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Hacking photosynthesis to stimulate plant growth might be more complex than previously thought

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To photosynthesize more and risking losing too much water, or to conserve water but lose out on photosynthesis? This is the plant’s perpetual dilemma, which has led to the evolution of stomata. University of Tartu plant biologists show that in the future, it would be better to prefer plants with fewer stomata, as they grow faster.

For plants, gas exchange with the surrounding air is even more important than it is for humans, because in addition to oxygen, they also need carbon dioxide from the air. To access air, plants have microscopic pores called stomata on the surface of their leaves, writes Ingmar Tulva, a researcher in plant physiology at the University of Tartu, in Novaator.

The Stomatal Dilemma: balancing photosynthesis and water loss

These stomata are movable: generally, a plant opens its stomata in stronger light and closes them in conditions of water scarcity. Water evaporates from the plant through these stomata, and drying out would not be healthy for the plant. Thus, plants continuously solve the optimization task of allowing in as much carbon dioxide as possible without losing a life-threatening amount of water through their stomata.

In addition to their openness, the conductance of stomata is determined by their number. There are quite a lot of stomata on the surface of a plant leaf: around a hundred per square millimeter. The complex genetic machinery responsible for ensuring a reasonable number of stomata during the early development of the leaf avoids the leaf surface becoming uncontrollably perforated.

This machinery has caught the attention of plant geneticists in the past decade, who are looking for ways to make agricultural plants more efficient. By adjusting just one or two genes, the density of stomata on a leaf can be changed several times. Stomata can be made denser to improve photosynthesis by providing better access to carbon dioxide, or sparser to reduce water loss.

Research groups around the world have tried both approaches and achieved promising results with both: some increase photosynthesis by increasing stomatal density, while others achieve better water management by reducing density. Since water loss can be compensated for with additional irrigation in greenhouse conditions, the first approach seems particularly promising at first glance. However, might the second approach be better suited for fine-tuning field crops?

Layout of the trays in the growth experiment. (a), an example tray on Day 0 (14th day after sowing). The region surrounded by the oval included the studied plants in randomized positions, others outside were Col-0. (b), an example control tray on Day 14; (c), an example low-RH tray on Day 14. Photo: from the original research paper.

Fewer pores, faster growth

In an article published with scientists from the Laboratory of Molecular Plant Physiology at the University of Tartu Institute of Technology, we aimed to clarify this confusion. To do this, we grew different lines of plants with altered stomatal density and openness under different humidity conditions. We conducted our study with Arabidopsis thaliana. Although this is a fairly insignificant plant species, its physiology and genetics are well-studied, and many mutants with peculiar traits are easily available.

Combining altered openness and density is a new idea. We wanted to check whether higher humidity favors greater stomatal density, ensuring better access to carbon dioxide, but might become a burden under lower humidity due to excessive water loss. Conversely, we wanted to know if some combination of higher density and lower openness might become a golden mean.

It turned out that indeed, increasing stomatal density gives a slight advantage in photosynthesis, but it consistently results in a lag in growth rate. Similarly, all plant lines grew worse in drier air—both those with an excess of stomata and those with a normal number—as if air dryness had nothing to do with how many water-losing pores were on the leaf surface.

The pattern is confirmed by the fact that although the openness of stomata also affects water loss, it had no significant impact on plant growth. Somehow, it is the large number of stomata that hinders growth, not the amount of water lost through them. At the same time, plants also lose growth in drier air, which likely has nothing to do with water loss.

Apparently, building stomata is inherently burdensome for the plant. It requires resources from the plant very early in development. These resources come at the expense of constructing other important organs, and therefore it would be more beneficial to create stomata according to the classic principle of as much as necessary, as little as possible.

Work continues 

We also discovered that manipulating air humidity influenced the pattern of stomatal distribution between the lower and upper sides of the leaf. Many plants, particularly in our latitude and especially deciduous trees, are unilateral in their stomatal placement, leaving the upper side of the leaf completely free of pores.

However, not all plants do this. Many species have a considerable number of stomata on the upper side of the leaf—typically somewhat fewer than on the lower side. This group includes the Arabidopsis thaliana we used in our study. For instance, in grasses, including major crops like wheat and barley, most stomata are located on the upper side.

The Role of Stomatal Placement on Plant Efficiency

This phenomenon has been known to scientists for over a century. Why most plants have stomata primarily on the lower side and why some species do not have any on the upper side remains an open question. Many vague ideas circulate on this topic, but no convincing explanation has yet been found.

In our experiments we observed that in drier air, the balance shifted slightly towards the upper side—although the difference was not significant, it was consistently present in all plant lines, and the overall trend was convincing. A higher upper/lower side density ratio might be related to plant yield. This is indirectly suggested by the fact that among agricultural crops, species with stomata-free upper sides are exceptions. However, demonstrating a clear connection and uncovering the genetic mechanisms requires much more work.

Does a greener future look like plants with higher or lower stomatal density? Based on our results, future efforts should focus on plant lines with lower stomatal density, even in artificial growth conditions. Further studies need to show whether the results obtained with our relatively young plants hold up with longer cultivation or with other species, and what role the less-studied upper side of the leaf might play.

The resesearch paper was published in The Plant Journal.

This article was published on the webpage of University of Tartu.


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