Cold Snap: the physics of food security

How a single mutation in one gene leads to cold-tolerance in rice

 

In the summer of 1980, Korean rice farmers were getting nervous.  The weather was cooler than usual. The unseasonable temperatures had begun in July and were continuing through late August.  When September began, things got worse. Even the autumn temperatures were lower than normal. In the end, it was the worst harvest since the Korean War. More than three quarters of a million hectares of rice crops had been damaged, equating to a loss of around 1.5 million tons of rice. To make up for the shortfall, the South Korean government had to spend an extra $1 billion on food grain imports at a time when the economy was already having problems.

New research suggests that this may have all hinged on the behaviour of a single protein.

Today, half the world’s population consumes rice. It’s cultivated in at least 100 countries on every continent except Antarctica. It’s an important staple but also one that’s incredibly sensitive to the vagaries of weather. Both hot and cold cause crop damage, leading to food shortages and financial losses that significantly impact local and national economies.

The Korean harvest of 1980 was not an isolated event, time and again around the world cool temperatures prove to be as disastrous to rice as heat.  Moreover, the temperature drop can seem deceptively mild. What may seem like a pleasant, crisp week to everyone else can damage a harvest.

 photo credit: © zephyr_p / Dollar Photo Club

Of course, this isn’t a new problem. Humans have been consuming rice for millennia. It began with the collection of wild rice species, and then sometime around 8,200 to 13,500 years ago domestication began in what would later become China.  Thousands of cycles of selection and breeding have now resulted in two major groups of Asian rice each representing a both a critical trait and a trade-off.  Indica rice (O. sativa ssp. indica) is high yield but cold-sensitive. Japonica rice (O. sativa ssp. japonica) has more moderate yields, but is cold tolerant.

The ideal average temperature for growing indica is somewhere around 25 °C / 77 °F, but a mercury dip to 15 °C / 59 °F can wreak havoc if it comes at the wrong time in a plant’s life cycle. This could just be an early frost, a later than usual thaw, or a very cool summer. Japonica, while also a summer crop, can nevertheless handle an average temperature a few degrees Celsius (several degrees Fahrenheit) lower than indica. That may not seem like much, but it means that the minimum temperature is low enough for it to handle unseasonably cool weather as well as farming at higher latitudes or altitudes. It becomes the difference between a good harvest and a failed one.

Japonica and Indica rice comparison

indica rice (left) and japonica rice (right); photo credit:  Hinata Masatika CC BY-ND 2.0

Both traits in one crop would be ideal, and efforts to produce hybrids have been underway for quite some time, with varying results. But one of the hurdles is the fact that no one really knew precisely why japonica could handle the cold so much better than indica. There was mounting evidence that a variety of different genes are turned on and off in response to cold, but what controls this in japonica was unknown.

In the thousands of years of honing this type of rice for northern climes and higher elevations, it’s reasonable to assume a vast number of genetic differences must have accumulated to result in cold tolerance. However, a team of geneticists in China have now identified a single mutation in just one gene. Their results were published this month in the journal Cell.

They dubbed the gene COLD1, which stands for CHILLING TOLERANCE DIVERGENCE 1 (in the fine scientific tradition of working the name around a good acronym). This gene instructs the cell to make the COLD1 protein. Yun Ma, Kang Chong and their colleagues were able to identify well known patterns in this protein that suggest that it does not float freely within the cell, but is instead embedded in a membrane. If you imagine the membrane as a cloth, and the protein as a thread, then it’s as though it’s been stitched in and out several times in a closely packed pattern. Consequently some parts of the protein sit on the top side of the membrane and some parts sit on the underside.

So how could a slight change in COLD1 help an entire plant become tolerant of cooler temperatures?  To find out, the research team first needed to figure out what role the protein normally plays. They identified a series of distinct signatures in COLD1 suggest it belongs to a family of proteins capable of conducting positively charged calcium ions (Ca2+) from one side of a membrane to the other, like a tiny voltage gate.

Ions are just atoms or molecules with an electric charge and the flow of ions across membranes is an important part of any cell’s ability to grow and thrive. Minute changes in levels of ions such as calcium act as ‘on’/’off’ signals for a staggering array of cell functions. Such tiny fluctuations are enabling your neurons to function as you read this (in addition to keeping you alive). Plant cells also rely on ion signals and there now exists quite a lot of evidence that calcium signals help plants re-establish growth after a stressor like cold temperature. Such signals can even change the patterns of which genes are activated as the plant endures the stress and then recovers.

In indica rice, cooler temperatures decrease the ability of COLD1 to transport calcium ions across the membrane.  The influx of calcium slows to a trickle. This in turn has a dampening effect on anything reliant on calcium signals, including pathways that control plant growth and height. Thus, when indica experiences a cold snap, things shut down and don’t recover. It is, in effect, an in-built temperature sensor.

To understand why this happens, we just need to take a quick look at how all proteins respond to changes in temperature. Protein structures have closely packed architectures, and their functions are intricately tuned to disturbances in those structures. At very low temperatures proteins become rigid, at high temperatures, they become less constrained. As such, a protein suited to moderate temperatures becomes too stiff to function in the cold and too floppy to function in the heat. But evolution has been onto this for a while now, give or take a few billion years.  This is why proteins in cold loving organisms have looser structures to begin with, so when they tighten up in cold temperatures, they still work. Conversely, proteins in heat loving organisms, such as those found in hot springs, have very rigid structures that loosen up nicely as the temperature rises. It’s also worth noting that that temperature can alter the fluidity of membranes. So if a protein happens to be embedded in a membrane, this can affect its freedom of movement, which in turn can dictate how well it works. Importantly, you don’t have to change a protein’s entire sequence to change its ability to function in a different temperature range or affect the way it interacts with its immediate surroundings. It just has to be the right changes in the right part of the structure and the follow-on effect can be substantial. In japonica it is:  when the temperature drops, COLD1 keeps working.

When the researchers compared the genetic sequences of cold sensitive indica rice with cold-tolerant japonica rice they found a change at a single nucleotide, which in turn changes the protein in one place. In indica rice, there is usually a moderately sized, uncharged amino acid at position 187 in the protein sequence (either methionine or a threonine). But in japonica COLD1, amino acid 187 is a lysine — it’s one of the biggest amino acids, and also carries a positive charge.

Somehow that lysine keeps the calcium flowing in cooler weather. It may be that such a disruptive replacement prevents that region of the protein from becoming too rigid, enabling it to maintain its connections with its molecular teammates at lower temperatures. Fluctuations in calcium levels remain possible as the temperature drops, and these in turn are able to trigger important growth signals within the cell.

Rice fields on terraced at Chiang Mai, Thailand

 photo credit: © narathip12 / Dollar Photo Club

Ma, Chong and their colleagues also determined that this important genetic change wasn’t a spontaneous mutation that turned up over the last few millennia. Precisely the same mutation exists in the ancient wild rice species called Oryza rufipogon, and this suggests that the farmers who cultivated japonica had deliberately selected this trait as they bred rice to grow in cooler climates. Now we know just what it was they were selecting.

The identification of COLD1 and the variations that affect its behaviour improve our understanding of temperature sensitivity in rice and this knowledge has the potential to significantly impact future breeding efforts. For plant biologists Prabha Manishankar and Jorg Kudla, who reviewed the paper, the implications are far reaching.

“This work may pave the way to tackle the food production insufficiency due to environmental changes and may contribute to food security by stabilizing the yield of a major crop that nurtures a large human population on this planet.”

 

Sources:

Ma, Y et al (2015) “COLD1 confers chilling tolerance in rice” Cell 160 (6) 1209–1221

Manishankar and Kudla (2015) “Cold tolerance encoded in one SNP” Cell 160 (6) 1045 – 1046

http://ricepedia.org/

The history of japonica rice http://http-server.carleton.ca/~bgordon/Rice/papers/sato99.htm

http://www.csmonitor.com/1981/0317/031750.html

http://aciar.gov.au/files/node/2301/pr101chapter02.pdf

http://www.researchgate.net/publication/265613956_Calcium_signaling_in_plant_cells_under_environmental_stress

http://onlinelibrary.wiley.com/doi/10.1002/fes3.25/full

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