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Scientists solve mystery of grass leaf formation

Simple modulations of growth rules, based on a common pattern of gene activities, create a wide diversity of leaf shapes
wp grass stock
Researchers applied the latest computational modelling and developmental genetic techniques and concluded that a formerly discarded 19th century theory of grass leaf shape was closer to the truth than more contemporary hypotheses.

WESTERN PRODUCER — Few plants are as resilient or grow back so quickly after being cut by mowers or chewed by animals as grass.

Now, evidence shows the actual shape of the grass leaf sets the stage for its abundant and repetitive growth.

The precise shape of the leaf has been a long-standing debate among plant scientists. However, the mystery of grass leaf formation was recently solved by a collaboration of scientists at the John Innes Centre (England) the University of Edinburgh (Scotland), Cornell University (New York) and the University of California, Berkeley.

They applied the latest computational modelling and developmental genetic techniques and concluded that a formerly discarded 19th century theory was closer to the truth than more contemporary hypotheses.

Crops such as wheat, rice and corn are all members of the grass family with the same type of leaf.

“We are fascinated in the diversity of shape that we see in the plant kingdom, and want to understand how the different shapes form,” said Annis Richardson, lecturer in molecular crop science at the Institute of Molecular Plant Sciences, University of Edinburgh.

“The grass leaf is interesting because it has a 3D structure that is important for how it grows. We likened it to a periscope, keeping the stem cells close to the ground but allowing the leaf to grow in height to compete for light with neighbours. We realized that we really didn’t understand how this kind of leaf could develop, or how it relates to the eudicot leaf, which we knew more about. This led us to try to make a model of the leaf and the project started from there.”

Richardson said that flowering plants are split into two clades — monocots (which include the grasses) and eudicots. Monocots have leaves that encircle the stem at their base and have parallel veins throughout.

Eudicots, which include brassicas, legumes and most common garden shrubs and trees, have leaves that are held away from the stem by stalks, termed petioles, and typically have broad laminas with net-like veins.

The base of the grass leaf forms a sheath that allows the plant to increase in height while keeping its growing tip close to the ground, protecting it from the blades of lawnmowers or incisors of herbivores.

“The monocots share an ensheathing leaf base (it wraps around the stem cells) and parallel venation,” she said. “Within the monocots we see variation in leaf shape. The grasses developed ligules and auricles at the boundary between the sheath and blade, which allows them to regulate the angle of the blade. This influences how much light it intercepts.”

Parallel venation refers to veins or veinlets running parallel to each other on the lamina of a leaf while a ligule is a thin tissue outgrowth at the junction of the leaf and the leaf stalk.

In the 19th century, botanists proposed that the grass sheath was equivalent to the petiole of eudicot leaves. But this view was challenged in the 20th century, when botanists noted that petioles have parallel veins, similar to the grass leaf, and concluded that the entire grass leaf (except for a tiny region at its tip) was derived from petiole.

The research team started by characterizing how the shape of the leaf changes from the start of its life. They found that it progressed through a series of clear shape changes, particularly in the earliest stages of development.

“We then started to develop a model that tried to capture these shape changes using some key principals about growth and plant tissue mechanics,” she said.

When they had made a model that could capture the shape changes, they looked at whether the hypothetical factors resembled real genes or proteins in the plant. For example, they had a protein that could be used to reveal polarity in plants because it only localized to one side of the cell.

“By looking at these we were able to test to see if the model predictions, for example where polarity would point, where certain genes would act or be expressed, were correct. If they were wrong, we knew that we needed to change the model. We also tested the model by seeing if it could recreate the leaf shape of well-known mutants. By removing model components that represent the genes responsible for the mutant, we could see if the model responded the same way a real leaf does. It if did not, we went back and changed the model. We call this the build-predict-test cycle. We had a lot of iterations.”

She said that one way to understand how a leaf develops is to compare it to a system that is more familiar and translate the information across. This means understanding which parts of the leaf relate to each other. She added that, when looking at evolution, it is like comparing hoofs to feet and wings to arms.

“For the grass leaf, we need to know what the sheath and blade relate to in the eudicot leaf, which has a petiole and lamina. The question was: is the sheath equivalent to the petiole?

The petiole is the stalk that connects the leaf to the stem. The green blade leaf is the major photosynthetic surface of the plant that is perpendicular to the stem.

All the different modelling hypotheses for how grass leaves grow led them back surprisingly to the support for the 19th century idea of sheath-petiole equivalence.

Richardson said in the news release that the study shows how simple modulations of growth rules, based on a common pattern of gene activities, create such remarkable diversity of different leaf shapes.

“It’s really quite remarkable that two leaves that look completely different and which are separated by some 50 million years of evolution use the same pattern of genes to define their leaf shape,” she said. “It tells us that the differences came about through small changes in how these genes influence growth rather than changing the pattern itself.”

Richardson’s lab next plans to investigate how the mechanism has been altered in different organs to generate different shapes.

“For example, the grass flower has an organ called a lemma which, in many grasses, has a long thin tip called an awn,” she said. “The lemma and awn have lots of roles, including influencing grain filling, seed dispersal, and germination and anyone who has baled hay or worked with awned barley or wheat knows that the awn is quite painful to get stuck in clothes. I am investigating how the lemma shape develops and what genes are involved. The hypothesis is that the same core genes as the leaf are important in setting up the pattern but the wider network that these patterning genes influence is different. By understanding what is different between the leaf and other organs we can find genes that could be targeted for breeding or gene engineering to optimize leaf shape separately from other organs and vice versa.”

The research was recently published in the journal Science.