Growing towards the light: how plants sense their neighbours, and how short wheat fed millions

Part 1: Plants that see their neighbours

1A seedling that germinates in a crowded field faces a problem. It cannot move, and if taller neighbours grow over it, it will be left in the shade with too little light for photosynthesis. Many plants solve this by detecting their neighbours early, often before they are actually shaded, and changing the way they grow. Their stems lengthen, their leaves are held more upright and some flower earlier. Together these changes are called the shade avoidance response. The response is controlled by a light-sensitive pigment, a set of transcription factors and several plant hormones.

2Light is both a resource and a source of information for plants. As well as the chlorophyll and other pigments used in photosynthesis, plants have several photoreceptor pigments that detect the colour, brightness and direction of light. The best understood is phytochrome, which was discovered in the 1950s. Phytochrome is a protein joined to a light-absorbing pigment molecule, and it is found in the cytoplasm of cells in most parts of the plant. Other photoreceptors, which absorb blue light, help the shoot to bend towards the brightest light.

3Phytochrome exists in two forms that can be converted into each other. The form called Pr absorbs red light, with a peak at a wavelength of about 660 nm, and is converted into the form called Pfr. Pfr absorbs far-red light, with a peak at about 730 nm, and is converted back into Pr. In darkness, Pfr is also slowly converted back into Pr. Pfr is the physiologically active form, which means that it is Pfr that brings about responses in the plant.

4Sunlight contains slightly more red light than far-red light, with a ratio of red to far-red of about 1.2. Leaves absorb most of the red light that falls on them, but they absorb very little far-red light, which is transmitted through the leaf or reflected from its surface. Under a dense canopy of leaves, the ratio of red to far-red light can fall to 0.2 or less. Even light reflected from the leaves of nearby plants lowers the ratio a little, which warns a seedling that competitors are close.

5In a seedling growing in open sunlight, much of the phytochrome is in the Pfr form. When the ratio of red to far-red light falls, more Pfr absorbs far-red light and is converted into Pr, while less Pr is converted into Pfr. The proportion of phytochrome present as Pfr therefore falls. The plant responds to this change rather than to the total amount of light, which is why the response can begin before the seedling is in deep shade.

6Pfr acts by moving from the cytoplasm into the nucleus. There it binds to a group of transcription factors called phytochrome-interacting factors, or PIFs, and causes them to be broken down. In shade, with less Pfr, PIFs build up in the nucleus. They bind to the promoters of many genes and increase their transcription. Some of these genes code for enzymes that make the plant hormone auxin, so auxin production increases in the leaves and shoot tip.

7Auxin moves down the stem and causes cells to elongate. According to the acid growth hypothesis, auxin stimulates proton pumps in the cell surface membrane, which pump hydrogen ions out of the cell into the cell wall. The lower pH activates proteins called expansins, which loosen the bonds between cellulose microfibrils in the wall. The cell takes up water by osmosis, and because the wall is now easier to stretch, the cell becomes longer.

8In an illustrative experiment, seedlings of the small plant Arabidopsis were grown for seven days under LED lights. Both groups received the same intensity of red and blue light, but one group also received extra far-red light, lowering the ratio of red to far-red light from 1.2 to 0.3. The mean length of the seedling stems was 2.4 mm in the high ratio group and 5.4 mm in the low ratio group. Plants grown on in low ratio light also flowered about a week earlier.

9Phytochrome also controls when some seeds germinate. Small seeds, such as those of lettuce, contain few food reserves and must germinate close to the soil surface where there is light. In a famous series of experiments in the 1950s, lettuce seeds given a brief flash of red light germinated, while seeds given red light followed by far-red light did not. When the seeds were given alternating flashes, only the colour of the last flash mattered. In nature, seeds that are buried, or that lie under a dense canopy, stay dormant.

10"Phytochrome is an incredibly simple switch, but plants use it to answer a surprisingly complicated question," says Dr Priya Raman, a plant physiologist who studies crop competition. "The question is: is it worth investing in height right now? Growing tall costs a lot of energy and materials, so a plant only wants to do it when its neighbours are about to take its light. If the plant is already deep in the shade of a forest, growing taller will not help, and many woodland plants hardly respond at all."

11The cost is real. Elongated stems are thinner and weaker, and the sugars and amino acids used to build them are not available for leaves, roots or seeds. In a natural plant community, shade avoidance can help an individual plant to survive. In a field of crop plants that are all the same height, though, every plant reacts to its neighbours, and the crop ends up wasting resources on competing with itself rather than producing grain. Breeders therefore try to produce crops in which each plant behaves less like a competitor and more like a member of a team.

Part 2: Short wheat and the Green Revolution

12Stem elongation is also controlled by a second group of plant hormones, the gibberellins. Gibberellins work by removing a brake on growth. Plant cells contain DELLA proteins, which bind to and inhibit transcription factors that switch on genes needed for growth, including the PIFs. When a gibberellin binds to its receptor protein, the receptor binds to the DELLA proteins, which are then broken down. The transcription factors are released and the growth genes are transcribed. Shade increases gibberellin production too.

13In the 1950s and 1960s, plant breeders led by Norman Borlaug in Mexico were trying to increase wheat yields by giving crops more nitrogen fertiliser. The tall wheat varieties of the time grew even taller with extra fertiliser, and when their heavy heads of grain were hit by wind and rain, the stems bent over and lay flat on the ground. This is called lodging, and much of the grain was lost. Borlaug crossed his wheat with a Japanese variety that carried dwarfing genes.

14The dwarfing genes, known as Rht genes, are mutant alleles of genes that code for DELLA proteins. The mutations remove the part of the DELLA protein that binds to the gibberellin receptor. The altered DELLA proteins are therefore not broken down when gibberellin is present, so they continue to inhibit the transcription of growth genes. The plants have shorter, stronger stems, and a greater proportion of the products of photosynthesis is used to make grain.

15Semi-dwarf wheat varieties spread rapidly through Mexico, India and Pakistan in the 1960s. Wheat production in India rose from about 12 million tonnes in 1965 to about 20 million tonnes in 1970, and many people who might otherwise have gone hungry were fed. Rice breeders made a similar change. The most widely used dwarf rice carries a mutation in a gene for an enzyme needed to make gibberellin, so the plants make less of the hormone. Borlaug was awarded the Nobel Peace Prize in 1970 for his work.

16There were drawbacks. The Rht wheat varieties produce a shorter shoot when the seed germinates, so they cannot be sown as deeply. This is a problem in dry regions, where the soil near the surface dries out quickly. The new varieties also gave their best yields only when they were given large amounts of fertiliser and water. Fertiliser washed from fields into rivers and lakes has contributed to eutrophication in many parts of the world.

17Breeders are now trying to make crops that ignore their neighbours. Planting maize or wheat more densely could increase the yield from each field, but only if the plants do not waste resources on shade avoidance. In an illustrative field trial, wheat plants in which one PIF gene had been inactivated using gene editing were planted at twice the normal density. Their stems were 12 per cent shorter than those of unedited plants at the same density, and grain yield per square metre was 9 per cent higher.

18Commercial growers already use light to control the shape of plants. Many greenhouses now use LED lighting, which can be set to give a particular ratio of red to far-red light. Growers who want short, bushy pot plants can give extra red light, while those growing cut flowers with long stems can add far-red light. This reduces the use of chemical growth regulators, many of which work by blocking the synthesis of gibberellins. Far-red light given at the end of the day has a particularly strong effect, because the phytochrome then stays mostly in the Pr form through the night.

19"The Green Revolution worked by accident, using mutations that breeders could see but did not understand," says Dr Raman. "Now that we understand the switches, from phytochrome to the DELLA proteins, we can choose exactly which part of the response to change. The challenge is to do it without making the crop less able to cope with drought, pests or a changing climate. Every change we make has to be tested in real fields, in real weather, over several seasons."