FROM blades of grass to the cup-like fly-catcher of the pitcher plant, the diversity of leaf shapes, sizes and structures is stunning. It is also incredibly useful, allowing plants to live nearly everywhere on Earth, from the deserts of the western US to the lush shores of the Amazon. Now the precise molecular switches that control the process are being unpicked.
鈥淲e are at the stage of putting together a blueprint of the genetic program controlling leaf shape,鈥� says Andrew Fleming, a leaf researcher at the University of Sheffield, UK. 鈥淭his opens the door to experiments whereby we can change leaf form in a targeted fashion.鈥� And it鈥檚 not just about creating weird and wonderful leaf shapes at will. The findings could be the first step in the next green revolution, leading to a new generation of crops with dramatically increased yields. They could also be better adapted to surviving in a warmer world.
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Because leaves are the main site of photosynthesis, they are ultimately the source of almost all food on the planet. By controlling the molecular basis of leaf shape, plant biologists may be able to enhance plants鈥� ability to adapt to a changing environment without the protracted guesswork involved in selective breeding. 鈥淭he question is: what does an optimal leaf look like and can we design one?鈥� says Fleming.
鈥淟eaves are the main site of photosynthesis, and so are the source of almost all food on the planet鈥�
Over the past year, several landmark papers have been published that shed light on how different leaf patterns are generated. They reveal that the genes and molecules that guide leaf patterns are very similar across a wide variety of plants.
鈥淢ore and more we鈥檙e seeing that it鈥檚 a combination of promoting and suppressing outgrowth,鈥� says Neelima Sinha at the University of California, Davis.
Sinha鈥檚 group has discovered that a growth hormone called auxin 鈥� previously known to boost the growth of leaf veins 鈥� plays a key role in controlling leaf shape. They applied auxin to one edge of a tomato leaf and found that it lost its serrated pattern and grew indiscriminately. The auxin-free side of the leaf developed normally (Development, ).
Miltos Tsiantis of the University of Oxford and his colleagues have also shown that the shape of complex leaflets in Cardamine hirsuta, a relative of mustard, is dependent on the action of auxin at distinct points at the edges of developing leaves, and that inhibiting its action prevents leaflet formation (Nature Genetics, ).
Meanwhile, Patrick Laufs at the French National Institute for Agricultural Research in Versailles has discovered 鈥渂oundary鈥� genes that are expressed in the small nook separating leaflets in pea, columbine, tomato and lamb鈥檚 cress. The genes seem to inhibit the growth of leaf cells (Science, ). 鈥淚f you remove them then the two outgrowths just flow into each other and become one,鈥� says Sinha. 鈥淏y doing this kind of punctuated 鈥榞row鈥� 鈥榙on鈥檛 grow鈥� 鈥榞row鈥� signalling program, you can start to change its shape.鈥�
Other genes involved in different aspects of shape are also emerging. Fleming has identified one that seems to make flat leaves goblet-shaped by suppressing cell division in certain areas of the leaf. And Michael Lenhard of the University of Potsdam in Germany and his colleagues recently identified a key gene involved in controlling the size of leaves, petals and seeds (Current Biology, ). Overexpressing the gene in Arabidopsis creates larger leaves, flowers and seeds. Preliminary studies also suggest that it might increase grain size in oil seed rape.
This last point is key. Plants are adapted to the environments they grow in naturally, but these can be very different from farmed settings. Understanding how plants optimise light capture is important, says Sinha. Many of our crops are grown in dense conditions where shading can be an issue, for instance. The emerging research might lead to crops with bigger leaves, or help work out whether certain leaf shapes are better suited to capture light in shadier conditions.
Modifying shape and size can go a long way to increasing a plant鈥檚 productivity, but it doesn鈥檛 end there. Stomata are the small pores on leaves that regulate how much carbon dioxide and water moves in and out of leaves. Leaves convert CO2 into sugars through photosynthesis (see 鈥淭weak photosynthesis鈥�) and water is key to both the plant鈥檚 temperature and ultimately its survival. Controlling whether stomata are open or shut and how many there are can therefore have a major impact on how well the leaf works.
Ikuko Hara-Nishimura at Kyoto University in Japan and her colleagues have found a gene called stomagen that increases the density of the pores. When they purified the protein it produces and applied it to Arabidopsis seedlings the leaves produced more stomata (Nature, ).
As well as boosting yields by optimising the amount of CO2 that plants can capture and therefore boosting the amount of sugars they produce, artificially manipulating stomata numbers may help create crops that are more resistent to drought or heat. Plants open their stomata to cool themselves down through transpiration, and close them to retain water. This suggests they may be able to adapt to climate change to some degree, but in extreme situations they may need a helping hand.
鈥淥ne of the things people have been worrying about for some time now is if we take a global warming scenario, where CO2 goes up and temperature goes up,鈥� says Dominique Bergmann of Stanford University in California. Plants naturally reduce stomata numbers in response to high CO2 concentrations. But in doing so they might lose their ability to cool themselves, and overheat and die. 鈥淚f stomata number is sensitive to a number of different environmental factors, they might not be able to uncouple those things in the time that they need to,鈥� says Bergmann.
Plant biologists believe that by artificially manipulating the number of stomata, it might be possible to boost plants鈥� natural ability to adapt and create more resilient plants as a result.
Fleming points out that a modified wheat that had shorter stems was in many ways the basis of the green revolution of the 20th century. Shorter stems meant the plant put more resources into producing grain that was easier to harvest. He thinks a similar revolution is overdue. 鈥淚f we鈥檙e going to support the growing global population, we need some sort of step change in the amount of food that we produce,鈥� he says.
Tweak photosynthesis to turbocharge rice
Rice is a staple food for much of the world, and will be an essential part of solving the looming global food crisis. One way of boosting yields may be to fundamentally change the way it photosynthesises 鈥� and that could involve tinkering with the cells that shuttle CO2 around the leaves.
Photosynthesis comes in two flavours: C3, and the more efficient C4. Rice, like most plants, is a C3 plant so researchers are seeking to make it C4. Early attempts to do this have focused on modifying photosynthetic enzymes 鈥� particularly rubisco, which fixes CO2 and makes it available to chloroplasts. 鈥淚t now appears clear that you need to adapt aspects of leaf form and anatomy as well,鈥� says Andrew Fleming at the University of Sheffield, UK.
In C3 leaves the CO2 diffuses into each leaf cell separately, where it is captured by rubisco to be turned into sugars. The catch is that rubisco occasionally binds to oxygen instead of CO2. In C4 leaves, on the other hand, concentric rings of cells 鈥減ump鈥� CO2 into specialised, rubisco-containing cells. By increasing the concentration of CO2 around the enzyme, this system reduces rubisco鈥檚 error rate, says Julian Hibberd of the University of Cambridge and a member of an international C4 rice project, funded by the Bill and Melinda Gates Foundation.
Hibberd and his colleagues are screening thousands of different rice mutants for subtle changes in leaf structure that could help them identify the genes responsible for this cellular organisation. The hope is that once they can find the genetic switches that create the cellular CO2 pump they will be able to implant it into C3 rice and turn them into C4 super-producers.
