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BLINKing stomata: an optogenetic approach to improve plant growth and water use

Photosynthesis needs water. Guest blogger Maria Papanatsiou has a new way of increasing water efficiency in plants, enabling them to do more with less.

Stomata are pores that are unique to plants and found on the epidermis of most aerial tissues. Stomata act as gatekeepers to allow the entry of carbon dioxide (CO2) into the leaf for photosynthesis at the expense of water vapour loss via transpiration. Opening and closing of stomata is controlled by guard cells, which swell up and shrink as ions move in and out of them, respectively (Figure 1).

Figure 1: Opening and closing stomata.

During stomatal opening, osmotically active solutes accumulate inside guard cells that increases the solute concentration resulting in greater osmotic pressure inside the cell. This imbalance of solutes between the inside and outside of the plasma membrane must be balanced by water flow into the cell that eventually causes changes in turgor pressure. An increase in turgor pressure forces the plasma membrane against the cell wall resulting in the enlargement of the guard cells that eventually bow outwards causing the stomatal pore to open. As solutes exit guard cells, the cell volume is decreased, causing the pore to close. Guard cell turgidity and volume changes in response to various environmental conditions such as atmospheric CO2 concentration, light, and water availability. Guard cells are great model systems to study ion transport, and to dissect the molecular links between plant physiology and the environment.

There are many studies investigating the interplay between stomata and the environment, but most of them are focusing on an individual environmental signal that is also often non-variable throughout the day, such as light intensity or temperature. In nature, plants face multifaceted and cumulative effects of climate change that often combine conflicting environmental cues such as high light intensities and droughts. Therefore, plants have to coordinate the molecular mechanics of stomata to ensure their growth and performance under a given environmental scenario. Similarly, plants need to decode the complicated signals arising from environmental conditions that fluctuate throughout the day, such as when clouds pass overhead or when shaded by neighbouring plants. In such a case, the photosynthetic machinery rapidly adjusts to the light conditions while the stomatal responses generally lag behind, either making photosynthesis less efficient or allowing excessive water loss. Slower responsiveness of stomata to light fluctuations impacts on plant growth and productivity.

Crop irrigation accounts for roughly 70% of fresh water use on the planet, and its use has expanded at unsustainable rates over the past three decades. Scientists have been trying to find ways to make plants grow with less water by maximizing the water use efficiency –squeezing the maximum amount of carbon fixed per unit of water used. Reducing the number of stomata results in less water loss. Yet, such attempts can come at the expense of reduced CO2 uptake and therefore reduced water use efficiency. From an agronomic point of view, this approach negatively impacts gain yields, making it not sustainable. Moreover, this approach will be beneficial only under certain environmental scenarios of prolonged duration, e.g. persistent drought periods, that are not necessarily often a true image of what is met in the field.

To bypass this inherent coupling of CO2 uptake and water vapour loss, Papanatsiou et al. (2019) used optogenetics to introduce a synthetic blue light-activated K+ ion channel, named BLINK, into the guard cells of the small mustard plant Arabidopsis. Optogenetics is a well-established technique used in the neurosciences to manipulate ion channel activity and modulate nervous signal transmission by using a light stimulus. The authors hypothesized that by using optogenetics they might modulate ion transport in guard cells of stomata to better synchronise stomatal movements in response to fluctuating light conditions and, as consequence, improve plant performance (Figure 2).

Complex diagram
Figure 2. BLINK protein speeds up stomatal movements in response to light fluctuations resulting in improved plant growth and water use. Doodle art created by Dr Mathis Riehle.

The authors showed that expression of BLINK in the guard cells of Arabidopsis introduced a K+ flux across the membrane of guard cells under blue light treatments. The additional K+ flux brought about by the presence of BLINK resulted in faster changes in stomatal opening and closing in response to light. Indeed, stomata expressing the BLINK protein required about half the time to reach a steady state response under the new light regime compared to that of control plants. In effect, BLINK acted as a light switch that synchronized stomatal movements with the incident light. To further explore the potential of the BLINK approach, the authors grew plants under various light conditions and scored for plant growth and biomass production. Plants expressing BLINK protein showed better performance, especially under fluctuating conditions that require fast adjustments in stomatal movements. Indeed, BLINK-expressing plants had significantly larger rosettes and showed a doubling in the dry biomass accumulation when compared to the control plants. Most importantly, the same effects were also apparent when plants grew under water-limiting conditions.

The study of Papanatsiou et al. (2019) advocates for the use of optogenetics to manipulate ion transport in plant cells. Ion transport is the driving force for changes on turgor pressure that underlie many plant processes such as stomatal movements and morphogenesis. Therefore, application of optogenetic tools similar to BLINK has great potential to improve plant performance. Most importantly, the research highlights the influence of stomatal behaviour on plant physiology and its impact on plant productivity. Manipulating the kinetics of stomatal responses has been discussed often as a promising strategy to match stomatal behaviour with water use efficiency. This study validates such propositions and highlights the efficacy of the BLINK strategy to balance the trade-off between photosynthesis and transpiration and to enhance plant performance under light conditions, typical of outdoor growth. The challenge now lies in whether the results presented in the study by Papanatsiou et al. can be translated into crops. Stomata of most major crops follow the same molecular rules with those of the Arabidopsis plant model organism. The authors therefore argued in favour of BLINK or similar optogenetic tools as an effective strategy to improve crop productivity under fluctuating light conditions, which are often met in agricultural settings.

About Maria Papanatsiou

My interest in biological research led me to the University of Glasgow, where I completed my undergraduate studies in Genetics. I continued my postgraduate studies in molecular, cellular and systems biology and I earned my PhD from University of Glasgow in 2014. My PhD work focused on the interplay between stomatal behaviour, plant physiology and environment. I then moved to join the group of Prof. Nagy at the University of Edinburgh, where I expanded my skills into the area of photobiology. This work investigated the molecular basis of signal transduction via the red-light receptor, phytochrome B. Subsequently, I returned to Glasgow to work with Prof. Blatt and in collaboration with Prof. Christie, where I used optogenetic tools to modulate ion transport in stomata to optimize plant physiology, growth and water use. I am currently working as post-doctoral researcher with Prof. Amtmann aiming to decode plant physiological responses to complex environmental scenarios, using Arabidopsis and soybean plants. Throughout my academic career, I have been passionate about science communication and I have participated to and organized several outreach activities. I have contributed commentaries about the latest developments in plant science and I am the social media editor for the scientific journal Plant, Cell and Environment.

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