Tackling plant growth-defense trade-offs by characterizing the role of PRL1 in Jasmonate responses

Project Information

SWEET JAZ

Grant agreement ID: 895792

DOI

10.3030/895792

Project closed

EC signature date 28 February 2020

Start date 1 April 2020

End date 31 March 2022

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 174 806,40

EU contribution

€ 174 806,40

Coordinated by

LEIBNIZ-INSTITUT FUR PFLANZENBIOCHEMIE
Germany

Periodic Reporting for period 1 - SWEET JAZ (Tackling plant growth-defense trade-offs by characterizing the role of PRL1 in Jasmonate responses)

Reporting period: 2020-04-01 to 2022-03-31

Summary of the context and overall objectives of the project

One of the key challenges beyond the 21st century will be food security. The entire human population is directly dependent on plants as vital sources of oxygen, food, medicines and other economically important products. Abiotic and biotic challenges pose serious risks to plant growth and crop production world-wide. Therefore, understanding how plants activate defense responses against environmental stresses represents a tremendous opportunity to improve plant yield and meet the agricultural output goals to feed the predicted ~10 billion human population by 2050. Insect pests in particular pose a significant threat to plant yield, crop production and food supply. Recent reports are alarming across the globe, with predictions that the occurring climate change and pesticide resistance will nearly double crop losses due to insects. The plant hormone Jasmonate (JA) is essential to protect plants against insect herbivory, mechanical wounding and necrotrophic pathogens. Upon these challenges, JA hormone levels increase and induce defense responses while stunting growth. Hence, understanding how plants balance growth-defense trade-offs during environmental stresses represents a tremendous opportunity to improve plant yield and meet the global need for increased food production. Through an extensive genetic approach in the model plant Arabidopsis thaliana, the host lab has identified PLEIOTROPIC REGULATORY LOCUS 1 (PRL1) as new putative regulator of the JA pathway. PRL1 is also known for its role in sugar signaling and metabolism, representing a probable integration node for balancing growth during stress responses. Hence, SWEET-JAZ aimed to characterize the role of PRL1 in activating the JA pathway and uncover how are sugar and defense signaling integrated during insect and fungal attacks. Specifically, the project used state-of-the-art cell biology, biochemistry and molecular biology approaches to answer the following questions: 1. How does PRL1 regulate JA responses? 2. How does PRL1 impact cell-type specific JA-mediated defense strategies? 3. How are PRL1- and JA-signaling pathways integrated? 4. What is the role of PRL1 in plant defense responses against insect herbivory and fungal pathogens? Overall, the longer term goal of the project is to contribute towards solving the current food security issues by providing novel targets and strategies granting plant resilience.

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

By using the cellulose deficient mutant korrigan1 (kor1), we have found that enlarged root cells resulting from weaker cell walls exert mechanical stress within tissues and activate JA biosynthesis (Mielke et al 2021). Specifically, enlarged root cortex cells lead to hormone production in endodermal and pericycle cells. The constitutive JA phenotype in kor1 could be restored to wild type conditions by (i) expressing the KOR1 protein specifically in cortex cells, by (ii) remodeling the cell wall composition via ESMERALDA 1, and by (iii) reducing turgor pressure with hyper-osmotic treatments, which also restored the cortex cell size and mechanical stress. In turn, the increase of root water uptake lead to root cell swelling and JA upregulation even in WT plants subjected to hypo-osmotic conditions. These findings revealed the importance of osmo-regulation in guiding hormone biosynthesis and established the basis to further characterize the molecular relationships between key osmo-regulators and hormone production. In fact, mutations in PRL1 also suppressed the JA phenotype in kor1. We used an extensive cell biology approach to characterize how genetic and chemical perturbations impact root morphology, growth and defense activation in prl1 mutants. Importantly, plant-insect bioassays further highlighted the importance of our work in understanding plant disease resistance. Outcomes of the SWEET-JAZ projects increased our basic understanding of the major plant defense hormone JA and its interplay with sugar signaling. This gain in fundamental knowledge, has the potential to inspire new strategies for crop improvement. The experimental results will be published in a peer-reviewed paper and the primary data will be made available through public repositories. In addition, we have also contributed to the understanding on how cellulose deficiency leads to disease resistance against the vascular pathogen Fusarium oxysporum (Menna et al 2021).
Open-access peer-review research articles
Two research articles with experiments performed in this project have already been published and recommended by Faculty Opinion:
1. Menna A, Dora S, Sancho-Andrés G, Kashya A, Meena MK, Sklodowski K, Gasperini D, Sánchez-Coll N, Sánchez-Rodríguez C (2021) A primary cell wall cellulose-dependent defence mechanism against vascular pathogens revealed by time-resolved dual-transcriptomics. BMC Biology, 19:161
2. Mielke S, Zimmer M, Meena MK, Dreos R, Stellmach H, Hause B, Voiniciuc C, Gasperini D (2021) Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression. Science Advances, 7(7): eabf0356
- preprint at BioRxiv, https://doi.org/10.1101/2020.09.29.319012
- Recommended by Faculty Opinions, https://facultyopinions.com/prime/739528667?ref=ypp

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)

Plant-insect herbivory and the molecular and biochemical basis of plant defense are active and important research areas. Due to the ongoing climate change and the toxic effects of pesticides, understanding the molecular mechanisms of plant-insect and plant-pathogen interactions is of utmost importance for granting food security. Pesticides have been serving a critical role in crop protection strategies, but their negative impact on the environment and human health are restricting their use. At the same time, pest abundance poses a significant threat to agronomical systems. Findings from the SWEET-JAZ project extend beyond the characterization of prl1 mutants in Arabidopsis thaliana, as they provide new knowledge on how plants balance sugar and defense signaling. Global warming and emerging pesticide tolerance in pathogens demand for safer and innovative solutions. In the long run, our understanding of plant defense responses in Arabidopsis is expected to assist in the development of strategies and protection policies to mitigate environmental change impacts on crop production. Therefore, the SWEET-JAZ project contributes toward solving the current and future food security issues by providing valuable scientific knowledge and tools for scientists, agronomists, and policymakers.

SWEET JAZ