Eric Ros-Moner, Tamara Jiménez-Góngora, Luis Villar-Martín, Lana Vogrinec, Víctor M. González-Miguel, Denis Kutnjak & Ignacio Rubio-Somoza. Conservation of molecular responses upon viral infection in the non-vascular plant Marchantia polymorpha. Nature Communications, https://doi.org/10.1038/s41467-024-52610-0

About the authors and funding of the study

The work in the MoRE lab is funded by RYC-2015-19154 (funded by MCIN/AEI/ 10.13039/501100011033 and by ″ESF Investing in your future″), RTI2018-097262-B-I00 (funded by MCIN/AEI/ 10.13039/501100011033 and by ″ERDF A way of making Europe″) and through the ″Severo Ochoa Program for Centres of Excellence in R&D″ 2016-2019 (SEV-2015-0533) and 2020-2023 (CEX2019-000902-S) funded by MCIN/AEI/ 10.13039/501100011033,CSIC-MCIN (Grant 202240I201) and the CERCA and SGR (2021-SGR-00875) programs from the Generalitat de Catalunya to I.R.S. T.J.G. was recipient of a Postdoctoral Fellowship from CRAG through the ″Severo Ochoa Program for Centres of Excellence in R&D″ 2016-2019 (SEV‐2015‐ 0533). L.V.-M. was supported by BES-2016-076986 (funded by MCIN/AEI/ 10.13039/ 501100011033 and by ″ESF Investing in your future″). The work at NIB was funded by Slovenian Research and Innovation Agency core and project financing P4-0407, P4-0165 and J4-4553