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The role of chromatin in the long-term adaptation of plants to abiotic stress

Periodic Reporting for period 4 - CHROMADAPT (The role of chromatin in the long-term adaptation of plants to abiotic stress)

Reporting period: 2021-11-01 to 2022-10-31

Abiotic stress is a major threat to global crop yields and this problem is likely to be exacerbated in the future. Therefore, it is very important to engineer crop plants with improved stress tolerance. A large body of research has focussed on the immediate stress responses. However, in nature stress is frequently chronic or recurring, suggesting that temporal dynamics are an important, but under-researched, component of plant stress responses. Indeed, plants can be primed by a stress exposure such that they respond more efficiently to the next stress incident. Such stress priming and memory may be particularly beneficial to plants due to their sessile life style. Typically, the memory of priming lasts for several days after the end of the stress. During the past few years, my group has initiated the molecular analysis of heat stress memory in Arabidopsis thaliana. Heat stress memory is associated with sustained gene induction and transcriptional memory and we have demonstrated that this involves lasting chromatin changes. The underlying molecular mechanisms, however, remain poorly understood.
With climate change, losses in crop productivity are likely to become more severe. The exploitation of stress priming and memory for improving stress tolerance of crop plants holds great potential, because acute induction of stress tolerance mechanisms is often correlated with a reduction in growth due to reallocation of nutrients or as an adaptation to stress conditions.
In the CHROMADAPT project we combined mechanistic dissection of heat stress memory in A. thaliana with concomitant translation of the results into the temperate cereal crop barley. In particular, we focused on the following questions: How does chromatin structure affect and regulate heat stress memory? How do the transcription factors involved mediate memory-specific outputs? How do histone modifications during stress memory interact with transcription, chromatin and nuclear organization? Is heat stress memory conserved in temperate cereal species? Can we engineer plants with improved stress memory? Using existing tools and new methodologies, the analyses yielded unprecedented insight into the long-term adaptation of plants to abiotic stress and opened up strategies for breeding stress-tolerant crops.
Our main goal was to unravel the molecular basis of heat stress memory and how chromatin regulation is involved in this process. We have identified two types of transcriptional memory; in the first type gene expression is sustained after heat stress has subsided, while in the second type gene induction is elevated after a recurrent stress compared to a primary stress. To identify protein components that regulate the transcriptional memory, we have performed a mutagenesis screen. From this we identified several FORGETTER (FGT1) genes. When they are mutated the plant has a reduced capacity for heat stress memory. Our findings show that FGT1 acts at so-called memory genes to maintain low nucleosome occupancy throughout the memory phase. This supports continuation of active transcription, probably by providing less obstacles to RNA Polymerase II. We also identified FGT3, which encodes a transcription factor that is specifically induced during the recovery phase and activates expression of memory genes. Through purification of FGT3-binding proteins and subsequent protein identification analysis, we have isolated several new putative regulators of heat stress-induced transcriptional memory. In another objective of the project we have characterized the physiological heat stress memory in a cereal crop and identified regulators of HS memory. The mechanism appears highly conserved between monocots and dicots. We performed targeted epigenetic editing to functionally confirm the role of histone modifications in HS memory.
The project will provide mechanistic insight into a memory process that is independent of a nervous system; second, it will elucidate the molecular function of two proteins that are highly conserved in mammals and are relevant for pathologies; third, this project will unravel the conservation of HS memory in temperate cereals and indicate strategies for new breeding approaches for heat-tolerant crops.

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