by Fernanda Ferreira
figures by Shannon McArdel
Semper augustus was once the most coveted flower in Holland . The Dutch were used to single-hued tulips, collectively called Couleren, but Semper augustus was something else. With its splashes of red on white, this bi-colored or variegated tulip became the symbol of tulipomania, a brief period during the Dutch Golden Age when a single tulip bulb could demand a buying price of thousands of guilders. But Semper augustus and its variegated tulip brethren had a problem: there was no guarantee that when one of its bulbs was planted, an equally beautiful tulip with flame-like streaks of color, would pop out of the ground. You might get a Semper augustus or you might end up with a single-hued Couleren tulip.
The reason behind the finickiness of Semper augustus bulbs began to be unraveled in 1928, three centuries after tulipomania, by Dorothy Cayley of the John Innes Horticultural Institution in London . She demonstrated that variegated tulips are not a separate species of tulips, but rather a single-hued tulip infected with the appropriately named tulip breaking virus (TBV). The long, filamentous virions of TBV “break” the color of tulips by modifying the accumulation of plant pigments, causing them to become bi-colored. These virions are transmitted from tulip to tulip by a number of species of aphids, a sap-loving insect that looks like a tick (Figure 1).
Though florists in 17th century Holland were unaware of the relationship between tulip, TBV and aphid, a visit from a TBV-transmitting aphid could mean the difference between selling a single-hued tulip for a handful of guilders and a variegated tulip for over a thousand. But plant viruses and aphids are not limited to tulips. And unlike a 17th century tulip enthusiast, not everyone considers a visit from a virus-transmitting insect a lucky break. For some, plant viruses are a real threat to food security and, unfortunately, our ability to plan for and manage such epidemics is further encumbered by climate change.
Food security and plant viruses
In many ways, the symptoms of Cassava Mosaic Disease (CMD) on the leaves of cassava plants, a woody shrub that produces an edible, tuberous root, are reminiscent of the variegated colors of Semper Augustus: streaks of yellow on a green background. For some plants, the consequences of viral infections are limited to a mosaic-like discoloring of leaves and fruit, with the virus having no effect on the nutritional value or health of the plant. This is not the case for CMD. CMD decreases the size of cassava plants and CMD-infected cassavas produce little to no tubers (Figure 2).
In 1988, a new virus, East African cassava mosaic virus-Uganda (EACMV-UG) that causes CMD, emerged in Uganda and was quickly spread throughout East and Central Africa by whiteflies. As EACMV-UG spread, it destroyed cassava plantations, forcing farmers to abandon the crop and causing famine and famine-related deaths .
What happened to cassava, the third most important source of calories in tropical regions, in the 1980s was not an isolated event. There are over one thousand virus species known to infect plants and, of the 32 orders of the class Insecta, seven transmit plant viruses. Therefore, plant viruses are widespread and can lead to crop losses that severely affect a regions food security, which the United Nations World Food Programme defines as having “availability and adequate access at all times to sufficient, safe, nutritious food to maintain a healthy and active life.”
Plant virus epidemics such as the one caused by EACMV-UG are particularly devastating when they affect staple crops like cassava. Staple foods are defined by the Food and Agriculture Organization of the United Nations (FAO) as “one that is eaten regularly and in such quantities as to constitute the dominant part of the diet and supply a major proportion of energy and nutrient needs.” For instance, the 15 staple crops listed by FAO provide 90% of the world’s food energy intake (Table 1).
A Warming Triangle
Plants, plant viruses and their insect vectors, exist in a triangle-like relationship, with each element influencing the other two. This relationship, however, does not exist in a vacuum; the environment exerts pressure on each vertex, thus affecting the relationship between plants, viruses and vectors. Take, for example, variegated tulips. A short winter leads to an extra generation of aphids, which causes an increase in aphid numbers and, subsequently, in TBV transmission events and “broken” tulips.
Rising temperatures in particular exert a strong influence on all three elements of the virus-disease triangle and the world has been getting warmer every year. 2016 was almost a full degree Celsius warmer than the average temperature for the 20th century, and global temperatures are expected to keep climbing. With thousands of plant-virus-insect interactions, it’s impossible to model how global warming will affect each relationship and its effect on food production, but certain general trends are expected.
As temperatures increase, plants, viruses and insects will migrate seeking their preferred temperatures. Crop patterns will also change as humans pursue land and weather conditions that are suitable for each crop. In general, these migrations will be towards the warming upper latitudes as well as higher altitudes. And as plants, viruses and insects move, they will come into contact with new indigenous species, with each encounter carrying with it the possibility of a novel plant virus epidemic. Global warming’s effects, however, will not be limited to only creating the potential for new plant virus epidemics, it can also increase the virulence and frequency of outbreaks of known plant viruses.
Aphids transmit a number of plant viruses beyond TBV, all with delightful names such as barley yellow dwarf virus (BYDV) and blueberry shoestring virus (BBSSV). More importantly, many of the viruses aphids transmit infect staple crops like potatoes, barley, soybean and cereals, making aphids an important threat to global food security. As temperatures rise, the aphid population sizes are expected to increase. For instance, in temperate zones, an additional five generations of aphids are predicted to occur yearly if the temperature increases by 2 oC.
Not all aphid species, however, will experience population growth in the face of global warming. How an aphid species responds to rising temperatures will vary depending on each species’ optimum temperature and their current latitude. Tropical aphids may see temperatures rise above their optimum and they will thus need to migrate to higher latitudes and elevations, quickly adapt to rising temperatures or perish. And what happens to aphids and other insect vectors will determine what happens to the plant viruses they transmit.
We tend to picture global warming as always leading to larger and more numerous plant epidemics, but in reality the rate and force of these epidemics will vary from region to region. In tropical areas, for instance, the rate of plant epidemics may actually go down as temperatures rise beyond what insect vectors can withstand. But in temperate regions, the rate of plant epidemics is predicted to go up as tropical and sub-tropical insects and their viruses move to higher latitudes and temperate insects experience higher numbers of offspring.
The Way Forward
Semper augustus left no descendants. The red and white flame-like markings that made it so famous were not the only consequence of TBV infection; the virus also made Semper augustus’ bulbs weak and stunted, leading to the end of the genetic lineage. The enthusiasm for striped tulips, however, never died down. One can still purchase a variegated tulip today, though most of these tulips are not the result of viral infections, but rather of genetic engineering .
The same way we can create a tulip that appears to be infected by a virus, we can also use genetic engineering and targeted plant breeding techniques to generate plant species that are resistant to plant viruses . Such approaches are particularly important as the world population continues to grow–it will hit 7.5 billion this year and it is projected to reach 9.6 billion by 2050– and climate change progresses, putting global food security at risk.
Fernanda Ferreira is a fourth-year graduate student at Harvard University. She is not a tulip enthusiast.
For more information:
R.A.C. Jones’ updated exploration of how climate change will affect plant virus pathogens
Johannes Bosschaert’s Still Life With Tulips (date unknown), Nationalmuseum (Photo: André Costa), public domain via Wikimedia Commons
Unknown Dutch artist’s Semper Augustus (before 1640), Norton Simon Art Foundation (Photo: Chris 73), public domain via Wikimedia Commons