Plasmodesmata: gatekeepers for cell-to-cell viral spread in plants

Project Information

PDgate

Grant agreement ID: 101023981

DOI

10.3030/101023981

Project closed

EC signature date 22 March 2021

Start date 1 May 2021

End date 30 April 2023

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 174 806,40

EU contribution

€ 174 806,40

Coordinated by

HEINRICH-HEINE-UNIVERSITAET DUESSELDORF
Germany

Periodic Reporting for period 1 - PDgate (Plasmodesmata: gatekeepers for cell-to-cell viral spread in plants)

Reporting period: 2021-05-01 to 2023-04-30

Summary of the context and overall objectives of the project

Viruses cause epidemics on all major cultures of agronomic importance, representing a serious threat to global food security. Widely employed in fields, the use of plant varieties carrying genetic resistances constitutes the most effective, economic, and ecological measure to control viral infections. However, these virus control measures are not available for all viruses and crops, and resistance can be overcome by evolved and new viruses. The emergence and spread of infectious viral diseases is associated to intrinsic viral and host components, as well as to environmental, agronomical and socioeconomical factors. Importantly, global warming and climate instability increase the difficulties in controlling viral diseases and promote the proliferation and expansion of emerging viruses. As obligate pathogens, viruses rely on the host machinery to multiply and invade their host. For successful infection, plant viruses must propagate from the initially infected cells to the rest of the plant. Cell-to-cell movement is critical for spread, and thus an ideal point for creating resistance. First, the virus moves intracellularly from the replication sites to plasmodesmata (PD), which are cytoplasmic communication channels crucial for the development and physiology of the plant. PD regulate the transport of signaling molecules such as proteins, RNAs, hormones, and metabolites. Selected molecules can pass PD on various different routes and PD can act as gatekeepers, indicating that they are complex machines. Plant viruses can exploit PD and has the ability to gate them increasing the size exclusion limit, enabling the spread of infectious particles. However, the ‘receptors’ by which viruses recognize PD and the mechanism of transport remain largely unidentified.
The mission of the PDgate project is to elucidate the molecular mechanisms used by plant viruses to exploit and spread through PD. This project offers the opportunity to identify and characterize potential targets for the development of improved crop plants against plant viruses, which is especially important for food production and food security. Since a new generation of resistant crops will be generated, it would also reduce pesticide use and minimize the spread of viruses due to global trade.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The research of the project was done in three work packages (WP1-WP3). WP1 included the identification of host PD components involved in viral infection. I generated Arabidopsis plants expressing TbID biotin ligase, set up the condicitons for labeling and pull-down of biotinylated proteins. We were able to identified 113 proteins in the vecinity of the TMV MP. In the WP2 I validated some of these candidate proteins and study their subcellular localization. Currently, I am study their role in the viral cell-to-cell transport and infection (WP3).
During the work on research projects, I supervised one master student (thesis defended on April 2023) and two PhD students (ongoing). In addition, I was involved in teaching in the Master Module 1203 at the Heinrich Heine University.
I have received training in advanced microscopy and quantitative proteomics. Further, I participated in the Academic Career Development Programme at HHU to advance my skills relating to leadership, science communication, and management. I have initiated fruitful collaborations with world leading scientists in developmental genetics (Prof. Rüdiger Simon), proteomics (Prof. Waltraud Schulze) and structural biology (Prof. Wolfgang Baumeister).
Results of my research was reported in 3 papers and 3 underway. The work has been presented in two conferences and the research has been popularized by social media.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

Owing to its multidisciplinary nature and the topic addressed, PDgate may yield long-lasting breakthroughs in different fields.

Scientific progress.- This proposal will lead to a series of groundbreaking outcomes in the field of plant virology, and will also open new avenues of research in the area of plant physiology, as transport through PD is also essential for carbon allocation and hormone signaling, both crucial processes in food production and pathogen defense. The development of novel concepts, methodologies and virus resistant plants are by themselves major insights that will derive from PDgate. The fundamental understanding gained of the viral proximity maps will push the frontiers of knowledge in plant virology. In addition, the novel multidisciplinary approach with the high-end- technologies that I am applying has never been explored so far in plant biology. The impact of PDgate goes beyond narrow categories of viral strains or host plants thanks to the complementary used of TMV as a model for ssRNA viruses (over 80% of known plant viruses). The new insights would be thus easily applicable to other plant virus. This maximises the importance of this proposal, since key insights will be established regarding the virus-host arms race. For example, proximity labeling workflow could be directly applied to other plants belonging to the tobamoviruses host range or to new viral species by developing new plants.

Climate change impact and socioeconomic aspects.- Plant virus infections account for global economic losses estimated in 30 billion annually and are responsible for nearly 50 % of plant diseases worldwide. Global warming and climate instability are promoting virus infections and virulence due to rising temperatures, the introduction of species into previously uncultivated areas, and the proliferation of vectors in new ecosystems. In addition, these new conditions increase virus epidemics and the appearance of emerging viruses against which there are often no sources of resistance. PDgate is a breakthrough proposal focused on the generation of new antiviral targets and developing new resistant crops through the study of viral transport and host response.
Efficient strategies targeting sustainable primary production are required and encouraged by EU policy. PDgate deals with the global challenges of Horizon Europe programme, specifically the cluster 6 “Food, Bioeconomy, Natural Resources, Agriculture and Environment” that aims to ensure food security and sustainable primary production. PDgate tackles some priorities of this cluster 6 premises: 1) strengthen agriculture contribution to the mitigation of greenhouse gas emissions and climate change effects, 2) making plants resistant to disease, 3) providing alternative approaches to pesticides, 4) deal with emerging risks, 5) avoid supply chain disruptions due to diseases or abiotic stresses, and 6) ensure consumer confidence in food security by mitigating the potential risks to plant health.
The production of pesticides is an important source of greenhouse gas emissions and their extensive use causes the appearance of pest resistance. The control of vectors that transmit viruses through the use of pesticides is a common practice in crop production. PDgate will help in the identification of antiviral genes that can be then study in crop plants and make them immune to viral infection that would reduce the use of pesticides, providing safer, more efficient and more environmentally friendly agricultural products. Such approaches are particularly important as the world population continues to grow–it will hit 7.5 billion this year and it is projected to reach 9.6 billion by 2050– and climate change progresses, putting global food security at risk.

Virus systemic infection. From cell-to-cell to phloam loading and spread