Keech, Olivier - Stress-induced senescence and its subsequent metabolic regulations

Research

Olivier Keech sitting at the desk in his office

Photo: Fredrik Larsson

Our research explores several aspects of the regulation of plant metabolism in response to stress, with a particular emphasis on mitochondrial metabolism. In plants, the process of aging as well as many environmental constraints may lead to the death of leaves. This particular type of cell death is often referred to as leaf senescence and can have a profoundly negative impact on crop yields and post-harvest shelf-life.

Aim: Leaves are essential plant structures and their well-being is crucial for plant development and survival. When a stress is applied, a plant has two options: try to cope with it or induce senescence and reallocate valuable nutrients towards new, developing or storage organs. A mutual antagonistic relationship can summarize this phenomenon as shown in figure 1. Our aim is to understand how the plant validates senescence over an adaptation strategy in response to stress (Fig. 1). This work mainly covers two aspects: 1) to unveil the communication and signalling mechanisms controlling the induction of leaf senescence and 2) to determine the subsequent metabolic regulation that occurs in response to stress, and ultimately during leaf senescence.

Illustration about the relationship between adaptation and senscence including metabolic/redox balance, hormonal homeostasis, gene regulatory network and different types of stress

Figure 1: Mutual antagonistic relationship between adaptation and induction of senescence in response to a stress (e.g. nutrient deficiency, light regime, temperatures, pathogene infection, etc).

1. Using dark-induced senescence as a proxy to decipher signalling pathways controlling the induction of leaf senescence

In earlier studies (Keech et al., 2007; Law et al., 2018), we have shown that a leaf from a plant entirely darkened (DP) can survive much longer than an individually-darkened leaf (IDL; Fig. 2), which suggests that upon the right signals, the induction of leaf senescence can be repressed and alternative metabolic strategies conferring extended longevity can occur.

On the left side, an individual leaf was darkened and this leaf turned yellow after 6 days of treatment. On the right side, an entire plant was darkended and stayed mostly green after 6 days of treatment.

Figure 2: Experimental setup for the two darkening treatments (Weaver and Amasino, 2001; Keech et al., 2007; Law et al., 2018).

Yet, our current knowledge on the respective metabolic adjustments remains highly fragmented. In 2018, we proposed the following working models (Fig. 3).

Illustration summarising metabolic strategies in plant leaves to darkening

Comic strip by Neil E. Robbins II illustrating the effects of shading in plants

Figure 3: A) Model summarising the different metabolic strategies employed by plants in response to partial or total darkening of the plant. Size and line-weight of the fonts and arrows are proportional to their implication to these metabolic processes. The large arrow behind the leaf in DP conditions depicts the conserved metabolic strategy main-tained between 3 and 6 days of darkening. Abbreviations: AAA - aromatic amino acids, BCAA - branched chain amino acids, Citr - citrate, mETC - mitochondrial electron trans-port chain, OAA - oxaloacetate, PPP - pentose phosphate pathway, Shik/Chor - shikimate/chorismate, TCA - tricarboxylic acid cycle (Law et al., 2018); B) "Are plants afraid of the dark?" Comic strip by Neil E. Robbins II explaining the content of the publication in a humoristic way. Find the full comic strip here: https://neilercomics.com/2018/05/18/are-plants-afraid-of-the-dark/

However, in order to challenge these hypotheses, we are currently investigating the metabolic regulations in a set of functional stay-green mutants issued from a genetic screen. This provides us with a much valuable tool to determine how cells can survive prolonged stress conditions.

2. Regulation of metabolism during leaf senescence

In a green leaf, the three energy organelles (peroxisome, mitochondrion and chloroplast) work in synergy to sustain an efficient assimilation of carbon while constantly maintaining the essential functions of the cell. However, when a leaf undergoes senescence (“yellowing”), whole cell-metabolism is drastically modified, and as chloroplasts are rapidly getting impaired, the remaining organelles acquire novel functions, particularly the mitochondrion. In animals, mitochondria have been shown to integrate various signals and to subsequently modulate cell death processes whereas in plants, the contribution of mitochondria in cell death regulation remains unclear, particularly during leaf senescence.

Therefore, we are currently investigating in more detail the role of mitochondria during both developmental (i.e. aging) and stress-induced leaf senescence (Fig. 4). Illustration of metabolic processes in the mitochondrium Figure 4: Production of glutamate, reducing equivalents and TCA cycle intermediates from catabolic reactions occurring in the mitochondrion during developmental leaf senescence (Chrobok et al., 2016). Transcriptomic overview of the mitochondrially localised portion of the following metabolic pathways: (I) Lysine degradation, (II) branched chain amino acid degradation, (III) D-2HG metabolism, (IV) Glycine and Alanine metabolism, (V) Urea Cycle and (VI) Proline metabolism. Specific genes of these pathways and their transcript abundance during developmental leaf senescence are illustrated here. Production of reducing equivalents is shown as an arrow with an electron (e-).

3. Towards sustainable food production

Among a few other things, we are also interested in complementary alternatives for food production systems. In particular, we are involved in several projects aiming at developing integrated aqua-agro systems in closed land-based units. The strategic implementation of numerous trophic layers within a production system is a natural way to achieve a higher sustainability while maintaining the whole production economically viable.

A concept scheme (Fig. 5), released for the PLATSEN* event end of 2016 depicts some of the interrelationships between the different trophic layers that can be implemented to for example urban farming system in order to achieve a circularity, i.e. a better use of biowaste, energy and resources.

Depiction of the nutrient cycle between the different components of the eMTE model

Schematic overview of the eMulti-Trophic Ecosystem (eMTE) concept

The eMulti-Trophic Ecosystem – a potential model for sustainable food production from Umeå University on Vimeo. Interview with Olivier Keech at PLATSEN in 2016 about the eMTE project. More information about the eMTE project and the exhibition at PLATSEN in 2016.

PLATSEN is thought as a platform where decision makers, politicians, scientists, NGOs and people from public and private sectors can meet and exchange and discuss ideas about sustainability in an urban environment. The 2016 event was initiated by the Swedish Scientific Council for Sustainability in collaboration with several other actors from the public and private sectors e.g. Umeå Municipality and Umeå University.