Dr Martin Balcerowicz
Temperature shapes plant growth
Plants display a remarkable degree of developmental plasticity: they constantly adjust their growth and morphology in response to their surroundings to maximise fitness and reproductive success. Temperature is arguably one of the most influential factors impacting plant fitness as it affects the rate of every physical and biochemical reaction; it is therefore of vital importance for the plant to be able to sense its temperature environment. With the progression of climate change, plants in temperate regions such as the UK are challenged by more frequent heat waves as well as an overall rise in temperature, and these effects already impact crop production: in wheat and barley, each 1 °C increase above optimal growth temperature is estimated to reduce crop yield by 5-6%. Gaining a deeper understanding of how plants perceive temperature cues and translate them into appropriate developmental and physiological responses is thus a central question in both fundamental plant science and agriculture.
In my lab we mainly use the model plant Arabidopsis thaliana to understand the fundamental processes of plant temperature signalling (Figure 1A). In Arabidopsis, prolonged exposure to warm temperatures triggers a set of developmental responses that we collectively refer to as thermomorphogenesis: plants show increased elongation growth of the hypocotyl (embryonic stem) and primary root, an upward bending of the leaves, reduced formation of stomata (microscopic pores for gas exchange and evaporation) as well as accelerated flowering and seed set. In addition to Arabidopsis, we are also looking to translate some of our research into barley;(Figure 1B), one of the UK’s staple crops, whose development and yield are highly sensitive to ambient temperature.
Sensing temperature at the molecular level
Research in the past two decades revealed that the protein family of PHYTOCHROME INTERACTING FACTORS (PIFs) acts at the heart of temperature signalling in Arabidopsis. These transcription factors control expression of a large set of genes in a temperature-dependent manner and thereby affect many aspects of thermomorphogenesis. But expression of PIFs is itself highly temperature-sensitive (Figure 2): transcription of the PIF4 gene increases when temperatures rise, which, in addition with increased protein stability, leads to strong accumulation of PIF4 protein in the heat. In case of PIF7, we find that warm temperatures do not affect its transcription, but enhance its translation rate, i.e. how much protein is made from its transcript. This process is in part mediated by a thermosensitive RNA structure (RNA thermoswitch), which changes its conformation upon a temperature shift (Chung*, Balcerowicz* et al., 2020). Similar structures exist in other transcripts, but whether they fulfil a similar function is yet unknown.
Using a combination of genetics, molecular biology, biochemistry and omics approaches, we pursue the following objectives:
- Identify novel regulators of the warm temperature response mining our RNA-seq and ribosome profiling datasets;
- Understand the mechanisms by which warm temperature selectively affects the translation of temperature signalling genes;
- Harness these mechanisms to customise a gene’s temperature sensitivity, with the long-term goal to render plants more resilient towards a changing climate.
Integrating light and temperature information in space and time
Temperature cues are not perceived in isolation but are integrated with a variety of other environmental and endogenous signals. In Arabidopsis, light and temperature sensing is particularly intertwined, using a largely overlapping set of genes including PIFs (Balcerowicz, 2020). Consequently, the expression of many genes is co-regulated by both signals, beautifully exemplified by the burst in gene expression observed at dawn (Balcerowicz*, Majhoub* et al., 2021). Looking closely at the developmental signalling programmes downstream of light and temperature signals, we find that plant hormones such as auxin, brassinosteroids and gibberellin feature prominently among them. These downstream programmes are believed to be highly dynamic, to change over time and to differ across tissues and organs. Until recently, however, we lacked the necessary tools to look at these processes directly and with high spatiotemporal resolution; hence, the precise nature of these temporal and spatial differences, and how they are established, remains largely unexplored.
To overcome these restrictions, we employ the newest generation of plant hormone biosensors in combination with precise genetic perturbations that allow visualisation of signalling processes in near real-time down to the cellular level. High resolution bioimaging using these tools, alongside state-of-the-art biochemical and transcriptomic approaches, allows us to pursue the following objectives:
- Characterise how molecular processes that are triggered by light and temperature signals change over time and differ across tissues and organs;
- Identify factors that provide spatial and temporal specificity to these light- and temperature-controlled processes.
Selected Research Articles
Balcerowicz, M.*, Mahjoub, M.*. Nguyen, D., Lan, H.. Stoeckle, D., Conde, S., Jaeger, K., Wigge, P., Ezer, D. (2021) An early-morning gene network controlled by phytochromes and cryptochromes regulates photomorphogenesis pathways in Arabidopsis. Mol. Plant 14: 983-996 (* shared first authors)
Chung, B.Y.W.*, Balcerowicz, M.*, Di Antonio, M., Jaeger, K.E., Geng, F., Franaszek, K., Marriot, P., Brierley, I., Firth, A.E., Wigge, P. (2020) An RNA thermoswitch controls daytime growth in Arabidopsis. Nat. Plants 6: 522-532 (* shared first authors)
Balcerowicz, M., Kerner, K., Schenkel, C., Hoecker, U. (2017) SPA Proteins Affect the Subcellular Localization of COP1 in the COP1/SPA Ubiquitin Ligase Complex during Photomorphogenesis. Plant Physiol. 174: 1314-1321.
Balcerowicz, M., Ranjan, A., Rupprecht, L., Fiene, G., Hoecker, U. (2014) Auxin represses stomatal development in dark-grown seedlings via Aux/IAA proteins. Development 141: 3165-3176.
Balcerowicz, M.*, Fittinghoff, K.*, Wirthmueller, L., Maier, A., Fackendahl, P., Fiene, G., Koncz, C., Hoecker, U. (2011) Light exposure of Arabidopsis seedlings causes rapid de-stabilization as well as selective post-translational inactivation of the repressor of photomorphogenesis SPA2. Plant J. 65: 712-723. (* shared first authors)
Balcerowicz, M., Shetty, K. N., Jones, A. M. (2021) Fluorescent biosensors illuminating plant hormone research. Plant Physiol. 187: 590-602.
Balcerowicz, M. (2020) PHYTOCHROME‐INTERACTING FACTORS at the interface of light and temperature signalling. Physiol. Plant. 169: 347–356.
Balcerowicz, M.# and Hoecker, U. (2014) Auxin – a novel regulator of stomatal development. Trends Plant Sci. 19: 747-749. (# corresponding author)