Researchers at Michigan State University have discovered two proteins that work together to determine the fate of cells in plants facing certain stresses.

Ironically, a key discovery in this finding, published recently in Nature Communications, was made right as the project’s leader was getting ready to destress.

Postdoctoral researcher Noelia Pastor-Cantizano was riding a bus to the airport to fly out for vacation, when she decided to share a promising result she had helped gather a day earlier.

“I didn’t want to wait ten days until I came back to send it. It took almost two years to get there,” said Pastor-Cantizano, who then worked in the Brandizzi lab in the MSU-DOE Plant Research Laboratory, or PRL.

“That’s what I remember at the moment,” Pastor-Cantizano said. “I was thinking ‘I can relax now, at least for one week.’

Pastor-Cantizano had been working to identify a gene in the model plant Arabidopsis that could control the plants response to stressors, which can lead to the plant’s death. She and her collaborators had identified a protein in Arabidopsis that seemed to control whether a plant would live or die under stress conditions.

Having identified the gene was just the beginning of the story, despite being years into the journey. It would take five more years to get to this new paper.

The researchers discovered that the proteins BON-associated protein 2, or BAP2, and inositol-requiring enzyme 1, or IRE1, work together when dealing with stress conditions—a matter of life and death for plant cells.

Understanding how these proteins function can help researchers breed plants that are more resilient to death conditions.

Creating plants that are more resistant to endoplasmic reticulum stress, or ER stress, has widespread implications in agriculture. If crops can be made to be more resilient in the face of drought or heat conditions, the plants stand a better chance of surviving and thriving, despite the changing climate.

“Research in our lab is fueled by enthusiasm and gratitude to be able to make important contributions to science,” said Federica Brandizzi, MSU Research Foundation Professor in the Department of Plant Biology and at the PRL. “The work was herculean, and has been possible only thanks to the patience, enthusiasm and dedication of a wonderful team. Noelia was simply fantastic.”

Working in tandem

Within eukaryotic cells is an organelle known as the endoplasmic reticulum, or ER. It creates proteins and folds them into shapes the cell can utilize. Like cutting up vegetables to use in a recipe, the proteins must be formed into the right shape before they can be used.

Protein making and protein folding capacity must be in balance, like a sous chef and a chef, working in tandem. If the sous chef is providing the chef with too little or too many ingredients, it throws off the balance in the kitchen.

When the ER cannot properly do its job, or the balance is thrown off, it enters a state known as ER stress. The cell will jumpstart a mechanism known as the unfolded protein response, or UPR, to decide what to do next. If the problem can be resolved, the cell will initiative life saving measures to resolve the problem. If it cannot be, the cell begins to shut down, ending its and potentially the plant’s life.

It was known that the enzyme IRE1 was responsible for directing the mechanisms that would either save the cell or kill it off.

But what calls IRE1 to action?

In this study, the Brandizzi lab researchers were searching for the master regulator of these pro-death processes, known as programmed cell death.

“I had the idea because I read that irritable bowel disease is linked to a mutation in a gene controlled by IRE1 that occurs among humans,” Brandizzi said. “Humans are diverse and so are plants. So I thought to look into plant diversity as a source of new important findings in the UPR.”

The researchers started by looking at hundreds of accessions, or plants of the same species but specific to one locale. For example, a plant that grows in Colombia will have genetic variations to the same species of plant that grows in Spain, and the ways they each respond to stress conditions could differ.

They found extensive variation in the response to ER stress between the different accessions. Taking the accessions whose responses were the most dissimilar, they tried to identify the differences in their genomes. This is where the BAP2 gene candidate came into play.

“We found that BAP2 responds to ER stress,” said Pastor-Cantizano, who is currently a postdoc at the University of Valencia. “And the cool thing is that it is able to control and modify the activity of IRE1. But also IRE1 is able to regulate BAP2 expression.”

BAP2 and IRE1 work together, signaling to each other what the best course of action for the cell is. Having one without the other results in the death of the plant when the ER homeostasis is unbalanced.

Seven years

From start to finish, this project took over seven years of dedicated work.

Day in and out, the researchers spent their time tediously placing seeds onto plates with a medium in which they could grow. Arabidopsis seeds are not much larger than grains of sand at their smallest, so this was delicate work that required time and attention.

From there, the researchers spent several more months with these plants, looking at the accessions offsprings and identifying how BAP2 worked within the plants. This took another few years.

“It has been a long road with its obstacles, but it has been worth it,” said Pastor-Cantizano. “When I started this project, I couldn’t imagine how it would end.”

An often-overlooked component of natural and human-driven disasters is their potential to affect plant health and thus food security at domestic and international scales. Most disasters have indirect effects on plant health through factors such as disruptions to supply chains and damaged infrastructure, but there is also the potential for direct effects from disasters, such as pathogen or vector dispersal caused by floods, hurricanes, and human migration.

These occurrences are rarely isolated and instead often occur simultaneously. We have seen examples of the concurrence of disasters in recent history through events such as market disruptions in the early days of the COVID-19 pandemic; the intense wildfires, hurricanes, and tornadoes that have ravaged in the years since 2020; the Ukraine-Russia war disrupting the global wheat supply; and so on.

The impacts of natural disasters on plant health can be seen after events such as when the soybean rust pathogen, Phakopsora pachyrhizi, was first detected in the United States in Louisiana shortly after Hurricane Ivan in 2004. Hurricane Ivan moved north from the lower Caribbean near Colombia and is believed to have moved spores into the United States.

Insect pests can also travel long distances during strong wind events. Bean golden yellow mosaic virus was likely introduced to Florida by Hurricane Andrew in 1992, which carried viruliferous whiteflies from the Caribbean islands. Bean golden yellow mosaic virus caused the reduction or collapse of bean production the following year and became established in Florida. Wildfires also pose a significant risk for the spread of plant pathogens.

Fire can damage forest ecosystems, leaving gaps that become habitats open to colonization by invasive pests and pathogens. For example, wildfires in California devastated the coastal mountain range, and new plantings to restore these areas were unknowingly contaminated with Phytophthora tentaculata, a quarantined pathogen that can cause root and crown rot. This has led to more complications, as forest managers now need to control both introduced diseases and future wildfires.

Human-driven disasters, such as armed conflicts, can also create conditions that are favorable to the spread of plant pathogens, leading to devastating consequences for crop production, food security, and overall instability in affected regions. Unrest may force farmers to rely on poor-quality seed with a higher risk of disease, resulting in low yields.

The current war in Ukraine is an example of how all countries are vulnerable to armed conflict, which not only leads to crop loss and disease spread but also disrupts the global exchange of commodities. The invasion of Ukraine disrupted the global wheat supply and caused a 50% increase in global fertilizer prices due to Russia’s significant role as a supplier, accounting for 13% of the world’s fertilizer production. In the twenty-first century, poverty, political unrest, and inefficient regulation have significantly influenced the development of major plant disease epidemics.

With the increase in frequency and severity of these disasters, a cross-disciplinary team of researchers and humanitarian experts from the United States, Benin, Ecuador, Kenya, the Netherlands, Peru, Tanzania, and Thailand and led by Berea Etherton from the Garrett Lab at the University of Florida, Gainesville, published “Disaster Plant Pathology: Smart Solutions for Threats to Global Plant Health from Natural and Human-Driven Disasters” in the journal Phytopathology.

The framework highlighted in the article provides a multidisciplinary perspective on current threats and solutions to plant health and food security, encompassing the risk from environmental factors such as climate change, while also including factors such as political instability and war. The international team utilized the One Health framework, which addresses the interconnections among human, animal, plant, and environmental health.

Disaster plant pathology provides a framework focusing on the impact of disasters on plant health, plant pathogens, and agricultural systems for tailored solutions and informed decision making. This framework promotes interdisciplinary collaboration, making it of common interest for communities of plant pathologists, humanitarian groups, economists, computer scientists, meteorologists, and sustainable development strategists.

Disaster plant pathology offers solutions through “smart agriculture.” Utilization of the robust capabilities of artificial intelligence (AI) can provide early warning information systems, risk assessment, crop monitoring, supply chain optimization, decision-support, real-time monitoring, and resilience strategies. There is potential for farmers and agricultural authorities to use these tools to make informed decisions and facilitate recovery efforts, thus minimizing the impact of disasters on agricultural systems.

Through the integration of satellite imagery, weather data, disease incidence reports, early warning systems, and other relevant information, these models can identify patterns and predict the trajectory of pathogen movement. Farmers and agricultural authorities can use these models to take preventive measures in areas at high risk of infection, effectively managing the spread of disease and accelerating recovery.

The interactions among natural and human-driven disasters, plant disease, and global food security are critical concerns that demand expertise and knowledge from scientists working in disaster plant pathology. Disaster plant pathology recommends actions for improving food security before and following disasters, including:

1. strengthening regional and global cooperation,
2. capacity building for rapid implementation of new technologies,
3. effective clean seed systems that can act quickly to replace seed lost in disasters,
4. resilient biosecurity infrastructure and risk assessment ready for rapid implementation, and
5. decision support systems that can adapt rapidly to unexpected scenarios.

Through predictive analyses, early warning systems, and real-time crop monitoring, humanitarian aid and governmental interventions can help to ensure the quality and safety of agricultural production for growers. The experts behind disaster plant pathology hope this framework incites collaboration at an international scale.

Lead author Etherton said, “Our team of global researchers and humanitarian experts synthesized current knowledge about disaster effects and strategies for planning and response. We developed this new perspective, disaster plant pathology, so that others working to protect plant health and food security can build on it.”

These intricate relationships require global cooperation, and in the face of climate change and geopolitical complexities, a collective and proactive response is needed to protect plant health.